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he Wilson Journal
of Ornithology
Volume 124 , Number 1 , March 2012
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Academy of Natural Science*
of Philadelphia
Published by the
Wilson Ornithological Society
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1
watcr^ns^mV^- J'he Northern Blac^ Swi,t (O pseloides niger borealis) is known to nest in moist and cool sites near
placed on Northern^ B hok^ r^ °! win.tering areas and migra‘»on paths is non-existent. Use of light-level geolocators
revealed the first known V- \W* . borealis in Costa
Rica in spring had no specimens collected for
confirmation (Stiles and Skutch 1990). Kiff
(1975) tentatively assigned a female swift col¬
lected in Costa Rica to C. n. borealis based on
1
2
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 1. March 2012
wing and tail measurements that are within ranges
for C. n. costarieensis, further highlighting the
uncertainty of migration and winter distribution
for this subspecies. Winter records for Northern
Black Swift arc non-existent.
Several factors contribute to the lack of
knowledge about migration and winter distribu¬
tion of this species, including difficulty in
accurate field identification of individuals due to
high and rapid flight, problems differentiating this
species from similar-size members of Cypseloides
that occupy Central and South America, and
inability to verify observation records. No band
recoveries exist outside of the United States from
~200 Northern Black Swifts banded from 1950 to
present (Bird Banding Laboratory, pers. comm.),
Currently, satellite tracking devices which
provide accurate tracking of individuals are not
sufficiently small to place on a species the size of
Black Swifts. However, light-level geolocators,
devices that record ambient light levels at fixed
intervals, are highly effective instruments for
tracking long-distance migratory species and are
sufficiently small to place on swifts. They are
battery-powered instruments with a microproces¬
sor, clock, and memory for data storage; geo¬
graphical positions can be calculated from the
data collected by the devices.
Geolocators must be retrieved to download
data, and the Black Swift is particularly suited to
recapture due to its high breeding colony fidelity
and an individual propensity to reuse the same
nest from year to year (Foerster 1987. Collins and
Foerster 1995, Marin 1997, Hirschman et al.
2007). We placed geolocators on four Northern
Black Swifts with the objective to gather infor¬
mation about the migratory path, timing, and
winter destination of this species.
Identifying the connectivity of a migrating
species between breeding sites and wintering
areas is crucial to understanding the species'
ecology and in guiding conservation efforts. Time
spent in widely separated and ecologically
disparate locations by migrating species and the
strength of this link can have great biological
consequences for individuals and populations,
me uding reproductive success, population dy¬
namics, behavioral ecology, evolution, and re-
^cctive pressures (Webster
can nr' . ^Advances in geolocator technology
ua"s a?h h rfol™‘ion by individ
betaus e 'nf Ut,0n- Wc ‘-™*'ded this study
because tnforntatton on migration and wintering
areas of Northern Black Swifts was virtually non¬
existent (Lowther and Collins 2002, Wiggins
2004). The small sample does not tell us how-
weak or strong the migratory connectivity is for
this subspecies, but forms a foundation for
additional knowledge of this species' ecology
and can guide future studies.
METHODS
Study Sites. — Northern Black Swifts nest at or
near waterfalls typically inaccessible due to steep
and vertical configuration (Knorr 1961. Levad
et al. 2008). More than 100 breeding sites of this
species have been documented in North America
(Lowther and Collins 2002, Levad et al. 2008)
with only a few records of alternate types of sites
such as sea caves in California (Legg 1956). small
cave-like boulder configurations in streams (Foer¬
ster and Collins 1990, Johnson 1990, Hurtado
2002), and caves (Davis 1964, Northern British
Columbia Caving Club 2003).
We chose Fulton Resurgence Cave (39 49' N.
107 24' W) and Ouray Box Canyon Falls (38 I'
N, 107 40' W) in Colorado because of accessi¬
bility and the probability of capturing and
recapturing Black Swifts using hand-held or mist
nets. These breeding colonies are two of the
largest in Colorado (Levad et al. 2008) with an
average of eight nesting pairs (range 7-9, n =
6 yrs) at Fulton Resurgence Cave (KMP, pers.
obs.) and an average of 1 1 nesting pairs (range 7-
15, n = 10 yrs) at Box Canyon Falls (Hirshman
et al. 2007, Levad et al. 2008). Fulton Resurgence
Cave is a limestone cave with a small stream
issuing from it. forming a microhabitat conducive
for a Black Swift breeding colony (Knorr 1961).
Mist nets placed near the mouth of the cave, the
only ingress/egress for swifts, have resulted in a
recapture rate of 41% since banding of adults
began in 2006 (KMP. pers. obs. ). Box Canyon Falls
is a popular tourist site and walkways provide
views of the falls. The walkways allow access to
several nest sites and. with the aid of ladders,
several nests can be reached with hand-held nets.
Data Collection. — We used four MklOS model
geolocators, manufactured by the British Antarc¬
tic Survey (BAS), programmed to continuously
measure light levels every minute and archive the
maximum measurement for each 10-min period.
The devices weighed 1.2 g, measured IS X 9 X
6 mm, and have a light sensor mounted at the tip
of a 10-mm stalk angled at 15 to prevent it from
being covered by feathers. The instruments are
Beason et al. • BLACK SWIFT MIGRATION AND WINTERING AREAS
3
encapsulated in a water-resistant housing with
two external terminals for commands and data
transfers.
We designed a backpack harness system
modified from Buehler et al. (1995) because
Black Swift legs are too attenuated for the leg-
loop harness often used for geolocators on
passerines (Rappole and Tipton 1991). The
harness material. 5 mm tubular Teflon ribbon
(Bally Ribbon Mills. Bally. PA, USA), was
attached at four points to the geolocator and
crossed under the keel. We secured the free ends
of the ribbon with size 69 bonded right twist
Kevlar thread (The Thread Exchange Inc., Wea-
verville. NC. USA) and stitched the ribbon where
ii crossed the keel to avoid shifting. We applied
cyanoacrylate glue on all stitches and cut ends to
prevent fraying.
We attached geolocators to four adult Black
Swifts in August 2009. three al Fulton Resurgence
Cave (2 females. I male) and one at Box Canyon
Falls (male); the birds weighed 49.5 51.5 g. Each
geolocator, including harness materials, weighed
1.5 g. representing 2.9-3% of body weight, well
within guidelines suggested by Caccamise and
Hedin (1985).
Delta Analysis. — We conducted pre-deployment
calibration for ~9 days and post-deployment
calibration for ~7 days by placing them at a
known location with a dear view' of the sky. We
retrieved Ihree of Ihe four geolocators in July and
August 2010.
We used software programs (BASTrak) devel¬
oped by BAS to download, process, and interpret
data archived by the loggers, each of which had
collected data throughout their entire deployment.
We rejected latitude data gathered ~30 days
before and after the equinoxes since day lengths at
the equinoxes are equal at all latitudes, resulting
in poor location fixes. Internal clocks maintained
accuracy during deployment and there was no
need to correct for clock drift.
Two values are required for analyzing and
plotting the geolocator data: the dusk/dawn light
transition threshold and the corresponding sun
elevation angle at this threshold. We chose a
sensitive light transition threshold value of two to
reduce variation in day length due to the effects of
shading which influences the resulting distribution
of location fixes. We used static pre-deployment
calibration to calculate the corresponding sun
elevation angles (-6.4 , -6.5 , and -6.6 ). We
calculated times of sunrise and sunset using
TransEdit2; positions were calculated with Bird-
Tracker which derives longitude from absolute
time of local midday/midnight and calculates
latitude by comparing day/night length, a tech¬
nique which provides two geographical positions/
day. Wc used only midnight fixes to produce
maps based on the assumption that sw'ifts were
roosting at night and migrated during die day. We
identified days with irregular shading events,
resulting in shorter day lengths or anomalous
transition limes, by visually inspecting sunrise and
sunset times and excluded them from the analysis.
An average of 145 fixes for each bird remained to
map wintering range and an average of 26 fixes
remained to map the spring migration path.
Mapping of fall migration was not possible due
to overlap with the fall equinox.
We calculated kernel density surfaces using the
wintering area data from each geolocator with the
Spatial Analyst Kernel Density function (ESRI
2009). This function calculates density of fixes in
a search radius around those fixes. These densities
lit a smoothly curved surface over each location.
The surface value was highest at the location of
the point and diminished with increasing distance
from the point. We used a fixed kernel with a
search radius of 185 km to compensate for the
approximate average error in latitude and longi¬
tude known to occur in geolocator data (Phillips et
al. 2004). The kernel function is based on the
quadratic kernel function described in Silverman
(1986). We calculated the density surfaces at
1-km resolution as this is adequate to capture
density at a small scale over a large geographic
area. We calculated 90%. 75%. and 50% density
polygons from the kernel density surfaces to
enhance graphic displays ot higher use density
areas. We used the average nearest-neighbor
distance function in Arclnfo Spatial Statistics
(ESRI 2009) to characterize the spatial point
pattern of winter locations. This function quanti¬
fies and characterizes the spatial pattern of each
geolocator and indicates if the pattern is evenly
dispersed, random, or clustered compared to a
spatial random distribution. We estimated approx¬
imate migration duration, arrival, and departure
events from plotting longitude and date. We used
the 50% kernel density polygons for
all three swifts to describe land cover use and
overlaid those with a global land cover layer usine
2009 satellite imagery at a 300-m resolution
produced by the European Space Agency Glob-
Cover 2009 Project (Bontemps et al. 2010).
4
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124, No. 1. March 2012
TABLE 1 . Phenology of migration stages of three North¬
ern Black Swifts".
Departure from Colorado
Arrival at wintering area
Time spent at wintering area
Departure from wintering area
Arrival in Colorado
Duration of southbound
migration
Duration of northbound
migration
14 Sep (10-19 Sep)
5 Oct (28 Sep-12 Oct)
220 days (209 to 227 days)
13 May (9-20 May)
1 Jun (23 May-18 Jun)
2 1 days ( 1 8 to 23 days)
20 days (14 to 29 days)
“ Arrival and departure dates are presented as means with range in
parenthesis.
RESULTS
Geolocators recovered from two females at
Fulton Resurgence Cave and one male at Box
Canyon Falls represent a 15% recovery rate. The
Black Swifts initiated fall migration from Colo¬
rado beginning on 10 September and continued
through 19 September 2009. We used longitudinal
information around the time of the autumnal
equinox and documented the swifts arrived at
their wintering location in South America be¬
tween 28 September and 12 October 2009.
Approximate dates of migration initiation north
from wintering areas began on 9 May and
continued through 20 May 2010. Dates of arrival
at breeding sites began 23 May and continued
through 18 June 2010 (Table L Fig. I).
Kernel density estimates indicate all three birds
over-wintered primarily in the lowland rainforest
of western Brazil with some kernels extending
into Bolivia, Colombia. Peru, and Venezuela
(Fig. 2). Average nearest-neighbor distance anal¬
ysis for all geolocators exhibited clustering with
nearest-neighbor ratios = 0.89 ( P = 0.02), 0.74
( P < 0.001), and 0.77 (P < 0.001) for geolocator
#553, #554. and #556, respectively. The distance
between the Ouray Box Canyon Falls breeding site
and the center of the wintering range in Brazil
(#554) is 6,901 km and the average distance
between the Fulton Resurgence Cave breeding site
and the center of the wintering range in Brazil
(#553 and #556) is 7.025 km. The swifts traveled at
an average speed of 341 km/day during the 2009
fall migration and an average speed of 393 km/day
duiing the 2010 spring migration. The inaccuracy
ol geolocators precludes precise calculation of an
average daily distance covered by each bird.
The land cover overlay maps for 50% kernel
density areas for all three birds indicate a
FIG. 1 . Spring migration routes for three (#'s 553. 554.
5561 individual Northern Black Swifts marked in Colorado.
dominant land cover (>86%) of closed to open
broadleaved evergreen or semi -deciduous forest
and a small percentage (2-10%) of the kernel
density areas are classified as closed to open
Beason et al. • BLACK SWIFT MIGRATION AND WINTERING AREAS
5
isws
SOUTW 7*WW
FIG. 2. Northern Black Swifts marked in Colorado
wintering distribution kernel density contours (red = 50%.
green = 15%. blue = 90%) from 28 September- 1 2 October
2009 to 9-20 .May 2010.
broadleaved forest regularly flooded. Areas of
mosaic cropland/vegetation, mosaic forest shrub-
land/grassland, closed to open shrubland or grass¬
land. bare areas, and water bodies represented
<2% use.
DISCUSSION
We documented the timing of fall and spring
migration, wintering area, and spring migration
paths for three Northern Black Swifts using
geolocators. The return dates to breeding sites
after spring migration and dates of the initiation of
fall migration correlate with data collected in
other research (Hirschman et al. 2007). Wintering
area locations were previously unknown, and only
sporadic reports existed which did not fully
delineate migratory paths.
The highest kernel density estimates indicate
the three birds wintered almost entirely within the
State of Amazonas, Brazil. The clustering of the
three individuals exhibited by nearest-neighbor
analysis might be expected based on the birds
seeking a physiologically optimal climate, pre¬
ferred habitat, abundant prey, or other factors
within a certain geographic area. Amazonas is
composed almost entirely (—98%) of lowland
rainforest at elevations between 34 and 116 m.
The area is sparsely populated with a density of
2.05 inhabitants/km2 with 78% of die population
in cities (IBGE 201 1). Amazonas has an equato¬
rial tropical rainforest climate with annual rainfall
of 1.50-2.50 m and all months have a mean
precipitation of at least 60 mm (IBGE 201 1 ). The
average temperature per day per year is 26.7 C
(23.3-31.4 Cl with high humidity (Brasil Travel
Guide 2011).
The three birds tracked in this study represent
only a small geographical subset of the Northern
Black Swift population and further studies are
needed to delineate more completely the full
extent of the wintering distribution of this
subspecies. The three birds wintered in the same
general area, suggesting a high level of connec¬
tivity between breeding and wintering popula¬
tions. Stutchbury et al. (2009) found a similar
connectivity for Wood Thrush ( Hylocichla mus-
lelina), not previously documented for migratory
songbirds. The large w intering areas may retied a
temporal movement noted for each bird.' The data
indicate a trend for each bird to be in the eastern
portion of the kernels in October with gradual
movement west in April and May. The most likely
explanation for this replicated non-random change
6
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124, No. 1, March 2012
in position is that the birds moved, perhaps
following their food source. This net westward
directional movement is less likely to be an
artifact due to shading or weather-related varia¬
tion because it was consistent among the three
birds tracked.
Northern Black Swift roost sites and roosting
behavior in South American wintering areas are
unknown. Waterfalls, caves, and dripping rock
faces serve as roosting and breeding sites in
breeding areas. There is only one documented
observation of a roost site for Northern Black
Swifts in South America, discovered during fall
1992 and 1993, on the walls of a steep gorge
along the Rio Caucu in the foothills of Colombia.
Black Swifts roosted consecutively at dusk for a
week in a compact group, mainly with White-
collared Swifts ( Slreptoproche zonaris ), clinging
to the volcanic rock of a 40- m cliff overlooking
the river, indicating that rocky river banks are
used as roosting sites during migration (Stiles and
Negret 1994). Similar .sites may be used in
wintering areas if available, but this information
is completely lacking. Non-brccding Common
Swifts (Apus apus) are known to ‘roost* aerially in
breeding areas and it is believed they spend
~9 months of the year continuously on the wing.
Non-breeding birds may fly continuously for
several years (Backman and Alerstam 2001,
Tarburton and Kaiser 2001), Common Swifts are
also known to occasionally roost at night by
hanging on the foliage of trees ( Holmgren 2004).
Any of these scenarios is possible for Northern
Black Swifts in wintering areas. Foraging activities
of the Northern Black Swift in wintering areas are
unknown but kernel densities indicate the swifts
range over a large area in winter, suggesting the
birds spend a lot of time on the wing.
The capability ot geolocators for tracking small
birds is still being explored and the potential is
great. However, the devices are not without
limitations. A major obstacle for success is that
once the devices are deployed, the bird must be
recaptured after a complete migration cycle has
occurred to obtain data. Our study indicates the
suitability of the Northern Black Swift for
geolocator deployment and recapture, primarily
due to this species* strong nesting colony fidelity
and abihty to carry small devices for lone periods
Calculation of latitude is unreliable around
equmox and near the equator because lengt
day and mght is equal. The accuracy of calcul
day length is especially affected for terrestrial
species hy shading factors that alter recorded light
levels such as cloudy weather, foliage, and
topographic shading of roost sites, resulting in
latitude uncertainties. Fudickar el al. (2011) found
the devices had an error of 201 ± 43 km for
latitude and 12 ± 3 km for longitude (±95% Cl)
for stationary geolocators (n = 30) in forested
habitat. The apparent retreat of bird #554 from
Colorado to the Pacific Ocean south of Baja
California (Fig. 1) during spring migration is the
result of one data point and the accuracy of this
fix is questionable. It may or may not represent an
actual movement by the bird and is possibly the
result of an extended period of shading. We did
not eliminate this position fix since the total day
length did not drastically differ from the other day
lengths of that time period.
Accurate longitudinal information can be ascer¬
tained as this is not affected by equinox and we
successfully used longitude near the autumnal
equinox to indicate when the birds arrived at their
wintering location. Black Swift breeding require¬
ments, such as nesting behind waterfalls in deeply
shaded niches in steep and narrow canyons, or in
caves where the performance of geolocators is
often compromised by darkness, resulted in some
unusable data during the breeding season. Docu¬
mented Black Swift nocturnal roosting behavior
during migration is limited and indicates this could
be a factor influencing the effectiveness of
geolocators for tracking this species. If winter
nocturnal roost sites are similar to those docu¬
mented in migration and al breeding sires, this will
also influence the accuracy of the data collected by
geolocators. Despite these limitations, geolocators
far surpass hand recovery information or depen¬
dence on sporadic sightings to identify migratory
paths and winter distribution of the Northern Black
Swift.
Understanding the theory behind geolocation is
extremely important for interpreting and using the
data collected to produce maps showing animal
movements (Hill 1994). Once the theory is
understood, knowledge of the behavior of the
animal being studied and of weather patterns in
the area where the animal was tracked can be used
to provide insight into movement patterns. The
mapped winter range of Black Swifts is an area
that typically experiences high cloud cover. Thus,
a significant number of the location fixes are most
likely shifted to the north artificially because of
cloud cover in the winter range as compared to the
Season et at. • BLACK SWIFT MIGRATION AND WINTERING AREAS
7
Colorado calibration location. Therefore, the
southern portion of the mapped winter range is
most likely the area where the swifts spent the
winter. The technical limitations of geolocalors
and lack of knowledge of Black Swift behavior in
wintering areas, such as daily foraging (light
distance, and roosting locations and tinting further
confound data interpretation.
The Black Swift is protected under the
Migratory Bird Treaty Act in the United States
and the Convention for the Protection of Migra¬
tory Birds and Game Mammals in Mexico. This
study documents Northern Black Swifts spending
-'220 days in Brazil during winter 2009-2010. the
first records of the species in this country. This
study identifies an annual non-breeding geogra¬
phic area of the Northern Black Swift and is a
significant step toward conservation of this
species.
Future studies could include use of geolocators
on subsets of Northern Black Swifts from other
areas of North America which would help
delineate the strength of migration connectivity
for this subspecies. Development of satellite
transmitters small enough for use on Black Swifts
will provide greater accuracy than geolocalors and
can possibly answer questions about roosting and
foraging behavior.
CONSERVATION IMPLICATIONS
Knowledge of migratory pathways and winter
distribution of a species enables evaluation of
those geographical areas, including ecologic
analysis and research, identification of potential
habitat threats, and development of conservation
strategies. The homogeneity of the wintering areas
for Northern Black Swifts evidenced in this study
suggests limited winter resource use by this
subspecies, which could have long-term conser¬
vation impacts. The current rate of deforestation
in Brazil could directly threaten this subspecies.
One of the most refined computer models for
simulating deforestation. SimAmazonia I. indi¬
cates the rale of deforestation in the State of
Amazonas will increase rapidly in the coming
decades which could result in a loss of up to 30%
of the forest cover by 2050 (Soares-Filho et al.
-006). Climate change and global warming
predictions also pose threats to habitat and prey
availability for this subspecies. Roberson and
Collins (2008) identified declines in some North¬
ern Black Swift populations but it is unknown if
declines are due to environmental problems in
breeding areas, during migration, in wintering
areas, or some combination of these possibilities.
ACKNOWLEDGMENTS
The authors thank Black Canyon Audubon Society,
Evergreen Audubon Society. Grand Valley Audubon
Society. Roaring Fork Audubon Society. Colorado Field
Ornithologists, and the Colorado Chapter of The Wildlife
Society for contributions to this project. D. M. Elwonger,
II. E. Kingery. L. R Patrick, A. R. Robinsong. and W. P.
Schmoker contributed funds to the Riehaal G. Levad
Memorial Fund held in trust at the Rocky Mountain Bird
Observatory to be used specifically for this project. The
Grand River Hospital perioperative staff contributed funds
to the M. A. Potter Memorial Fund to be used specifically
for this project. Significant assistance with interpretation
of geolocator data was received from N. B. F. Cousens and
D. M. Morrison. A. O. Panjabi and L. L. Jenks provided
thoughtful reviews of the manuscript. N. M. Goedert. T. W.
Patrick, and C. W. Reichert contributed invaluable support
during Black Swift banding expeditions to Fulton Resur¬
gence Cave. We thank die White River National Forest for
project support and logistics. K. It. Knudsen for access to
research library resources, and S. E. Hirshnian for
coordinating access to Box Canyon Falls. Knowledgeable
suggestions by peer reviewers C. T. Collins and A. M.
Fudickar were invaluable. This publication is dedicated to
the memory and spiritual guidance of our friend and
colleague Richard G. Levad.
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Backman. .1. AND T. AlERSTAM. 2001. Confronting the
winds: orientation and flight behavior of roosting
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Bontkmps, S.. P. Dp.fourny. and F. Van Boc.aert. 2010.
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The Wilson Journal of Ornithology 124(1 ):9- 1 4. 2012
DURATION AND RATE OF SPRING MIGRATION OF
KIRTLAND’S WARBLERS
DAVID N. EWERT,16 KIMBERLY R. HALL,1 JOSEPH M. WUNDERLE JR.,2
DAVE CURRIE.2 ’ SARAH M. ROCKWELL.4
SCOTT B. JOHNSON/5 AND JENNIFER D. WHITE2’
ABSTRACT. — The duration of migration of the endangered Rutland's Warbler (Setophaga kirtlandii) has not been
previously documented. We estimated the average duration of spring migration for five male Kirtland's Warblers by
observ ing uniquely color-handed indiv iduals at or near both the beginning and end of spring migration in Eleuthera. The
Bahamas, and Michigan, respectively. We estimated the average duration of spring migration for these live individuals to
have been no more than 15.8 days (range 13-23 days) and the average distance traveled to have been 144.5 km/day (96. 1 —
169.1 km/day). Received 12 April 2011. Accepted II November 2011.
The migratory period is typically the most
poorly understood aspect of a migratory species'
life history (Faaborg et al. 2010a. b) because of
difficulties in studying birds during migration.
This information gap constrains our ability lo
comprehensively describe population demograph¬
ics, and reduces our ability to effectively imple¬
ment conservation measures (Faaborg el al.
2010a. b) as mortality of adult migratory song¬
birds is apparently high during migration (Sillctt
and Holmes 2002). Lack of information on
duration of migration, and its relationship to
breeding and wintering season conditions, limits
our ability lo infer sensitivity of populations to
changes in the amount and distribution of habitat
required by migrating birds (Faaborg ct al.
20 1 Ob). The challenge of understanding duration
of migration, and integrating this information into
models of avian population dynamics, is pressing
for rare migratory landhirds that are infrequently
observed during migration.
Models that help explain duration of migration
are complex, as many possible intrinsic (c.g..
body condition, experience) and extrinsic (e.g..
weather, habitat distribution, stopover site condi¬
tions) factors influence rates and total duration of
The Nature Conservancy. 101 East Grand River
Avenue. Lansing. MI 48906. USA.
International Institute of Tropical Forestry. USDA
Forest Service, Sabuna Field Research Station. MC 02
box 6205, Luquillo, Puerto Rico 00773.
Puerto Rican Conservation Foundation, P. O. Box
362495. San Juan. Puerto Rico 00936.
Department of Biology. University of Maryland,
College Park. MD 20742. USA.
Department of Biology. St. Mary's College of Mary¬
land. St. Mary's City. MD 20686, USA.
"Corresponding author; e-mail; dewert@tnc.org
migration. For example, Cochran and Wikelski
(2005) developed a model for Catharus thrushes
based on ihe condition of an individual, weather
conditions, orientation of flight, and flight dura¬
tion on any given night; they predicted it could
take up to 40 days for an individual to travel
between the Gulf Coast of Louisiana and its
Canadian breeding areas.
Estimates of migration duration for passerines
have largely been based on extrapolations from
banding recoveries of birds en route (Ellegren
1993. Fransson 1995. Newton 2008. Yohannes et
al. 2009) rather than documented departure and
arrival dates of individual birds from wintering
and breeding areas. However, given potential
differences in rates of migration along different
portions of the route (Stutchbury et al. 2011).
duration estimates for banded birds are best
obtained over die complete migration (Fransson
1995, Yohannes et al. 2009). New technologies,
such as geolocators, now enable researchers to
describe the location and duration of migration for
individual birds (Stutchbury et al. 2009. 2011;
Bachler ct al. 2010, Robinson et al. 2010. Bridge
ct al. 201 1. Heckscher et aJ. 2011. Ryder et al.
201 1 ). Use of these techniques is currently limited
to species larger than small passerines and, even
as the weight of geolocators continues to decrease,
their use must be carefully evaluated for imperiled
species. Only in rare cases can we estimate
duration of an individual’s migration based on
observations of birds with unique color-band
combinations at the beginning and ending of
migration.
We report empirical estimates of the duration of
spring migration for uniquely color-bunded indi¬
vidual Kirtland's Warblers {Setophaga kirtlandii)
observed in the field at the beginning and ending
9
10
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 1. March 2012
of migration. The Kirtland’s Warbler, a species
designated as federally endangered in the United
States and Canada, has a small core breeding
range ( — 7 1 km’), and breeds almost exclusively
in one distinct habitat type, young stands of jack
pine ( Pinas hanksiana) on sandy oulwash soils in
the northern Lower Peninsula of Michigan (May-
field 1960. Donner et al. 2008 ). Small numbers of
birds also breed in similar habitat in Michigan's
Upper Peninsula, Wisconsin (Probst et al. 2003,
Trick et al. 2008), and southern Ontario (Richard
2008). The total number of singing male Kirt-
land's Warblers was estimated to be 1,750 in 2010
(Elaine Carlson, pers. comm.). T his warbler is one
of a few passerine species for which it is feasible
to search breeding areas for individuals color-
banded in wintering areas because locations of all
singing males are mapped during an annual
population survey (Probst et al. 2005); there arc
a relatively small number of birds and sites to
check for arriving color-banded individuals.
Our objective was to document the duration of
spring migration for individual Kirtland’s War¬
blers based on field observations of departure and
arrival times of uniquely color-banded birds. To
our knowledge, these estimates of spring migra¬
tion duration of Kirtland’s Warblers arc the first
derived from observations of the same color-
banded individuals in wintering and breeding
areas. They also provide comparative data for
estimates of migration rates and duration gener¬
ated from other methods.
METHODS
Teams based in The Bahamas, Michigan.
Wisconsin, and Ontario searched the Kirt land's
Warbler winter and breeding habitat to estimate
duration of migration as part of a coordinated
effort to study linkages between winter and
summer ranges. We captured 232 Kirtland’s
Warblers from 2002 to 2010 in mist nets and
color-banded birds at several sites (Wunderle et
al. 2010) within 30 km of each other on southern
Eleuthera, The Bahamas (—25 N. 76 W; Fig. I
Many of the banded individuals were observei
repeatedly during a given wintering season. Wi
visited Eleuthera sites with several color- bandei
Kirtland’s Warblers three to 15 times/season fron
mid-April through I May 2003-2010 to documen
a date as close to departure as possible. Many o
these warMcrs show winter site fidelity (Syke
and Clench 1998. Wunderle et al. 2010), bu
relocating birds in winter is challenging because
some individuals move to different sites, and are
difficult to locate and identify in the Lhick shrubby
habitats.
The Kirtland’s Warbler breeding habitat was
searched for color-banded birds from 2003 to
2010. This species often shows breeding site
fidelity (Walkinshuw 1983, Mayfield 1992, Bo-
cetti 1994; SMR, unpubl. data), like many
territorial migrant landbirds. although a few birds
disperse to new sites between years (Walkinshuw
1983; DNE and KRH, unpubl. data). We could
often estimate arrival dates of individuals return¬
ing to their territories the following spring by
checking sites occupied by banded warblers in
previous years. Our searches focused on a subset
of banded birds that we were able to relocate
between mid-to-late April in The Bahamas, for
which we had georeferenced their breeding
territories in the Lower Peninsula of Michigan in
previous years.
We monitored territories for a minimum of
30 min/day every I to 3 days from early May
through 30 May or until the bird was found.
Observers walked through an area encompassing
roughly a 200-400 m radius around the georefer¬
enced site during these visits, searching for color-
banded birds. Data for birds with known territo¬
ries were supplemented with records of individ¬
uals for w hich we had recorded last observation
dates from Eleuthera in mid-to-late April and
then opportunistically observed the same bird
in Michigan while systematically searching for
returning territory holders. Field work was ini¬
tiated each spring, soon after the first confirmed
arrival dale of a Kirtland's Warbler in the
breeding areas.
We calculated each individual's duration of
migration, and average distance covered per day
from these departure and arrival date estimates.
Duration was estimated by calculating the number
of nights between the last observation date in The
Bahamas (assuming the bird left on the night of
the last date it was observed) and the night
previous to the first observation in Michigan. The
interval between these dates represents the
maximum duration of migration. Actual times of
migration could be less than the durations
reported here because an individual may not have
departed immediately following the last Bahamas
observation. In addition, individuals may not have
been observed on their first day of arrival in
Michigan, especially males that did not sing
within our sampling period or females. Average
Ewert et al. • KIRTLAND'S WARBLER SPRING MIGRATION
11
F-IG. 1. (A) Approximate breeding and wintering locations of color- banded Kirtland’s Warblers for which we estimated
duration and distance of spring migration. (B) Breeding locations of color-banded Kirtland's Warblers in the Lower
Peninsula of Michigan by county. (C) Approximate location of wintering sites sampled on southern Eleuthera, The
Bahamas (described in Wundcrlc et al. 2010).
distance traveled/day was calculated by dividing
Ihe linear distance traveled between wintering and
breeding areas by the number of nights between
the last observation of an individual on Eleuthera
and the first observation of the same bird in
Michigan. Values for both the maximum duration
of migration and average distance traveled/day are
presented as means ± SD.
RESULTS
Kirtland’s Warblers were consistently seen on
lileuthera through late April 2003-2010 (Wun-
derle et al., unpubl. data) with the latest date in
any year being 2 May 2006. First arrival dates of
males reported anywhere in the Lower Peninsula
‘>1 Michigan ranged from 2 to 7 May during our
study and the total number of Bahamas-banded
Kirtland’s Warblers observed in breeding areas
during the study period in any given year was 7 to
23 (Table 1 ). In comparison, mean arrival dates of
males from 2006 to 2010 ranged from 13 to 22
May for the warblers at a subset of Kirtland's
Warbler siles in Michigan’s Lower Peninsula
(SMR, unpubl. data).
The estimated mean duration of migration for
five uniquely color-banded male Kirtland’s War¬
blers observed in breeding areas (Fig. 1 ) was 15.8
± 4.2 days (Table 2). Four of these five birds
were observed on the first day the territory was
checked and the fifth (band # 2221-08906) was
observed 3 days after the territory was last visited.
Thus, it is likely the actual mean duration of
spring migration for these five individuals was
less than the calculated mean of 15.8 days. The
mean distance traveled/day, based on this esti¬
mated duration, was 144.5 t 31.2 km.
Some observations were not included in our
calculations of mean duration of migration
because the birds were found opportunistically,
and were not detected until relatively late in May
12
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 1. March 2012
TABLE I. Number of color-bandcd Kirtland's
Warblers from southern Eleuthera. The Bahamas found in
breeding areas and dates of first observation of males in the
Lower Peninsula of Michigan.
Year
Number found in breeding areas
First observation
2005
8
7 May
2006
12
4 May
2007
23
5 May
2008
14
4 May
2009
16
3 May
2010
7
2 May
after the arrival date for most individuals. For
example, the range of maximum duration of
migration observed for an additional subset of
birds, last seen on Eleuthera in mid-to-late April,
that were found relatively late in the breeding
season in Michigan, was 27-48 days. We also
documented that one female, last seen on 27 April
2006 on Eleuthera and first seen in Michigan on
24 May 2006. had a maximum migration duration
of 27 days. Estimating arrival dates of females is
particularly difficult, even with systematic search¬
es. as they do not sing and may escape detection.
DISCUSSION
The maximum duration of spring migration for
male Kirtland's Warblers from Eleuthera (range =
13-23 days) was shorter than predicted based on
models developed for thrushes bv Cochran and
Wikelski (2005), but similar to the 13-14 day
period for four trans-Gulf spring migrating Wood
Thrushes ( Hylocichla mu.stelina ) (Stuchbury el al.
2009). However. Wood Thrushes migrate a longer
distance of —3,700 km. compared to -2.200 km
by Kirtland’s Warblers.
The mean distance traveled/day by male Kin-
land's Warblers. 144.5 km. was similar to the
spring migration rate of two female Eurasian
Hoopoes ( Upupa epops) (122 km/dav and 163
km/day) between the Sahel of western Africa and
Switzerland (Baehler et al. 2010) that were
tracked with geolocators and within the range of
105-375 km/day traveled during spring migration
by a Swainson's Thrush ( Catharus ustulaius » that
w-as studied by radiotelemetry between Illinois
and Manitoba (Cochran 1987). Daily rates were
also within the range of estimates for spring
migration of five Sylvia warbler species to Great
Britain (range -- 97-232 km/day) and Scandina¬
via (range = 98-163 km/day). based on median
capture and recovery dates in the Mediterranean
region (Fransson 1995). and for II European
passerine species on the European (50-260 kin/
day ) and desert ( 120-150 km/day) portions of the
migration route, estimated from median passage
rates between Africa and northern Europe (Yo-
hannes el al. 2009). One individual fall-migrating
Willow Warbler (Phylloscopus trochilus ) traveled
145 km/day (Hilden and Saurola 1982) and
another 218 km/day (Hedenstrbm and Peitersson
TABLE 2. Estimated duration of migration for color-banded male Kirtland’s Warblers from southern Eleuthera, The
Bahamas to known breeding territory locations in the Lower Peninsula of Michigan. Loeations are given in decimal
degree coordinates.
Individual
Last Bahamas observation
First Michigan observation
and location
and location
Migration distance (kin)
Max duration (days)
Migration rate (km/day)
1821-91208
25 Apr 2008
8 May 2008
2.199
13
169.1
24.90787 N
44.4629 N
76.17171 W
84.1809 W
2221-08944
25 Apr 2008
9 May 2008
2.212
14
158.0
24.97589 N
44.4998 N
76.15257 W
83.5794 W
2131-75811
25 Apr 2007
1 1 May 2007
2.222
16
130.7
24.90010 N
44.53544 N
76.14831 W
83.53937 W
2221-08906
24 Apr 2007
17 May 2007
2,211
23
96.1
24.90091 N
44.58206 N
2221-08922
76.15911 W
84.60934 W
27 Apr 2007
24.96263 N
10 May 2007
44.46725 N
2,192
13
168.6
76. 1 7809 W 84.29917 VV
Ewert et al • KIRTLAND’S WARBLER SPRING MIGRATION
13
1987). comparable to the migration rates of
Kirtland's Warblers sampled.
Daily rates of migration by male Kirtland's
Warblers were similar to some species, but other
species travel at faster rates during spring
migration. For instance, four Wood Thrushes
migrating from Honduras and Nicaragua to
Pennsylvania across the Gulf of Mexico in spring
averaged 263 km/day (Stutchbury et al. 2009) and
two Purple Martins ( Prague subis ) averaged 281
and 577 km/day during their spring migration
from Brazil to Pennsylvania, a distance of
—7.550 km. Similarly, five spring migrating
Veeries ( Cathants fuscescens) tracked with geo¬
locators. whose estimated migration distance
ranged from 5,950 to 10.290 km. migrated faster
(209-350 km/day) than Kirtland's Warblers
(Heckscher et al. 201 1). and an Aquatic Warbler
(Aaocephcilm paliulicola) averaged 280 km/day
within Africa during fall migration (Cramp 1992).
Overall, however, daily rates of spring migration
by these species and our estimates for male
Kirtland's Warblers indicate that many near¬
passerines and passerines migrate at rates close
to the upper range of migration rates reported in
Newton (2008).
We obtained estimates of the duration of
migration for a small number of males during
two spring migration seasons. Ecological, meter
ological, physiological, and other factors that
affect duration and rate of migration will be better
understood (Fransson 1995. kaess 2008. Tottrup
et al. 2008, Yohanncs et al, 2009. Stutchbury et al.
201 1) as geolocators and other techniques become
available to follow larger numbers of individual
birds throughout migration (Robinson et al. 2010.
Bridge et al. 2011). It may then be possible to
describe other aspects of Kirtland's Warbler
migration and connectivity such as distribution
of frequently used stopover areas, when and
where along the migratory route Kirtland's
Warbler are most vulnerable, and inter-seasonal
interactions, important hut missing information
needed to develop a comprehensive conservation
program for the species.
ACKNOWLEDGMENTS
We thank ihe L'.S. Fish and Wildlife Service. Huron-
Manistee National Forest, and Michigan Departmenl of
Natural Resources for permission to enter Kirtland's
Warbler Management units. The International Program of
the L'SDA Forest Service. Michigan Department of Natural
Resources, Smithsonian Institution, and The Nature
Conservancy funded our work. We greatly appreciate the
efforts of Andrew Fra/.ee, P. W. Huber, Samara Lawrentz,
Ingeria Miller. Z.oko McKenzie, Ray Perez, Michael
Petrucha. Keith Philippe. .1. R. Probsl, Montara Roberts,
Robert Slcbodnik, S. .1. Sjogren, Jim Stevens, Mark
Thomas, and Jerry Wcinrieh who searched for early-
arriving color-handed birds in breeding areas. Joe Fargione,
M. L. Herbert. Peter Kareiva. Krista Kirkham, Robert
Lalasz. Christopher Rimmer. J. J. Nocera, Peter Weaver,
and one anonymous reviewer provided suggestions that
greatly improved the manuscript. Sagar Mysorekar pre¬
pared the figure. The work was done in cooperation with
the Bahamas National Trust. Puerto Rican Conservation
Foundation. University of Puerto Rico, and the Kirtland's
Warbler Recovery Team.
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The Wilson Journal of Ornithology 124(1): 15-23, 2012
A NEW AREA OF ENDEMISM FOR AMAZONIAN BIRDS IN THE RIO
NEGRO BASIN
SERGIO H. BORGES1,3'4 AND JOSE M. C. DA SILVA2
ABSTRACT. — We describe a new area of endemism for Amazonian birds which we designate as the Jau Area of
Endemism. This area of endemism in central-western Amazonia north of the Rio Solimoes was identified through
congruent distributions of six avian taxa: Psophia crepitans ochroptera Pelzeln 1857. Nonnula amaurocephala Chapman
1921. Pteroglossus azara azara Vieilot 1819, Picumnus lafresnayi pusillus Pinto 1936. Synallaxis rutilans confinis Zimmer
1935, and Myrmoborus myotherinus ardesiacus Todd 1927. The southern and eastern limits of this area of endemism are
the middle courses of the Solimoes and Negro rivers, respectively. The northern limits apparently coincide with sandy soil
vegetation along the middle Rio Negro. The western boundary remains undefined, but could involve the Japura or Iya rivers
north of the upper Solimoes. Taxonomic studies and expansion of ornithological collections are needed to more precisely
delimit the Jau Area of Endemism. It is possible the avian taxa restricted to the Jau Area of Endemism are derived through
parapatric or peripatric speciation events from taxa whose ranges were centered in the Imeri and Napo areas of endemism.
Alternatively, tectonic events that affect the lower course of the Rio Negro could influence bird distribution in this region if
they serve as vicariance mechanisms. Received 27 June 2007, Accepted 15 July 2011.
An area of endemism (AOE) is a "geographical
region comprising the distributions of two or more
monophyletic taxa that exhibit a phylogenetic and
distributional congruence and having their respec¬
tive relatives occurring in other such-defined
regions” (Harold and Mooi 1994:261). Areas of
endemism are important for at least two reasons.
First, they represent the smallest geographical
units for postulating hypotheses about the history
of their biotas (Cracraft 1988, 1994; Morrone
1994; Morrone and Crisci 1995). Second, these
areas are considered priorities for establishment of
conservation action because they contain unique
biotas (Fjeldsa 1993, Slallerslidd cl al. 1998).
There are modern approaches to identifying
AOEs including parsimony analyses of endemic-
ity (Morrone 1994. Morrone and Crisci 1995,
Silva et al. 2004) and optimality criterion (Szumik
et al. 2002, Szumik and Goloboff 2004). Tradi¬
tionally. however, these areas have been identified
through mapping the congruent geographical
distribution of taxa based on extensive area of
sympatry but not necessarily complete overlap of
distributions (Platnick 1991).
Eight AOEs have been recognized for birds in
the Amazonian lowlands (Fig. I; Haffer 1974,
Departamcnto de Zoolog ia. Museu Paraense Emilio
Goeldi. Belem. Para. Brazil.
‘Conservation International do Brazil, Avenue Nazare.
541/sala 310. 66035-170, Belem. Para. Brazil.
Current address: Fundayao Vitoria Amazonica, Rua R/
S. casa 07. Quadra Q. Morada do Sol. 69060-080. Manaus.
AM. Brazil.
4 Corresponding author; e-mail: sergio@fva.org.br
1978; Cracraft 1985; Silva et al. 2002). Most
areas have boundaries coinciding with major
rivers of the Amazon Basin (Wallace 1852,
Haffer 1978. Cracraft 1985. Ayres and Clutton-
Brock 1992). We identified a number of avian
taxa during a study of bird species distribution
whose ranges apparently are restricted to the
lower course of the Rio Negro (Borges 2004a,
Borges 2007). Mapping the distributions of these
taxa resulted in identification of an AOE not
recognized in previous biogeographic anal¬
yses (Haffer 1978, Cracraft 1985). Our objec¬
tive is to describe the new area of endemism
based on congruent distributions of six avian
taxa.
METHODS
Study Area. — The study region encompasses the
right margin of the lower Rio Negro (Fig. 2). Most
specimens analyzed were collected in Jau National
Park (JNP), one of the largest (2,272.000 ha)
protected areas in Brazil. The avifauna of JNP has
been studied for the last 15 years including
assessment of species diversity and general eco¬
logical requirements for most bird species (Borges
and Carvalhaes 2000; Borges et al. 2001; Borges
2004a. b; Borges and Almeida 201 1).
Biogeographic Analysis.— We compiled a list
of bird species and subspecies recorded in the
study area (Borges et al. 2001, Borges 20()4a,
Borges 2007, Borges and Almeida 2011). The
taxonomic status and distribution of birds re¬
corded in the study region were evaluated
through specimens housed at Museu Paraense
Emilio Goeldi (MPEG), Museu de Zoologia da
15
16
THE WILSON JOURNAL OF ORNITHOLOGY • Vo/. 124. No. 1. March 2012
cZZtoJSXSttL SST recosnized for birds in the Amazonia lowla"ds bascd - Haffa ,1974' 1978
Universidade de Sao Paulo (MZUSP), Bird Cc
lection of Instituto Nacional de Pesquisas <
Amazonia (INPA), Field Museum of Natur
History (FMNH), and American Museum
Natural History (AMNH). We also compih
information on specimens collected in the Negr
Japura interfluvium (e.g., Maraa, Barcelos, Man
capuru) deposited in MPEG. All relevant inform
tion available from the taxonomic literature w;
also used (Pinto 1944. 1978; Sherman 199-
Winkler and Christie 2002; Borges 2004a). W
did not attempt a complete and detailed taxonom
revision of the bird taxa. but checked if the specit
°heir cTof'f T" m°tphologically distinct fro,
,heir ranges ™
The new area of endemism is at proximities r
endemic to the Napo and Imeri areas of endemism
as originally proposed by Haffer (1978) and
Cracraft (1985).
RESULTS
The taxonomic and geographical distributions ol
383 bird species and subspecies were assessed in
the study region. The geographic distribution of
one species, Chestnut-headed Nunlet (Nonnula
amaurocephala), and five subspecies, Grey¬
winged Trumpeter (Psophia crepitans ochropierdl
Ivory-billed Aracan ( Pteroglossus azora azQto)-
Lafresnayes’s Piculet (Picumnns lafresnayi pail-
lus). Ruddy Spinetai! (SynalUixis rutilims confinis).
and Black-faced Antbird ( Myrrnoboms mother-
inns ardesiacus) are restricted to the west of the
lower Rio Negro anil north of the Rio Solimocs.
I hese taxa are considered endemic to the study
region.
Borges and Silva • A NEW AREA OF ENDEMISM FOR AMAZONIAN BIRDS
17
«8WW
TW*V
Tabocal
Barcelos
Muirapinina
Japura
^ Manaus
Igarape
>— Cacau /
Pereira
Manacapuru (
CodajSs
HMl3
Castanheiro
Santa Maria
Acajatuba
FIG. 2. Northwestern Amazonia, showing the study region and municipalities cited in the text. The light gray area
indicates the suggested limits of the Jati Areu of Endemism.
Grey-winged Trumpeter (Psophia crepitans
ochroptera Pelzeln 1857). Pcl/.eln described this
trumpeter as a distinct species. Psophia ochrop¬
tera. Ochroptera is treated as a subspecies of P.
leucoptera in recent taxonomic literature (Pinto
1978. Sherman 1996). We agree with Haffer
(1974) who proposed that ochroptera is a
subspecies of P. crepitans , the trumpeter species
distributed north of the Amazon River. P.
crepitans has two other subspecies in addition to
ochroptera: crepitans inhabiting the Guianan
AOE and napensis. inhabiting the Napo and Imeri
AOEs. P. c. ochroptera has been recorded mostly
in white-sand woodland and terra finite forest in
JNP (Borges et al. 2001, Borges and Almeida
701 1 ). where an adult female was collected (INPA
# 576). A recent molecular systematic study
i Ribas et al. 201 1 ). in addition to morphological
assessment (Haffer 1974). found that ochroptera
is diagnosable from the other subspecies in the
Psophia crepitans complex.
Chestnut-headed Nunlet (Nonnula anmuroce-
phula Chapman 1921). This rare puffbird was
known only from specimens collected in Mana¬
capuru used in the original description until it
was rediscovered in JNP (Whittaker et al. 1995).
It is associated with seasonally flooded black-
water forest or Igapo forest (Whittaker et al.
1995, Borges et al. 2001). The MZUSP has skins
collected in Manacapuru (MZUSP 16561) and
Codajas (MZUSP 16387), and one specimen was
collected in JNP (MPEG 55855) in addition to
specimens mentioned in Whittaker et al. (1995).
The northernmost record of N. amaurocephala is
the Unini River (Whittaker et al. 1995) and the
easternmost is the Amana River (M. Cohn-Haft,
pers. comm.) with no confirmed records from the
upper portion of the Rio Negro (Haffer and
Fitzpatrick 1985). It is suggested that N.
amaurocephala forms a superspecies with N.
ruficapilla and N. frontalis (Rassmussen and
Collar 2002)
Ivory-billed Aracari {Pterogtossus azara azara
Vieilot 1819). This subspecies of the Ivory-billed
Aracari has the upper mandible brownish colored
and is recorded from Castanheiro. Codajas.
Igarape Cacau Pereira (Haffer 1974). Manacapuru
(MZUSP 16833 and 16834), Maraa (MPEG
18
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124. No. I. March 2012
42505-42507), and JNP (Borges et al. 2001,
Borges 2007). It is replaced by P. a. flavir osiris in
the Napo and Imeri AOEs and by P. a. marine
south of the Solimdes (Haffer 1974). There is
some evidence of hybridization between marine and
azara near the mouth of the Purus River (Haffer
1974: 222-223). This Aracari has been recorded in
both terra finne and Hooded forests in JNP (Borges
et al. 2001. Borges and Almeida 201 1).
Lafresnaye's Piculet (Picumnus lafresnayi
pusillus Pinto 1936). P. pusillus was described
from Codajas on the left margin of the Rio
Solimdes. by Pinto (1936). This taxon was later
reassigned as a subspecies of P. aurifrons
(Peters 1948). Recent taxonomy considered
pusillus as a subspecies of Picumnus lafresnayi
(Winkler et al. 1995, Winkler and Christie
2002). P. lafresnayi forms a superspecies with
P. puniilus that is apparently restricted to
southern Venezuela and northwestern Brazil
(Winkler and Christie 2002). There are six
MZUSP specimens identified as P. I. pusilus
collected in the Manacapuru region (MZUSP
16614-16619). The plumage of a single speci¬
men collected in JNP and deposited in the INPA
Bird Collection matched better with P. /.
pusillus than with P. puniilus. The geographical
distribution of pusillus appears to be restricted
to the region west of the lower Rio Negro being
replaced by P. puniilus in the Imeri AOK
(Fig. 2). P. I. pusillus has been found mainly
in Hooded forests and secondary growth in
20 fl )(B°rgeS Ct al' 2°01, Borges and Almeida
Ruddy Spinetail ( SynaJlaxis rutihms confin
Zimmer 1935). This subspecies was describe
from specimens collected in Igarape Caca
Pereira in the lower portion of Rio Negro. It ,
replaced by S. r. dissors on the left margin of Ri
Negro, which has been found in Manaus and i
the upper Rio Negro at Sao Gabriel da Cachoeir
and along the Casiquiare channel (Friedman
1948 Pinto 1978). A better delimitation of th
distribution of S. r . eonfinis will require specime
collections south of die Negro and Uaupes riven
p '• “>,ir,,,is is replaced in Napo AGE (easier
Ecuador and northeastern Peru) by ,V. r. caque
south onhe's AOE ,upper
by * r-
(ms) LFnTZ
moborus myotherinus and concluded that arde-
siacus was a diagnosable taxon This subspecies
was described from Manacapuru and has been
recorded in Igarape Cacau Pereira. Santa Maria.
Codajas (Zimmer 1932, Pinto 1978), Mania
(MPEG 42654-42672), and Jau National Park
(MPEG 50614—50620). and is replaced in Imeri
and Napo by M. tn. elegans and in Inambari by M.
m. myotherinus (Haffer and Fitzpatrick 1985).
This antbird has been recorded in mature upland
forest, white-sand campinaranas, and secondary
growth forest in JNP (Borges et al. 2001. Borges
and Almeida 20 1 I ).
Another seven avian taxa also are apparently
restricted to centra I -western Amazonia: Anuizona
autumnaUs diadema. Braehygalbula lugubm
phaeonota, Nunnula rubecula simidatrix, Hyki
estastes stresemanni stresemanni . Sc! e runts rufi-
gularis hrunnescens, Myrmoborus lugubris Stic-
top terns, and Hylophylax naevius ohscunts. These
subspecies, however, are known only from a few
specimens and their taxonomic status and distri¬
bution needs additional evaluation.
Napo and Imeri Areas of Endemism.— The Imeri
and Napo areas of endemism were supported by 21
and 56 avian taxa as originally described (Haffer
1978. Cracraft 1985). An updated distributional
and taxonomic assessment decreased these num¬
bers to six species (or subspecies) endemic to linen
and 42 endemic to the Napo AOE (Appendix).
Several bird species previously thought to be
restricted to the upper reaches of the Rio Negro
have had their geographical distribution extended
southward and to northern Peru (Borges et al
2001, Alonso and Whitney 2003, Borges and
Almeida 201 I ). Other Imeri birds are restricted to
the northwestern portion of the Amazon Basin
with no confirmed records in the lower reach ol
the Rio Negro or northern Peru. Most species
restricted to Imeri AOE are specialists in white
sand campinas (Cyanocorax helprirti and Myrvu-
eiza pelzelni ), montane and pre-montanc forests
( Percnostola caurensis), and flooded forest (77m
pophaga cherriei) (Zimmer 1999; Hilty 2003:
SMB. unpub], data).
Similarly, some birds previously thought to be
endemic to the Napo region had their distributions
extended east to the Rio Negro, as in the case of
My mint hernia ignota and Pteroglossus pluricinc-
tus (Borges and Almeida 201 1). Some species are
even more widespread than previously described,
but there are species endemic to northwestern
(Imeri endemics), upper north Amazon (Napo
Borges and Silva • A NEW AREA OF ENDEMISM FOR AMAZONIAN BIRDS
19
endemics), and the central-western portion of the
basin (this study).
DISCUSSION
We describe a previously undesignated area of
endemism in central-western Amazonia that is
supported by the congruent distribution of six
avian taxa. Haffer and Fitzpatrick (19X5) noted
that a small number of strongly differentiated
bird populations were restricted to this region
but did not recognize it formally as an AOE due
the reduced number of avian taxa (J. Haffer,
pers. comm.). Conceptually and operationally,
however, an AOE could be recognized with just
two species (Platinick 1991, Harold and Mooi
1994).
Amorin and Pires (1999) also identified a small
AOE bounded by the Rio Solimoes and Rio Negro
without offering information about which species
supported this biogeographic component (Amorim
and Pires 1999: fig. 27). We suggest naming this
new area of endemism as Jau in recognition of the
importance of the National Park to biodiversity
conservation in the Amazon. This area appears
nominated as Rio Negro Area ol Endemism in
previous publications (Borges 2007, Ribas et al.
2011). However, we believe that Jau Area of
Endemism is more appropriate to the geographical
setting of the area (Fig. 2).
The precise geographical limits of this area are
only partially identifiable. The southern and
eastern limits probably coincide with middle
portions of ihe Solimoes and Negro, large rivers
known to isolate bird populations (Sick 1967,
Haffer 1992). The northern boundary is more
complicated, but from the middle Rio Negro
northward the landscapes dominated by terra
Jirme forests are extensively replaced by forests
and fields growing in sandy soils called 'campi-
naranas' and 'campinas' (Anderson 1981. IBGE
1997), This more open vegetation occupies
thousands of square kilometers between the
middle and the upper Rio Negro. It is possible
this discontinuity in vegetation serves as a barrier
(or filler) to dispersal for some bird species,
especially those that occur more frequently in
terra firme forest on clay soils. The western
boundary of Jau AOE also is difficult to identify
due to the scarcity of bird collections from the
region between Maraa to the Brazilian-Colombian
border. We tentatively suggest the courses of the
Japura or l^a rivers as the western boundary of Jau
AOE, although additional fieldwork will be
necessary (Fig. 2). We also note this region of
faunal turnover could be not coincident with any
river course as happens in the southern portion of
the Amazon Basin (Haffer 1992).
One fundamental concern in recognizing and
delimiting the Jau AOE is the current taxonomy
of the birds considered endemics. The use of
subspecies in biogeographic analyses is problematic
because an unknown number of bird taxa described
in the ornithological literature are not discrete
evolutionary units (Cracraft 19X5, Haffer 1987).
Some authors have been successful in using
subspecies for biogeographic analysis (Bates et al.
1998, Borges 2007). Analyzing polytypical species
as a single entity tends to over-estimate the
geographical distributions of taxa and potentially
ignores relevant units for conservation and bioge¬
ography (Bates and Demos 2001). We considered
only taxa with accentuated morphological differen¬
tiation. However, the taxonomic status of Amazo¬
nian bird species, including those discussed here,
needs to be continuously evaluated and their
phylogenetic relationships clearly established.
These taxonomic and biogeographic studies will
require additional ornithological collections in the
northern portion of the upper Rio Solimoes and in
the middle to upper Rio Negro, principally along the
right margin ol' the latter, as these regions are likely
contact zones.
The phylogenetic relationships of the species
and subspecies endemic to the Jau AOE are not
adequately known. However, three taxa (Pter-
oglossas azara azara. Picummis lafresnayi pusil-
Iti.s, and Mynnoboriis myotherinus artlesiacus)
appear to have their closest relatives in Ihe lmcri
and Napo AOEs. This is supported by Borges
(2007), who applied quantitative methods (parsi¬
mony analysis of endemicity and cluster analyses)
to analyze the biogeographic relationships be¬
tween avifaunas from different Amazonian AOEs.
The avifauna of the JNP shares more species and
subspecies with localities in the Imeri and Napo
AOEs than with localities in the Inambari and
Guiana AOEs (Borges 2007). This suggests the
barrier effect of the Negro and Solimoes rivers is
stronger than the barrier effect in the western
border ol the Jau AOE. A working hypothesis to
the evolutionary history' of the six taxa restricted
to the Jaii AOE is that they wea* derived through
parapatric or peri panic speciation from ancient
species whose ranges were once centered in the
Imeri and \apo AOEs. Alternatively , tectonic
events that affect the lower course of the Rio
20
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 1. March 2012
Negro (Forsberg et al. 2000. Almeida-Filho and
Miranda 2007, Silva et al. 2007) could influence
bird distribution in this region if they serve as
vicariance mechanisms (Ribas et al. 2011).
We call attention to the urgent need to review the
currently recognized AOEs for Amazonian birds. The
last review of these areas w as compiled over 20 years
ago (Cracraft 1985), and taxonomic and geographical
distribution data have continued to accumulate. The
areas of endemism for Amazonian birds should be re¬
evaluated through modem biogeographic approaches
(Morronc and Crisci 1995, Szumik and Goloboff
2004) facilitated by continuous progress increasing
the data base of geographical distribution and
systematics of neotropical birds.
ACKNOWLEDGMENTS
SHB acknowledges Capes. WWF-Brazil, and Fundajao
Vitdria Ama/onica for financial and technical support. We
thank Brazil's federal agency of environmental protection
(IBAMA) for permission to work in Jaii National Park. Luis
Fdbio Silvcira, Maria Luiza. Alexandre Aleixo, and Mario
Cohn-Haft kindly permitted us to examine bird collections
under their care, Marcelo Moreirn kindly prepared the
maps. Morton Isler, Charles Zartman. and Camila Ribas
helped in first versions of the paper. We appreciate the
improvements in English usage by Pltil Stouffcr through the
Association of Field Ornithologists' program of editorial
assistance. We are also grateful to J. M. Bates and Jurgen
Haffer for careful reviews of this paper and useful
suggestions. We dedicate this paper to the memory of Dr.
Jurgen Haffer for his inestimable contribution to the
biogeography of neotropical birds.
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APPEMDEX. Distribution of avian taxa in Imeri and Napo areas of endemism as originally proposed bv Haffer (1978.
ss “h — »ith c>- ^ -- «">■
Original name
Crypturellus casiquiare — H
C. duidae — C
Aramides calopierus — H
Mini sal vini — H & C
M. tomentosa — H
Neomorphus pucheranii — C
C ampv lop terns villa viscensio — C
Leucippus chlorocercus — H & C
Heliodoxa gularis — H & C
Topaza pyra — H & C
Phlogophilus hemileucurus
Pyrrhura albipectus — H & C
Galbula tombacea — H
G. leucogastra chalcothorax
G. pastazae — H
Gal ba I cyrhynch us leucotis — H
Nonnula ruficapilla rufipectus — C
N. brunnea — H
Notharchus ordii — H
Pteroglossus f. flavirostris — H
P • pluricinclus — H
Selenidera r. reinwardtii — H & C
S. nattereri — H & C
Picumnus pumillus- — H & C
Celeus spectabilis — H & C
Hylexetastes stresemanni insignis—
Synallaxis moesta — H & C
Thripophaga cherriei — H & C
Neoctanies niger ■ — H
Current name
Imeri
Napo
Jad1
Crypturellus casiquiare 2
C. duidae •'
A ramides calopierus
Mini salvini
M. tomentosum
Neomorphus p. pucheranii 4
C ampyiopterus villaviscensio
Leucippus chlorocercus
Heliodoxa gularis
Topaza p. pyra 5
Phlogophilus hemileucurus
Pyrrhura albipectus
Galbula tombacea tombacea 6
G. chalcothorax’
G. pastazae
Galbal cyrhynchus leucotis
Nonnula ruficapilla rufipectus
N. brunnea
Notharchus ordii *
Pteroglossus azara flavirostris
P pluricinclus
Selenidera r. reimvardtii
S. nattereri
Picumnus pumillus
Celeus spectabilis spectabilis
Hylexetastes stresemanni insignis
Synallaxis moesta
Thripophaga cherriei
Neoctanies niger'’
x
x
E
E
x
E
E
E
x
E
E
E
E
E
E
E
E
x
X
X
E
Borges and Silva • A NEW AREA OF ENDEMISM FOR AMAZONIAN BIRDS
23
APPENDIX. Continued.
Original name
Current name
Imeri
Napo
Jau*
Myrmotherula sunensis — H & C
Myrmotherula sunensis sunensis10
E
M. obscura — H
M. ignota obscura"
X
X
X
A/, longicauda soderstromi — C
M. longicauda soderstromi
E
V/. cherriei — H & C
M. cherriei'1
X
X
X
V/ ambigua — H & C
M. ambigua
X
X
Herpsilochrius stictunis dugandi — H & C
Herpsilochmus dugandi
E
H. dorsimaculaius — H
H. dorsimaculaius 13
X
X
Hypocnemis hypoxunthu — C
Hypocnemis h. hypoxantha 14
X
X
X
Pitlivs casianea — C
Pithys castaneus ,s
E
Rltegmuturhinu m. melanosticta — C
Rhegmatorhina m. melanosticta
E
R. iris lata — C
R. cristata
X
X
Mynneciza rnelanoceps — H
Mynneciza rnelanoceps16
E
M. pelzelni— H & C
M. pelzelni
E
M. ilisjuncta — II & C
M. disjuncta'1
X
X
Gymnopilhys leucaspis casianea — C
Gymnopilhys leucaspis castaneus
E
G. leucaspis late mil is — C
G. leucaspis lateralis
X
X
Thamnophius praecox — H & C
Thamnophius praecox
E
Pe re nos tola cau rensi v — H
Schistocichla caurensis 18
E
Grallaria Jigidssima — H & C
Grallaria dignissima
E
G. futviveniris — H & C
Hylopezus f fulviventris
E
Pipra coronata coronata — H
Lepidotrhix coronata coronata
E
P. coronata caquetae — C
L coronata caquetae
E
P. pipra discolor — C
Dixiphia pipra discolor
E
Heterocercus aurantiivertex — H & C
Heterocercus aurantiivertex
E
H. Jlavi vertex — II & C
H. flavivertex 19
X
X
Attiia ciiriniventris — H & C
A ttila citrini ventris20
X
X
X
A. torridus — C
A. torridus
E
Myiophobus cryptoxantluis — H & C
Myiophobus cryptoxantluis
E
Ramphotrigon fuscicauda — H
Ramphotrigon fuscicauda1'
E
Todirostnnn c. ctdopterum — H & C
Poeciiotriccus culoptertts
E
/. c. capiiale — H
P. capitalis 11
E
Contopus n. nigrescens — C
Contopus n. nigrescens
E
M icrnbales cinereivennis — H
Microbates cinereiventris hormotus 23
E
Cyphorimis arudus sidvini — C
Cyphorinus aruda sulvini
E
Microcerculus bamhla albigularis — C
Microcerculus bamhla albigularis14
E
Cacicus sclateri — II & C
Cacicus sclateri
E
Ocyatus latiroslrix—C
Ocyalus latirostris
E
Hylophilus hypoxanlhus fuscicapiUus- C
llylophilus hypoxanthus fuscicapiUus
E
//. b. brunneiceps — C
H. brunneiceps 16
X
X
Cyanocarux heilprini — H & C
Cyanacora. \ he Up tin i
E
Dolnspingus fringilloides — H & C
Dnlospingus fringilloides 26
X
X
Ia"wmic and distributional noles 1 1 1 Kefen-mcs lot species records in the )aii Area of Endemism were Borges e! al. (2001) and Borges and Almeida (201 1).
I- 1 Recently recorded in northern Peru (Alonso and Whitney 2001), (}) Recently recorded in northern Pern (Alonso and Whitney 2003.1. (4) Subspecies N. p.
:-;'i,l„phanei occurs south of Kio Soli miles (Payne 1997). Ilaffcr I 1997) reported ,V. p. pucherani tn rhe upj>er Rio Negro (Intern. (5) Recorded in sou-
ihcni Venezuela i Hilly 2003 1. (6i Subspecies G i mrnitilh recorded south of Rm Solimfle* (Inambari) (Tobias el al. 2002). (7) Also recorded in (he Jurud River
iln.unhinl i I'obias cl al. 2002). ( Kl Recently recorded in Inamhan AOE (Guilhenne and Borges 201 1 r. id) Records from Inambari. Imcri. and Tapajos AOEs
1 Zimmer and Isler 2003) ( lOl Subspecies M >. mvu pi recorded in Junta River < Inambari l (Zimmer and Isler 2003). (II) Also recorded in Inambari AOE (Zimmer
• n.l Isler 2001) r 12) Recently recorded in rtWtliem Hem (Alonso and Whilney 2003). 1 1 3 1 Also recorded in Guiana AOE (Cohn-Hafi et a). 1097. Zimmer and Isler
2**03. Naka et al 2006). 1 14) Also irvm.lcil in Inambari AOE (Zimmer and Isler 200.3). 1 15) Recently rediscovered in field (Lane el al. 2006). I ten Also recorded in
Inambari AOE (Zimmer and Isler 2003 1. 1 7 1 Recently recorded in Guiana AOE (Naka cl al. 2006). 1 18) Recently rediscovered in field (Zimmer 1999). (|9) Also
recorded in Guiana AOE (Snow 2004 Naka el al 2006). i20) Recently recorded in Inamhan AOE (Guilherme and Borges 2011). (21 1 Considered monofypic
*>lf) several records south of (lie Amazon, is River w ith an isolated population in the .Vapo region (Fil/pairick 2004). (22) Considered mondlypic with a
population recorded in Kondoniu AOE (FiUpafrick 20(4) (23) Dislribulton and taxonomy follow Resell el al. (2006). (24/ Distribution and latonomv follow
Rcsiall (2006) (25 1 Considered as tnonoiypte by Ridgely and Tudor (198V) (2 6) Recently recorded in Guiana AOE iRobbtns cl a). 2005)
The following rasa were not considered in the analysis. ( 1 1 Topaat petta pamprrpur. considered as a synonym with f p. smam&hiD hs f Ti
*5* Mtlrgupsii barrinyrrr hybrid between t‘htegop$,s enthropiera and /■ mgromocutat a (Zimmer and Isler 2003); (6) Pmra ifsi snrea'i l.cJb , *'
Himugh ihc Amazon; (7) Mionectn uteaginru* huuxwrth race M. o. ImuswriU inseparable from nominate (Fiupitrick MU’
The Wilson Journal of Ornithology 124( l):24-30, 2012
GRASSLAND BIRD COMMUNTIY RESPONSE TO LARGE WILDFIRES
ANTHONY J. ROBERTS,1*67 CLINT W. BOAL,2 DAVID B. WESTER,34
SANDRA RIDEOUT-HANZAK.3 AND HEATHER A. WHITLAW5
ABSTRACT.- We studied breeding season communities of grassland birds on short-grass and mixed-grass prairie sites
during the second and third breeding seasons following two large wildfires in March 2006 in the Texas panhandle. USA
Associated' wlihTfr? 77^' aV,a" CommuQi,y imposition following the tires due to species-specific shifts
s3Bmss t n Z , T\VCfm,0n Preferences- SPCC>(* ,hat Prcfer sparse vegetation and bare ground on
Meadowlik “ ,° h remophila alpestris ), benefited from wildfires, while others, such as Western
srecies'sDeci fic^shif/^*' ”*** deMC Vegeta,ion’ were ^lively impacted. Mixed-grass sites had
srimlar’bv "oost h , ’ 7° 7,'"* T*™* ^ f,res; grassland bird communities on burned plots were
M'^ng wddfires. Many
sbr-” -
Fire is a driving ecological process of healthy
giassland ecosystems. Following a history of fire
suppression, the application of prescribed fire
has become a contemporary method to manage
grasslands. However, it is unclear how well
prescribed fires can replicate the ecological values
°f natural fires. For example, studies of grassland
bird response to lire have focused on effects of
prescribed fire (e.g., Huber and Steuter 1984
Madden et al. 1999. Kirkpatrick et al. 2002. Grant
et al. 2010); no published studies have examined
the impact of wildfires on avian communities in
Great Plains grasslands. Prescribed fires are
generally conducted in low wind and high
humidity conditions that promote controlled
burning. Wildfires may be more intense than
presented fires and cover larger spatial scales.
Litter is decreased, woody plants are often killed
or burned completely, and live plants are killed at
high rates (Rideout-Hanzak et al. 2011) This
removes structure from the landscape, affecting
'Department of Natural Resources Management. To
lech University. Luhbock, TX 79409. USA
oC0l0gical Survc>'- Texas Cooperative Fish :
S Unit- Te,as T“h
’ Department of Animal. Rangeland, and Wildl
A*M n3" KlebCrg Wi,d,ifc Research Institute. Tex
■V S FkhrMta i-,?tSV,,1C' Ki,,8sviUc» 78363. US/
Old Dcpartmenl- 52-
Corresponding author;
e-mail: tony.roberts@aggicmail.usu.edu
24
(he poorly understood avian community in
unknown ways (Smith 2000). There is potential
lor increased frequency and size of wildfires in
the coming decades due to warmer temperatures
and less precipitation, as predicted by current
climate change models (North American Bird
Initiative 2010). Numerous bird species of
concern occur in the short-grass prairies of the
southern Great Plains, an assemblage of some of
the least ecologically understood of all grassland
birds (Askins et al. 2007). The effects of wildfires
on these and other species are unknown.
Two large wildfires ignited east of Amarillo in
the Texas panhandle. USA on 12 March 2006.
Together the fires burned 360.000 ha of predom¬
inantly private lands in what is known as the East
Amarillo Complex (EAC) wildfires (Zane et al.
2006). Widespread vegetation loss on the mixed-
grass and short-grass ecosystems had potentially
large negative impacts on numerous species of
grassland obligate songbirds that breed in the
Southern High Plains. The EAC presented a rare
opportunity to examine the effects of large-scale
wildfires on grassland bird populations. The
objectives of our study were to: (1) examine the
changes in avian species densities after a wildfire,
and (2) how avian community composition
adjusts in the years following the wildfires.
METHODS
This study was conducted on private ranches
in Roberts. Gray, and Donley counties in the
Texas panhandle. This area is in the Rolling
Plains ecoregion of Texas, a transition zone
between short-grass and mixed-grass prairie
types in the Southern High Plains. The landscape
Roberts et al. • WILDFIRE AND GRASSLAND BIRDS
25
is characterized by rolling hills leading to flat
plains interspersed with ephemeral wetland
depressions known as playas (Williams and
Welker 1966). Elevation ranges from 420 to
>600 m. The climate is characterized by hot
summers and cold to mild winters, but temper¬
atures fluctuate extensively within seasons (Wil¬
liams and Welker 1966). The mean summer
temperature (May-Jul) for 2007 and 2008 was
22.3 C (U.S. Department of Commerce 2009).
Historically the Texas panhandle received an
average of 53 cm of precipitation a year
(Williams and Welker 1966); the study area
received ~61 cm of precipitation annually
during the study period.
Study Plot Selection. — We selected 20 survey
plots for study based on access to private property,
bum history', and vegetation community type of
either short-grass or mixed-grass prairie (cen¬
tered at 14 S 342427 E, 3928890 N). The latter
distinction was based on soil type and dominant
vegetation. Burn type, either burned or unburned
area, was established by talking with landowners
and local officials, and visual examination of any
woody vegetation in the area such as prickly pear
cactus ( Opuntia spp.), catelaw mimosa {Mimosa
aculeaticarpa), or sand sagebrush ( Artemisia
fdifolia). We were unable to initiate this study
and select sites until the fall following the EAC
tires and were unable to examine avian commu¬
nities during the breeding season directly after
the fires occurred. The 20 plots were equally
distributed among areas identified as short-grass
burned, short-grass unburned, mixed-grass
burned, and mixed-grass unbumed. Individual
plots were at least I km apart and 0.5 km from
a known fire boundary, roads, or other vegetation
or topographic changes. We analyzed each
vegetation type separately to examine within-type
differences among five replicates each of burned
and unburned plots. All study sites were on
private property and we were unable to alter
grazing regimes; sites ranged from no grazing to
moderate slocking levels.
Breeding Season Surveys. — We used fixed-
radius point counts to survey avian populations
within the 20 plots, May-June, 2007 and 2008. We
conducted surveys using a three by three grid of
nine 75-m radius point counts for a total survey
area of ~|6 ha at each plot. We used three
observers throughout the study, all of w'hom had
either prior experience with grassland bird
identification or were trained prior to surveys.
Point-count centers were placed 200 m apart to
minimize, risk of recounting individuals (Ralph
et al. 1 993). We conducted surveys between 0.5 hrs
before and 3 hrs after sunrise. We did not survey
points during inclement weather such as rain, or in
winds >16 km/hr (Ralph et al. 1993). Observers
recorded all birds flushed within 75 in of the point
when walking to a point. All birds heard or seen
in the 75-m radii within a 7-min window' were
recorded and the distance from the observer was
estimated (Reynolds et al. 1980). Birds seen while
walking between points and birds that flew
overhead but not using the area within the radii
were not recorded.
Data Analysis.— We used both the May and
June surveys to create a measure of average
abundance and species diversity measures over
the breeding season. Average abundance was
calculated by averaging the count of each species
between the two survey periods. We calculated
species diversity using the Shannon diversity
index (H'; Shannon and Weaver 1963). Taylor
(1978) suggested that diversities calculated over
a variety of samples arc normally distributed,
but we used the more robust /-test suggested by
Hutcheson (1970) to compare H' across burn
conditions. Hutcheson's /-test uses the number of
individuals to calculate degrees of freedom, often
resulting in large numbers. We derived evenness
(E) from H' using the ratio of observed to
maximum diversity as described by Magurran
(1988).
We only used singing males from June surveys
to calculate density estimates. We were only
interested in the number of breeding territories
supported in each habitat type in contrast to
richness and diversity measures. June surveys
were during the height of the breeding season
when territories were established, and indicative
of the density of breeding pairs. We used actual
counts of singing males rather than estimates of
density derived using detection probabilities.
Species-specific estimates of detection probabili¬
ties introduce additional sources of variability
(Johnson 2008), and we believed detection
probability in a grassland landscape is close to
one and similar across bum conditions, especially
given our survey was based on territorial males
that are announcing their presence (Thompson
et al. 2009). Density estimates are an average of
the five plots in each treatment. We compared
densities among years and burn treatments using
a t- test with an alpha level of 0.05. Our interest
26
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 1. March 2012
1 ABLE 1 . Avian community measures for breeding season birds among burned and unburned plots associaled with ihe
East Amarillo, Texas Complex wildfires of 2006.
Short-
•grass
Mixed-
grass
Burned In = 5)
Unburned In = 5)
Bunted In = 5)
Unbumed 10% of all species detected
overall (Table 2). Effect sizes suggest Lark
SpaiTow densities were greater (/8 = 1.18, P =
0.14, d = 0.73) on burned (0.35/ha) compared to
unbumed (0.14/ha) plots in 2007: differences
between years within plot types were not
significant (Table 2). Lark Sparrow densities were
similar in 2008 on both burned (0.28/ha) and
unbumed (0.15/ha) plots. Moderate effect sizes
suggests densities were higher on burned plots in
2008 ( d = 0.57).
Roberts et al. • WILDFIRE AND GRASSLAND BIRDS
27
TABLE 2. Avian abundance (percent composition) on burned and unburned short-grass plots associated with
the East Amarillo, Texas Complex wildfires of 2006.
Short-grass
2007
2008
Species
Burned (/i = 5)
Unbumed (n = 5)
Burned (n = 5)
Unbumed (n = 5)
Totals
Northern Bobwhite (Colinus virginianus)
0
0
1 (0.8)
0
1 (0.2)
Scaled Quail ( Callipepla squamata)
0
2(1.9)
0
0
2 (0.4)
Killdeer (Charadrius vociferous)
1 (0.7)
0
1 (0.8)
1 (0.8)
3 (0.6)
Mourning Dove ( Zenoida macroura)
0
0
4(3.1)
5 (4.3)
9(1.8)
Common Nighthawk ( Chordeiles minor)
X (5.8)
1 (0.9)
7 (5.3)
5 (4.3)
21 (4.3)
ScissOr-tailed Flycatcher (Tymnnus jorfieatus)
2(1.4)
3 (2.9)
2(1.5)
4 (3.4)
1 1 (2.2)
Homed Lark ( Eremophila alpestris)
31 (22.4)
15 (14.4)
25 (19.1)
15 (12.9)
86 (17.6)
Cliff Swallow (Petrochelidon pyrrhonota)
0
1 (0.9)
1 (0.8)
0
2 (0.4)
Bam Swallow ( Hirundo rustica)
1 (0.7)
1 (0.9)
2 (1.5)
0
4 (0.8)
Dickcissel i Spiro americana )
2(1.4)
1 (0.9)
0
0
3 (0.6)
Cassin's Sparrow ( Peucaea cassinii)
4 (2.9)
2(1.9)
6 (4.6)
6 (5.2)
18 (3.7)
Grasshopper Sparrow ( Ammodramus savannarum)
33 (23.9)
33 (31.7)
27 (20.6)
30 (25.9)
124 (25.3)
Lark Sparrow ( Cltondestes grarnmacus)
26(18.8)
11 (10.6)
21 (16.0)
12 (10.3)
70 (14.3)
Western Meadowlark ( Stumella neglecta)
28 (20.3)
33 (31.7)
26 (19.8)
33 (28.4)
120 (24.5)
Brown-headed Cowbird ( Molothrus ater)
2(1.4)
1 (0.9)
6 (4.6)
5 (4.3)
14 (2.9)
Common Crackle (Quiscalus quisculd)
0
0
2(1.5)
0
2 (0.4)
Totals
138
131
104
89
490
Mixed-grass.— We observed 12 species on
mixed-grass plots in 2007 during the breeding
season with nine detected on burned and 1 1 on
unburned plots (Table 1). We detected 17 species
tut mixed-grass plots in 2008. Bam Swallow
(Hirundo rustica). Eastern Kingbird (Ty ramus
tyrunnus), Killdeer ( Chamdrius vociferous ), and
Lesser Prairie-Chicken ( Tym/mmchus pallidicinc-
tus) were all observed in low numbers on burned
plots, but were not detected on unbumed plots
(Table 3). There was no difference in diversity
between burned and unburned plots in 2007.
However, diversity on unburned mixed-grass plots
in 2008 increased (a6 s = 3.45. P < 0.001) from
that in 2007 and was higher (r^s = 2,59, P =
0.01) among burned plots (Table I). No change
was detected in diversity between years on burned
plots.
We analyzed Western Meadowlark. Cassin's
Sparrow ( Peucaea cassini /), Lark Sparrow, and
Grasshopper Sparrow densities on mixed-grass
plots. Western Meadowlark densities ranged from
0.3 1 to 0.45 birds/ha; no differences were detected
between bum conditions (/8 = 0.39. P = 0.35) or
years (tH = 0.17 ,P = 0.43). Estimated densities of
Cassin’s Sparrows in 2007 were 0.36/ha on
unburned compared to 0.29/ha on burned plots
({h = 0.35, P = 0.36, d 0.3). Densities did nol
change significantly on burned plots (/8 = 0.07.
P = 0.47, d = 0. 1 ) or unburned plots (/8 = 0.39.
P = 0.35, d = —0.3); Cassin’s Sparrows occurred
at identical abundance by 2008 on both plot types
(0.30/ha). Grasshopper Sparrows occurred at
significantly higher (/8 = 2.2, P = 0.031, d =
1.5) densities on unburned (0.45/ha) than burned
plots (0.12/ha) in 2007. Densities numerically
decreased (/8 = 1,26. P = 0,12, d = -0.9) in
2008 on unburned plots (0.35/ha) and effect size
suggest densities increased (/« = 1.17. P = 0.13, d
- 0.8) on burned plots (0.32/ha). Lark Sparrow
densities were nearly identical on burned (0.23/
ha) and unburned (0.24/ha) plots in 2007. The
following year densities on both burn conditions
were 0.15/ha; although the numerical decreases
were not significant, it appears there was a
noticeable effect of year on both burned (f8 =
0.83. P = 0.22. d = 0.53) or unburned (/8 = 0.85,
P =0.21, d = 0.55) plots.
DISCUSSION
Grasshopper Sparrows were the most abundant
species among short-grass plots, and were present
in consistent numbers regardless of year or burn
condition. This species was significantly more
abundant on unbumed plots after a wildfire in
Montana shrubsteppe (Bock and Bock 1987),
suggesting preference for denser vegetation in
arid western landscapes. In contrast, lower
numbers of Grasshopper Sparrows were detected
on burned areas for 2 years follow ing a grassland
28
THE WILSON JOURNAL OF ORNITHOLOGY • Vo/. 124. No. 1. March 2012
TABLE 3. Avian abundance (percent composition) on burned and unbumed mixed-grass plots associated with the East
Amarillo. Texas Complex wildfires of 2006.
Species
Northern Bobwhite
Lesser Prairie-Chicken
( Tympanuchus pallidicinctus )
Killdeer
Mourning Dove
Common Nighthawk
Eastern Kingbird ( Tyrcmnus tyrannus )
Scissor-tuiled Flycatcher
Horned Lark
Cliff Swallow
Barn Swallow
Blue Grosbeak (Passerina caerulea)
Dickcissel
Cassin’s Sparrow
Grasshopper Sparrow
Lark Sparrow
Western Meadowlark
Eastern Meadowlark ( Sturnella magna)
Brown-headed Cowbird
Bullock's Oriole ( Icterus hullockii )
Totals
Mixed-grass
2007
Burned (n = 5) Unbumed (n = 5) Burned (n = 5)
1 (LI)
0
0
0
4 (4.5)
0
3 (3.4)
0
0
0
0
3 (3.4)
22 (24.7)
9 (10.1)
18 (20.2)
25 (28.1)
0
4 (4.5)
0
89
2 (1.5)
0
0
3 (2.3)
7 (5.3)
0
0
0
0
5 (3.8)
I (0.8)
3 (2.3)
28 (21.1)
35 (26.3)
19 (14.3)
29 (21.8)
0
I (0.8)
0
120
2(1.7)
1 (0.8)
2(1.7)
2 (1.7)
12 (10.0)
I (0.8)
2(1.7)
0
0
1 (0.8)
0
0
31 (25.8)
23 (19.2)
12 (10.0)
29 (25.2)
0
2 (1.7)
0
133
2008
Unburned (« =
5) Totals
6 (4.3)
11(2.3)
0
1 (0.2)
0
2 (0.4)
16 (11.4)
21 (4.4)
7 (5.0)
30 (6.2)
0
1 (0.2)
3 (2.1)
8(1.7)
1 (0.7)
1 (0.2)
3 (2.1)
3 (0.6)
0
6 (1.2)
0
1 (0.2)
0
6 (1.2)
27 (19.3)
108 (22.4)
22 (15.7)
89(18.5)
12 (8.6)
61 (12.7)
30 (21.4)
113(23.4)
3 (2.1)
3 (0.6)
8 (5.7)
15 (3.1)
2(1.4)
2 (0.4)
140 482
wildfire in Arizona (Bock and Bock 1992). High
effect sizes indicate the higher densities of
Western Meadowlarks on burned plots in 2007
may have been biologically relevant, but were not
statistically significant in our study. The above¬
ground plant biomass among burned and un¬
burned plots was similar bv 2008 (Rideout-
Hanzak et al. 2011), likely providing similar
nesting sites and foraging opportunities across
burn conditions. Horned Larks prefer areas with a
high percentage ol bare ground across their range
(Beason 1995). Consistent with this general
habitat association. Horned Larks decreased in
density as burned areas were revegetated and
more litter formed.
The composition of avian communities difft
on mixed-grass plots in 2007 despite siir
diversity and evenness measures across t
conditions. Abundances of Cassia's and Gr;
hopper sparrows were higher on unburned t
burned plots in mixed-grass areas. Howe’
ensities ol these species on burned plots w
similar to unburned plots by 2008. Lark Spam-
on both short- and mixed-grass plots decreased
burned areas from 2007 to 2008. Long-term Li
Sparrow abundance decreased along with i
decrease in woody vegetation after a fire in
sagebrush ( Artemisia spp.) grasslands in Wash¬
ington State (Eamst et al. 2009). This suggests the
avian community may have returned to densities
similar to unbumed areas by the third breeding
season alter the wildfires. A homogeneous
landscape with plant biomass and structure similar
to unburned areas 3 years after the wildfires
( Rideout-Hanzak et al. 2011) may have promoted
similar avian communities across the landscape.
Historically, lire was a major ecological factor
in both short- and mixed-grass ecosystems until
intense livestock grazing and fire suppression
altered vegetation and fuels so fires could not burn
with historic frequency or intensity (Wright and
Bailey 1982). Some areas of the Great Plains have
seen lire return to the landscape in the form of
prescribed fire. The EAC wildfires occurred
during high winds and low humidity, different
conditions than proscribed for prescribed fires.
Prescribed tires appear to have similar influences
on the avian community as the EAC wildfires
despite ditterences in intensity and environmental
conditions during the wildfire.
Many ol the responses measured in our study of
wildfire were similar to those observed following
Roberts et al. • WILDFIRE AND GRASSLAND BIRDS
29
prescribed fires. Wintering Cassin’s Sparrows in
Arizona responded negatively to burning after a
prescribed fire, but Grasshopper Sparrows showed
no response (Gordon 2000). Abundance of
Grasshopper and Cassia's sparrows increased
after a prescribed fire in Texas mesquite (Prosopis
spp.) savanna (Lee 2006). Prescribed fire in North
Dakota mixed-grass prairie decreased populations
of most species during the breeding season
following the fires (Grant el al. 2010); however.
3 years after the prescribed fires, avian popula¬
tions had increased and stabilized, recovering in a
similar time span as in our study. Many species,
including Grasshopper Sparrows and Western
Meadowlarks, were positively correlated with
use of prescribed fire in mixed-grass prairies
(Madden et al. 1999). Western Meadowlarks in
prairie Canada declined in abundance during the
breeding season following prescribed fire, but had
comparable densities on burned and unburned
areas 3 years post-fire (Pylypec 1991).
We found an apparent temporary shift in avian
community composition following wildfires due
to species-specific shifts associated with life-
history traits and vegetation preferences. The
avian community appeared to be similar to that
on unburned plots of similar grass types 3 years
following the wildfires. This was consistent with
vegetation recovery (Rideout-Hanzak et al. 201 1 ).
A homogeneous landscape in grasslands decreases
the diversity of grassland birds (Fuhlendorf et al.
2006) and the grassland bird community reaches
peak densities with increased periodic disturbance
in short-grass and mixed-grass landscapes. Two of
the most common species detected on short-grass
plots. Grasshopper Sparrow and Horned Lark, are
among 20 common North American birds expe¬
riencing the steepest population declines (Butcher
and Niven 2007). The area burned by the EAC
wildfires may not only provide important habitat
for continued persistence of species of concern,
but fire may be an integral component of habitat
health for the avian community.
Persistence of a diverse and abundant avian
community is dependent on periodic disturbances
such as wildfire or prescribed fire, grazing, and
drought to provide patches of habitat in varying
stages of growth after disturbance (Fuhlendorf and
Engel 2001). Prescribed fire has been used to
mimic wildfire effects and reduce wildfire
potential (Pattison 1998). Rideout-Hanzak et al.
(2011) suggest the EAC fires may not have
created drastically different conditions than a
prescribed fire in this ecosystem; this was
corroborated by the avian community response.
The wildfires may have been ecologically bene¬
ficial in providing similar services to plants and
soil as historic fire regimes on the Southern High
Plains. The combination of varying grazing
regimes and periodic prescribed fire in the Texas
panhandle would facilitate development of a
mosaic of grassland patches in varying stages of
recovery from disturbance, and offer a wide
variety of niches for grassland birds.
ACKNOWLEDGMENTS
We thank the many landowners who allowed access to
their properties for this research This study was funded by
the Natural Resources Conservation Serv ice. Texas Parks
and Wildlife Department, and Texas Tech University.
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The Wilson Journal of Ornithology 1 24( 1 ):3 1 —39, 2012
ARTHROPOD ABUNDANCE AND SEASONAL BIRD USE OF
BOTTOMLAND FOREST HARVEST GAPS
CHRISTOPHER E. MOORMAN,1 4 LIESSA T. BOWEN,' JOHN C. KILGO,2
JAMES L. HANULA/ SCOTT HORN,' AND MICHAEL D. ULYSHEN3
ABSTRACT. — We investigated the influence of aitliropod abundance and vegetation structure on shifts in avian use of
canopy gap, gap edge, and surrounding forest understory in a bottomland hardwood forest in the Upper Coastal Plain of
South Carolina. We compared captures of foliage-gleaning birds among locations during four periods (spring migration,
breeding, post-breeding, and fall migration). Foliage arthropod densities were greatest in the forest understory in all four
seasons, but understory vegetation density was greatest in gaps. Foliage-gleaning bird abundance was positively associated
with foliage-dwelling arthropods during the breeding (F 18.5, F < 0.001) and post-breeding periods (F - 9.4, P =
0.004). and negatively associated with foliage-dwelling arthropods during fall migration (F = 5.4, P = 0.03). Relationships
between birds and arthropods were inconsistent, but the arthropod prey base seemed to he least important during migratory
periods. Conversely, bird captures were positively correlated with understory vegetation density during all four periods
IF < 0.001 ). Our study suggests high bird abundance associated with canopy gaps during the non-breeding period resulted
less from high arthropod food resource availability than from complex underston and midstory vegetation structure.
Received 25 January 2011. Accepted $ August 2011.
Many bird species, including those of early-
successional habitats and those of small tree-fall
gaps within mature forest, select disturbed
habitats during some portion of the year (Hunter
et al. 2001). Several studies have documented
greater bird abundance in forest canopy gaps
created by natural treefalls (Willson et al. 1982,
Blake and Hoppes 1986. Martin and Karr 1986) or
group-selection harvest (Kilgo et al. 1999. Moorman
and Guynn 2001) than in the mature forest
surrounding gaps. Some mature-forest breeders
shift into more densely vegetated habitats between
breeding and post-breeding periods (Anders el al.
1998: Vega Rivera et al. 1998, 2003; Pagen et al.
2000; Viiz and Rodewald 2006). Birds use a variety
of forested habitats during migratory periods (Petit
2000. Rodewald and Brittingham 2002), but
mature-forest edges and early-succession habitats
may experience relatively greater use (Rodewald
and Brittingham 2004). Reasons for greater use of
disturbed habitats by birds during certain periods
remain speculative, but abundant food and protec¬
tion from predators have been proposed (Marshall
et al. 2003).
Fisheries. Wildlife, and Conservation Biology Program.
Department of Forestry and Environmental Resources.
North Carolina State University. Campus Box 7646,
Raleigh. NC 27695. USA.
L'SDA, Forest Service Southern Research Station, P O.
Box 700. New Ellcnlon, SC 29809. USA.
USDA. Forest Service, 320 Green Street. Athens, GA
30602, USA.
'Corresponding author; e-mail:
chris_moorman@ncsu.edu
Arthropod populations also are influenced by
season and habitat type (Johnson and Sherry 2001,
Greenberg and Forrest 2003) as well as canopy
gap size (Shurc and Phillips 1991). It should be
advantageous for birds to choose sites with the
greatest resource availability (Martin and Kan-
1986), and greater invertebrate biomass has been
positively correlated to bird abundance (Blake and
Hoppes 1986. Holmes el al. 1986), daily nest
survival rates, growth rales of nestlings (Duguay
et al. 2000). and liming of warbler migration
(Graber and Graber 1983). Studies of experimen¬
tal prey removal have not linked decreased prey
abundance with negative consequences for the
local bird community (Nagy and Smith 1997,
Marshall et al. 2002, Champlin ct al. 2009).
Bowen et al. (2007) documented seasonal shifts
in relative use by birds of canopy gap and forest
habitat. They speculated these shifts may be
driven by seasonal changes in arthropod abun¬
dance in gaps. Previous studies have not investi¬
gated seasonal shifts in avian habitat use as related
to resource availability over multiple periods.
Our objectives were to: (I) investigate whether
bird use of forest gaps was associated with
arthropod abundance or vegetation structure, and
(2) ascertain if shifts in relative use of gap and
forest understory were related to spatial and
temporal variation in arthropod abundance. We
predicted positive relationships between avian
habitat use and arthropod abundance (i.e.. relative
bird use of gap vs. forest underston will shift
based on changes in local arthropod abundance )
from spring migration through fall migration.
31
32
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 1. March 2012
METHODS
Study Area. — We sampled foliage-gleaning
birds and foliage-dwelling arthropods within
forest canopy gaps, gap edges, and mature
bottomland forest understory during 2001 and
2002 at the Savannah River Site, a 78.000-ha
National Environmental Research Park owned by
the U.S. Department of Energy. The site was a
mature stand of bottomland hardwoods, 120 ha in
size, in Barnwell County in the Upper Coastal
Plain Region of South Carolina. Birds, arthropods,
and vegetation structure were surveyed in 12
group-selection gaps harvested in December 1094
and in the mature forest understory adjacent to
gaps. Minimum spacing between gap centers was
100 m. and the mean distance between a gap's
edge and the edge of its nearest neighbor was
102.7 m (range = 44-230 m). The gaps were in
their seventh and eighth growing seasons post-
harvest during the study. They were of three sizes
(0.13. 0.26. and 0.50 ha) with four replicates of
each size. Previous research within this size range
in these gaps identified a threshold in response by
breeding (Moorman and Guynn 2001) and fall
migrant birds (Kilgo et al. 1999). The mature
lorest canopy was dominated by laurel oak
( Quercus lauri folia), cherry bark oak (Q. falcuta
var. pagodaefolia), sweetgum ( Uquidamhar styr-
aciflua ), and loblolly pine (Pinus taeda). The
midstory was patchily developed, consisting
primarily of red mulberry {Monts rubra), iron-
wood < Carp inns caroUniamis). and American
holly (Ilex opaca). The understorv contained
patches of dwarf palmetto (Saba! ' minor) and
switchcane (Arundinaria gigantea ). Vegetation in
the gaps varied from I to 8 m in height and was
dominated by regenerating trees (primarily sweet-
gum, loblolly pine, sycamore [Platanus occiden-
tahs). green ash [Fraxinus pennsy/vanica], oaks,
and black willow [Salix nigra]) and patches of
blackberry (Rubus spp.). dwarf palmetto, and
switchcane.
Sampling Design.- We surveyed birds and
arthropods during four avian activity periods in
, °°' and 2002;. sP,ing migration (25 Mar through
15 May), breeding ( 16 May through 30 Jun), post-
breeding (1 jul through 31 Aug), and fall
migration (I Sep through 18 Oct). These begin-
n>ng and endmg dates are estimates of biologi-
Ca ly meanuigfU| periods, and each overlaps
SStLdith 'he Ull’Cr Ma"y individuaJs
initiated breeding on our study area before 16
May, but transient species that bred to the north
continued to migrate through South Carolina
until mid-May. Similarly, some individuals mi¬
grated from or through our study area before 1
September, but most fall migration occurred after
I September. Wc established a sampling transect
radiating southward from the center of each gap to
investigate bird-arthropod relationships within
each period with three bird and arthropod
sampling stations along each transect: one in the
gap center, one at the southern edge of the gap.
and one 50 m into the forest.
Vegetation Measurements. — We measured veg¬
etation structure during June 2001 and 2002 along
10-m transects on each side of and parallel to all
mist-net stations. 1,5 m from each net. We
measured vertical distribution of vegetation mod¬
ified Irom Karr (1971 ) at I -m intervals along each
1 0-m transect (total 20 points). We recorded the
number of times vegetation touched a 2-m pole or
the height intervals directly above the pole at 12
height intervals (0-0.25, 0.26-0.50. 0.51-075.
0.76-1, 1. 1-1.5. 1.6-2, 2.1-3. 3.1-5.5.1-10. II-
20, 21-25, and 26-30 in). Touches >2 ni high
were estimated visually. The percent cover for
each height interval was calculated from the
percentage of the 20 sampling points with
vegetation touches in that interval. We calculated
the mean number of pole touches for height
intervals <3 m as an index of foliage density for
understory vegetation.
Arthropod Collection.— Wc sampled foliage¬
dwelling arthropods at each station during each
avian activity period in 2001 and 2002. We used
foliage clipping (Cooper and Whitmore 1990) to
sample foliage-dwelling arthropods on each oi
live target plant species groups: (I) white oaks
(white oak 1 Quercus alba), swamp chestnut oak
[(?• michauxif). overcup oak | Q. lyrata). Durand
oak ]Q. durandii J), (2) lobed red oaks (cherry bark
oak). (3) u n lobed red oaks (water oak [ Q . m§ro\.
laurel oak. willow oak [<9. p hellos]). (4) sweet-
gum. and (5) switchcane. This suite of species was
selected to represent dominant members of the
understory and overstory, as well as species
important as avian foraging substrates (Buffington
et al. 2000. Kilgo 2005). Each sample consisted of
25 branch tips from each target species group
(total sample = 125 branch tips) collected in the
vicinity of each sampling station (i.e.. staying
within the target habitat type). Each branch-tip
dipping was 2.54-15.24 cm in length and usually
came from the end of a branch where most leaves
Moorman et al. • SEASONAL BIRD USE OF HABITATS AND ARTHROPODS
33
were clustered on the target plant species groups
(Cooper and Whitmore 1990). We collected
foliage from ground level to about 2.3 m. We
placed clippings immediately in plastic bags to
avoid evasive movements of arthropods, hut
highly mobile arthropods (a group of less interest
lor this study) were not as effectively sampled.
We did not sample above 2.3 m because we
considered it appropriate to sample arthropods
only in the same stratum in which we sampled
birds (i.e., 3-m mist nets). Samples were placed in
a freezer for 24 hrs to kill all arthropods. We then
shook the foliage to collect the arthropods, placed
them in alcohol, and identified them to Order.
Foliage was oven-dried for 48 hrs at 40 C and
weighed.
Mist Netting.— We placed a single mist net
(12 m long x 3 m tall with 30-mm mesh) at each
of the three sampling stations at each of the 12
study gaps, Netting was conducted once each
week at each station during the spring migration,
post -breeding, and fall migration periods, rotating
between stations on a regular weekly schedule.
Nets were operated once every 2 weeks during the
breeding period, because birds remain fairly
stationary during this period. Nets were opened
at first light and operated for 4-6 hrs, depending
on daily weather conditions. Netting was not
conducted when wind exceeded 16 km/hr or
during steady rainfall. We banded captured birds
with a U.S. Geological Survey aluminum leg
band.
Statistical Analyses. — We assigned birds
(Table 1) to the foliage-gleaning guild following
Ehrlich et al. (1988) and Hamel (1992). Birds
considered winter residents, present only front late
fall through early spring, were not included in
analyses.
We used a linear mixed model (PROC MIXED)
tSAS Institute 2000) to conduct analysis of
variance (ANOVA) with covariates and interac¬
tions to analyze the effects of net location (gup.
edge, forest understory), period, and arthropod
abundance on bird captures. We used mean
captures of foliage-gleaning birds/ 1 00 net hrs as
the dependent variable. We considered net
location and period as fixed effects with net
location as a split plot factor and period as the
repeated measure. Arthropod abundance was a
continuous covariate. We included all two-way
interactions. We used a linear mixed model to
examine the relationship between bird captures
and understory (0-3 m) vegetation density with
TABLE 1. Foliage-gleaning bird species captured in
mist nets at least once during 2001-2002 in South
Carolina. USA.
Species
Scientific name
Yellow-billed Cuckoo
Coccyzus americanus
Ruby-throated Hummingbird
Archilochus coluhris
White-eyed Vireo
Vireo griseus
Blue-headed Vireo
V. solitarius
Red-eyed Vireo
V. olivaceus
Carolina Chickadee
Poecile carolinensis
Tufted Titmouse
Bueolophus bicolor
Blue-gray Gnatcatcher
Polioptila caerulea
Gray Catbird
Dumetella carolinensis
Worm-eating Warbler
Helmitheros vermivomm
Golden-winged Warbler
Vermivora chrysoptera
Blue-winged Warbler
V. cyanoptera
Kentucky Warbler
Geothlypis formosa
Common Yellowthroat
G. trie has
Hooded Warbler
Setophaga citrina
American Redstart
S. ruticilla
Northern Bum la
S. americana
Magnolia Warhlcr
S. magnolia
Chestnut-sided Warbler
S. pensylvanica
Black-throated Blue Warbler
S. caerulescens
Pine Warbler
S. pinus
Prairie Warbler
S. discolor
Yellow-breasted Chat
Icteria virens
Summer Tanagcr
Piranga rubra
Northern Cardinal
Cardinalis cardinalis
vegetation as the covariate. Vegetation was only
recorded once each year, so this model did not
include a repeated measure. Year and gap size
were not significant (P > 0.05) in any models,
and these variables were not included in final
models. Arthropod captures were standardized by
number of arthropods/ 100 g of dry foliage. We
modeled bird abundance with abundance of
Lepidoptera because previous studies have shown
Lepidoptera to be a primary avian food source
(Holmes et al. 1986, McMartin et al. 2002).
RESULTS
The greatest understory vegetation density
occurred in gaps (Fig. 1). Gaps had dense
understory vegetation with no canopy, whereas
forest had relatively open understory and midstory
and well-developed canopy.
We captured arthropods representing 21 Orders
during 2001 and 2002. Total arthropod density
( number of arthropods/ 100 g of foliage} was lower
during spring migration than in the other three
periods and greater in the forest understory than in
gaps and at gap edges (Table 2). Total arthropod
34
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124. No. 1. March 2012
Mean pole touches per understory (<3 m) height interval
FIG. I. Seasonal foliage-gleaning bird caplures plotted against mea
Caro^naPUSAnderSt0ry hdght ** CaCh "Ct loca,ion in a
understory foliage density (mean vegetation pole
bottomland forest during 2001-2002 in South
density was greater at gap edges than in g;
except during the breeding season when densit
were greater in gaps (Table 2). The five m.
frequently encountered arthropod Orders rep
senting at least 150 individuals, were Arane;
Coleoptera, Homoptera, Hymenoptera. and Lei
doptera. Aramds. hymenopterans, and lepidoptt
ans followed the same general pattern as .
arthropods combined, but coleopteran densi
decreased from spring to fall migration. Lepido
tera density was highest in the forest during sprii
migration, breeding, and post-breeding perioc
but densities were similar among sampli,
locations during fall migration.
Bird and arthropod relationships were inconsi
tent across the four seasons (Table 3). Folia*
g eanmg bird abundance was positively associate
«th lol.age dwelhng arthropods during the brecc
periods ^
1-2, P = 0.28) (Table 3). Foliage-gleaning birds
were positively associated with understory vegeta¬
tion density during all periods (Table 4; Fig. 1).
DISCUSSION
Seasonal shifts in relative bird use of gaps and
forest understory in bottomland hardwood forests
W'ere not driven by changes in arthropod avail¬
ability. Bowen et al. (2007) documented a
seasonal shift in habitat use for several bird
groups at our site with relative bird use of mature
forest habitat greatest during the breeding period:
they speculated these shifts may correspond to
seasonal changes in arthropod abundance among
habitats. However, arthropod abundance remained
greater in forest understory than in gaps in all
seasons, and we did not document an increase in
total arthropods or any arthropod Order in die
lores! during the breeding season when relative
bird use of torest understory was greatest. The
highest arthropod densities in gaps occurred
during the breeding season, the period when birds
least used gaps. Foliage-gleaning birds on our
study site, based on crop flushes, consumed
Sti number o( arthropods/ 100 g of dry foliage for most abundant arthropod Orders by period and net location in a bottomland forest during 2001-2002, South
Moorman et al. • SEASONAL BIRD USE OF HABITATS AND ARTHROPODS
35
35
CO C3
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The Wilson Journal of Ornithology 124(l):40-50. 2012
SEASONAL VARIATION IN SHOREBIRD ABUNDANCE
IN THE STATE OF RIO GRANDE DO SUL, SOUTHERN BRAZIL
ANGELO L. SCHERER1-2 AND MARIA V. PETRY'
ABSTRACT — We describe the frequency of occurrence and seasonal variations of shorebirds (Charadriidae and
Scolopacidae) along a 120-km transect of beach between Balnefirio Pinhal and Mostardas north of Lagoa do Peixe
National Park. Rio Grande do Sul State over a 2-vear period (Oct 2007 to Sep 2009). A total of 96.889 shorebirds was
recorded. The greatest abundance occurred between October and April and the lowest occurred between May and
September. The most abundant of the 17 species recorded were Sanderlings (Calidris alba). White-rumped Sandpipers tC
fuscicollis ) . and Red Knots (C. camttus). The least abundant were Senupalmated Sandpipers (C. pusilta). Rufous-chested
Ploxers ( Charadrius mode slits), and Hudsonian Godwits ( Li most/ haemastiea). Fourteen species were migrants from the
Northern Hemisphere, one was a migrant from the Southern Hemisphere, and two were residents. Nine species were
recorded regularly, two were recorded sporadically, and six were recorded occasionally. Six Nearctic species were
recorded in June and July most likely indicating the presence of non-breeding immatures. The beaches of Rio Grande do
Sul are important migration stopover and wintering sites for many shorebirds in southern Brazil and should be a focu> of
conservation efforts, especially given the increasing development pressure that threatens these areas. Received 10
February 2011. Accepted 25 October 2011.
Brazil is visited by thousands of birds that
migrate seasonally from the Northern lo Southern
Hemisphere and vice-versa (Morrison and Ross
1989, Chesser 1994). Those that come from the
north prior to the boreal winter (Antas 1994)
arrive in Brazil seeking wintering sites rich in
food resources (Telino-Junior et al. 2003). Shore-
birds from the Northern Hemisphere occur in
Brazil during the austral summer and those from
the Southern Hemisphere occur in the country
during the austral winter. Immature individuals of
certain shorebirds occur throughout nearly the
entire year, as they are not yet capable of breeding
and return to breeding areas only when they are
sufficiently mature to begin nesting (Sick 1979.
Azevedo-Junior and Larrazabal 1994. Azevedo-
Junior et al. 2001a. b).
The sites at which shorebirds stop during
migrations are of considerable importance for
conservation. Lagoa do Peixe National Park and
nearby beaches on the coast of the State of Rio
Grande do Sul in southern Brazil attract large
concentrations of migratory shorebirds (Lara-
Resende and Leeuwenberg 1987. Morrison and
Ross 1989. Vooren and Chiaradia 1990. Belton
2000). The availability of food resources at these
sites oilers the birds the opportunity to gain body
Graduate Program in Biology. Laboratory of Ormtl
ogy and Marine Animals. Center for Health Scienc
Va'1' d° Ri,> dos Si™s- Avenida Unisin
. ‘ °‘ ^0'-2-°00. P. o. Box 275. Room 2D223E. 5
Leopoldo. Rio Grande do Sul, Brazil
Corresponding author; e-mail: alscherer@pop.com.bi
mass and acquire adequate energy for molting
and return to breeding areas (Azevedo Junior
et al. 2001a, b; Baker et al. 2004, Fedrizzi et al.
2004).
Shorebird populations fluctuate during (he
breeding and wintering periods in number of
individuals and migratory species using the
beaches of southern Brazil (Lara-Resende and
Leeuwenberg 1987, Barbieri et al. 2003. Telino-
Junior et al. 2003. Barbieri and Mendon^a 2005)
The greatest abundance occurs from September to
April along the Brazilian shoreline with slight
temporal variations (Barbieri 2007. Barbieri and
Hvenegaard 2008. Barbieri and Paes 2008). In
southern Brazil. Lara-Resende and Leeuwenberg
1 19X7) found the highest abundance of shorebirds
from November to April in Lagoa do Peixe
National Park (Ramsar site) (31 21’ S; 05 1 03’
W). I he beaches from Balneario Pinhal to
Mostardas. which are north of this conservation
unit, offer adequate stopover, feeding, and resting
sites for migratory shorebirds and are important
locations for their conservation (A. L. Scherer,
pers. obs.).
The coast of Rio Grande do Sul is considered a
key area for shorebird conserv ation in the Western
Hemisphere (Serrano 2008). Our objectives were
to: ( I ) record the occurrence and seasonal
variations ot shorebirds (Charadriidae and Scolo¬
pacidae) along a 120-km transect of beach north
of Lagoa do Peixe National Park, and (2)
document the frequency of occurrence of species
of shorebirds over a 2-year period.
40
Scherer and Petry • SEASONAL VARIATION IN SHOREBIRD ABUNDANCE
41
0 15 30 6Q
Mostardas
Lagoa do Peixe National Park
51 WW
Balneario Pinhal
-f
PARAGUAY
BRAZIL
L-'v
1 \
S -
f (
J
ARGENTINA J*
/
RO GRANDE DO SUL TOMES
BAI MiAMpmUAI
1 ■
URUGUAY
-\
•y
. \.
\ « _ < - V-.
j/
Legend
Lakes
Agriculture
Urban area
Dunes and Fields
Forest
-31 ws
— i -
J9-OCTW
TkJ. I, Transect (120 km) of study area between municipalities of Balnedrio Pinhal (30J 14' 57' S. 050 13 48.4 W)
and Mostardas (31 10' 52" S. 050 50’ 03” W) on the coast of Rio Grande do Sul. southern Brazil.
METHODS
S'/u/v Area.— We studied shorebirds along the
coast °I the State of Rio Grande do Sul (southern
Brazil) between the municipalities of Mostardas
1,1 the south (31 10' 52" S. 050 50' 03" W) and
Balneario Pinhal in the north (30 14' 51" S. 050
1 48.4” W), totaling 120 km of beach (Fig. I).
The area is characterized by large sandy beaches
dlul Stines with a series of coastal lakes beyond
!i>e dunes (Belton 2000). Human occupation along
'his region has altered the landscape, which is
US«J (or tourism and recreation. Fifteen kilome-
,ers °f shoreline in Balneario Pinhal are highly
urbanized and the entire region is used intensively
lor irrigated crops and tree plantations.
The climate of the region is wet subtropical
VVl|h a mean temperature of 17 C and annual
'ainfall of 1 .200 mm. The width of the 120-km
s,reteh of beach ranges from 50 to 1 20 m. at times
reaching 200 m. The beach has a low slope and
'he wash zone is broad, generally -10 m with
a high density of invertebrates. The dominant
species are bivalve mollusks including yellow
clams ( Mesodesma mcictroides) and wedge clams
( Donax hanleyamis), crustaceans such as mole
crabs (Enterita brasiliensis) and cirolanid isopods
( Excirolana armata), and polychaetes ( Euzonus
furciferus and Spin gaucha) (Gianuca 1983).
Surveys.— Monthly surveys (n = 24) were
conducted between October 2007 and September
2009 along the 120 km of beach in an automobile
traveling from north to south at a maximum speed
of 20 km/hr between 0700 and 1700 hrs. Direct
counts were made of the individuals of each spe¬
cies (Bibby et al. 2000). Surveys were conducted
by two observers on randomly chosen sunny days.
Shorebird abundance was recorded at a distance
(50 to 100 m) to keep birds from Hushing. The
first observer recorded the birds from the edge of
the water to the middle portion of the beach and
the second observer recorded the birds from this
portion to the dunes, taking care to avoid recounts.
Data were recorded on a portable voice recorder
and field spreadsheets. Birds were identified with
42
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 1. March 2012
TABLE 1. Occurrence and total abundance of
shorebirds (in decreasing order) from October 2007 to
September 2000 on the coast of Rio Grande do Sul.
southern Brazil. Status: seasonal visitor from the Northern
Hemisphere (VN). seasonal visitor from the Southern
Hemisphere (VS), and Resident ( R ).
Species
Slums
Abundance
*
Sanderling
Calidris alba
VN
78.247
80.8
White-rumped Sandpiper
C. fiuscicollis
VN
7.588
7.8
Red Knot
C. canutus
VN
5,103
5.3
Collared Plover
Charadrius collaris
R
2.042
2.1
Lesser Yellowlegs
Tringa flavipes
VN
1.517
1.6
Grey Plover
Pluvialis squatarola
VN
822
0.8
Semipalmated Plover
Charadrius semipalmatus
VN
547
0.6
Southern Lapwing
Vanellus cliilensis
R
481
0.5
American Golden Plover
Pluvialis dominica
VN
218
0.2
Ruddy Turnstone
Arenaria inierpres
VN
127
0.1
Greater Yellowlegs
Tringa rnelanoleuca
VN
95
0.1
Solitary Sandpiper
T. solitaria
VN
36
0.04
Buff-breasted Sandpiper
Tryngites subrupcoUis
VN
35
0.04
Whimbrel
Numenius phaeopus
VN
17
0.02
Semipalmated Sandpiper
Calidris pusilla
VN
7
0.01
Rufous-chested Plover
Charadrius modestus
VS
6
0.01
Hudsonian Godwit
Limosa haeinastica
VN
1
0.001
Totals
96.889 100
the aid ol 10 X 50 binoculars and use of field
guides (Crossley et al. 2006, Mata et al. 2006).
Flocks of shorebirds with <100 individuals were
considered small, those with between 100 and
1,000 individuals were considered medium-sized,
and those with >1,000 individuals were consid¬
ered large. The seasons are in accordance with the
Southern Hemisphere: austral summer (Oct to
Mar) and austral winter (Apr to Sep). The
frequency of occurrence (C) of each species was
calculated using the equation C = 1J x 1 00/A' in
which P is the number of counts containing the
species, and N is the total number of counts
throughout the study period ( n = 24). Classifica¬
tions recorded were: regular (present in >50% of
counts), sporadic (present between 25 and 50% of
counts), occasional (present <25% of counts),
and absent (not present in counts) (Dajoz 1983).
RESULTS
Seventeen species of shorebirds were recorded,
six species of Charadriidae and 1 1 Scolopacidae,
totaling 96.889 individuals. Sanderlings (Calidw
alba). White-rumped Sandpipers (C. fuscicoUh).
and Red Knots (C. canutus) were the most
abundant species, accounting for 93.9% of the
overall abundance. Sanderlings accounted for
80.8% of the overall abundance. Collared Plover
( Charadrius col laris) and Lesser Yellowlegs
(Tringa flavipes) accounted for >1% of the overall
abundance, whereas the remaining 12 species
accounted for <1% (Table 1 j. The greatest
abundance of shorebirds occurred between October
(arrival at stopover or wintering areas) and April
(return to breeding areas), and the lowest occurred
between May and September (Fig. 2).
Nine species were recorded regularly over a 2-year
period (2007 to 2009) (all but the Red Knot were also
regular when years were analyzed separately/ two
were sporadic, and six were occasional (Table 2).
The Hudsotiian Godwit (Limosa haemastica ) was
absent throughout the 2007/2008 period and only one
individual was recorded in January 2009. The
Rufous-chested Plover ( Charadrius modestus). a
visitor from the Southern Hemisphere, was recorded
as occurring occasionally. One individual was
recorded in July 2008 and five were recorded in
May 2009, Five Semipalmated Sandpipers (Calidris
pusilla ) were observed in February 2008 and two in
September 2009. Six Buff-breasted Sandpiper^
(Tryngites mbruficollis) were observ ed in November
2007 and 29 (distributed among three sites) were
recorded in October 2008. Abundances during
monthly surveys varied seasonally (Fig. 3).
The frequency of occurrence of the Southern
Lapwing ( Vanellus chilensis), a resident species, was
regular as it was recorded in all counts. The greatest
abundance of this species occurred between April aid
July with a peak (n = 81) in July 2008. and was
lowest between October and December with only one
individual recorded in November 2008. The Amer¬
ican Golden Plover (Pluvialis dominica) was occa¬
sional but present in 4 months with a peak (n = 126)
in February 2009; six individuals were recorded in
April in the 2007/2(X)8 period. The frequency of
occurrence of Grey Plovers (P. squatarola) was
Scherer and Petry • SEASONAL VARIATION IN SHOREBIRD ABUNDANCE
43
14000 ■
12000 ■
10000 ■
o 8000
ONDJ FMAMJJASONDJ FMAMJ J AS
2007- 2009
FIG. 2. Monthly abundance of shorebirds (Charadriidae and Scolopacidae) from October 2007 to September 2009 on
the coast of Rio Grande do Sul. southern Brazil.
regular with greatest abundance occurring between
October and February (n = 353 in Feb 2009) tuid
lowest between April and September, this species
was absent in June and July.
The frequency of occurrence of Semipalmated
Plovers (Charadrius semlpalmutus ) was sporadic
'» the 2007/2008 period and regular in 2008/2009.
ihe greatest abundance was recorded between
February and March 2008, and between April and
May 2009 with no records of occurrence between
(Mober and January in either year. The frequency
of occurrence of Collared Plovers was regular
and the species was recorded in all months. The
greatest abundance of this species occurred
between March and August, and was lowest
between September and February. A large part
of the increase in abundance beginning in March
was due to the presence of young of the year,
which were observed foraging in the w'ash zone
and near the drainage sandbars of lakes. Abun¬
dance was considerably higher in May, June, and
August 2008 than during the same period in 2009.
TABLE 2. Frequency of occurrence (C) of shorebirds from October 2007 to September 2009
Orande do Sul, southern Brazil.
Oct 2007 to Sep 2008
Oct 2008 to Sep 2009
Specie*
c
Constancy
C
Constancy
c
Southern Lapwing
1 00
Regular
100
Regular
100
American Golden Plover
8
Occasional
33
Sporadic
21
Grey Plover
58
Constant
83
Regular
71
Semipalmated Plover
33
Sporadic
50
Regular
42
Collared Plover
100
Regular
UK)
Regular
100
Rufous-chested Plover
8
Occasional
8
Occasional
8
Uudsonian Godwii
0
Absent
8
Occasional
8
'A'himbrel
0
Absent
33
Sporadic
17
Solitary Sandpiper
33
Sporadic
17
Occasional
25
Greater Yellowlegs
50
Regular
67
Regular
58
^csser Yellowlegs
83
Regular
92
Regular
88
Ruddy Turnstone
67
Regular
58
Regular
63
Red Knot
67
Regular
33
Sporadic
58
Sanderling
100
Regular
100
Regular
100
Semipalmated Sandpiper
8
Occasional
8
Occasional
8
vvhiic-rumped Sandpiper
83
Regular
67
Regular
75
Ruff-breasted Sandpiper
8
Occasional
8
Occasional
8
2007 to 2000
Constancy
Occasional
Occasional
44
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. I. March 2012
FIG.
do Sul.
2007-2009 2007-2009
2007-2009
20
18
16
• 14
Jl2
fio
< 8
6
4
2
0 •
Solitary Sandpiper
J
ONDJFMAMJJAsONDJFMAMjJAS
2007-2009
^ 2007-2009
. southern Brazil. *" °* shorehirds sPecies from October 2007 to September 2009 on the coast of Rio Grande
Scherer and Petry • SEASONAL VARIATION IN SHORE BIRD ABUNDANCE
45
2007-2009
80
70
60
ti
v
=50
v
=40
£
<30
20
10
0
Ruddy Turnstone
111
ONDJ FMAMJJASONDJFMAMJJAS
2007-2009
2007-2009
F,G- 3. Continued.
The frequency of occurrence of Whirabrels
l ‘'Wnu« phaeopus) was occasional as the
species was absent in 2007/2008 and sporadic in
-008/2009. The greatest number of individuals
■v*» recorded in November 2008 (n = 6) and May
-009 i/i = 9) only one individual was observed
in«»ch of two other months. Solitary Sandpipers
'Thnga solitaria) occurred sporadically in 2007/
4*08 and occasionally in 2008/2009. This spe-
c*es had no clear tendency of occurrence, but was
2007 - 2009
recorded in two consecutive months (Nov and
Dec 2007) with greatest abundance (n = 18) in
November 2007.
The frequency of occurrence of Greater Yel-
lowlegs (T. melanoleuca) was regular over both
years. The greatest abundance occurred between
May and September with a peak in July 2008 tn =
16) and in September 2009 (n = 16). This species
exhibited abrupt variation from one month to the
next as observed in May. June, and July 2008 w ith
46
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124. No. 1. March 2012
13, 1, and 16 individuals observed, respectively.
December. March, and April were the only
months in which there were no records of this
species. The frequency of occurrence of Lesser
Yellowlegs was regular over both years with
greatest abundance between May and October,
and lowest between December and April. Abun¬
dance beginning in May 2008 increased the
following month and then decreased until Sep¬
tember with a significant increase in October
2008, reaching 270 individuals before rapidly
declining in November. This species was absent in
October and November 2007. and April 2009.
Ruddy Turnstones (Aren aria interpret,) were
regularly observed every month of the 2-year
period, and had low abundance ranging from one
to six individuals. However, 15 individuals were
observed in December 2007 and the greatest
abundance occurred in April 2009 with 70 in¬
dividuals distributed among three flocks of 30, 15.
and 25 individuals spatially separated I and 7 km
from one another, respectively.
The Red Knot was the ihird most abundant
species and was observed regularly in the first
year and sporadically in the second year. The
greatest abundance occurred between April and
September with uneven distribution among the
remaining months of the year. Monthly abundance
in 2008 ranged from 1,669 individuals in April to
96 individuals in May, and rising in June and July.
A considerable number of individuals (/? = 322)
was recorded in April 2009. but only four were
observed in May, none in June or July, before
becoming abundant in September (n = 1.562).
This species w'as absent in December and March
with only one individual recorded in February
2009, two individuals in October 2007, and two in
January 2008. Thirty-eight and 71 Red Knots
were observed in June and July 2008, respective¬
ly; some were in nuptial plumage while in flocks
with non-breeding plumage birds, which were
likely not migrants that year.
The Sanderling was the most abundant species
with regular frequency of occurrence. The greatest
numbers occurred between September and April
with an abrupt increase and decline at the be¬
ginning and end ol this period. Peaks (// = 5.943)
were recorded at the beginning of the austral
summer (Nov 2007) and beginnine (n = 10 757)
of theifus>™' winter (Apr 2008); the same pattern
in °C'0ber 2I,0H = s-2%' and
Apr.! 2009 („ = 9,759). The lowest abundance
occurred between May and August, and flocks
most likely consisted of non-breeding immature
individuals. The lowest numbers were recorded in
July (n = 1) and August (// - 3) 2008.
The frequency of occurrence of White-ramped
Sandpipers was regular and this species was the
second most abundant. This species also had two
yearly peaks of abundance with largest numbers
in November 2007 (n = 1,204) and March 2008
(n = 1,060). and in August 2008 ( n = 561) and
February 2009 (n = 1,012). This species was
absent in May. June, and July in both years.
DISCUSSION
The presence of 1 7 species of shorebirds, some
highly abundant, confirms the importance of the
beaches (Balncario Pinhal to Mostardas) on the
coast of Rio Grande do Sul State (southern Brazil)
as stopover and wintering sites for migratory
shorebirds. Fourteen species of shorebirds record¬
ed in the present study were migratory that breed
in the Northern Hemisphere. These shorebirds use
the beaches of Rio Grande do Sul as stopover or
wintering areas for feeding and resting, mainly
between October and April. This period coincides
with greater availability of macroinvertebrates
along the beaches and banks of coastal lakes
( Lara-Resende and Leeuwenberg 1987). when
lower water levels allow greater foraging area.
The number of shorebirds was lowest between
May and September when most populations
migrate to breeding areas in the Northern
Hemisphere. However, a small number of repro-
ductively immature juveniles (Semipahnated Plo¬
ver. Greater Yellowlegs, Lesser Yellowlegs. Red
Knot, Sanderling, and White-rumped Sandpiper)
remain on the beach throughout the austral winter,
as has also been reported for beaches in northern
and northeastern Brazil ( Azevedo-Jtinior and
Larra/abal 1994, Azevedo-Junior et al. 2001a. b:
Barbicri and Mendon^a 2005. Barbieri and
Hvenegaard 2008).
1 he most frequent and abundant species on the
beaches between Balncario Pinhal and Mostardas
were Sanderlings, White-rumped Sandpipers, and
Red Knots. These species have previously been
recorded on other beaches of Rio Grande do Sul
( Lara-Resende and Leeuwenberg 1987. Vooren and
Chiaradia 1 990). The Rio Grande do Sul beaches ate
among the most important wintering areas on the
Atlantic Coast of South America for Sanderling1'
(Morrison and Ross 1989). The three species are
highly abundant in Lagoa do Peixe National Park
(Lara-Resende and Leeuwenberg 1987), using the
Scherer and Petry • SEASONAL VARIATION IN SHOREBIRD ABUNDANCE
47
area as either a wintering site or stopover point for
the part of the population that winters in areas
further south, such as Tietra del Fuego (Harrington
et al. 1986. Morrison et al. 200), Piersma 2007).
Nine species had a regular frequency of
occurrence over the 2-vear period, whereas other
species occurred occasionally and in low abun¬
dance (Rufous-chested Plover. Hudsonian God-
wit. .Semipalmated Sandpiper, and Buff-breasted
Sandpiper). The Rufous-chested Plover is an
austral winter visitor from Patagonia, where it
breeds (Belton 2000). This species occurs in low
abundance on the beaches of southern Brazil
lLara-Resende and Leeuwenberg 1087, Vooren
and Chiaradia 1990, Belton 2000) and Argentina
iBIanco et al, 2006). Hudsonian Godwits occur
throughout the year in Lagoa do Peixc with
highest abundance in November during its
migration south (up to 1.300 individuals) and in
March prior to migration north (Lara-Resende and
Leeuwenberg 1987). Up to 3.000 individuals have
been recorded at the site (Harrington et al. 1986.
Morrison and Ross 1989). This species is highly
sensitive to disturbed environments (Parker et al.
19%) and is rarely seen on beaches with people
and vehicles. The Semipalmated Sandpiper occurs
with low frequency and abundance in southern
Brazil (Lara-Resende and Leeuwenberg 1987,
Vooren and Chiaradia 1990. Costa and Sander
-(||)8), but is frequent and abundant on beaches of
northern and northeastern Brazil, where it winters
Morrison and Ross 1989, Azevedo- Junior et al.
20Ulb, Telino-Junior et al. 2003, Barbieri 2007).
The Buff-breasted Sandpiper is considered
endangered (BirdLife International 201 i ) and
0CCUrs in wet grassland areas and grazed
pasturelands near lagoons (Lara-Resende and
Leeuwenberg 1987. Lanctol et al. 2002). This
species generally migrates through the interior
the continent, using the central Amazon/
Pantanal wetland route, where it follows large
rivers and wetlands until reaching Paraguay and
Argentina (Antas 1984). This explains the low
frequency and abundance on the beaches
between Balneario Pinhal and Mosturdas. where
11 recorded on only two occasions (Nov
2007 and Oct 2008).
The resident Southern Lapwing, which is
Cndemic to South America, was among the species
*rith regular frequency of occurrence and was
observed on all counts. This species is common in
grassland areas of Rio Grande do Sul. where it
breeds, and Belton (2000) considered its occur¬
rence on the shore as rare. It is observed with
greater frequency foraging on the beach near
sandbars with drainage of waters from lakes
between April and July: lower numbers are
observed between October and December when
this species is in its breeding season (Belton 2000).
The American Golden Plover had a lesser
frequency of occurrence and lower abundance
than the Grey Plover with greatest abundance
occurring between November and March, as
previously reported for wintering areas in south¬
ern Brazil (Lara-Resende and Leeuwenberg 1987,
Vooren and Chiaradia 1990). This species is
found mostly on beaches within the proximity of
Lagoa do Peixe (Morrison and Ross 1989) where
they encounter habitat with less direct influence
from humans and vehicles along the beach. The
Grey Plover had low frequency and abundance
along the beach throughout the year (Lara-
Resende and Leeuwenberg 1987, Vooren and
Chiaradia 1990).
The frequency of the Semipalmated Plover was
uneven with greater abundance in February and
March 2008, and April and May 2009. However,
this species has been observed in low abundance
in southern Brazil (Lara-Resende and Leeuwen¬
berg 1987, Vooren and Chiaradia 1990). It is more
abundant on beaches of northeastern Brazil, where
most of the population winters (Rodrigues 2000,
Telino-Junior et al. 2003, Barbieri 2007. Barbieri
and Hvenegaard 2008). The resident Collared
Plover, which breeds among the dunes along the
Brazilian coast, occurs throughout the year. Little
is known about this species. Its greatest abun¬
dance on the beaches between Balneario Pinhal
and Mostardas was between March and August.
This was during the breeding season, which
extends from November to January, when the
species is frequently found foraging near dunes
where it breeds, as well as throughout (he non¬
breeding season in the austral winter (Lara-
Resende and Leeuwenberg 1987, Belton 2000).
Juveniles were observed foraging in (he wash
zone and drainage sandbars of lakes in every
month of the year, but with a considerable
increase beginning in March and greater abun¬
dance in the subsequent months.
Whimbrel occurred in low frequency and
abundance. This species needs conserved envi¬
ronments due to high sensitivity to environmental
disturbances (Parker et al. 1996), The largest
flocks occur in the northern and northeastern
regions of Brazil , and northern portion of South
48
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 1. March 2012
America (Morrison and Ross 1989. Azevedo-
Junior and Larrazabal 1994. Azevedo-Junior et al.
2004). This species in southern Brazil is only
observed foraging in small numbers in Lagoa do
Peixe (// < 8) (Lara-Resende and Leeuwenberg
1987) and in the surrounding beaches.
Solitary Sandpipers were observed sporadically
and in small numbers along the beach, as reported
by Costa and Sander (2008) on other beaches in
Rio Grande do Sul. Greater Yellowlegs were
observed regularly in both years as reported by
Lara-Resende and Leeuwenberg (1987) with
peaks of abundance in July and September, but
was much rarer than Lesser Yellowlegs. Many
non-migrating individuals of Greater Yellowlegs
that winter in interior areas of the state, according
to Belton (2000). concentrate on the beach during
the austral winter. Lesser Yellowlegs are recorded
in every month of the year in Rio Grande do Sul.
appearing rarely during the austral winter and
more commonly from September to March
(Belton 2000). However, we found the species
was more abundant between May and October
and was rare between November and April. Those
observed from May to July were likely flocks of
juveniles that had wintered on the beaches and
lakes in the interior of Rio Grande do Sul and then
concentrated on the coast. The greatest abundance
in October coincides with migration to South
America with the species using beaches and lakes
as either wintering or stopover areas. Lesser and
Greater yellowlegs were observed foraging on the
banks of small lakes near dunes and drainage
sandbars of these lakes and. at times, in the wash
zone.
The Ruddy Turnstone is common along the
coast of the Province of Buenos Aires (Myers and
Myers 1979. Blanco et al. 2006) during the austral
summer. We found low abundance of this species
on the beaches from Balneario Pinhal to Mostar-
das with greater frequencies occurring between
April and July, and between September and
December. This has also been reported in previous
studies (Harrington et al. 1986, Lara-Resende and
Leeuwenberg 1987. Voorcn and Chiaradia 1990).
This indicates that small groups stop to feed and
rest during migrations south and north between
wintering and breeding areas in Argentina and the
Northern Hemisphere, respectively.
The pattern of occurrence of the Red Knot
corroborates that observed at other sites in
southern Brazil (Lara-Resende and Leeuwenberg
1987, Vooren and Chiaradia 1990). The greater
abundance in September indicates arrival of
migrants from the Northern Hemisphere moving
toward wintering areas in Patagonia and Tierradel
Fuego. This species use the lakes and beaches of
Rio Grande do Sul as stopover areas for feeding,
resting, and molting. A few individuals remain in
winter and join flocks that stopover in April on
return to breeding areas in the Northern Hemi¬
sphere. The stopover period on the beaches from
Balneario Pinhal to Mostardas is short, but of
considerable importance to the migratory process
between the extremes of the two hemispheres
(Piersma 2007). This beach serves as one of the
most important stopover sites during the molting
process and for gain in body mass (Mormon and
Ross 1989, Vooren and Chiaradia 1990).
The regular frequency throughout the year and
high abundance of Sanderlings confirms the bea¬
ches of Rio Grande do Sul are one of the mow
important wintering areas for this species along
the Atlantic Coast of South America (Harrington
el al. 1986. Lara-Resende and Leeuwenberg 1987,
Morrison and Ross 1989, Myers et al. 1990i.
Large flocks begin to arrive in September with
peak abundance in October and a decrease in
the following month as the areas are used as a
stopover site during migration farther south to
wintering areas. The abundance of Sanderlings
remains stable from November to February
because of individuals that winter in the area,
decreases from February to March, when these
same individuals begin to migrate north, and
reaches its largest peak in April, when those that
wintered to the south (Argentina and Patagonia1
again use the site as a stopover, and declines in
May. We found the species in greater densities
than at other sites in southern Brazil (Vooren and
Chiaradia 1990. Costa and Sander 2008). indicat¬
ing greater availability of food resources on these
beaches and lower human impacts.
White -rumped Sandpipers occurred in number*
and pattern of occurrence similar to that of the
Red Knot. This species is reported in Lagoa ck
Peixe to be highly abundant between November
and January, both on the lake and the beach (Lara-
Resende and Leeuwenberg 1987). and part of the
population uses the site as stopover and wintering
areas (Morrison and Ross 1989). The greater
abundance occurs at the beginning of the austr.il
summer with arrival of migrants from !h<
Northern Hemisphere to winter in Lagoa do Pci'1'
and Argentina, where they are abundant through
out the austral summer (Myers and Myers 1979. 1
Scherer and Petry • SEASONAL VARIATION IN SHOREBIRD ABUNDANCE
49
Lara-Resende and Leeuwenberg 1987, Morrison
and Ross 1989. Blanco et al. 2006). We observed
a few individuals on the beaches from Balneario
Pinha] to Mostardas during the austral summer
with abundance increasing at the beginning of the
austral autumn (Mar and Apr), when the popula¬
tion returns from wintering areas on migration to
North America. This indicates the importance of
these beaches for stopover and feeding sites prior
to migration.
CONSERVATION IMPLICATIONS
Knowledge of stopover and wintering areas is
critical to the conservation of migratory shore-
birds. as these sites require special care (Lara-
Resende and Leeuwenberg 1987, Myers et al.
1990) through an internationally coordinated
effort directed al protecting breeding, stopover,
and wintering areas (Morrison 1984, Morrison
et al. 2004). The beaches from Balneario Pinhal
to Mostardas in the Stale of Rio Grande do Sul
(southern Brazil) are used by large numbers of
shorebirds as stopover and wintering areas,
especially Sanderlings, White-rumped Sandpip¬
ers and Red Knots. Our study underscores the
importance of these beaches as priority areas for
implementation of conservation projects directed
at these shorebirds and serves as a basis for future
comparisons addressing the impact of environ¬
mental changes on these species (Piersma and
Lindsirorn 2004).
ACKNOWLEDGMENTS
Ihe authors are grateful to the Wildlife Conservation
s"ciei.v (WCS) for funding (his study (Contract « 2008005).
v L Scherer is grateful to the Brazilian fostering agency
1 'Vinlena^ao de Apcrfciyoamcnto de Pcssoal de Ensino
'jperior (CAPES) for a study grant awarded from the
1 digram a de Supoiie h Pds-Graduayao de InstituiyoCS de
Ensino Paniculares (PROSUP). We thank R. (i. de Mourn
11 'r help drawing Figure I. and S. M. A/cvedo-Junior and
L H. Oliveira for helpful comments and reviews.
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The Wilson Journal of Ornithology 1 24( 1 ):5 1 -56, 20 1 2
PLASTICITY OF HABITAT SELECTION BY RED-BACKED SHRIKES
{LANIUS COLLURIO) BREEDING IN DIFFERENT LANDSCAPES
FEDERICO MORELLI1
ABSTRACT.— Environmental parameters in different breeding habitats of Red-backed Shrikes ( Lanius collurio) in
central Italy were examined at altitudes ranging from 0 to 1.200 m. I he most suitable habitats lor breeding were. ( I )
cultivated areas with hedgerows, and (2) high altitude grasslands. Similar population densities were recorded in both
habitats (0.27 pairs/10 ha in farmland vs. 0.30 pairs/10 ha in meadows) and as were the number of fledged young per
breeding pair (3.38 in farmland vs. 3.75 in meadows). The structural characteristics of ‘open space' and 'edge density'
differed in the two breeding habitats. Use of species of trees and bushes for nesting depended on habitat type, but nests were
in die more abundant thorny shrubs (blackthorn | Primus spinosa) in farmland and juniper \Junipems communis | in
meadows). Red-backed Shrikes in farmland appear to prefer to nest in the most heterogeneous territories, those with the
presence of uncultivated areas and shrub patches. Plasticity of habitat selection by the species was evident. Reiei\ed _/
June 2011. Accepted 14 September 201 1
Characteristics of breeding territories of Red-
backed Shrikes ( Lanius collurio ) have previously
been described in a number of studies (Cramp and
Perrins 1993, Olsson 1995b. Lefranc and Worfolk
1997, Harris and Franklin 2000. Guerriere and
Castaldi 2006, Casale and Brambilla 2009). The
greatest density of breeding pairs in Europe is in
farmland ecosystems (Cramp and Perrins 1993,
Parkas et al. 1997, Golawski and Golawska 2007)
with these landscapes providing highly varied
ecological conditions for many bird species and
'beir prey (Golawski 2006). The Red-backed
Shrike has been shown to prefer agricultural
landscapes lhal are 'not intensively farmed' and
are characterized by reduced functional heteroge¬
neity. This is especially true when there arc
hedgerows and shrub patches that function as both
key hahitat for many plants and animals, and
wildlife corridors that enable dispersal and
movement between habitats (Vermeulen 1994,
Vcrmeulen and Opdam 1995).
Habitats used for breeding have an essential
n»le in the life-cycle of a bird, and many factors
van influence the selection of breeding territories;
two most important of which are minimization
of predation (Cody 1985. Martin 1995. Roos
-••021 and presence of adequate food (Martin
'^7, Cramp and Perrins 1993, Golawski and
Meissner 2008).
The Red-backed Shrike is considered a I arm-
land breeding species in the Marche Region ol
Cen*ra| Italy (Pandolfi and Giacchini 1995,
Forconi 2007. Morel I i et al. 2007). Hedgerows
Jrc a familiar feature of most farmlands, and were
OiSTcVA, University of Urbinp, Scientific Campus,
6j929 Urbino, Italy; e-mail: federico.morelli@uniurb.it
traditionally planted as boundaries by both
farmers and townspeople, albeit for different
purposes. Currently, in areas which once had
much greater coverage, they arc now only present
as residual boundary lines of trees and shrubs, and
are slightly >20 m in length and <5 m in width.
Recent censuses indicate that Red-backed Shrikes
may, however, use other habitat types for breed¬
ing in the Marche Region of central Italy (Forconi
2007, Morelli et al. 2007).
Detailed information about habitats and eco¬
logical requirements of a species is needed if it is
to be successfully conserved. This is especially
true for the Red-backcd Shrike which, except for
a few areas of relative stability (PEC'BMS 2009),
has experienced a marked population decline in
western and northern Europe over the last three
decades. The Italian population has been esti¬
mated at 50,000 lo 120,000 reproductive pairs
(Birdlife International 2004), but with a negative
trend (Meschini and Frugis 1993, Pandolfi and
Giacchini 1995, Dinetti 1997).
The causes of this decline are poorly under¬
stood. and it has been suggested that reduction
in suitable habitats, habitat modifications, use of
intensive agriculture systems, decline in food
resources, and climatic changes are the main
reasons (Tucker et al. 1994. Yosef 1994, Fuller
et al. 1995). Rapid changes in agricultural
ecosystems can result in the loss of a bird species
in just a few years. Thus, it is important lo
examine the ability of a species to colonize and
breed in areas other than agricultural farmland.
This is because the capacity to breed or forage in a
greater number of habitat types can improve the
survival potential of birds which settle in a
territory that includes an optimal proportion of
51
52
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 1. March 2012
habitats suitable for successful breeding and
survival (Soderstrom 2001, Golawski and Meiss¬
ner 2008).
My objectives were to examine one population
ot Red-backed Shrikes breeding in high altitude
meadows (>900-1,100 m asl) and another in low-
hill farmlands to compare environmental charac¬
teristics of these two habitat types.
Methods
Study Area. — The study was conducted during
2009 in the Marche Region of central Italy, which
is characterized by a temperate climate, high
spring and summer temperatures, and a marked
summer drought (Tomaselli et al. 1972). The
study area contained two breeding zones of
5,573 ha total (farmland: 43° 47' 27.81" N, 12"
39 39.91 E; 4,975 ha; high altitude meadows:
43" 37' 51.84" N. 12 45’ 48.18" E; 598 ha).
Monitoring Frequency.— The study area was
monitored for breeding Red-backed Shrikes every
5 days from early May to mid-July 2009.
Occupied territories were surveyed at least once
every 3 days during the breeding period to find
nest sites (Bibby et al. 1997). Red-backed Shrikes
are particularly sensitive to disturbance during
nest building, egg-laying, and early incubation
(Olsson 1995a. Tryjanowski and Kuzniak 1999),
and the number of visits to each nesting site was
kept to a minimum. Location of each nest site
was recorded using a Global Positioning System
(GPS) and numbers of fledged young per pair near
a nest were recorded. The density of Red-backed
Shrike territories in the two habitat types was
calculated as breeding pairs per 10 ha.
Environmental Parameters.- The typical size
ot a Red-backed Shrike territory varies from I-?
to 5-6 ha (Cramp and Perrins 1993. Lefranc I993~
Olsson 1995b. Harris and Franklin 2000). A 3-ha
territory size around the nest site was standardized
to enable territory preferences to be studied
ArcGIS 9 software (ESR1 2009) was used to
delineate a polygon with a 100-m radius around
(AAVV w'„fnd a llmd'USC "'ap ":l0-00<»
I i ." .' ) was llsccl to characterize the
habitat in the polygons.
The environmental parameters studied for each
nest site were: (1) nest shrub: the plant species
where breeding pairs placed their nest and w e
very high (>5() items); (3) the altitude of the
nesting site (m above sea level); and (4) com¬
position and percentage of land-use types around
the nesting area (cultivated, uncultivated vine
yard, shrub, forest, reforestation, grassland, river,
buildings, and roads)
The features and structural characteristics
studied for each nest site were: ( I ) ‘open space'
around the nesting site: percentage of cover of
roads, grasslands, uncultivated land, and shrubs:
(2) 'edge density' as the sum of the perimeters of
all polygons in the buffer zone per number of
land-use types/ 1 00 (as a surrogate of the habitat
fragmentation level in the buffer zone); (3) road
type (paved, unpaved); (4) distance from the
nearest road (m); and (5) distance to the nearest
building (m).
Statistical Analysis. — Differences in the plani
species used for nesting in the two habitat type-'
were compared with Chi-square tests using
standardized residual analyses to highlight the
associations of plant species with habitat tjpes. A
Mann- Whitney U- test was also performed to ex¬
amine differences in environmental parameters of
breeding sites in farmland areas versus those in
high altitude meadows. The structural cbaiacler-
islics (open space and edge density) between the
two habitats were further compared with a Chi-
square test.
I also performed a logistic regression analysis to
identity which variables best explained the pre¬
sence or absence of Red-backed Shrikes in the
farmland study area. Presence and absence of
active nests were used as response variables, while
composition and percentage of land-use types
around the nesting area, structural characteristics,
and road and building distance were the explana¬
tory variables. Internal validation was performed
by calculating the non- parametric confidence
interval of the AUC (Area Under the Curve1
values. The AUC generally ranges from 0,5 lor
models with no discrimination ability to 1.0 l°r
models with perfect discrimination. Data are pre¬
sented as means ± SE and all tests were conducted
with SPSS lor Windows software. Version I ■ 11
(® SPSS Inc.. Chicago. 1L. USA. www.spss.com
RESULTS
I monitored and characterized 150 Red-backed
Shrike nest sites in two breeding zones: 132 m
farmland (mean altitude = 347.2 ± 138.8 m asl) and
1 8 in high altitude meadows (mean altitude = 837.6
— 1 15.5 m asl) (Fig. 1). The density o! breeding
Morelli • HABITAT SELECTION BY RED-BACKED SHRIKES
53
FIG. 1. Nest site localization in two different Red-backed Shrike breeding habitat types.
pairs per 10 ha was 0.27 for farmland and 0.30 for
high altitude meadows, respectively. The number of
fledged young per pair was similar in the two
habitats: 3.38 ± 1 .05 (n = 31) for farmland and 3.75
- A-86 (// = 12) for meadows. These differences
were not significant (U = 148. P = 0.282).
Plant Species Used as Nest Sites.— AW nest
sites were in shrubs. Plant species used differed in
the two breeding habitats (xJ - 71.3, P < 0.05)
'■'•ith blackthorn ( Prumis spinosa) being most
t48.5% ) used in farmland followed by dog rose
canirue, 25.8%), elm-leaf blackberry (Paints
*lnifolius\ 12.1%). and common hawthorn
t Crataegus monogyna ; 8.3%) (Table 1). Plant
■species used most frequently in high altitude
meadows were juniper (Juniperus communis ;
50%), blackthorn (22.2%), elm-leaf blackberry
(11.1%). European beech ( Fagus sylvaticcr,
I 1.1%), and dog rose (5.6%) (Table 1).
Land-use Cover in Farmland and High Altitude
Meadow Breeding Sites.— The percent cover of
the types of land-use around nest sites differed
between the two breeding habitats studied. Up to
six habitat types (mean = 3.7) were recorded for
farmland with cultivated land, shrubs, and grass¬
land dominating (Table I). Five habitat types
(mean = 2.9) were recorded in meadows, where
grassland and forest prevailed (Table 1).
Characteristics and Structural Differences Be¬
tween Breeding Habitats.— Open space and edge
TABLE 1. Plant species used for nest sites by Red-backed Shrikes in farmlands and high altitude meadows in
central Italy. _
Farmland High altitude meadows
Species
Name
n
%
Abundance
n
%
Abundance
Clematis vitalha
Clematis
3
2.3
Low
Cnaagus monagxna
Common hawthorn
11
8.3
Medium
Pvgus sylvatica
Beech
2
11.1
Low
hmipena communis
Juniper
9
50.0
Very high
1 11 Hums spina-christi
Christ’s thorn
1
0.8
Very low
Paimis spinosa
Blackthorn
64
48.5
Very high
4
22.2
Medium
fobinia pseudoacacia
Black locust
1
0.8
High
R°sa canina
Doe rose
34
25.8
High
I
5.6
Medium
Rubus ulmifolius
Elm-leaf hackberry
16
12.1
High
2
11.1
Medium
Sambucus nigra
Elderberry
2
1.5
Medium
54
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. I. March 2012
TABLE 2. Characteristics ot environmental parameters of farmland and high altitude meadows used by Red-backed
Shrikes for breeding in central Italy.
Characteristics
Farmland (n = 132)
Meadows (n = 18)
u
p
Building, %
Cultivated. %
Vineyards, %
Forest. %
Grasslands, %
Uncultivated and shrubs, %
Water. %
Roads, %
Landuse categories, number
Near road, m
Near building, m
3.4 ± 6.8
57.4 ± 26.1
0.9 ± 3.6
6.7 ± 13.2
14.2 ±21.5
1 1.0 ± 19.9
0.3 ± 1.4
6.0 ± 3.2
3.7 ± 1.2
30.6 ± 43.7
186.4 ± 136.7
0.8 ± 2.6
2.4 ± 3.9
0.0 ± 0.0
27.6 ± 28.4
65.2 ± 27.9
0.6 ± 2.1
2.2 ± 8.4
1.2 ± 2.6
2.9 ± LI
145.6 ± 123.6
781.6 ± 475.2
862.0
64.0
1.080.0
490.0
189.0
818.5
1.052.5
362.0
692.5
369.5
355.5
0.028
0.000*
0.184
0.000*
0.000*
0.016
0.070
0.000*
0.003*
0.000*
0.000*
* Significant at P < 0.01.
density values differed between the two areas used
for breeding (Z2 = 47.3, P < 0.05). The percentage
of open space in high altitude meadows (67.0 ±
28.2%) was higher than in farmland (31.3 ±
26.5%). In particular, the main types of land-use
cover functioning as open space in farmland were
roads, and uncultivated land, while in meadows the
main type was grassland. The edge density value in
farmland (93.4 ± 45.8) was higher than in meadows
(50.9 ± 54.3).
There were significant structural differences
between the two habitats in terms of distance of
nests from the nearest road and building (the
shortest distance was in farmland) (Table 2). The
model produced using stepwise logistic regression
analysis was based on 35 nest sites selected at
random from the farmland breeding habitat and 35
other sues where the species had not been present
Oeal absence) within the same studied farmland
Only five variables had a substantial effect on
probability of the occurrence of the species in
farmland (Table 3). These were: edge density
open space, uncultivated land, and shrubs forests’
and grassland. The first three had a positive effect
on the probability of the occurrence of Red-
backed Shrikes, whereas the other two had a
marginally negative effect.
DISCUSSION
Red-backed Shrikes seem to be much more cc
mon ,n low-altitude farmland than in mount
environments in the Marche Region of central It
(FoKon, ,007. Morel li and Pandojfi 2009. Mon
-01 la), as is also the case in other parts oft
country. However, the results of my study indie-
•bat Red-backed Shrikes can us/very 7fte
environments and select, if available, high meadow
areas for nesting.
1 he two populations studied were in very dif¬
ferent altitude zones with farmland birds breeding
at a mean elevation of 350 m. while the mea¬
dow- population was at an elevation >800 mask
However, population densities of shrikes were
similar in both areas, as were numbers of fledged
young per pair.
1 hese results highlight the ecological plasticity
of Red-backed Shrikes in selecting breeding
habitats, as this species can use different types
ol landscape in central Italy for breeding. This
suggests these two habitat types meet the eco¬
logical requirements of Red-backed Shrikes.
Farmlands where Red-backed Shrikes were
detected were characterized by higher landscape
heterogeneity (edge-density values, roads and
buildings in the vicinity), reducing risks from
predators or providing natural hunting perches
(Lefranc 1993, Yosef and Grubb 1994, Lefranc
and Worfolk 1997, Bechet et al. 1998, Tryjanow-
ski et al. 2000. Roos 2002. Roos and Part 2004 1
Variables that appear to have made a major con¬
tribution to the suitability of farmland as breeding
TABLE 3. Logistic regression of presence and absence
ol breeding Red-backed Shrikes in farmlands (only
significantly associated
variables are
shown).
Variable
B
SE
P
Edge density
0.05
0.012
<0.001
Open space
45.12
17.67
0.01 1
Uncultivated and shrub
1.13
0.525
<0.001
Forest
-1.12
0.436
0.012
Grassland
-21.42
9.21
0.05
Morelli • HABITAT SELECTION BY RED-BACKED SHRIKES
55
habitat for Red-backed Shrikes were edge density,
which indicates a certain functional heterogeneity
i Benton et al. 2003), open spaces, uncultivated
land, and shrubs for nesting. In contrast, the spe¬
cies does not seem to favor farmland with forest
patches or grassland cover.
Meadows frequented by Red-backed Shrikes
were less fragmented than the farmland. They also
contained virtually no roads or building structures,
but abundant shrubs were uniformly distributed
across open grasslands. These high altitude
meadows can provide another important resource
to maximize foraging ecology of shrikes in the
increased availability of 'open space', as open
grasslands at high altitude are optimal for finding
and capturing prey (Fernandez-Juricic et al. 2004,
Golawski 2006. Morelli 2011b). Recent studies
reveal that meadows, in comparison with other
habitat types, support the highest number and
biomass of invertebrate prey of Red-backed
Shrikes (Golawski and Meissner 2008).
‘Open space’ had different features in each type
ol breeding habitat (mainly roads in farmland and
grassland in meadows). The Red-backed Shrike
used different kinds of shrubs in which to nest and
perch in the two habitats; generally, the most
abundant, suitable species (blackthorn in farmland
and juniper in meadows).
These characteristics, which highlight the Red-
backed Shrike's relative ecological plasticity,
C0l,ld be important when defining 'suitable
habitat’ and ‘habitat availability' for the species,
ihese findings should be used to identify new
potential breeding sites and expansion areas for
Red-backed Shrikes in central Italy. Future studies
focused on breeding success of shrikes in different
habitat types may be necessary if wc are to obtain
reformation required to understand the biological
requirements of this species. This information
lna> have an important role in the success ol bird
conservation programs (Hoffmann and Greet
Salem 2003, Morelli et al. 2007).
ACKNOWLEDGMENTS
Wc 'bank Maurizio Saltarelli and Chiara Tagnani for
*lelp in the field, and Marco Girardello and Maria Balsamo
1('r valuable suggestions on ihc text. A special note ot
’banks is owed to the anonymous reviewers lor suggesting
'■Veral improvements in the original manuscript.
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The Wilson Journal of Ornithology 124( 1 ):57-65, 2012
TERRITORY DISTRIBUTION AND HABITAT SELECTION OF
THE SERRA FINCH ( EMBERNAGRA LONGICAUDA ) IN
SERRA DO CIP6, BRAZIL
GUILHERME H. S. FREITAS' 2 AND MARCOS RODRIGUES'
ABSTRACT.— The near-threalened Serra Finch ( Embemagra longicauda) is restricted to the main mountain ranges in
eastern Brazil inhabiting compos rupestres (rocky fields). We mapped 17 mated pairs in a 138-ha area within Serra do Cipo
National Park; a density of 0.25 adults/ha. Estimated average territory size varied from 2.52 ± 0.77 ha (95% kernel ) to 3.35
• 0.90 ha f 100% minimum convex polygon). The distance between territory centers of neighboring pairs was 162.38 ±
28.93 m, The overlap between neighboring territories was 15.3 ± 5.9% (95% kernel) and 2.0 — 2.3 r (polygon metho ).
Pairs remained together throughout the year in the same territories and defended these against intruding neighbors.
Analyses of habitat selection indicated preference for woodland and scrubland habitats associated with humid valleys, whi e
grasslands were avoided The Serra Finch used the available habitats more than expected from random at ditferent spatial
sales. Our data identified habitats that should be priority for conservation of the Serra Finch. Received 8 Septan er _
•T cepted 24 September 201 1.
The Serra Finch ( Embemagra longicauda) is a
poorly understood species, known for more than a
century based on only two specimens from an
unspecified locality in South America (O’Brien
l%S. Mattos and Sick 1985). Recent studies have
found it to be restricted to mountaintops in eastern
Brazil, mainly in the states of Minas Gerais and
Bahia, and particularly Hie Espinha^o Range,
Sena da Mantiqueira and Serra do Caparad
iVasconcelos 2008). This species may be easily
observed on mountains above 900 m. frequenting
habitats on quartzite, gneiss, and iron rich soils.
Thus species typically places its nest on rocky
outcrops (Hoffmann et al. 2009, Rodrigues et al.
tends to forage in pairs for arthropods and
B«hy fruits among herbs, grasses and bushes
'Hoffmann et al. 2009). and pairs arc known to
Ning a duet < Freitas and Rodrigues 2007), a typical
behavior of territory defense (Catchpole and
Slater 1995).
The Serra Finch has been categorized as near-
Oireatened due to a perceived population decline
possibly resulting from significant habitat loss,
primarily due to cattle ranching, land conversion,
and intensive mining activity (BirdLife Interna-
honal 2011). Thus, there is a need of focused
ecological studies of the species to identify its
Habitat requirements (Stotz et al. 1996. BirdLite
International 2011). Accurate assessment o!
' Gboratorio de Ornilologia, Departamenlo de Zoologia.
H'tiiuto dc Ciencias Biological, Univcrsidade Federal de
Minas Gerais, CP 486. 31270-901. Bclo Horizonte. Minas
Gerais. Brazil.
Corresponding author;
e'ma‘l: guilhermehsfreitas@gmail.com
habitat requirements, population size, and den¬
sity are paramount to undertaking any successful
conservation measures (Bibby et al. 2000). The
objectives of our study were to: (1) quantify and
map all territories of Serra Finches in a study site
within Serra do Cipo National Park in south¬
eastern Brazil, and (2) identify specific habitats
favored by this species.
METHODS
Study Aren. — Our study was conducted in a
138-ha area near Indaifi Stream, in the ’Alto do
Palacio’ region (19 15' S, 43 31' W) in the
northern part of Serra do C’ipo National Park in
the southern portion of the greater Espinha^o
Range of southeastern Brazil (Fig. I). Alto do
Palacio is near the ridge of the eastern slope of the
Serra do Cipo Mountains at an altitude of 1 .280 to
1,380 m. This region is humid throughout the
year, even in the dry season, and is characterized
by frequently misty weather conditions (Ribeiro
et al. 2009); the bird community is closely
associated with the Atlantic Forest (Rodrigues
et al. 2011).
The study area is a mosaic of habitats traversed
by numerous small valleys. Seven habitats were
identified. (I) Rocky outcrops, referring to areas
wilh soils derived from quartzite, that are domi¬
nated by several species of herbs, shrubs (such as
Bromeliaceae. Orchidaceae. Velloziaceae. and
Cactaceae), and small trees up to 3 in in height,
including Eremanthus erythropappus and E. cro-
tomides ( Asteraceae). (2) Dr y grasslands, domi¬
nated by Lagenocarpus tenuifolius (Cype raceae),
Panicum lore um (Poaceae). and Paepa Ion thus spp.
57
58
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 1. March 2012
(Eriocaulaceae). (3) Wet grasslands, dominated I
Lagenocar/ius rigidus in marshy areas close
watercourses. (4) Dry scrubland, which has son
plants that also occur in the rocky outcrop habit:
but which is dominated by Coccoloba acrosi
choides (Poligonaceae) and Aulonemia effic
(Poaceae) in sandy soil with substantial gravel
some hilltop areas. (5) Wet scrubland, dominate
by small trees up to 2 m in height, such ;
Tibouchina spp., Lavoisiera imbrkata (Melasti
mataceae), and Baccharis ilatiaiae (Asteraceae) i
marshy areas. (6) Riparian woodlands, charactei
■zed by dense vegetation and dominated by 4 t
10-m tall trees including Miconia chartace,
(Melastomataceae) and Hololepis peduncular
(Asteraceae). (7) Candeial , a specific formatioi
of dense groups of 3 to 5-m tall Eremanthm spr
(Asteraceae) trees, known as ‘candeia’. The tern
dry is not associative of arid conditions bu
differentiates from saturated soil conditions of the
wet habitats.
processing individuals (—80 hrs), and locating
birds.
We captured Serra Finches using mist nets and
banded each with unique combinations of colored
leg bands to allow individual identification and
numbered metal leg bands supplied by Centro
Nacional de Pesquisa para Conserva^ao de Aves
Silvestres (CEMAVE/IBAMA. license # 1 161/3
and I 161/5). Surveys were conducted throughout
the study area. Locations of Serra Finches were
recorded using a hand-held Garmin (Olathe. KS
USA) global positioning system (GPS) unit lo
within 9 m accuracy. All GPS locations corre¬
spond to pairs because finches were always
detected in pairs. Locations were recorded every
H> m of a pair's movements (not caused by
observer presence) until lost from view. Habitat
type was recorded where birds were observed.
Territory Distribution.— We took GPS loca¬
tions lor all marked and unmarked pairs detected
in the study area. Pairs were detected mainly
while singing a duet from a perch, which was
interpreted as evidence of a particular mated
pair's territory. Locations were recorded through¬
out the year (dry and wet seasons), as we did not
Freitas and Rodrigues • TERRITORY SIZE AND HABITAT USE OF SERRA FINCH
59
observe significant seasonal changes in spatial
distribution and general territory defense of mated
pairs. We performed spatial analyses using Arc-
View G1S Version 3.2 (ESR1 1998). The distance
between nearest neighboring pairs was calculated
from the arithmetic mean of the locations of each
mapped pair. We calculated the density of in¬
dividuals in the study area by mapping territories
■ Bibby et al. 2000).
Territory size was calculated using the Home
Range Extension Version 1.1 (Rodgers and Can"
1998) We used the following estimators: 95%
fixed kernel using the least-squares cross-valida¬
tion smoothing parameter (Worton 1989. Seaman
and Powell 1996): 50% fixed kernel for the core
areas (Powell 2000); and 100% minimum convex
polygon (MCP; Mohr 1947). We chose the kernel
method because it is the most recommended
(Laver and Kelly 2008) and MCP for comparison
because it is the most used and emphasized
the boundaries of space used (Kernohan et al.
2001), This is important for territory character
ization based on the concept of use of an exclusive
area ( Pitelka 1959). We measured territory size
only for pairs with >30 locations to avoid im¬
precision and bias in the size estimates (Seaman
ctal. 1999, Kernohan et al. 2001).
Habitat Selection.— Wo analyzed habitat selec¬
tion by comparing habitat use and that expected
based on availability. We used the described ha¬
bitat classifications for availability and delineated
habitats based on satellite images from Google
forth (2010) in combination with direct observa¬
tions iri the field and measured with X-tools
extension for ArcView Version 3.2 (ESRI 1998).
We calculated habitat selection using three
approaches. First, we compared the number ol all
$erra Finch locations within each habitat with the
Proportion of available habitats in the study area.
Lbi-square tests were used to evaluate the null
hypothesis that actual use of different habitat
'ypes is directly proportional to their availability
'Neu et al. 1974). Bonferroni confidence intervals
11 = 0.05) were calculated from the observed
Proportions of habitat use to identity which ha-
bitat types were selected (Ncu et al. 1974, Byers
and Steinhorst 1984). Second, we compared the
Proportions of habitat within the 95% kernel
territory boundaries to proportions of available
habitats in the study area (second-order habitat
election sens,, Johnson 1980). Third, we com¬
pared the proportion ol locations in each territory
10 the proportion of available habitats within the
95% kernel territory boundaries (third-order
habitat selection sensu Johnson 1980).
We used compositional analysis (Aebischer
et al. 1993) for the second and third-order
approach. This analysis used the Wilks' lambda
statistic test for overall differences in habitat use.
Comparisons of particular habitat types w'ere
made with paired /-tests (Aebischer et al. 1993)
if the Wilks' test suggested differential habitat
use. Significance was set at P < 0.05. Habitat
types were ranked from most to least selected
using a matrix of mean and standard deviation of
log ratio differences for all habitat types it
selection was significantly non random. Missing
values (zero) in the data matrix were replaced by
O.OOI. The minimum number ot individuals
needed for compositional analysis is six (Ae¬
bischer et al. 1993). Thus, all Sena Finches with
>10 locations were used and those with <10
locations were excluded from the analyses. Leban
et al. (2001) noted that compositional analysis is
primarily affected by the number of animals
sampled and did not vary much with number ot
locations (as few as 10 observations). We
conducted the habitat selection analyses using
Resource Selection for Windows, Version 1.0
(Leban 1999).
RESULTS
Territory Distribution.— Twenty-one individual
birds were marked with colored leg bands and 17
were relocated distributed among 1 1 mated pairs.
The four individuals not relocated included a
juvenile and three possibly adult floaters. Six
additional mated pairs of unmarked individuals
were also detected (during at least 2 different
days) occupying areas between some ot the
marked pair’s territories. Those pairs were
reliably identified because the adjacent pairs often
sang duets at the same time. Thus, at those
moments it was possible to hear up to three
different pairs. Territories of 17 total pairs were
mapped by 3 18 GPS locations in the entire 138-ha
area during the study period (Fig. 1). This was a
density of adults with established territories of
0.25 birds/ha or 0.12 pairs/ha. Distance between
territory centers was 162.38 ± 28.93 (range =
119.95-233.85 m. n = 17). Territory size
estimates (mean ± SD) of five pairs that were
located most often ranged from 2.52 ± 0.77 ha
(MCP) to 3.35 ± 0.90 ha (95% kernel) (Table I).
The area of common use between territories
(MCP) was 991.27 nr for pairs A (4.68% of
60
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 1. March 2012
TABLE 1 . Data for nine best sampled pairs of the Serra
Finch in Serra do Cipo National Park. Brazil. Values of
100% minimum convex polygon (MCP); and by 95% and
50% kernel in ha.
Bird pair
Number of
locations
Sampling
days
Sampling
period"
100%
MCP
95%
Kernel
50%
Kernel
A
43
6
435
2.11
3.29
0.85
B
57
14
412
3.30
3.62
1.02
C
52
9
273
2.68
2.84
0.63
D
44
6
168
3.09
4.69
1.16
E
14
3
32
0.78
2.66
0.75
F
13
3
113
1.46
4.87
1.23
G
30
4
169
1.42
2.32
0.55
H
12
3
1 12
1.24
4.78
1.15
K
16
4
169
0.88
1.85
0.40
Number of days elapsed between the first and the last locations.
territory) and B (3.00%), and 19.34 nr for pairs C
(0.07%) and D (0.06%) (Fig. I). The estimated
overlap in area between territories (95% fixed
kernel) was 7,204.59 nr for pairs A (20.72%) and
B ( 1 9.35%), and 3,673.5 1 nr for pairs C ( 1 3.09%)
and D (7.94%) (Fig. 2). The eore areas over¬
lapped for 1,155.62 m2 for pairs A (12.03%) and
B (10.99%), and did not overlap between pairs (’
and D.
approaches. Dry and wet grassland were essen¬
tially avoided by all individuals (Table 3), and we
excluded them from the compositional analysis.
The proportion of habitat use based on 95%
kernel territories in the second-order approach
was non random relative to that available in the
study area (A = 0.13, df = 4. X2 = 18.30, P <
0.05). A ranking matrix ordered the habitat types
in the sequence: wet scrubland > riparian
woodland > rocky outcrop > candeial > dr.
scrubland (Table 4). Serra Finch territories had
significantly more wet scrubland and nparian
woodland than dry scrubland.
Habitat use of territory locations versus 95%
kernels in the third-order approach significantly
differed from random (X = 0.20, df - 4. X: =
14.41, 11 < 0.05). The matrix ranked the habitat in
the order: candeial > riparian woodland > rocky
outcrop > dry scrubland > wet scrubland.
Candeial was significantly more used than rocky
outcrop, dry scrubland, and wet scrubland, the last
was significantly less used than riparian woodland
(Table 4).
DISCUSSION
We did not observe any changes in the
composition of mated pairs or in their territories,
indicating these birds have annual site fidelity and
a socially monogamous mating system. All pairs
were observed singing duets on perches, appar¬
ently defending their territories throughout the
year, even outside the breeding season. We
observed agonistic events („ = 4) on territory
boundaries, when two pairs stayed in close
proximity performing a unison duet, and ending
in a physical confrontation on two occasions. One
of those, between pairs A and B. occurred within
the MCP overlap area.
Habitat Selection.- The 3 1 8 locations recorded
in the habitat types were not distributed as
expected from availability in the study area (I1
< 0.001, x2 = 686.82, df = 6; Table 2). The
candeial. rocky oulcrops, wet and dry scrubland,
and riparian woodland habitats were used more
t an expected by chance as the proportions of
expected use were below the Bonferroni confi¬
dence intervals for observed use. Use of dry and
we grassland habitats was lower than what could
be expected by chance (Table ~>)
We used the location data of nine Serra Finches
which had >10 locations (Tables 1-3) to examine
hab,lat Wfecllon by (he .second and third orZ
territory Distribution. — The number ot —
Serra finches that we found is high compared
with other species that inhabit open areas in
central Brazil. Our results revealed higher densi¬
ties than 1 1 species studied by Braz (2008).
including the closely related Black-masked Finch
( Cotyphuspiza melanntis) (0.23 individuals/hai
and Wedge-tailed Grass Finch [Emberizoides
Iwrbicola) (0.15 individuals/ha). Silva (2008)
reported 1 1 individuals/ha for Serra Finch. Hoff¬
man (201 1 ) estimated a density of 0.44 ± 0.08
individuals/ha for Gray-backed Taehuri ( Polystic ■
tus supereiliaris). a tyrant-flycatcher with a range
distribution similar to the Serra Finch (Vasconce-
los 2008). Population density is highly dependent
on the quality of a particular ecosystem (Makar-
ieva et al. 2005, Johnson 2007). Our density data
are for a population of the Serra Finch occurnng
in an undisturbed area, which may serve as a
baseline lor comparison with future studies o! this
species.
Mattos and Sick (1985) reported 400 in as the
distance between pairs of Serra Finch, which is
higher than the average distance estimated for the
birds at our study site. Our results were derived
Irom small sample sizes, but it is the most
accurate estimate available, particularly given
Freitas and Rodrigues • TERRITORY SIZE AND HABITAT USE OF SERRA FINCH
61
TERRITORY D
TERRITORY C
£ 1
4 . . i
95% kernel
□ 50% kernel
g 100% MCP
^neighbor 95% kernel (overlap)
^ Candeial
°ry grassland
■ Wet grassland
1 1 1 Rocky outcrop
iziDry scrubland
Wet scrubland
m. Riparian woodland
w
90 m s
FIG- 2- Habitat components of the 95% kernel territories
^onal Park. Brazil.
of four pairs (A-D) of the Serra Finch in Serra do Cipo
Mottos and Sick (1985) did not specify how
'heir values were calculated.
The mean MCP territory size of Serra Finch
"as relatively small compared to published
territory estimates for other species that inhabit
,he Cerrado Biome including the Rufous- fronted
Thornbird ( Phacellodomus rufifrons ) (3.43 ±
0.62 ha; Rodrigues and Carrara 2004), Suiriri
Flycatcher (Suiriri suiriri ) (14 ± 1.9 ha; Lopes
and Marini 2006), Chapada Flycatcher ( S . isler-
orum ) (1 1.2 ±0.6 ha; Lopes and Marini 2006).
Crested Black Tyrant (Knipotegus loplwtes) (7.3
± 0.57 ha; Ribeiroet a I. 2002), Cinnamon Tanager
( Schistochlamys ruficapillus) (8.4 ± 1.9 ha;
62
THE WILSON JOURNAL OF ORNITHOLOGY • Voi 124. No. 1. March 2012
TABLE 2. Habitat selection of Serra Finches in Serra do Cipo National Park, Brazil. The proportion expected was
calculated from the relative proportion of each habitat available within the study area, and the proportion observed in
relation to 318 locations obtained for 17 pairs. Habitat selection is indicated for differences <0.05 significance; positive {+)
for expected proportions below the Bonferroni confidence interval, and negative (-) for expected proportions above
the interval.
Habilal
Proportion expected
Proportion observed P,
Confidence interval
Selection
Candeial
0.003
0.053
0.039 < P, < 0.068
+
Dry grassland
0.793
0.019
0.010 < P, < 0.028
Wet grassland
0.079
0.025
0.015 < P} < 0.352
_
Rocky outcrop
0.047
0.366
0.334 < P4 < 0.397
+
Dry scrubland
0.016
0.072
0.055 < /J, < 0.089
-f
Wet scrubland
0.038
0.234
0.207 < Pf, < 0.262
+
Riparian woodland
0.022
0.231
0.204 < P1 < 0.259
+
Domingues and Rodrigues 2007), Shrike-like Tan-
ager (Neothraupis fascia ta) (4.3 ha; Alves 1990),
Henna-capped Foliage-gleaner (Hylocryptus rectir-
ostris) (2.9 ± 1.4 ha; Faria el al. 2007), C.ray-
hacked Tachuri (4.3 ± 1 .2 ha; Hoffmann 2006), and
Cipo Canastero (Astltenes luizae ) (4.0 ± 2.6 ha;
Freitas 2011). These studies all used similar
methods, without radiotelemetry (except Freitas
2011). The home range area of those species could
be larger than reported (Anich et al. 2009).
The Serra Finch appears to be similar to most
tropical bird species, maintaining a long-term pair
bond and a territory throughout (he year (Stuehbury
and Morton 2001), at times making it difficult to
discern the territory space of the total home range
area (Lopes and Marini 2006). The territorial
behavior was illustrated by the annual site fidelity
associated with duet song performance, and mini¬
mum overlap of the used area visualized by the MCP.
Habitat Selection. — Johnson ( 1980) proposed a
natural order to the process of habitat selection
according to the scale of observation. First-order
selection identifies the physical or geographical
distribution of a species which, for the Serra Finch,
is the mountaintop habitat complex that occurs
throughout eastern Brazil (Vasconcelos 2008).
Second-order selection delineates the home-
range area of an individual or social group. Serra
Finches did not establish territories at random and
second-order selection was visually demonstrated
by the localization of the 1 7 Serra Finch territories
closely associated with watercourses (Fig. 1). We
also found that wet scrubland and riparian wood¬
land habitats delineated establishment of the
N JinnBu p\ rr <%) in relali°n ,0 locations of lhe sampled Pairs of Serra Finches in Serra do Cip4
National Park. Braz.l, and the habitat composition within each 95<7r kernel territory, area.
Habilal
% locations
Candeial 16.28
Dry grassland 6.98
Wet grassland 0.00
Rocky outcrop 0.00
Dry scrubland 25.58
Wet scrubland 18.60
Riparian woodland 32.56
% territory
Candeial 3 34
Dry grassland 38.77
Wet grassland 130
Rocky outcrop Q.QQ
Dry scrubland 27.24
Wet scrubland 19.56
Riparian woodland 9.«o
0.00
0.00
3.51
8.77
0.00
50.88
36.84
0.00
42.32
10.54
5.30
0.00
35.54
6.30
5.77
3.85
3.85
78.85
0.00
7.69
0.00
1.83
30.73
6.41
53.94
0.00
7.09
0.00
0.(K)
0.00
0.00
75.00
0.00
9.09
15.91
0.00
26.46
1.41
62.55
0.00
7.09
2.49
14.29
0.00
7.14
28.57
14.29
21.43
14.29
1.03
62.93
10.98
3.46
4.44
13.57
3.60
0.00
0.00
0.00
69.23
0.00
15.38
15.38
0.00
67.31
5.47
22.78
0.00
2.67
1.78
6.67
0.00
6.67
33.33
3.33
23.33
26.67
0.72
56.73
8.24
14.56
0.61
7.54
11.60
16.67
0.00
0.00
16.67
25.00
16.67
25.00
1.27
73.22
4.74
1.77
4.88
4.21
9.92
0.00
0.00
6.25
25.00
0.00
37.50
31.25
0.00
51.84
18.95
7.69
0.00
16.90
4.62
Freitas and Rodrigues • TERRITORY SIZE AND HABITAT USE OF SERRA FINCH
63
TABLE 4. Habitat ranking matrices for nine Serra Finch pairs in Sena do Cipd National Park, derived from log-ratio
differences based on compositional analysis. Triple sign represents significant deviation from random at /’ < 0.05. Second-
aider habitat selection compared proportion of habitat used within 05% kernel territories with proportion ot total available
habitat in the study area, and third-order compared the proportion of locations for each animal in each habitat type with the
piuportionofeach habitat type within the finches's 95% kernel territories. Rank from the least to the most preferred habitat.
Candeial
Rocky outcrop
Dry scrubland
Wet scrubland
Woodland
Second-order
Candeial
-
+
-
—
Rocky outcrop
+
+■
—
Dry scrubland
-
-
—
Wet scrubland
+
+
+++
+
Woodland
+
+
+++
—
Third-order
Candeial
+++
+++
+++
+
Rocky outcrop
—
+
+
Dry scrubland
—
-
+
Wet scrubland
—
-
-
—
Woodland
-
+
+
+++
boundaries of the pair’s territory. This preference
may be the result of higher concentration of fruits,
mostly Malastomataceae fruits, which are an
important resource for the Serra Finch (Hoffmann
et al. 2009; GHSF, pers. obs.). Species of
Melastomataceae are highly diverse in the compos
rupestres (Giullieti el al. 1997) and produce fleshy
"mithucoric fruits, which are abundant in riparian
woodlands, rocky outcrops, and scrublands, while
almost 'H» fleshy fruits are available in grasslands,
die distribution of these particular plants closely
mmches the pattern of habitat use by Serra
inches in our study area.
f bird-order selection examines the specific use
01 ,lat)itut components within the home-range area
'Johnson 1980). Our ranking at this spatial scale
'election indicates a preference for candeial. This
vegetation is typically on the western slopes ot the
Wi do Cipo (Melo-Junior ct al. 2001), and is
Patchily distributed in the study area. This habitat
dors hoi supply fruits hut does supply arthropods
perches. We also detected more preference
1 r riparian woodland than wet scrubland at this
%ale suggesting preference for habitals with
w°ody elements. This contrasts with previous
'"formation about Serra Finch preference for open
'fetation habitats (Mattes and Sick 1985,
vasconcelos 2001. Hoffmann et al. 2009).
CONSERVATION IMPLICATIONS
We identified the most important habitat types
ln foe compos rupestres complex for the Serra
Finch and described the spatial distribution that
should influence development of better long-term
conservation strategies. Actions that contribute to
reduce habitat quality for the species should be
avoided (BirdLife International 2011). The con¬
servation priority should be maintenance ot the
most preferred habitats ot the Serra Finch that po¬
ssibly contribute most to species fitness (Garshelis
2000). Preservation of valleys, woodlands and
scrublands, and water in the mountains within the
species range must be prioritized; especially
important is protection and maintenance of
riparian woodlands and candeial. Those habitats
have been intensely exploited in the region for
production of wood and also for oil extraction in
the candeial (Ribeiro et al. 2009).
The mountain range where the Serra Finch
occurs is critically threatened due to increasing
land conversion and no effective conservation
plans (Jacobi et al. 2007, Martinelli 2007). The
actual habitat protection law is under review
which may be detrimental to the currently
protected areas (Ribeiro and Freitas 2010).
One of the most common threats for the compos
rupestres complex are annual fires, mainly
promoted to benefit livestock. Annual fires tend
to reduce the extent of scrublands and woody
elements while increasing the dominance of
grassland habitats (Coutinho 1990. Moreira
2000). The Alto do Palacio is a protected area
and (here have been no recent reports of fires,
unlike in neighboring areas (Franca and Ribeiro
64
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124, No. 1. March 2012
2008). We would expect to find a more grassland-
dominated landscape, less woody vegetation, and
fewer shrubs in areas with annual burning regimes
and, consequently, a lower density of Serra
Finches. Thus, areas with annual burning need a
fire protection program for habitat restoration and
conservation.
ACKNOWLEDGMENTS
We thank the student volunteers who assisted us in the
field. We arc grateful to the TCMBiu .Serra do Cipd staff for
lodging and support and to Bruno Crepaldi and G, G.
Teixeira for help with the figures. We appreciate the
important comments and suggestions on this manuscript by
C. E. Braun and L. M. Costa, and the efforts of J. A.
Mobley in reviewing our work and helping with the English
language. We also thank I'undayAo O Boticario de Pmteyfio
a Natureza, CNPq (473428/2004 0 and 473809/2008-7) and
FAPEMIG (CRA APQ-0434-5.03/07) for supporting this
study. M. R. is grateful to CNPq for fellowship support
during this study.
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The Wilson Journal of Ornithology 124(l):66-72, 2012
FORAGING OVER SARGASSUM BY WESTERN NORTH
ATLANTIC SEABIRDS
MARY L. MOSER'-24 AND DAVID S. LEE'
ABSTRACT. — Drifting reefs of Sargassum (a brown alga) are used by a variety of pelagic seabirds in the western
Atlantic Ocean. We examined gut contents from 964 individuals of 39 seabird species collected 5 to 60 km off the coast of
North Carolina for evidence of Sargassum use. Sargassum pieces or Sargassum- associated prey were found in nine of 10
Procellariiformes species and less frequently among Charadriiformes ( 1 2 of 25 species). No Surgassum-associaied prey was
found in Pclecani formes examined, but observational data indicated that Atlantic tropiebirds ( Phocthon Upturns 25% and high volumes of Sargassum -associated prey
Audubon's Shearwater ( Puffinus Utemmieri). Royal Tent ( Thalttsseus muximus). Bridled Tern (Onychoprion anaedirtu. n
and Red-necked Phalarope ( Pltalaropus lobatus). Seven species fed in Sargassum to a lesser extent, and nine species had
ingested Sargassum pieces, but contained no Sargassum-ussoc’e.Hcd prey. It is likely that other seabird species foray;
regularly over Sargassum. as our conclusions are based on relatively small sample sizes taken during random sampling in
the open ocean, Our conservative analysis and extensive observational data indicate the Sargassum community is critical
for leeding lor some western North Atlantic seabirds. Degradation of Sargassum habitats by oil development, harvest, and
or ocean acidification would undoubtedly have negative effects on Illness ol these birds Received 22 March 2011
Accepted 7 October 2011.
Consolidated reefs of floating pelagic brown
algae of the genus Sargassum are important and
recurring features of tropical and sub-tropical
marine environments. Holopelagic S. natans and
S.fluitans support a diverse and abundant fish and
invertebrate fauna in the western Atlantic Ocean
(Fine 1970, Settle 1993, Casazza and Ross 2008).
Recent remote sensing data indicates Sargassum
reefs originate in the northwestern Gulf of Mexico
in June each year and are advected into the
western Atlantic in early summer by ihe Loop
Current, moving northward with (lie Gulf Stream
(Gower and King 201 1 ). The floating weed moves
to the south and west in fall and winter, becoming
less buoyant with age. The circulation of Sargas¬
sum is consistent among years and is driven by
predictable currents and trade winds (Gower and
King 201 1).
Floating Sargassum can be extensive, yet
ephemeral habitat for seabirds. Airborne imagery
indicated that drift lines of the algae extend for
continuous lengths ot at least 5 km and primarily
consist ot 20-80 nr’ reefs of Sargassum (Marmor-
ino et al. 2011). Satellite images indicate
' Zoology Department. North Carolina State Universi
Raleigh, NC 27695. USA.
u ,CUr?w address; Northwcst Fisheries Science Cem
National Marme Fisheries Service. 272 5 Montlake Bou
vard East. Seattle, WA 98112. USA,
28336.euSA°iSe R ° B°X 7,,K2' White Lake.
J Corresponding author; e-mail: mary.moser@noaa.gov
Sargassum slicks can be even larger, ranging
from 100 to 1,000 m in width and up to hundreds
of kilometers in length (Gower et al. 2006).
However, consolidated drift lines of Sargassum
off the coast of Florida start to disintegrate as
wind speeds exceed 5 m/sec (Marmorino et al
201 1 ). The amount of pelagic Sargassum in the
North Atlantic was estimated at 0.54 metric ions;
km’ in the Gulf Stream and 0.02 metric lons/knr
over ihe Continental Shelf, for a combined
standing crop of >50,000 metric tons off the
Carolina*; (Howard and Menzies 1969). Gowei
and King (2011) estimated the wet weight of
Sargassum in the Atlantic has regularly exceeded
1 .8 million metric tons during the past decade and
that even greater amounts can occur in the Gull ol
Mexico. Thus. Sargassum reefs are important
feeding stations and possible roosting sites lot
pelagic seabirds (Haney 19S6).
Studies to date have used observations of
seabird behavior around Sargassum reefs to reach
conclusions about why seabirds are attracted to
this habitat (Haney 1985. 1986). We examined the
gut contents of 39 species of pelagic seabirds for
evidence of foraging over Sargassum. Percent
frequency ol occurrence, numerical abundance
and volume of Sargassum-assoclmed prey weft-
used to ascertain the relative extent of Sargassum
foraging exhibited by the species sampled. These
data were supported by extensive visual observa-
lion ol marine birds feeding in pelagic habitats off
the coast of North Carolina. Our objectives were
66
Moser and Lee • SARGASSUM REEFS AND SEABIRD FORAGING
67
lo: (1) identify seabird species that rely most
heavily on pelagic Sargassum for feeding, and (2)
document prey items most frequently targeted by
these birds.
METHODS
Gut content analysis from 964 individual
seabirds of 39 species collected 5 to 60 km off
the North Carolina coast was conducted as
described in Moser and Lee (1992). In addition,
visual observations of seabird foraging were made
from a vessel during 23 1 day trips (averaging 1 .20 1
seabird observations and 25.2 species/trip). Birds
were collected during all seasons between 1975
and 1989. although fewer sampling and observa¬
tion trips were made in winter. Observations and
collections occurred over a wide geographic area in
;tn attempt to census inshore coastal waters, the
inner and outer Continental Shelf, and deeper
waters over the Shelf's edge. Lee and Socii (1998)
mapped the areas surveyed by month.
Documentation of Sargassum use was not the
original focus of seabird collections or observa¬
tions. The birds used in this study were collected
opportunistically during their entire period of
occurrence in North Carolina waters to obtain data
on heavy metal accumulation, plastic ingestion,
a£e and sex ratios, body temperature, parasite
load, moll sequence, behavior, and ecology (e.g.,
Moser and Lee 1992, Lee 1995, Lee and Haney
!'Wii. Foraging flocks quickly dispersed when
approached by our survey boats and birds foraging
over Sargassum were not targeted, nor were they
particularly easier to collect. Sargassum is
typically found in the vicinity of the outer
Continental Shelf along the western wall of the
rj"lf Stream and. to a lesser extent, in wind rows
w'thin the Stream. Only 40% of the surveys were
near the Shelf edge where Sargassum typically
"Ccun., and the alga was frequently not in the
'■"mediate vicinity of our survey sites.
Contents from the stomach and gizzard ol each
b|rd were combined, and birds with empty upper
digestive tracts were excluded from the analysis.
Percent frequency of occurrence of Sargassum
''eaves or bladders) and Sargassum- associated
Luna was calculated for each seabird species
'"umber of birds with prey ‘A' divided by the
,0tol number of birds X 100). Sargassum
associates were defined as those species (fish,
chistaceans, and gastropods) that reside in Sar-
Wmm during the life history phase when
'"gested (following Dooley 1972, Settle 1993).
Unidentifiable prey items were assumed not to be
Sargassum associates, and the mean percent
volume of Sargassum- associated prey in the
digestive tract was used as a direct measure of
the relative importance of Sargassum for foraging
within species. Thus, our estimates of Sargassum
use are conservative.
RESULTS
Gnt contents of birds from three Orders, five
families, 16 genera, and 39 species were analyzed.
Twenty-one species (53.8%) had ingested Sar¬
gassum pieces or Sargassum-ussociated prey
(Table l). Birds were classified as Sargassum
specialists (species that had >25% occurrence of
Sargassum- associated prey). Sargassum users
(those with up to 25% occurrence of Sargassum
or associated prey), and Sargassum incidentals
(species (hat contained only pieces of Sargassum
and no associated prey ). We regarded the presence
of alga in digestive tracts as evidence of foraging
associated with pelagic Sargassum. Its presence
among gut contents that lacked any identifiable
Sa rgo.v.vHm-associated prey was probably a result
of the bird’s inability to rapidly digest the alga.
Evidence of Sargassum foraging was found in
most Proccl I arii formes (9 of 10 species) and less
frequently in Charadriiformcs ( 1 2 of 25 species). It
is possible that Sooty Tern ( Onychoprlon fuscatus)
could be added lo the species that use Sargassum ,
as four of 1 1 birds sampled contained Hying fish
(Exocoetidae). There was equivocal evidence from
digestive tract analysis for Sargassum use by two
of the four Pelecani formes. Relatively few indi¬
viduals of these species were collected. Our
extensive visual observations of the pelagic
members of this family indicated they forage over
algal mats. Moreover, two of five White-tailed
Tropicbirds ( Phaethan Icpturus) and two of three
Red-billed Tropicbirds (P. aethereus) ingested
flying fish.
Species that had no Sargassum or identifiable
Sargassum- associated prey in their digestive tracts
included: Band-rumped Storm-Petrel (Oceano-
droma castro , n = 12), White-tailed Tropicbird
(n - 5). Red-billed Tropicbird (n = 3), Northern
Gan net (Morns bassanus. n = 5), Double-crested
Cormorant (Phalacrocorax auritus. n — I),
Parasitic Jaeger (Stercorarius parasiticus, n = 4),
Great Skua (S. skua, n = 1). Great Black-hacked
Gull ( Lartis marinas, n = I). Herring Gull (L.
argenlatus , n = 2), Ring-billed Gull (L dektwar-
ensis, n = 2), Arctic Tern ( Sterna paradisaea .
68
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 1. March 2012
n = 2), Caspian Tern ( Hydroprogne caspia, n = 2),
Forster’s Tem ( S.forsteri , n — 3), Gull-billed Tern
(Gelochelidon ni lotion, n — 3), Least Tem (Sterna la
cintillarnm. n = 1). Sandwich Tem ( Thalctsseus
sandvicensis , n = 8), Sooty Tem (n = II), and
Brown Noddy (Anous stolid us. n = 2).
Four species of seabirds had frequencies of
Sargassum-associated prey >25% and were
considered Sargassum specialists (Table I ). The
single Sabine’s Gull (Xenia sabini) sampled
contained a seahorse (Hippocampus sp.), which
is a Sargassutn dweller. These gulls were
observed following Sargassutn drift lines during
migration but. sample size did not support
including this gull in the Sargassutn specialists
category. The four specialists contained almost
exclusively Sargassutn- associated prey, as evi¬
denced by high volumes of identifiable prey items
in their digestive tracts (Table 2). Sargassutn
users, birds that contained Sargassutn prey less
frequently (7 species), also Contained high
volumes ot Sargownw-associated prey.
Most birds feeding in Sargassutn contained
small Sargassutn- associated fishes (Table 2). The
only exceptions were the two species of phala-
ropes, which had consumed Sargassum shrimp
(Latreutes fucorunt) and the Sargassutn- associat¬
ed gastropod. Litiopa inelanosioma. This gastro¬
pod was also found in Cory’s Shearwaters
( Calonectris diomedea). Specialists fed on a
minimum of seven Sargassum-dssocialed fish
species, and most measurable fish prey were
<50 mm standard length (Table 2). However.
Royal Terns (Thalasseus maximus) generally
consumed slightly larger fish (range^ = 40-
105 mm) than the other birds we examined (range
- 6-75 mm). Filefish (Monacanthus sp.) occurred
with the highest frequency in Audubon’s Shear¬
waters (Puff inns Iherminieri ), Bridled Terns
( Onychoprion anaeihetus), and Royal Terns, but
numerical abundance of filefish was highest only
in Audubon's Shearwaters and Royal Terns
(Fig. 1A. C). The mean number of filefish per
bird was five. Bridled Terns (Fig. IB) had the
highest number of tetradontids (mean number of
puffers/bi rd = 6) and also consumed large
numbers of ostraciids (mean number of trunk-
fish/bird = 4).
DISCUSSION
Gut content analysis identified four Sareasv,
spec.ahsts, while visual observations indicat
ha. several add.tional species target this habi
for feeding. Audubon’s Shearwater. Royal Tem.
Bridled Tern, and Red-necked Phalarope iPhahtr-
opus lobatus) contained relatively high levels a
Sargassutn- associated prey. The single Sabine-
Gull examined contained a 5argaw«m-associaied
prey item and this species was observed to follov
Sargassutn drift lines. Visual observations indi¬
cated Bridled Terns regularly associated with
Sargassutn patches and tended to use the mats and
associated flotsam as roosting sites (Duncan and
Harvard 1980, Haney 1986). Our observational
data also indicated that Masked Boobies I Sulo
dactylatra) and the two species of tropicbinh
target Sargassutn patches while feeding as also
reported by Haney et al. ( 1999).
Diet analysis underestimated prey from Sargas-
sum habitat and excluded some seabird species. For
example, the digestive tracts of Bridled Terns in our
study contained insects of terrestrial origin, which
we did not consider to be Sargassutn associates (5
consumed Lepidoptera, 6 ate Coleoptera. 2 ale
Hymenoptera. and 6 contained unidentified in¬
sects). Haney ef al. (1999) reported insects were (lie
second most common food item in Bridled Temv
These insects may have been resting on Sargassutn
mats when ingested, We commonly observed both
species of Atlantic tropiebirds feeding around
Sargassutn reefs. Flying fish were recovered from
their digestive tracts, but this was not direct
evidence of Sargassum use. as flying fish regularly
occur where Sargassum is absent (Casa/za and
Ross 2008). We observed tropiebirds as they
plunged near and sometimes under the Sargassum
The same was true of Masked Boobies, a species
seen infrequently off the Carolinas but usually tn
association with Sargassum.
Some seabird species may not feed directly over
Sargassum , but the alga is critical habitat Ion-
certain life stages of their fish prey. For example
(lying fish can represent >50% of the total diet
ot the two tropiebirds collected off North Carolina
( Lee et al. 1981, Lee and Irvin 1 983 1 and Hying fish
are important prey in other parts of their range (Lee
and Walsh-McGchee 1998). Flying fish use
Sargassum for spawning and rearing, and Sargas-
sum is essential habitat for these and other fish
species (Casa/za and Ross 2008). Thus. Sargassum
contributes indirectly to the fitness of tropiebirds
and other seabirds, notably Sooty Terns and
Masked Boobies.
Sargassum specialists used a variety of foraging
modes, including surface-seizing, plunging (aerial
diving), pursuit plunging/diving, pattering, and
Moser and Lee • SARGASSUM REEFS AND SEABIRD FORAGING
69
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70
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 1. March 2012
TABLE 2. Frequency of occurrence (%) and size range (standard length in mm) of individual fish taxa ingested by
three Sargassum specialists: Audubon’s Shearwater (/i = 48), Bridled Terns (n = 16), and Royal Terns (n = 8).
Frequency of occurrence (%) and size range (mm)
Audubon's Shearwalcr
Bridled Tern
Royal Tern
Exocoetidae (flying fish)
6.2 (40-60)
6.2 (30)
0
Syngnathidae (pipefish)
0
6.2 (23)
0
Priaccmlhus sp. (bigeye)
4.2 (15)
12.5 (20)
0
Heteropriacamhus cruentatus (glasseye)
2.1 (45)
0
0
Caranx sp. (jack)
14.6 (45-50)
0
12.5 (70)
C. hippos (erevalle jack)
2.1 (25)
0
0
Decapterus sp. (scad)
4.2
6.2
0
Trachurus laihami (rough scad)
2.1 (75)
0
0
Stromatcidae (buiterfish)
4.2 (15)
12.5 (30-40)
12.5
Psenes sp. (driftfish)
0
0
12.5 (70-105)
Balistidae (triggerfish)
8.3 (15-20)
25.0 (20)
0
Aluterus sp. (filefish)
12.5 (40)
0
12.5 (40)
Monacanthus sp. (filefish)
68.8 (15-50)
31.2 (10-22)
62.5 (40)
Monacanthus ciliatus (fringed filefish)
2.1 (25)
0
0
Stephanolepis hispidus (planehead filefish)
2.1 (30-52)
0
12.5 (45)
Uictophrys sp. (trunkfish)
0
12.5 (6-10)
0
Chilomycterus sp. (biinfish)
0
0
12.5
Sphoeroides sp. (puffer)
2.1 (7-12)
18.7 (10-20)
0
S. maculatus (northern puffer)
0
6.2 (10-12)
0
dipping (following Ashmole 1971). We observed
Audubon s Shearwater feeding near the surface,
either by shallow diving (1-2 m), surface-seizing,
or hydroplaning in and around Sargassum reefs.
However, in the Bahamas, this shearwater feeds
by pursuit diving during the nesting season with
dives averaging 7.6 m (n = 136) to a maximum of
29 m (Mackin 2004). Phalaropes. which prey on
aquatic invertebrates in shallow pools in the
tundra by surface feeding (Haney 1985), use the
same behavior when seizing snails and crusta¬
ceans from Sargassum mats. The spinning beha\
ior associated with phalaropc feeding in freshw.
ter habitats (Obst ct al. 1996) was not observed ;
sea. Sargass um-associ ated prey taken by sma
seabirds were rarely >50 mm. indicating thes
birds picked prey from within the alga, as oppose
to diving beneath it where larger fish are typical I
found (Moser et al. 1998). An advantage c
foraging in Sargassum reefs is that piscivorou
predators drive prey up into the Sargassum mat?
where it is more accessible to the smaller-bodie
seabirds (Safina and Burger 1985, Haney 1986).
Prey types in digestive tracts provided additions
information about seabird feeding. Both frequenc
,°n rCTTL? Hnd numeric«' abundance offish pre:
■n Bridled Terns indicated they select relative.;
uncommon members of the Sargassum fish fauna
tetradontids (puffers), ostraciids (trunkfishes), stro-
mateids (driftfish), and priacanthids (bigeyes)
(Dooley 1972, Settle 1993). However, these fishes
may occur at the periphery of Sargassum patches,
where they are less frequently collected during
Sargassum sampling with nets (Casazza and Ross
2008). In contrast. Royal Terns, Audubon’s Shear¬
waters. and Red Phalaropes fed on prey that are
dominant members of the Sargassum community-
filefishcs. jacks, and Sargassum shrimp (Fine 1 970.
Dooley 1972, Settle 1993, Casazza and Ross 2008).
Haney (1986) found a significant relationship
between bird hotly size and Sargassum patch size
We noted that large-bodied Royal Terns contained
relatively large prey: but this was likely a function
of their feeding mode (plunging) rather than
Sargassum patch size.
Sargassum foraging w as documented during all
months of the year despite the Sargussuin mat
structure and attendant fish community changing
seasonally and in response to w eather I Moser
et al. 1998, Casazza and Ross 2008. Gower and
King 2011). Fine (1970) noted that faunal
composition in Sargassum collected from tk
Gulf Stream and Sargasso Sea was similar, bid
that non-colonial macrofauna were more abundant
in spring than in full. This may affect the way
seabirds use Sargassum habitat. Royal Terns
Moser and Lee • SARGASSUM REEFS AND SEABIRD FORAGING
71
I Numerical percentage (numbers of prey item
^ divided by the total number of prey items X 100) ol
V«a«unt-associated fishes in the digestive tracts of
Chon's Shearwaters (A) (// = 48). Bridled Terns (Bl
16). and Royal Terns (Cj (n = 8).
' ■"ntnute daily from Outer Banks nesting colonies
,IJ forage in Sargassum mats along ihe edge ol
,hc outer continental shelf, a round trip of up to
160 km or more (DSL. unpubl. data). Common
lS,fw hirundo) and Black ( Chlidonias niger )
lenis, and Sabine's Gulls seasonally migrate north
^ south, and likely use rows of Sargassum along
the western edge of the Gulf Stream and drift lines
within the Stream to both orient and feed.
Reduction in the Sargassum community would
have negative effects on a number of western
North Atlantic seabirds, based on digestive tract
analysis and at-sea observations, including five
tropical species considered to be of conservation
concern (Schreiber 2000). Observations of Ber¬
muda Petrels (Pterodronui t allow) and Roseate
Terns ( Sterna dougallii) indicated these Endan¬
gered Species also use Sargassum to forage.
Sargassum use by seabirds in the Pacific and
Indian oceans is unknown, but it is likely that
many of the same species and their ecological
counterparts exploit Sargassum reefs in those
oceans as well. Commercial harvest threatens to
reduce the standing crop of Sargassum in the
western North Atlantic (Settle 1997). and there are
possible negative impacts to Sargassum from oil
and gas exploration on the outer Continental
Shelf off the coast of North Carolina (Lee 1999).
Seabird surveys in the Gulf of Mexico shortly
after the Deepwater Horizon oil spill (April 2010)
indicated Sargassum habitat was damaged by this
event (J. C. Haney and DSL. unpubl. data). Global
climate change and attendant ocean acidification
may also affect Sargassum (Porzio et al. 201 1).
Significant reduction in the amount or quality of
Sargassum habitat could reduce seabird abun¬
dance, influence marine distribution, alter season¬
al movements, and/or jeopardize the birds
physiological condition.
ACKNOWLEDGMENTS
Wc thank S. W. Ross Cor help with fish identification
and Cor reviewing an early version ol this manuscript. H. J.
Porter aided in gastropod identification. .1. M. Butzerin,
T P. Good. J. C. Haney. W. A. Mackin. R. L. Pitman, and
an anonymous reviewer provided helpful reviews of this
manuscript. Funding Cor this study was provided in part by
Ihe National Marine Fisheries Service, U.S. Fish and
Wildlife Service. U.S. Army Corps of Engineers, and U.S.
Department of the Navy.
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The Wilson Journal of Ornithology 124(1 ):73-8(), 2012
MALE COMMON LOONS SIGNAL GREATER AGGRESSIVE
MOTIVATION BY LENGTHENING TERRITORIAL YODELS
JOHN N. MAGER III.' 4 CHARLES WALCOTT.2 AND WALTER H. PIPER'
ABSTRACT— We examined two critical predictions of the hypothesis that male Common Loons (Gavin irnmer)
communicate greater aggressive motivation by increasing the number ol repeat syllables within their territorial yodels. We
observed (from >3.500 hrs of field observations of 58 males) the probability that territorial interactions escalated from
territorial flyovers by intraders to stereotyped 'social gatherings' to escalated tights between residents and intruders was
positively correlated to the number of repeat syllables given by individually-banded males. Males yodcling during these
escalated contests often assumed the upright 'vulture' posture rather than the usual 'crouch' posture, reflecting an escalated
aggressive motivational state. Territorial pairs responded sooner and with more threat and alarm vocalizations to playback
yodels that contained more repeat phrases. This reflected a greater willingness to attack by residents to perceived intrusions
by males of higher aggressive motivational slate. Our study demonstrates the ability ol loons to communicate greater
aggressive motivation by lengthening acoustic territorial threat signals, which not only may be important toi conveying
imminent attack, but may also reflect important tactics for individuals of poorer lighting ability to deter territorial es ictions.
Our results also raise questions regarding what receiver-dependent and receiver-independent selective factors are
responsible for maintaining signal honesty in this non-osdne bird. Received M January 2011. Accepted 15 July 2011.
Most threat signals communicate information
regarding an individual's inherent, or condition-
dependent fighting ability (Parker 1974) and/or
willingness to attack (or aggressive motivation)
(Maynard Smith 1982, Bradbury and Vchrencatnp
1998. Hurd and Enquist 2001). Features that
communicate fighting ability often reflect stable
physical attributes, like physical size, that predict
success in aggressive encounters (Parker 1974.
Archer 1988). An animal’s willingness to attack is
Men influenced by ephemeral factors such as
health and motivational state of both the animal
and its competitors (Maynard Smith 1982, Hurd
ai>d Enquist 2001), Many birds benefit from
communicating varying levels of aggressive moti¬
vation wuthin territorial signals to avoid conflicts
‘hat consume energy and can cause serious injury.
B'r One University Drive. Orange, CA 92866. USA,
Corresponding author: e-mail: j-mager@onu.edu
Male Common Loons (Gavia irnmer) defend all¬
purpose territories on freshwater lakes by aggres¬
sive threat vocalizations called yodels (Sjolander
and Argen 1972: Rummel and Goetzinger 1975.
1978). Yodels are given only by male Common
Loons, and are considered to be territorial threat
signals because males aggressively approach and
yodel at eonspecific territorial intruders (Vogel
1995; J. N. Mager. unpubl. data). Structurally,
yodels consist of a 3-4 note introductory phrase
followed by a strophe of two-syllable repeat
phrases (Fig. I). Most frequency elements of a
yodel exhibit low intra-individual variability
(Barklow 1979; Vogel 1995; Walcott et al.
1999; Mager et al. 2007a, b) and each male can
lengthen yodels by increasing the number of
repeat phrases. Barklow (1979) observed males
added more repeat phrases to their yodels when
intruders wandered deeply into breeding territo¬
ries, and suggested that because intrusions pose a
greater threat to resident males, longer yodels
might communicate a greater willingness to
attack. This hypothesis has been generally accept¬
ed. but has been supported by few. and only
anecdotal, data. For example, males add repeat
phrases to yodels when territory quality (and
resource value) is enhanced (Mager et al. 2007b),
which may indicate they defend higher quality
territories more aggressively. There has been no
published study to date that has examined critical
predictions of this long-standing hypothesis.
We specifically tested Bark low's hypothesis
that yodels containing more repeat phrases reflect
a greater motivational state by examining two
73
74
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124. No. 1. March 2012
FIG. 1 . Spectrogram above) indicating change in frequency (in kHz.) over time (sec) and waveform (below) indicating
? "!L 'ff (MPa.) over time (sec) of a typical yodel of the Common Loon. Yodels consist of two fundamental
varv'thp “ t "“f ,ntroduc'ory Phrase’ followed *>.v a scries of two-syllable repeat phrases in which each individual can
vary the number ol repeat phrases for each of the yodels they produce (this example has 5 repeat phrases).
critical predictions: (I) males should give longer
yodels during social situations in which (he
probability of attack is greatest, and (2) territorial
pairs should respond more aggressively to yodels
that vary only in number of repeat phrases.
METHODS
Stmly Site and Resident Population.— W(
conducted this study from 2002 to 2007 or
~100 study lakes in Oneida County. Wisconsin
USA, northwest of Rhinelander (45° 42' N
89- 37' W). Loons are genetically monogamous
and exhibit high territory and male fidelity (indi¬
viduals return to the same territories for 3-7 years
on average; Piper et al. 1997a). Territorial intrusions
occur frequently between April and July (Mageranc
Walcott 2007) and occur most often between 043C
and 1 100 hrs each day (Mager 1995 ).
Assessing the Effect of Social Context on
Yodel Duration.— We assessed the impact of
varying number of repeat phrases on behavior ol
signalers and receivers by considering whether
longer yodels were given during five stages of the
intrusion process in which the probability of
resulted* f" ** pr°porlion °‘‘ situations that
Pre.l ^
conspecifics flew over the' \eZory, % when
conspeafics landed on the territory bu, remained
fr°m the res,dem male, (3) when intruders
approached to within 20 m of the resident male
bin did not engage in ‘social gatherings' that
consist of stereotyped circling on the water's
surlace in head-to-tail orientation that may
include ‘splash dives’ (Sjdlander and Argen
1972) with pair members, (4) when participants
engaged in social gatherings, and (5) when
intruders attacked or fought a resident. Daw
collected between 2002 and 2004 verified that
residents were more likely to attack an intruder
(repeated-measures ANOVA F3.246 = 1.654. P <
0.0001; Fig. 2 ). when intrusions transitioned from
flyovers to actual landings (paired / = 8.093. df -
1^?- P < 0.0001). from landings to approaches
(paired t = 2.178. df = 155. P = 0.0073), and
from approaches to social gatherings (paired t =
6.969, df = 155, P < 0.000 1 ; Fig. 2).
Observations of Natural Yodels.— We observed
58 pairs of individually-banded loons between I-
April and 31 July 2002-2007 between 0430 and
1430 hrs (CDT). We conducted daily M11
behavioral-time samples (Altmann 1974) of 4-6
territorial pairs, using ‘all-occurrences’ recording
methods (Martin and Bateson 1993) to count
flyovers, the extent of intrusions (e.g.. did pairs
approach within 20 m of the intruder, did die
residents and intruders engage in 3 social
gathering), aggressive behavior (e.g.. surlace
chases involving the swimming and flapping of
wings of one individual toward another, or actual
Mageretal- LOONS SIGNAL HIGH AGGRESSION WITH LONGER YODELS
Flyover Distant intruder Close intruder Social gathering
FIG. 2. Mean (± SE) probability of attack under different social contexts based upon >3,530 hrs of observation of
Common Loons between 2002 and 2004 (/•\4g = 75.448. P < 0.0001, n = 84 males).
fights in which individuals actually grab one
another by cither the bill or neck and beal one
another with their wings, following descriptions in
McIntyre (1988) and Piper et al. (2008), and
yodels. We recorded the time of day. the yodeler's
physical posture (i.e.. ‘crouch’ or ‘vulture’ after
Rummel and Goetzinger 1978). the estimated
distance between yodeler and perceived receiver,
and the number of repeat phrases given when each
male yodeled.
Playback Experiment.— We assessed how loons
responded to yodels having fewer/more repeal
syllables by recording vocal responses of local
pairs to broadcast yodels that simulated an
unfamiliar male’s intrusion into the territory. We
““d a Portadat MDP 500 acoustic recorder
HHB. London, UK) equipped with a Sennheiscr
MHK-70 shotgun microphone (Old Lyme, CT,
^A) to broadcast yodels from males recorded
e«fflier that season at a distance between 15 and
^ m from males in the study area whose
territories were >8 km from a focal pair's
territory (to reduce social recognition) (Waas
lwk Mager et al. 2010). and did not play the
^me yodel to more than one pair (to prevent
pscudoreplication ) (Kroodsma 1989). Wc created
undistorted yodels containing one. lour, and seven
repeat phrases by adding identical repeat phrases
t'Jthe same yodel using Canary acoustic soilware
lVenion 1.5, Cornell University Bioacoustics
^‘search Program, Ithaca. NY, USA), Thus, each
yodel was identical in all acoustic parameters
ex«pt for the number of repeat phrases. We
playbacks between 2130 and 0230 hrs on
three successive nights. We randomized the cider
yodels were played on the three nights (e.g.,
1 -repeat phrase the first night, 7-repeats the
second, and 4-repeats the third night to one pair;
4, 7, I repeat phrases on successive nights to
another pair, etc.). Each night, we broadcast
yodels through a RadioShack (Fort Worth, TX.
USA) 20-Watt amplifier and Super PowerHorn
model 40-1 .445 speaker at 90 dB (measured 10 m
from the speaker) and rebroadcast the same yodel
(having the same number oi repeat phrases) at 5
and 10 min after the first. We recorded the time
and type of all vocal responses during the 15-nun
period following the first playback using the same
recorder and microphone from which we recorded
the playback yodels,
We quantified the number of tremolo, wail, and
yodel responses from focal pairs in addition to the
latency before first vocalization. We interpreted the
number of tremolos to reflect the extent pairs were
threatened by the yodel, and the number of wa.l
responses to reflect the pair’s level of alarm and
interest to contact following Barklow (1979) and
McIntyre (1988). We used repeated-measures
ANOVA and associated post-hoc tests to investigate
differential responses hy pairs to the three classes ol
playback. We used the PROC MIXED procedure
(SAS after Singer 1998, Johnson 2002) to construct
linear growth models to examine whether responses
given could be attributed to more repeat phrases
while controlling for variability among pairs. We
accepted significance at a Bonferroni -corrected a of
0.05 for all statistical tests.
RESULTS
We recorded conspecific intrusions on 57
territories and the yodeling responses of 58 banded
males defending those territories (x ± SE number
76
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. I. March 2012
of Fclch' oerS!!=n„“,mbe; m T?" ^ C°mmon L°°ns * ”cial “»««■ Gray bats reprcSen, number
or crouch yodels per event and black bars represent number of ‘vulture' yodels per event.
of seasons an individual was observed = 3.7 ± 0.2
median = 3 seasons) during 3,900 hrs of
observation covered by our 6-year study. The
number of prospecting loons flying over territories
varied significantly with each territory (F5M3I =
1.718, P = 0.0051), but the frequency of distant
intrusions (F56, 15 , = 1.505, P = 0.0268), ap¬
proaches (F5615| = 0.862, P = 0.7349) social
gatherings (FS6,J51 = 1.316, P = 0.0975), and
aggressive chases/fights (F5()il5, = 1.202, P =
0.1914) did not vary with territory. Intrusions that
involved the close approach of the intruder without
a social gathering occurred rarely; consequently,
we report mean yodel ing responses by males to
these types of intrusions, but omit them from
repeated-measures analyses of vodeling rates and
number of repeat phrases given with stage of
territorial intrusion. None of the contests resulted in
eviction of territorial males.
we observed 1,495 yodels from 58 banded m
(mean ± SD; 13 ± I yodels recorded/individ
year, range = 1-51). Forty-eighl of the 58 m;
yodeled in al least two of the five social com,
between 2002 and 2007; few gave yodels in all f
Pooling all yodels from all males, males yotk
primarily at conspoeiRcn (87.5% of all yodels)
also yodeled al humans ( 10.8%). and Bald Eat
hetT“ '*mac‘ph“lu-,> d-7%). We obser
siom T'S i°',ni"in8 infn-‘‘'ucnl in,
territorial in^o, 48 0^56 1
years). n,e frequency (# yodelsfoccurrenee) ma
yodeled at conspecifics was related to the extent
of intrusion (Friedman’s ANOVA f = 25.394. n
= males, df = 3, P < 0.0001; Fig. 3). Males
gave significantly more yodels when intruders
landed on the territory than when intruders flew
over the territory (Wilcoxon Z = 2.99. P =
0.0028). and gave progressively fewer yodels per
social gathering (Wilcoxon Z = 2.92. P =
0.0035). However, male vodeling rate did not
decrease as social gatherings escalated into chases
or fights (Wilcoxon Z = 0.62. P = 0.54). Close
intrusions that did not lead to social gatherings
rarely occurred, but the likelihood that a resident
nude would yodel was lowest (14.3% of all such
occurrences) during this situation, implying some
signal, or assessment of lower threat, associated
with the intruding loon.
Males gave most calls as ‘crouch’ yodels (94%
°l given), but only gave crouch yodels at
flyovers, distant intruders, and close intruders that
did not escalate into social gatherings. Males gave
more 'vulture-posture’ yodels when territorial
contests escalated; 1 0. 1 % of all calls given during
social gatherings were crouch yodels, but 678f
of all yodels given during physical chases, and/or
fights were vulture-posture yodels (Fig. 3). Male'
(/i ' 25) observed yodel ing in both the crouch and
vulture postures during a given vear gave yodels
with more repeat phrases when in the vulture-
posture (X ± SE = 4.95 ± 0.40) than in the
crouch-posture (3.72 ± 0.26; paired l = 3.10.
df - 24, P = 0.0049). Intruders rarely yodeled on
territories of residents (130 yodels in the 6 years
Mager el al. • LOONS SIGNAL HIGH AGGRESSION WITH LONGER YODELS
77
6.0
Flyover Distant intruder Close intruder Social gathering C base Fight
FIG. 4. Mean (± SE) number of repeat syllables per yodel given by resident male Common Loons under social contexts
associated with greater levels of agression.
of study), and tended lo give proportionately more
vulture yodels (33/130 or 25.4% of yodels) than
residents (84/1.495. or 5.6% of yodels).
Males had 3.6 ± 0.1 repeat phrases/yodel
(range = 0.0-20.0). although the number of
repeat phrases each male produced was a function
of the number of yodels heard (y = 3.320 log x +
1.064; r = 0.613; P < 0.0001). Most yodels
(S6.l%) contained between two and five repeat
phrases (mode = 3). There was individual
variation in the number of repeat phrases given
hv males per crouch posture yodel (ANOVA
^7.129 = 3.270. P < 0.0001 ). but not per vulture
Posture (ANOVA F2S, 12 = 1.431. P = 0.26)
.'"del. not controlling for the different contexts of
territorial intrusion.
Males had 42.9% more repeat phrases per yodel as
intrusions escalated from flyovers and landings to
wia| gatherings and physical attacks (Fig. 4). Males
^ lunger yodels when flyovers escalated to landings
'Nred 1 = 3.158, df = 39, P = 0.003 1 ); did not give
’significantly longer yodels when intruders came
U|1hin 20 in of the male (paired / = 0.025, dl =
P ~ 0.98); and gave longer yodels when close
"'tnisions transitioned into social gatherings (paired
t = 3.I68. df = 10, P = 0.01), but not when social
gatherings transitioned into chases and/or fights
(paired t — 0.09, df = 17, P — 0.93).
There was a clear difference in how pairs
responded vocally to broadcast yodels that differed
in the number of repeat phrases. Pairs vocalized
over twice as quickly, and gave almost tour times
as many tremolos to longer yodels. Resident males
gave four times as many yodels to seven-repeat
yodels versus one-repeat yodels (Table I ).
DISCUSSION
Individuals that experience frequent territorial
contests often produce graded threat displays to
communicate a heightened state of aggressive
motivation (van Rhijn 1980, Bradbury and
Vehrencamp 1998). Populations experience fre¬
quent conspecific intrusions that escalate into
potentially lethal confrontations (Piper et al.
1997b. 2000), and it is not surprising that male
Common Loons, as Barklow (1979) proposed,
lengthen territorial yodels to communicate greater
aggressive motivation.
Territorial interactions between residents and
intruders among loons proceed through a se-
T«U I. Vocal responses of territorial parrs („ - 3S> of Common Loons to playback yodels having one. four, and
ieven rePeai phrases.
Response
One repeal
Four repeats
Seven repeals
Individual growth
model Fi n j
p
bivariate response
^ ^0Cali7fltinnc
9.68 ± 2.96
17.80 ± 5.06
26.76 ± 4.85
6.89
0.0099
* Tremolos
5.92 ± 2.79
14.72 ± 4.91
20.08 ± 4.53
5.26
0.0237
* Wails
3.95 ±1.14
2.44 ± 0.79
4.54 ± 0.91
0.12
0.7288
# Yodels
0.18 ± 0.08
0.36 ±0.14
0.73 ± 0.20
6.51
0.0121
patency before 1st vocalization (sec)
128.20 ± 52.72
131.72 ± 49.12
62.87 ± 17.27
12.37
0.0006
78
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124. No. 1. March 2012
quence of actions that provide more reliable
information about fighting ability but entail
greater costs consistent with sequential-assess¬
ment models of contests (Enquist and Leimar
1983. 1987). Flyovers provide intruders informa¬
tion about territory quality (Piper ct al. 2006). but
if a resident yodels, it also provides the prospect¬
ing loons information about territory occupancy,
the resident male's identity (Walcott et al. 1999,
2006; Mager et al. 2010), and fighting ability
(Mager et al. 2007a). Flyovers constitute a lesser
threat to a resident male versus a close intruder.
Males yodel less often (-1 of every 3 flyovers),
and always assume the low-risk, low-cost
crouch posture. Not only is the “crouch" posture
less costly physiologically to assume versus the
"vulture" posture, but it also places the signaler in
a less vulnerable posture for receiver attack
(although no attack could possibly occur during
a flyover) and a more effective posture to transmit
information over great distances (McIntyre 1988).
It is likely that both residents and intruders
obtain more reliable or perhaps additional infor¬
mation about each other’s fighting ability and
motivation when intruders approach within 20 m
of the resident pair and engage in social
gatherings. Residents, in response, yodel more
often (yodel ing approximately once for each such
intrusion), and give more repeat phrases in each
yodel. Longer yodels likely provide intruders
more reliable information about the identity,
health, and vigor of the signaler. However, this
information comes with considerable costs to the
signaler. Physiologically, longer yodels necessar¬
ily are more energetically expensive to produce. A
male that produces longer yodels must be able to
endure these costs. Producing longer yodels could
also place the signaler at a greater risk of
retaliation from the receiver. Our results have
shown that longer yodels evoke quicker responses
by and more tremolos (signaling greater alarm)
and yodels (signaling greater threat) from con-
specific receivers. These receiver-independent
and receiver-dependent costs of producing longer
yodels ultimately could prevent males from
luffing about their motivation, and act as
seective processes to maintain signal honesty
(Vehrencamp 2000. Hurd and Enquist 2001) We
fee both types of easts are likely more than offset
by the significant costs of lighting, as aSfire„ivc
pursutts end fighls (Rumntel Li S
1975, McIntyre 1988, Pnruk 2006) ettn lead to
resident s evict, on or death (McIntyre 1988. pJruk
1999. Piper et al. 2008). However, more detailed
analyses are needed to consider these factor,
regarding fitness costs associated with pnxiucing
longer yodels.
We found loons yodel in the vulture posture
most olten when contests escalate into social
gatherings and actual chases/fights. The vulture
posture may amplily/reinlorce the communication
of a higher motivational state and/or it may sene
as u separate signal of aggression (Rummel and
Goetzinger 1978, Johnstone 1996). The posture is
clearly more costly for males to assume, as they
must vigorously paddle their feet to "stand"
upright upon the Water surface and extend dieir
wings outward while ‘pointing’ their bills toward
the potential receiver (McIntyre 1988).
We provide empirical support of Barklow's
(1979) contention that male Common Loons
signal greater aggressive motivation hy adding
repeat phrases to territorial yodels. However,
signaling motivation by lengthening territorial
vocalizations is not the conventional way birds
signal greater motivation (e.g., Morton 1977,
1982: Ripmeester et al. 2007). Many species that
sing longer songs tend to communicate greater
lighting ability (e.g., Lambrechts and Dhondt
1986, 1987; Appleby and Redpath 1997). In
contrast, male Common Loons communicate
fighting ability through the dominant acoustic
frequencies ot yodels: larger males of better
fighting ability produce lower-frequency yodels
and smaller males of poorer fighting ability
produce higher-frequency yodels (Mager et al.
2007a). Past studies have shown that males that
signal lower fighting ability produce yodels with
more repeat phrases (Mager et al. 2007a). We
believe that males of poorer fighting ability must
be more aggressively motivated (and produce
longer yodels) to successfully defend their
territories based on our empirical support of
Barklow's (1979) hypothesis that males commu¬
nicate greater aggressive motiv ation by lengthen¬
ing yodels. This strategy may not be limited to
loons, as other species similarly lengthen threat
signals when more motivated to attack. Many
examples are non-oscines (e.g.. Martin-Vivaldi el
al. 2004), including some waterbirds (e.g.. Nelson
1984, Ewins and Weseloh 1999. Mow bray et al.
2002) living in open water environments where
acoustic scatter and absorption are minimal. This
raises the question regarding those selective
factors associated with signal production, propa¬
gation. and reception among birds that call over
Mageretal • LOONS SIGNAL HIGH AGGRESSION WITH LONGER YODELS
79
open water that would favor this means of honest
communication of aggressive motivation.
ACKNOWLEDGMENTS
Parts of this manuscript were presented as partial
Liniment of requirements of J. N. Mager's Doctor of
Philosophy degree, in agreement with guidelines of IACUC
approval 97-12-02 at Cornell University. Support was
provided by Cornell University (Cornell Laboratory of
Ornithology Walter Benning Fellowship, Department of
N'eurobtology and Behavior Student Research Grant. Edna
Bailey Suzman Fellowship. Kieckhefcr Adirondack pel
owship. Local Sigma Xi Grunts-in-Aid-of-Research Grant.
University Travel Gram), the Sigurd Olson Environmental
Institute Loon Research Award, ihe Denison University
Visiting Scholar Program, and the Ohio Northern l Jnivcrsity
F.iculty Summer Research Grant. We thank A. A Dhondt. H.
K. Reeve, and S. L. Vehrencamp for constructive recom¬
mendations in study design and manuscript preparation,
kareu Grace-Martin and F. M. Vcrmcylcn lor statistical
consulting, A. R. Lindsay. M. W. Meyer for assistance, the
many held assistants for their hard work, and private
limdown«S for access to lakes, encouragement, and support.
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Walcott, C„ J. N. Mager, and w. H, Piper. 2006.
Changing territories, changing tunes: male loons.
Gavia immer. change their vocalizations when they
change territories. Animal Behaviour 71: 673-683.
Walcott. C., D. Evers. M. Froehler, and A. Kr.ak.aier
1999. Individuality in ‘yodel' calls recorded from a
banded population of Common Loons. Gavia immer
Bioacoustics 10: 101-114.
The Wilson Journal of Ornithology 124(1): 81 -86, 2012
TERRITORIAL FIDELITY TO NECTAR SOURCES BY
PURPLE-THROATED CARIBS, EULAMP1S JUGULARIS
VINITA GOWDA,1 24 ETHAN J. TEMELES.1 AND W. JOHN KRESS2
ABSTRACT— We present the first record of territorial site-fidelity across multiple years by Purple-throated Caribs
lEulampis jugularis) on three different islands in the eastern Caribbean, St. Kitts. Dominica, and St. Vincent. Marked male
Purple-throated Caribs were monitored throughout the flowering season ot their main nectar resources. Heliconia carihaea
St. Kitts and Dominica) and H. hihai (St. Vincent), both native perennial herbs. Individual males were observed defending
the tat Heliconia patches for 3 years (St Vincent). 4 years (St Kilts). and 5 years (Dominica), and remained near these
patcho e.en when they were not in flower. The territorial behavior and resource dependence of Purple-throated Caribs on
native heliconias likely have a key role in the coevolution of this specialized plant-pollinator interaction. Received 17
Man h 201 1. Accepted 2 August 2011.
Territoriality is a costly and often complex
behavior involving exclusive possession and/or
defense of an area against conspecific and hetero-
specific animals (Carpenter 1958; Brown 1964.
'W; Pyke 1979). Territorial defense of food
resources is common by nectar- feeding birds (Gill
and Wall J975,Cruden and Hermann-Parker 1977,
tf 100 ramets) in a given year (Berry
and Kress 1991). Each ramet bears one multi¬
tiered inflorescence which consists of several
sequentially opening flowers within a bract and
several sequentially opening bracts within an
inflorescence. Each flower within a bract lasts
only a single day and flowers remain open from
dawn to dusk (Temeles et al. 2005, Gowda and
Kress 2008).
Puqile-throated Caribs were banded at each site
(Table 1) during March and April with unique
color-coded darvic bands (www.avinet.com) and
observed for 24 hrs (8 hrs/day X 3 days) per month
in March. April, May, June. July, September.
November, December, and January . These months
represent both the peak (Mar to Jul) and the non-
peak (Aug to Feb) flowering seasons of the two
native heliconias (Gowda 2009) and also cover tie
breeding period of Purple-throated Caribs (Mar i>>
Jul) (Wolf 1975, Temeles and Kress 2010). All
observations of territoriality by Purple- throated
Caribs on St. Kills and Dominica were made at
marked clumps of H. caribaea plants over multiple
years. H. caribaea is very rare on St, Vincent (only
2 clumps found in the forest); thus, observations
of territoriality by Purple-throated Caribs wen
conducted on marked clumps of H. bihai. We
delineated the boundaries of territories by noting
the point at which territorial males evicted
intruders, which included both conspecific males
and females, and heterospecifics (Temeles et al
2005). We concluded that males were display¬
ing ‘territorial fidelity' if the same marked
territorial bird was observed and recaptured at the
same marked feeding plants for >2 yrs after first
capture. We also recorded the number of flowers
within the clump on each observation day to assess
use of Heliconia patches by males in relation to
flowering.
RESULTS
Territoriality at Heliconia caribaea.— We ob¬
served few visits (4-5 visits/day) by male Purple-
throated Caribs to clumps of H. caribaea in the
beginning of March when budding inflorescences
were visible but no open flowers were available
Male Purple-throated Caribs on all islands, but
especially on Dominica, increased their visitation
frequency as the flowering season progressed
(Fig. 2) and spent more lime on the territory
defending against incoming visitors to single
flowering inflorescences or often even at inflo¬
rescences without flowers. Male Purple-throated
Caribs rarely left the vicinity for more than a fe'v
hours a day or rarely for an entire day dunng the
beginning of the flowering season of H. caribaea
indhdditfs momWdn' !*! °' ' PurplcM,m>aled Caribs from three eastern Caribbean Islands. Number
- 1 _ PU lsljnd "■ individuals displaying territoriality = T. and individuals displaying site fidelity =
Island
Territorial months on
non -Hdiconia plan's
Gowda el al. • TERRITORIAL FIDELITY OF THE PURPLE-THROATED CARIB
83
y
c.
X
0
X
3
•C
0
T3
C
0
35
30-
25-
20-
15-
10-
*
3
•a
y
a.
0
35
(A) Dominica
1 30
1
Q.
X
X
Q
(B) St. Kitts
X
\ X
300
250
200
150
100
50
0
-300
o
03
3
=3
-250
C
3
a-
- 200
o
~t
c
—5
- 150
o
£
- 100
o
C/3
-a
-50
o
-n
a.
03
- 0
D Chases per hour
Fin in . . u. PmT>lc-throated Caribs at H. cariboeo and H. bihoi clumps
• fcX, vistts and observed cha*s b m . Purple .hr=m ' vjs,,s (open) and chases
■:Z “T a'Tr h * error. The dotted line represent rhe mean
Ln 3S month across a single year, rtritowfa ™ibaea on St. Kitts and Dominica, and H. MW on
" vincent*,
H two male Purple-throated Caribs in Domin- bv mid-April, the peak flowering season of H.
ica were not observed on their territory on two caribaea , and allowed only females to feed within
'fparate davs Male Purple-throated Caribs territories, which often consummated in a mating
st)0Wed aggressive territorial defense (Fig. 2A) event. Conspecific females, males, and heterospecifics
84
THE WILSON JOURNAL OF ORNITHOLOGY . Vo/. 124, No. 1, March 2012
(Green-throated Carib [Eulampis holosericeus],
Antillean Crested Hummingbird [Orthorhynchus
cristatus], Lesser Antillean Bullfinch [LaxigilUt
noctis], Bananaquit | Coereba fluveola]) were
chased from the territory by the resident male
Purple-throated Carib. Displacement of a resident
male Purple-throated Carib was observed only
once during the study (Dominica. Carholme site).
A new male Purple-throated Carib displaced the
resident focal male in the second year of
observation after a rapid aerial chasing and scrub-
level scuffle.
Territorial defense at H. caribaea by male
Purple-throated Caribs lasted from March to July
on Dominica (Table 1). Territorial defense had
higher temporal variation on St. Kitts and St.
Vincent (Fig. 2B, C; Table 1). For example, on
St. Kitts, an all-day territorial presence at H.
caribaea clump by Purp I e- throated Caribs was
observed only from March to May, whereas
territorial defense by Purple-throated Caribs on
St. Vincent was observed only in April and May
and was further restricted within a day, between
0900 to 1500 hrs (Fig. 2C). Territorial defense by
females was rare and only observed on St. Vincent
where females chased conspccific females (4
times) and nonspecific males (2 times). However,
females chasing males could not be distinguished
from their mating repertoire.
Territorial Fidelity at Heliconia Patches.— Ail
marked males on the three islands were faithful
to their feeding territories across multiple years
(Table 1). Individual males remained faithful to
their Heliconia patches for 3 years on St. Vincent,
4 years on St. Kitts, and 5 years on Dominica.
Females did not show territorial behavior during
the breeding season but the same female was
recaptured in 2 years in the same feeding clump of
H. bihai and H. caribaea on Dominica. Similarly,
a banded, non-territorial female Purple-throated
Carib was repeatedly observed at the same patch
of H. bihai on St. Lucia over 2 years (EJT, unpubl.
data) and in St. Vincent for 2 years. Thus, females
may not defend territories, but thev apparently
exhibit site fidelity to Heliconia patches when
traplining.
Purple throated Carib Territoriality and Site
P Hi"' ^ Absence of Heliconias.- Male
Purple- throated Caribs exhibited territorial behav-
ZeTof ,h ofkothcr P,mt *peci« during
tunes of the year when H. caribaea was not
(lowering. We observed the birds defending Citrus
P" US SP" Ge**eria cymosa, Heliconia
psittacorum, H. wagneriana , Inga ingoides, Lobe¬
lia cirsiifolia, Marcgravia umbellate. Musa sp..
and Wercklea tulipiflora. Seven of nine resident
males, despite the complete absence of floweraof
H. caribaea from August to March, were observed
in the general vicinity ol their H. caribaea territory
in September, November. December. and January
on St. Kitts (2 of 3 birds) and Dominica (5 of 6
birds). One or more of the non -H. caribaea species
was present within 200-1.000 m of Heliconia
patches for all of these males. Male Purple-throated
Caribs shitted their territorial defense to these plant
species, although one of the marked birds was
observed in a citrus farm >1 km distant.
DISCUSSION
Territoriality, foraging, and mate-selection in
hummingbirds are behaviors strongly known to be
influenced by local energy sources (Carpenter
1958. Gass et al. 1976, DeJBenedictis et al. I97S.
Gass 1978, Kodric-Brown and Brown 1978;
Montgomerie el al. 1984. Gass and Sutherland
1985. Temeles and Kress 2010). The abundant
heliconias in the eastern Caribbean Islands repre¬
sent critical sources of nectar for hummingbirds
due to the: ( I ) clonal habit of the plant that assure"
high density within a small radius (2 to 3J
individuals/m*), (2) nectar rich flowers within the
same inflorescence (up to 10 to 12/inflorescence),
and (3) long flowering season lasting several
months (Apr to Jul) that assures a stead},
dependable food source (Temeles et al. 2005.
Gowda 2009, Temeles and Kress 2010). The
presence of territoriality by Purple-throated Caribs
throughout the flowering season of the heliconias
and their associated multi-year site-fidelity con¬
firms the two heliconias (H. caribaea in St. Kilt'
and Dominica, and H. bihai on St. Vincent) at*
critical nectar sources for Purple-throated Carib'
The presence of the same individuals at specific
Heliconia clumps within a flowering season arid
across years suggests the Purple-throated Caribs on
these islands have a long-term imprint of high-
quality loraging sites that are not abandoned eiihct
within or between years. Hummingbirds use both
fine (Miller et al. 1985, Sutherland and Gass 1995
and coarse-grained memory' (Armstrong et at
1987) to locate optimal food resources. Purple-
throated Caribs likely use coarse-grained spatial
memories to re-defend the same clump of Li
caribaea year after year (Baida and Kamil 1989).
Our observations of Purple-throated Caribs in
the genera! vicinity of their territorial sites during
Gowda et aL • TERRITORIAL FIDELITY OF THE PURPLE-THROATED CARIB
85
the non -H. caribaea flowering season suggest
they may be aiding their spatial memory by main¬
lining site-fidelity even when heliconias arc not
in Hotter. On a broader level, many migratory
North American hummingbird species have been
a-capiured at the same general locations between
successive years (Bassett and Cubie 2009), and
vitne lekking hummingbird species return to the
sime leks between years (Stiles and Woll 1979).
Long-term spatial memory may be a general
characteristic of hummingbirds, although it may
have evolved through a variety of different con¬
texts (feeding, migration, and mating).
Our observation of strong fidelity to Helicon ia
patches by Purple-throated Caribs has implica¬
tions for coevolution between hummingbirds and
Hcliconia. Bill morphology, body size, and
energetics of male and female Purple-throated
< aribs arc closely related to one or the other
species of Heliconia on the islands of St. Lucia
and Dominica (H. caribaea with males: H. bihai
with females; Temeles et al. 2000, Tcmeles and
Kress 2003). Close correspondence between
hummingbirds and flowers suggests these islands
^ 'hotspots’ (Thompson 2005) of reciprocal
evolution. Thompson (2005) noted that gene flow
among populations can dilute and weaken recip-
10031 adaptation. However, year-to-year fidelity
"• territorial male Purple-throated Caribs to the
'•'me patches of heliconias combined with territo-
"Ol exclusion of intruding conspecifics and hetero-
•c-ecifics would reduce gene flow in both plants and
hummingbirds, resulting in strong coevolution of
^Tic-throated Caribs with //. caribaea through
toiprocal selection for flower numbers and male
tod fighting ability (Temeles and Kress
Similar fidelity by traplining females may
‘^-'contribute to strong ecological interactions and
1 duuonary interactions with II bihai through
flower size and shape and bill morphology
'Temeles et al. 2009). Benkman et al. (2003)
sported a case of coevolutionary interactions
fvttteen a non-migratory population ot Red
Cr,Abil|s [Loxia cunirosira) and lodgcpole pine
lp'n“s contorta spp. latifolia) where reciprocal
■election has largely shaped their bill morphology
^ ^rd defenses, respectively.
Our observations indicate that male Puiple-
'hroated Caribs continue to associate with patches
caribaea even when these plants are not in
This raises the questions of whether males
*** defending and exhibiting fidelity to the
Hcliconia species, or to the sites in which these
plant species occur. We suggest it may be both and
have no doubt that heliconias arc the resource
magnet that attracts hummingbirds to these sites.
Our contention is supported by the observation that
with the exception of introduced plants (e.g.,
bananas, citrus, and some ornamentals): we have
found no native plant species on these islands that
are as rewarding as heliconias in terms ol overall
nectar production (flowers of these heliconias
produce 60 to 300 pi per day: Gowda and Kress
2008). Thus, fidelity to a long-lived, highly-
rewarding resource, even when it is not in flower,
may be a viable territorial strategy, especially if
alternative low-quality resources are locally avail¬
able. Once a territory is abandoned, it may be
energetically more costly to re-establish it than to
maintain it during times of low flower availability.
acknowledgments
Wo thank the Minisiry ot Agriculture and the Environ¬
ment; Forestry. Wildlife, and Patks Division; Common¬
wealth of Dominica. Government of St. Christopher and
Nevis, and Forestry Department. Ministry of Agriculture
and Fisheries, St. Vincent and the Grenadines tor
facilitating this study. We also thank Arlington James. Enc
1 1\ polite. Ida Lopez. Anne Jno Baptiste, and Gregory
Pereira for logistic help and discussion. Wc thank C. E.
Braun and two anonymous reviewers lor helpful comments
and assistance on this manuscript. This work was supported
by a Weiniraub Graduate Fellowship from the Department
of Biological Sciences. The George Washington Univers.ty
to VG and also by the Cosmos Club. Sigma-Xi. and the
Smithsonian Institution, Field work for ibis study was
supported by grants from National Science Foundation
(DEB-06142 IS) to E. J. Temeles and W, J. Kress.
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The Wilson Journal of Ornithology 1 24( 1 ):87— 95, 2012
BREEDING AND FORAGING VARIATION OF THE PLUSH-CRESTED
JAY ( CYANOCORAX CHRYSOPS) IN THE BRAZILIAN
ATLANTIC FOREST
ANGELICA MARIA KAZUE UEJ1MA,1' ANDREA LARISSA BOESING.24
AND LUIZ DOS ANJOS2
ABSTRACT.— We monitored six flocks and five active nests of the Plush-crested Jay (Cycmocorcix chnsops) at three
in the Atlantic Forest in southern Brazil. The sites had different vegetation compositions and spanned different levels
i thropogemc disturbance. Home ranee size in full/wimci was 20-30 ha and the breeding territory size in spring/summer
5-10 lu in size. Territories were smaller across sites with higher anthropogenic food supplementation. Hock sizes were
5-11 individuals during spring/summer and 8-15 individuals during lall/winter. The Plush-crested Jay is a cooperative
breeder, nesh were 4-7 m above ground level, the incubation period WB# 18*20 days, brood si/e (\ ± SD* was 3.4 ± 0.80
vesper nest, and nestlings fledged 23 T 1 2b days after hatching. This species occupies all forest strata but tends to use the
underaory -and middle levels most (G = 178.2; P < 0.01). Invertebrates were the most frequently consumed item in all
-rSfi. but percent consumption varied among sites (G = 105.06; P < 0.01). We observed 110 >ood caching events
throughout the year, primarily seeds at Araucaria august (folia, maize, and coconuts. Caches were on the ground in - 40).
m epiphytes (n = 47). and on branches in - 23). Levels of anthropogenic food supplementation resulted in variation in
territory and home-range size, nestling survival rates, strata occupation, and diet composition of the Plusli-crcsted Jay.
Romed 6 tehruary 2011, Accepted 29 August 2 Oil.
Ihe family Corvidae is represented in South
America by the genera Cyitnoconix and Cyanolyca
i Madge and Bum 1994). These genera occur across
dte neotropical region and include 17 species of
^‘inocorax and nine species of Cyanolyca (Gill
“d Donsker 2011). The Plush-crested Jay ( Cya -
'"wruv chrysops) is widely distributed throughout
l'0Ul^ America from Amazonia to northeastern
Argentina occupying a variety of habitats that
l llude >everal types of forests: mixed rainforest,
-mi-deciduous foresi, Cerrado (one of the largest
:al savannas of the world) (Silva and Bates
- "'-I. scrub, and also semi-urban areas. It is not
"u'ly found in the interior of primary forest, but
to be more frequent at the borders and in
-^life's (Goodwin 1976. Anjos 2009). It is poorly
l^eations. — Field observations
were made 6 days per month in each area from
87
88
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 1. March 2012
FICi. I Study areas in southern Brazil (Parana State) where Plush-crested Jay flocks were monitored: VVP (Vila Velh.
State Park), KEP (Klabin Ecological Park), and RTF (Ribeirao do Tigre Farm).
October 1995 to December 1996. We used 8 X
35 binoculars for observations that began at
sunrise and lasted all day. Field observations
were conducted during 1.800 hrs. The daily
procedure was to walk along previously estab¬
lished transects to find one flock, anti lo follow
this Hock throughout the day. Particular meth¬
ods were used to document breeding and
foraging behaviors. The birds were not banded
but we were able to distinguish different flocks
(at least 2) at each site as American jays maintain
an area of dominance around active nests (Anjos
et al. 2009). We followed Gill and Donsker (201 1 )
for nomenclature of birds and the Missouri
Botanical Garden (2010) for nomenclature of
vegetation.
Flock Size. Home Range, and Territory. — Wc
recorded the number of individuals in the Hocks :i;
the different sites and periods. We separated the
year into two periods: the first when aggressive
territorial behavior was observed between differ¬
ent flocks (the territorial period), and the second
when aggressive behavior was not observed (the
home-range period). We plotted each observation
of Plush -crested Jay flocks on each transect onto a
map (Luginbuhl et al. 2001) for both territorial
and home-range estimates. We used these obser¬
vations to calculate the size of the overall territorv
VJA.BI,5 C|iaracienstics of areas where Plush-crested Jays were monitored in the Atlantic Forest, southern Bra/-
V.la Velha Slate Park I VVP), Klabin Ecological Park (KEP). and Ribeirao do Tigre Rum (RTF).
vvp
KEP
Vegetation type*
No. tree species**
Dominant tree species
Climate*
Average temperature*
Average rainfall*
Coordinates
Total area
Sample area
Forest cover
Grassland
Human built
Agriculture
RTF
Mixed rainforest (MF)
350 species: 13% endemic
Araucaria cingustifolia. Hex paraguariensis,
Camponesia xanthocarpa, Ocolea porosa,
O. odorfera
Cft>
>8 C 19.5 =c
1,550 mm 1.700 mm
25 15' S, 50 05' W 24° 17' S, 50 ’35' W
3,790 ha 11,196 ha
150 ha
23%
60%
17%
140 ha
60%
30%
10%
Seasonal semi-deciduous forest (Sf
220 species; 10% endemic
Aspidosperma polyneuram. Cedrt
fissilis, Balfourodendron
riedelianum
Cfa
21 C
1,600 mm
23° 27' S. 51° 15' W
1.285 ha
150 ha
20%
20%
* Mcndonya and Danni-
warin: Cfa = subtropical
— — - - - - - 60%
humid w7th warm summer-.111* Ro,la 1 ^kf = subtropical humid with warm summer t
Uejimaet al. • BREEDING AND FORAGING OF THE PLUSH-CRESTED JAY
89
and home range of the jays using the minimum
convex polygon method (MCP) (Mohr 1947,
Odum and Kuenzler 1955). This consists of
joining the outermost observation points for each
flock with a straight line. The largest polygon
obtained was taken as the size of the territory of
a flock. This procedure was chosen due to its
simplicity and wide use in ornithology (e.g..
Jullien and Thiollay 1998. Wiktander el al. 2001.
Ribeiro et al, 2002. Duca et al. 2006).
Reproduction.— Reproductive activities were
observed dunng -720 hrs of field observations
(240 hrs/area). We recorded the number of eggs
hid and hatching data, and monitored the
development of nestlings. Nestlings were mea¬
sured the second week post-hatching. A nest was
considered depredated when the entire brood
disappeared or when there was no evidence inside
or underneath the nest of any other kind of loss.
Activities related to incubation, provisioning of
the brooding bird or nestlings, and cleaning of the
nesf 'verc also recorded. Two fledglings were
color banded. The nests were measured (height,
diameter, brood chamber diameter and diameter
' ivv'rs used in its construction) alter nesting
activities had ceased, collected, and deposited at
the Capuo da Inibuia Museum ot Natural History
tC. uritiba. Brazil) and the Klabin Ecological Park
Museu,n (Telemaeo Borba, Brazil).
paging.- We made field observations of
'paging behavior during 1.080 hrs (360 hrs/area).
'• used focal animal sampling following Altmann
with 5-min breaks between observ ation of
?erem individuals or flocks (scan-sampling).
procedure should have increased data inde-
penT^nce. The food item, capture substrate, and
"“lum were recorded for each foraging event of
1,1 individual jay. We considered three levels ol
strata, besides the ground: undergrowth (up
Jj1 - m above the ground), middle level (from 2 to
ll: and suheanopy (from 7 m above the ground
1 'ii below the canopy). The substrates were:
c! Jun{T branches, leaves or epiphytes, and air lor
foraging.
. Statistical Analyses.— The R X C test for
dependence (G-test) was used to evaluate the
Mgnificance (P = 0.01) of proportions of events
dated to foraging behaviors among the three sites
'.Fowler and Cohen 1986).
RESULTS
Rock Sizes, Home Range, and Territory —
lerritorial behavior was first observed in early
October (spring). The size (x ± SD) of flocks
during this period was smaller at VVP (6 ± 0.8
individuals) and at RTF (5 ± 0.2 individuals) than
at KF.P (II ± 0.6 individuals). Territories were
smaller at VVP (5 ± 0.3 ha) and KEP (5 ± 0.7 ha)
than at RTF (10 ± 0.4 ha: Fig. 2). Territories at
KF.P and RET did not overlap and were separated
by 350 and 500 m. respectively. However, over¬
lapping (~ 20 %) of territories was detected at
VVP. The area of greatest anthropogenic food
supplementation had the greatest overlap at VVP,
and aggressive territorial behavior was frequently
observed at this site. Aggressive territorial
behavior between individuals started with “bob¬
bing", (described by Hardy 1961). followed by
alarm calls. Direct contact between individuals
was recorded when the dominant individual
touched the back of an opponent after sweeping
flights. At times, the opponent persisted and the
two individuals attacked each other with their feet
while the remainder of the individuals in the (lock
stayed close, emitting alarm calls. Territorial
behavior was relaxed throughout the end of
summer (Mar). Flock sizes were largest in the
home-range period (Apr-Sep, mostly fall/wintei )
at KEP ( 15 ± 1.92 individuals), followed by RTF
(11 ± 1.48 individuals), and VVP (8 ± 1.63
individuals). Home ranges were smaller at VVP
(20 ± 1.34 ha) than at KEP (30 ± 0.89 ha) and
RTF' (30 ± 1 .04 ha; Fig. 2). Overlapping of home
ranges (where aggressive behavior was not
recorded among individuals ol difterent flocks)
was —25% in all areas.
Reproduction.— Five active nests were found,
three at VVP and two at KEP. The first active nest
was found in mid-October at VVP. Nests were
placed closer to the animal breeding center at
KEP and to the restaurant at VVP. Only one nest
was successful at VVP. The other two nests found
in this area were depredated several times (n - 4)
after hatching. Nests were reconstructed (each 1 8
to 21 days after depredation) into February, but
none was successful. Two new nests were 50 m
from the previous nests and the other two were
in trees that were closer, but no new nests were
found in the same tree in which a nest was pre¬
viously depredated.
Nests 7 = 5) were placed in a fork between 4
and 7 m above the ground in the middle stratum of
the forest, and were rounded and consisted of a
platform with a brood chamber in the center. They
were built with sticks up to 3 mm in diameter, and
the brood chamber was lined with twigs <1 mm
90
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 1. March 2012
Spring
Fall/winter
w so*co n measurements (mm) in the Atlantic Forest, southern Brazil: Klabin Ecological Park
(KEP) and Vila Velha State Park (VVP).
Nesi U
Nest height
Nest diameter
1 KEP
2 VVP
3 VVP
4 KEP
5 KEP
Mean ± SD
Brood chamber height
Brood chamber diaroMW
152
180
190
125
108
152 ± 31.27
287
282
275
290
343
295.4 ± 24.33
99
120
108
90
80
99.4 ± 13.88
180
170
162
150
148
162 ± 12.07
Uejima et al • BREEDING AND FORAGING OF THE PLUSH-CRESTED JAY
91
FIG. 3.
Eggs of Plush-crested Jays in Klabin Ecological Park (KEP) in southern Brazil. Photograph by A. F. R. Gatto.
and offspring care. Food was brought to the
brooding bird by helpers in the flock after
constant calling for food. The helpers either
directly delivered food to the nestlings or to the
lJl|ll in the nest; this individual received the food
Jl|d redistributed it to the nestlings. The average
dumber of visits to provision nestlings varied
’froughout their development: the average was
t;'c visits/hr in the lirsl week; seven visits/hr in
L second week, and nine visits/hr in the third
l-' The average visitation rate was the same
-Prdless of brood size. Helpers were recorded
"uing fecal sacs from the nest and providing
(ic!ense against predators in addition to helping
Pjov'ision the nestlings. Up to six helpers were
:,early observed defending a nest against tufted
capuchins ( Cebus cippelci), which were kept far
front the nest.
Nestlings left the nest ~23 ± 1.26 days after
hatching and, for the next 20 days, they solely
depended on food provided by the parents and
helpers. Fledglings began feeding by themselves
after 25 days and were completely independent at
90 days. The two color banded fledglings marked
in 2005 were observed helping in 2006.
Foraging.— We observed 3.508 foraging events
(1.209 at VVP; 1,700 at KliP; and 599 at RTF;
Table 4). The capture technique used by Plush-
crested Jays was ‘gleaning' (described by Robin¬
son and Holmes 1982). The diet (recorded in all
3.508 events) included invertebrates (spiders,
millipedes, beetles, caterpillars, grasshoppers,
I KEP
2KEP
3 KEP
3 KEP
5VVp
6 Wp
7 KEP
8 KEP
’KEP
Mean ± SD
Tarsus
38.8
36.4
36.5
39
38
36
39.1
36.8
40.5
37.9 ± L46
Cut men
20.2
18.2
19.4
20.6
15.2
19
17.6
17.5
18.2
18.4 ± 1.53
Noslril/Bitl
Wing
12.2
92
11
80
12.7
89.3
12.1
89
12
110
14.1
110
10.7
82.4
11.3
82.4
11.1
82.5
11.9 ± 0.99
90.8 ± 10.90
Mass
140
115
120
130
100
100
115 ± 12.47
92
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 1. March 2012
4p wwof £?Tency (,PerCenIage) °f f°°dS COnSUmed by adu,t Plush-crested Jays in southern Brazil: Vila
cilia State Park (VYP). Klahin Ecological Park (KEP), and Ribeirao do Tigre Farm (RTF).
Food item
VVP
KEP
RTF
Total
Insects/ invertebrates
External resources*
Fruit
Vertebrates
Totals
964 (80)
134 (11)
31 (3)
80 (7)
1.209 (100)
1.457 (86)
103 (6)
89 (5)
51 (3)
1.700 (100)
559 (93)
21 (4)
1 1 (2)
8 (1)
599 (100)
2,980 (84.9)
258 (7.4)
131 (3.7)
139 (4)
3.508 (100)
* Garbage, maize seeds.
and mol I asks), fruit, many kinds of foodstuffs
given or discarded by humans (garbage, bread,
meal, cookies, grain plants, and maize), and
vertebrates (frogs, eggs, and nestlings, and small
reptiles). Invertebrates were the most commonly
used tood resource at all ihree areas, but the
percentages of each item varied (G = 105.06;
df = 6; P < 0.01; Table 4). Food resulting from
human activities was used more at VVP and KEP
than at RTF where the most commonly consumed
items were insects and invertebrates.
Plush-crested Jays fed on fruit from 24 plant
species, but only the fruits of Syagrus roman-
zofficma were commonly eaten in all three are,;'
( fable 5). A greater variety of fruit was observed
to be consumed at KEP ( 13 species). while 10 and
five Iruit species were recorded at VVP and RTF.
respectively. The fruits most frequently recorded
were: Eriobotrya japonica , Diospyros kaki. Phil¬
odendron spp., Casearia sylvestris. Rapanea
ferruginea, Syagrus romanzoffianum, and Fine
enormis.
TAELE 5. Plant species used by Plush-crested Jays and
relative frequencies of fruits consumed in southern Brazil-
“ ,VVPX **
(KEP), and Ribeirao do Tigre Farm (RTF).
Plant species
VVP
Urera haccifera
Psidium cattleianum
Paullinia carpopoda
Lepismium cruciforme
Ficus enormis
F. insipida
F. monckii
Melia azedaracli
Syagrus romanzoffiana
Casearia sylvestris
Rapanea ferruginea
R. umbel lata
Philodendron spp.
Cestrum calycinum
Miconia spp.
Sty rax leprosus
Citronella gongonha
Morus nigra
Trema micrantha
Diospyrus kaki
Citrus spp.
Eriobotrya japonica
Peschiera australis
Celt is iguanaea
Totals
KEP
RTF
3
4
2
1
3
0
2
1
4
7
4
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
2
12
15
6
14
4
1
I
1
6
1
9
0
13
0
0
85
0
0
0
0
0
I
0
I
7
0
0
0
0
0
0
0
0
0
0
0
1
0
1
1
12
The foraging forest stratum and capture sub¬
strate were recorded at 2,980 foraging events (964
VVP, 1,457 KEP, 559 RTF; Table 6). 'Hie pro¬
portion ol observations related to foraging stratum
differed among the areas studied (G = 178.2; df
=* 6; P < 0.01). The understory and the middle
level were the most frequently used strata in all
areas, but the ground and the subcanopy were
proportionally used more at VVP and RTF
respectively.
The proportions of use of the capture substrate'
also differed among the three areas (G - 80.84.
df = 8; P < 0.01). Branches and leaves were
generally the most frequently used substrates in
the understory and the middle level in all art4>
(C = 24.18; df = 6; P < 0.01): epiphytes were
less used, particularly in the subcanopy, and the
air was the least used.
Food caching behav ior was also observed and
recorded (n = 110). Each individual had its own
cache up to 100 m from where the food was
captured. Each cache contained only one unit ot a
given item (except for maize, for which each cache
could contain up to 12 seeds). Leaves or small
sticks were laid over the food cache. We did not
observe individuals defending their caches. Cach¬
es locations were in the ground ( n — 40), in
epiphytes (// = 47). and on branches (n = 23). The
caches mainly contained seeds of .4. angustifolia,
bones, maize, and seeds of 5. romanzoffianum).
Uejima el al. • BREEDING AND FORAGING OF THE PLUSH-CRESTED JAY
93
TABLE 6. Number of feeding events by strata and
aging substrate of Plush-crested Jays at each of the study
lies in southern Brazil: Vila Velha State Park (VVP),
Klabin Ecological Park (KEP), and Ribeirao do Tigre
Farm l RTF I.
Sc*
VVP
KEP
RTF
Totals
Indemon
Branches
164
204
56
424
Leaves
132
187
70
389
Epiphytes
81
106
30
217
.Air
8
17
13
38
Subtotals
385
514
169
1.068
Middle level
Branches
122
168
89
379
Leaves
138
224
90
452
Epiphytes
82
137
39
258
Air
6
17
8
31
Subtotals
348
546
226
1.120
Subcanopy
Branches
11
118
42
171
Leaves
17
93
56
166
Epiphytes
17
32
18
67
.Air
0
12
6
18
Subtotals
45
255
122
422
Ground
186
142
42
370
Totals
964
1.457
559
2.980
Ihe number of foods cached did not differ between
seasons (G =
2.06; df =
3; P > 0.01 ).
DISCUSSION
' l;lrger size of the territory at RTF than a
'pand KEP was probably related to the amount
01 SuPplementary food at the two latter sites.
L:ir^ territory sizes at RTF may compensate for
'u' *vith lower food availability. Marzluft and
VJlherlm (2006) observed that crows and ravens
1 1 ' spp.) had smaller home ranges and higher
ambers of fledglings near settlements. However,
1 tound larger home ranges at KEP than at VVP.
;ilhougb nock Size was similar. This may be due
l| higher predation rates at VVP (lower fledgling
Auction) than at KEP. allowing a smaller home
r^e- Territory size expanded at all sites during
!!,c summer (Fig. 2). probably due to addition of
iledglings to flocks or possible variation in food
abundance.
of the available data published on
•oiiocorux species indicate communal bleeding
"[Un active nest in each group and helpers in
IL‘ nest during the nesting period and while the
.’"iing are dependent (Anjos el al. 2009). We
documented this system in our study of the Plush-
crested .lay. Alternation among individuals was
observed during the incubation period, unlike for
most Cyanocorax jays, where only one individual
incubates (e.g.. Inca Jay |C. yncas |: Alvarez
1975). This behavior appears similar to that of
the Curl-crested Jay (C. crisiatellus), where short
substitutions were observed (Amaral and Macedo
2003). Two individuals were observed incubating
for Azure Jays (C caendeus). at times with relief
(Boesing and Anjos. In Press). Brooding Plush-
crested Jays were observed being ted by several
individuals of the flock, as reported for most
Cyanocorax jays (e.g.. Moore 1938. Crossin
1967). The type of vocalization (pair call) before
feeding lias also been recorded for other Cyano-
coiilx species: Curl-crested Jay (Amaral and
Macedo 2003), Tufted Jay (C. dickeyi) (Moore
1938. Skutch 1987), and Azure Jay t Anjos and
Vielliard 1993; Boesing and Anjos. In Press).
Feeding of both nestlings and the brooding
bird by helpers is common in several species of
Cyanocorax jays (e.g.. Bosque and Molina 2002.
Amaral and Macedo 2003). Breeders assisted by
helpers were observed to fledge more young in
the case of the Florida Scrub Jay (Aphelocoma
coerulescens) (Woolfenden and Fitzpatrick 1984).
a cooperative jay in North America. We observed
possible predation of nestlings and fledglings by
hawks (Roadside Hawk | Huteo magnirostris] and
Yellow-headed C.aracara \Milvago chimachima]),
marsupials (e.g.. Didelphis spp.), and reptiles
(e.g.. Tupinambis spp.). One South American
coati (Nasna nasua) was recorded preying on a
fledgling on the ground. The most common cause
of the lack of reproductive success in nests of
corvids is predation (Marzluff 1985).
Neotropical jays occupy different forest strata,
but preferences vary among species (Anjos et al.
2009). The Plush-crested Jay frequents all lorest
strata, but seems to prefer the understory and
middle level of the forest, despite frequently using
the ground, where food is available (VVP and
KEP). All available layer-,, including the ground,
are used by Inca Jays (Alvarez 1975) and
Purplish-backed Jays (C. beecheii ) (Raitt and
Hardy 1979). Azure Jays often only frequent the
canopy of the forest (Anjos 1991). The availabil¬
ity of food at VVP favors use of resources on the
ground, whereas the density of vegetation pro¬
motes the use of higher strata at RTF and KEP.
Caching behaviors are widespread throughout
the Corvidae. Food storage is commonly observed
94
THE WILSON JOURNAL OF ORNITHOLOGY • Voi 124. No. 1. March 2012
when birds have more food available than they are
able or willing to eat at once, especially if the food is
of a kind that will remain edible for some lime
(Goodwin 1976). This behavior is poorly documented
in Cyarutcomx jays. Caching behavior was observed
in captivity by the Tufted Jay. but it does not appear
to have been observed in the wild (Crossin 1967).
Anjos (1991 ) observed this behavior in Azure Jays in
both captivity and in the wild; this species was
observed storing seeds of Araucaria crngustifolia in
the canopy of the MF (Anjos 1991). The Flush-
crested Jay caches the seed of A. angustifoliu on the
ground, and it should be considered as an incidental
disperser ol this tree species. Some seedlings of A.
angustifolia were recorded in places, around the
animal breeding center at KEP, where individual
Plush-crested Jays were observed caching seeds of
this tree species.
The Plush-crested Jay exhibited variations in: ( I )
forest strata occupancy (preference for the under-
story and middle level ol the forest, frequently
using the ground where there was human food
supplementation); (2) territory and home range
sizes (both smaller when food supplementation was
available); and (3) foraging behaviors (more
diverse in less disturbed habitats). These charac¬
teristics demonstrate the plasticity of this species in
habitat use, similar to most species of Corvidae.
ACKNOWLEDGMENTS
We are graietul tor logistical support in Vila Vclhn Stale
Park. Klabin Ecological Park and Ribeirao do Tigre Farm.
Personal of the Environmental Police of Parana State also
assisted us during field work. Plants were identified by M.
C. Dias (State University of Londrina). Financial support
for field work was provided by the Federal University of
Parana (UFPR>. Pedro Sherer-Neto, L. C. Millco, and F. C.
Straube made important suggestions during the field work
and revised an earlier version of the manuscript, which was
presented as a Master Thesis at UFPR. We appreciate the
valuable suggestions by J. M. Mar/luff. Tom Webber, and
C. E. Braun, which improved the last version of this
manuscript. The authors received research grants from
CNPq (Brazilian Council for Development of Science and
Technology) to the first and third authors, and from CAPES
(Coordination for the Improvement of Higher Level
Personnel. DS). to the second author.
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The Wilson Journal of Ornithology 124(1):96-105, 2012
SEXUAL SELECTION AND MATING CHRONOLOGY OF
LESSER PRAIRIE-CHICKENS
ADAM C. BEHNEY,157 BLAKE A. GRISHAM.' CLINT W. BOAL,* 2 *
HEATHER A. WHITE AW.' 6 7 AND DAVID A. HAUKO 5S4
ABSTRACT. — Little is known about mate selection and lek dynamics of Lesser Prairie-Chickens ( Tympanuchus
pallidicinctus). We collected data on male territory size and location on leks. behavior, and morphological characteristics
and assessed the importance of these variables on male Lesser Prairie-Chicken mating success during spring 2008 and 2009
in the Texas Southern High Plains. Wc used discrete choice models and found that males that were less idle were chosen
more often for mating. Our results also suggest that males with smaller territories obtained more copulations.
Morphological characteristics were weaker predictors of male mating success. Peak female attendance at leks occurred
during the 1 -week interval starting 13 April during both years of study. Male prairie-chickens appear to make exploratory
movements to. and from, leks early in the lekking season; 13 of 19 males banded early (23 Feb-13 Mar) in the lekking
season departed the lek of capture and were not reobserved ( I I yearlings, 2 adults). Thirty-three percent (range = 26-51' h
of males on a lek mated (yearlings = 44%. adults - 20%) and males that were more active experienced greater mating
success. Received 2 May 2 Oil. Accepted 2S July 2 Oil.
Males in lek mating systems aggregate on
arenas (leks) which females visit for breeding;
males provide no parental care or resources to
females, other than genetic material (Hoglund and
Alatalo 1995). Sexual selection is typically strong
in lek mating systems where some individuals
obtain many mating opportunities while others
obtain none (Robel 1966, Gibson and Bradbury
1985, McDonald 1989) and, in many species,
males have evolved elaborate courtship displays
and ornaments. Females are thought to select the
highest quality males to maximize direct (survival
or clutch size.) or indirect benefits (good genes)
(Bradbury and Gibson 1983, Reynolds and Gross
1990).
Vocal, morphological, territorial, and behavior¬
al characteristics have been examined among
lekking grouse species with regard to mate choice
(e.g., Robel 1966. Gibson and Bradbury 1985,
'Texas Cooperative Fish and Wildlife Research Unit,
Department of Natural Resources Management. Texas Tech
University. Lubbock. TX 79409, USA.
2 U.S. Geological Survey, Texas Cooperative Fish and
Wildlife Research Unit. Department of Natural Resources
Management, Texas Tech University. Lubbock, TX 79409,
USA.
'Texas Parks and Wildlife Department, Texas Tech
University, Lubbock, TX 79409, USA.
U.S. f ish and Wildlife Service, Texas Tech University
Lubbock, TX 79409, USA.
5 Current address: Cooperative Wildlife Research Labo¬
ratory. Southern Illinois University, Carbondale. IL 62901
USA.
"Current address: U.S. Fish and Wildlife Service. T<
tech University, Lubbock. TX 79409. USA
7 Corresponding author; e-mail; abehney@siu edu
Gibson et al. 1991, Gibson 1996. Hoglund et al.
1997, Nooker and Sandercock 2008). Correlates
of male mating status (mated vs. non-mated) for
Greater Sage-Grouse ( Centrocercus urophasia-
nus) included display rate, lek attendance, and a
vocal component (Gibson and Bradbury 1985).
Gibson cl al. (1991) found that female choice in
Greater Sage-Grouse was related to male vocal¬
ization performance, previous mating locations o?
females, and choices of other females. Specifical¬
ly, initial attraction of female Greater Sage-
Grouse to males was based on vocalizations while
probability of mating was related to male display
rate (Gibson 1996). Male Sharp-tailed Grouse
( Tympanuchus phasianellus) holding central ter¬
ritories obtained more copulations than peripheral
males (Gratson et al. 1991), although Gratson
(1993) concluded that dance time and auditory
characteristics were better predictors of matin;:
success than territory' location. Alternatively,
display and aggressive behaviors were better
predictors of male mating success for Greater
Prairie-Chickens (T. cupido) than territory char¬
acteristics (Nooker and Sandercock 2008).
Lesser Prairie-Chickens (T. pallidicinctus) are a
lek-mating gaxise. inhabiting short and mixed
grass prairies of the southern Great Plains. Signit
icant population declines throughout much of l her
historic range (Hagen and Giesen 2005) have
resulted in their designation as a 'candidate for
protection under the Endangered Species Ad
(USDI 2008). Little is known about sexual selection
and lek dynamics of Lesser Prairie-Chickens, and
future research and conservation could benefit I rod
information on when prairie-chickens mate, how
96
Behneyetal. • PRAIRIE-CHICKEN BREEDING BEHAVIOR
97
many males mate, and what characteristics influ¬
ence male mating success. The objectives ot our
study were to (1.) assess the roles of behavioral,
territorial, and morphological characteristics tor
Lesser Prairie-Chicken mate choice, (2) report dates
if peak female attendance and copulations, and (3)
issess the extent of mating skew on prairie-chicken
Ids.
METHODS
S ntd\ Area,— Our study occurred on private
itos in Cochran and Yoakum counties in the
lews Southern High Plains Ecoregion (Llano
Esiacado). The area consists of a matrix of
grassland and cropland (Wu et al. 2001) among
j level to gently undulating landscape with small
■egetated dunes providing infrequent topograph¬
'll relief. The dominant vegetation was shinnery
to iQuercus havardii ) intermixed with sand
■agebnish ( Artemisia filifolia), grasses, and forbs
'Pettit 1979, Woodward et al. 2001 ).
ihe mean annual precipitation was 48.3 cm for
to period 2000-2009 (50.3 and 45.2 cm in 2008
■to 2009. respectively) with average summer
Tun-Aug) and winter (Dec-Feb) temperatures
’I 35.4 and 5.4 C, respectively. Extreme high
to low temperatures were 39.5 and -13.4 C,
especti vely (U.S. Department of Commerce
-1 h) The average elevation of the study area is
'"U00 m.
Held Methods,— "We conducted this study on
|,l||r different leks during spring 2008 and 2009.
I " ° leks were sampled in 2008 and three in 2009
""h °ne sampled in both years. Grass cover on
rv leks was too high and dense to see the birds
Ts continuously. Thus, we selected leks lor this
'toy based on vegetation characteristics that
1 ditated identification of color bands on legs ot
I^aine-chickens.
'Ve captured male Lesser Prairie-Chickens
walk-in-funnel traps (l laukos ct al. 1990.
Boeder and Braun 1991) early in the lekking
eas,|n date Feb-early Mar). We also captured
males 1
opportunistically with a bownct throughout
* lcLking season. We did not attempt to capture
iales with the bownet while females were present
Wi. Each captured male was fitted with a
,u4ue color band combination (Association ot
lC'd Ornithologists, Manomet, MA. USA) and a
tobered aluminum Texas Parks and Wildlife
bailment band (size 6). We measured mass (g).
Sh pinnae length (mm), right tarsus length
nni), and right unflattened wing cord length from
bend of wing to tip of longest primary (mm) for
each captured male. We classified prairie-chicken
age as either adult or yearling based on plumage
characteristics. Yearlings exhibited frayed tips of
the ninth and tenth primaries and spotting within
2.5 cm of the tip of the tenth primary whereas
adults lacked frayed primaries and had no spotting
within 2.5 cm of the tip of the tenth primary
(Copelin 1963). Four males (2 yearlings, 2
adults) were marked with necklace style radio
transmitters.
We placed a grid of points centered on the
activity center of each study lek to facilitate
mapping of male territories. Grid points consisted
of numbered, orange-colored, blocks ot wood (7.6
X 5 1 X 5,1 cm), placed every 5 m encompassing
the entire lek area. Some leks were sufficiently
small to be covered with a 5 X 8 grid (20 X 35 m)
while others required a 10 X 10 grid (45 X 45 m).
Grids were placed on leks in February before
birds started attending leks.
We conducted observations from a blind
(Primos Ground Max. Flora, MS, USA.) placed
within 10 m of the edge of the lek during morning
and evening lekking periods. We used binoculars
and spotting scopes to identify males, and assess
locations and behavior. We used the grid points
as a reference to plot locations ot males onto a
corresponding paper copy of the grid during 10-
min interval scan samples. Lek observations were
not conducted if a lek had walk-m-iunnel traps
present or after the bownet had been triggered
Observations were made 2-3 days/week Irom 2
February to 21 May 2008 and 5 March to 10 May
o()09 The order of leks to be monitored was
randomly selected, weekly. Leks were not ob¬
served when lightning was present or winds
exceeded ~45 km/hr. .
We recorded a description of male Lesser Prairie-
Chicken behavior every time a location was plotted.
Behavioral categories included display, moving
face off. fighting, and idle. Display involved
erecting pinnae, enlarging eye-combs, elevating
tail drooping wings, extending head and neck
forward, stamping feet, inflating esophageal air
sacs, and emitting booming vocalization (Hagen
and Giesen 2005). Moving was when the male was
walking or running but not displaying. Face off
consisted of two males in close proximity (<1 m),
facing each other at a territory boundary. lypically
in a semiprone position, but not displaying, moving,
or fighting (Hagen and Giesen 2005). Fighting
consisted of two males actively fighting each other
98
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 1. March 2012
with one typically charging the other with rapid
aggressive movements. Idle was recorded when a
male was not doing any of the other behaviors.
We noted the male that performed any
copulation attempt and the location. A copulation
attempt was defined as anytime a male was able to
put at least one foot on the female’s back. Most
copulation attempts were interrupted by other
males at varying times throughout the attempt.
We classified copulation attempts as successful
when females vigorously ruffled their feathers and
departed the lek after copulating (Hagen and
Giesen 2005).
Statistical Analyses— We used .Skew Calcula¬
tor 2003 (Nonacs 2003) to analyze mating skew
on leks. We used two indices of mating skew: X
and R (Binomial Skew Index). Lambda values
ranged from 0 to I with larger values indicating
greater skew (Kokko and Lindstrom 1997).
Positive values of R indicate some monopoliza¬
tion ot matings (skew), while 0 indicated random
mating, and negative values indicated a more
equal distribution (Nonacs 2000). /i-values, gen¬
erally. ranged from - 1 to I. although it is possible
to obtain values >1. Confidence intervals and P
values can be calculated for R (Nonacs 2000). Lek
attendance rates were calculated as the number of
days a male was observed on the lek divided by
the number ol days the lek was observed and at
least one male was present.
We assessed two characteristics of territories:
size and distance to center of lek activity. We
calculated two measures of territory size, 95%
kernel and 95% minimum convex polygon
(MCP) estimates, using plotted male locations
with >24 locations/behavioral observations.
Both metrics were computed in the ADEHABI-
TAT package (Calenge 2006) of Program R (R
Development Core Team 2008). Lesser Prairie-
Chickens appear to spend a disproportionate
amount of time at territory boundaries and we
suspect that kernel estimators overestimated
territory size. MCPs only outline the outer points
of a distribution and may be more accurate in
assessing individual territory sizes of ickking
prairie-chickens. Thus, only MCP estimates of
territory size were used Tor modeling. We report
ernel estimates of territory size for comparative
puiposas with other studies of lekking grouse
( g„ Nooker and Sandcrcock 2008). Kernel
(r =aoo«Te a "ed With MCP est'mates
, • )' A ma,c s center of activity was
computed as the centroid of all its locations Each
male’s centroid was averaged to ascertain the
center of activity for the lek.
Discrete choice models (DCM) allow inference
to be drawn about resource preferences based on
the attributes of the resource (Cooper and Mill-
spaugh 1999). These models predict the probabil¬
ity that an individual will select a certain resource
as opposed to any of the other available resources
and assume that individuals make choices that
will maximize utility (Cooper and Millspaugh
1999). DCMs are used more frequently in habitat
selection studies (e.g., Lesmeister et al. 2008.
Vanak and Gompper 2010). We followed the
example of Nooker and Sandercock's (2008)
Studies of Greater Prairie-Chickens and used
DCMs (PROC MDC, SAS Version 9.1. Can',
NC, USA) to assess correlates of male mating
success for Lesser Prairie-Chickens. Each copu¬
lation attempt represents one sample in the DCM
A female chooses one male to mate with among a
group ol males, which is considered the choice
set. DCMs allow the choice set to vary by sample,
which is necessary when multiple leks are
involved. The males (or sample of males) on
one lek compose the choice set for each
copulation attempt on that lek. We had to colled
>24 location/behavior points on the male in¬
volved in the copulation attempt for it to be
included in this analysis. Not every male on a Id
was included in the analysis, but we believe our
sample is representative of all males attending the
lek. We trapped across the entire lek area and did
not focus trapping efforts on central or peripheral
males.
Behavioral variables included the proportion ol
observations recorded as each behavior category
display, face off, fighting, idle, and moving
Morphological variables included wing cord length
(cm), tarsus length (cm), pinnae length (cm), and
mass (g). Territorial variables included distant
to lek center (m), and territory size (MCP. m
We did not use all variables in discrete choice
models due to small sample sizes. We selected the
behavioral variables display and idle to use w
models because they were uncorrelated (r = "9.1,
P — 0.59) and represented what we hypothesized to
be important in mate choice. We selected the
morphological variables mass and pinnae length
because they were uncorrelated (/• = 0.1 ,P~ 0.591
and represent a size component (mass) and a
secondary sexual characteristic (pinnae). We ah'"
included territory size, distance to lek center, and
age in models.
Belviev et al. • PRAIRIE-CHICKEN BREEDING BEHAVIOR
99
Variables were standardized by replacing each
observation by ixrx^/sXi for each lek to facilitate
dual comparison of parameter estimates as effect
AIK (Gnison et al. 1991. Agresti 2002. Nooker
and Sandercock 2008). The sign of the slope
i 'efficients indicate if that variable is positively
• negatively correlated with male mating success
and the magnitude of coefficients are directly
comparable indices of effect size. We used
\kaike’s Information Criterion corrected lor
small -amples I AIC( ) and model averaged slope
coefficient estimates across all models in the
model set to avoid basing inference on a single
model (Anderson 2008).
We only considered models with ^3 variables
due to small sample sizes. Each variable appeared
an equal number of times in the model set to
facilitate model averaging and calculating relative
importance values (Anderson 2008). We evaluat¬
'd models based on all copulation attempts
regardless of whether it was successful, and only
successful copulation attempts. We also calculat¬
ed Pearson’s correlation coefficient (r) between
each variable and the proportion of all and
'Uccessful copulations each male obtained on
>ls’ respective lek.
is generally not good practice to use all
possible models but we believe il was justified
due lo the exploratory nature of this type of
analysis. Previous studies have not examined
e*ua! selection of Lesser Prairie-Chickens and
°Ur goal was to provide a baseline for more in-
kp'h future experimental work. All models were
biologically and theoretically possible and we
USl'd model averaging to derive parameter esti
ina!es as indices of effect sizes so inference was
1,111 placed on any single model (Anderson el al.
20f|0. Anderson 2008).
RESULTS
We spent 272.5 hrs observing Lesser Prairie-
f-hicken behavior at leks during spring 2008 and
(mean ± SE = 47.9 ± 6.9 hrs/lek/yr). Study
averaged 10.5 males/morning (range = 4.4-
during the spring lekking season. Wc
Captured 22 and 14 birds in 2008 and 2009.
Actively. Thirteen of nineteen males (M
yearlings, 2 adults) captured during early trapping
essions between 23 February and 1 3 March 2008,
Were not reobserved even after extensively
Aching within 4 km of the leks of capture.
Tto*se 13 birds were not included in the analyses.
Additionally, two males in 2008 and 2009 were
banded but we were unable to collect all
morphological measurements. This left us with 7
and 12 individuals, respectively, in 2008 and 2009
with complete morphological measurements to
use for analysis.
Mean ± SE lek attendance rate of marked
males that were reobserved on study leks at least
once was 0.88 ± 0.04. We noted 163 and 76
female observations on leks in 2008 and 2009,
respectively. Female lek attendance peaked during
the 7-day interval starting 13 April in both years
(Fig. 1A). The maximum number of females
observed on a lek simultaneously was 17. We
observed females on leks during evening display
periods on one and two occasions in 2008 and
2009, respectively, and in 2008 we observed toui
copulation attempts during evening lekking.
Overall, male mating success was skewed (X -
0.60; 5-valuc = 0.30. P < 0.001). We observed 62
copulation attempts on leks in 2008. 30 ot which
were deemed successful. Copulation attempts
peaked during the 7-day interval starting 27 April
(Fig. IB). Four males were responsible for all
copulation attempts on lek Bl, which averaged
15.2 males per morning!/. = 0.54; 5-value - 0.27.
P < 0.001). Three males were responsible for
97% of copulation attempts, two ol which were
responsible for 82% of all copulation attempts.
Five males were responsible for all copulation
attempts on lek B2, which averaged 16.0 males per
morning (X = 0.77; /7-value = 0.53. P < 0.001 .
Three males were responsible tor 93 ’b of al
copulation attempts, one of which performed
79% of all copulation attempts. We observed 2)
copulation attempts in 2009, 12 of which were
deemed successful. Copulation attempts peaked
during the interval starting 13 April (Fig. I B). We
only observed one copulation attempt on lek B ,
and this lek was removed from the skew analysis.
Three males were responsible for all copulation
attempts on lek B4, which averaged 9.2 males per
morning (X = 0.58; 5-value = 0.24, P -- 0.001).
Two males were responsible for 88% of all
copulation attempts. Four males performed all
copulation attempts on lek R5, which averaged 7.8
males per morning ( X = 0.52; 5-value = 0.15, P =
0.006) with two of the males performing 82% of all
copulation attempts. The percentage of adult and
yearling marked birds that attempted ^1 copula¬
tion w'as 20 and 44%, respectively. The mean ± SE
percentage of copulations obtained on a lek for
adults and yearlings was 0.09 ± 0.06 and 0.18 ±
0.05, respectively.
100
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 1. March 2012
9
JS' !tTle Tdr 0.1) with
proportion of copulations obtained
The most parsimonious model, considering ail
copulation attempts (n = 52 copulation attempts-
19 males), included percent of time spent idle anct
MCP, and obtained 39% of the Akaike weigh1
(Table 2). All models containing idle were tanked
higher than those not containing idle, which also
had the greatest model averaged slope coefficient
(Fig. 3). The third and fourth best model1-
appeared competitive but contained pretending
variables, which contribute little to model lit as
evidenced by similar deviance values. Relame
importance values for idle. MCP. age, pinnae,
display, distance, and mass were 1.00. 0.52. 04
0. J 3, 0. 1 2. 0.00, and 0.00. respectively.
T he most parsimonious model, considering only
successful copulation attempts (n = 30 copulations.
Behneyetal. • PRAIRIE-CHICKEN BREEDING BEHAVIOR
101
TABLE 1. Characteristics measured for male Lesser
:0()9 in ihe Texas Southern High Plains.
Prairie-Chickens observed at two leks in
2008 and three leks in
Mean i SE
Calfjorv
Trail
Adult in = 10)
Yearling ( n = 9)
CV
Behavior6
Territory
Morphology
Display
Face off
Fighting
Idle
Moving
Distance to lek center (m)
Kernel size (nr)
MCP size (nr)
Wing cord (cm)
Tarsus (cm)
Pinnae (cm)
Mass (g)
0.29 ± 0.02
0.33 ± 0.03
0.00 ± o.oo
0.25 ± 0.03
0.13 ± 0.02
12.66 ± 1.40
245.07 ±41.26
108.50 ± 17.49
21.69 ± 0.12
5.83 ± 0.06
6.64 ± 0.13
783.10 ± 9.03
0.30 ± 0.03
0.35 ± 0.04
0.01 ± 0.00
0.19 ± 0.02
0.15 ± 0.01
1 1.09 ± 1.75
109.68 ± 10.73
43.29 ± 5.46
21.54 ± 0.09
5.47 ±0.11
6.88 ± 0.22
780.22 ± 13.65
36.57
41.63
295.55
53.36
44.64
56.44
81.92
84.27
2.17
7.42
11.08
6.20
h Coefncicnl of Variation values computed from pooled adult and yearling values.
’ |W»w variables are proportion of observations in each behavior category for nn individual male.
males), included idle and MCP hut obtained an
Akaike weight of only 23% (Table 3). All models
containing idle outperformed those not containing
ihe variable and it had the greatest model averaged
slope coefficient (Fig. 3). Relative importance
values for idle, MCP, age, mass, pinnae, display,
and distance were 1.00, 0.43. 0.39. 0.27, 0.17,0.08,
and 0.05. respectively.
DISCUSSION
found significant skew in male mating,
S|milar to those reported for Greater Prairie-
chickens (Nooker and Sandercock 2008). It is
tlear (hat male Lesser Prairie-Chickens that are
less idle experience greater mating success,
darling males with smaller territories also tended
’"k selected more often for mating in our study.
Morphological characteristics exhibited weaker
effects on male mating success. Males displayed
high territory fidelity within a season (alter initial
territory establishment).
Males that were less idle were more likely to
mate which we interpret to indicate that males
that are generally more active experience greater
mating success. It has been repeatedly tound that
males that display more, mate more (Gibson and
Bradbury 1985. Hdglund and Lundberg 1987,
Nooker and Sandercock 2008). Being idle likely
requires less energy than participating in other
behaviors and Gibson and Bradbury (1985)
suggest that energetic factors may have a role in
observed variation in display rates. A host ot
reasons exist for female choice based on behav¬
ioral characteristics including direct survival
benefits for the female or indirect genetic benefits
for her offspring. For example, males that do not
2. Pearson’s correlation coefficient ^^^."^Ton let-in meTex^s'stu'themffigh Plains during 2008 and
4. Splay' JIS Me. aTmoving are ,he proportion of behaviors recorded in each behavior category.
Pittance = distance from territory center to lek center. MCP = territory size tmmtntnm convex polygon). Wmg, tarsus,
P'nnae. and mass are morphological characteristics.
102
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124. No. 1. March 2012
TABLE 2. Top (A < 20) conditional logit discrete choice models of male Lesser Prairie-Chicken mating success in the
Texas Southern High Plains during 2008 and 2009 incorporating 19 males and 52 copulations regardless of success.
Model'
Deviance
Idle + MCP
Idle + Age
Idle + MCP + Pinnae
Idle + Age + Display
Idle + Dist + Mass
Idle + Pinnae
Idle + Mass
Idle + Dist + Pinnae
Idle
AIC,
AAIC,
w ,
60.95
61.17
60.95
61.14
72.80
75.58
77.32
75.21
81.47
65.17
65.38
67.40
67.58
79.24
79.79
81.53
81.66
83.54
0.00
0.21
2.22
2.41
14.07
14.62
16.36
16.48
18.37
0.40
0.36
0.13
0.12
0.00
0.00
0.00
0.00
0.00
fiESSSe 2 227-3222222125 SUES!" “ — «» ■ — “
display often may indicate a poorer physiological
condition and inability to acquire sufficient "food
resources compared to other males.
Males with smaller territories tended to mate
more, as reported by others (Wiley 1973, Hovi
et al. 1994). Our finding of distance to lek center
having little to no effect on mating success is in
contrast to most previous research (Ballard and
Robel 1974, Kruijt and de Vos 1988, Gratson et al.
1991, Rintamaki el al. 1995) although Gibson
and Bradbury (1985) and Nooker and Sandercock
(2008) also found that territory location was not
important in mate choice. Our correlation analysis
suggested that males closer to the center of the lek
mated more than peripheral males. Smaller terri¬
tories are typically associated with areas on the lek
with higher male density (Wiley 1973). Areas of
high male density arc thought to be a result of
males relocating their territories around successful
males and intruding into their territories in hope of
gaining copulations (Landel 1 989). Rintamaki et al.
(1995) noted this phenomenon as the ‘spatial spill*
hypothesis (hotshot hypothesis, Arak 1984),
whereas males cluster around dominant males in
hope of gaining copulations. Rintamaki et al.
(1995) speculated the reason for these ‘spillover
copulations may include a surplus of females
attempting to copulate with the dominant male and
competition lor that male may cause females to
mate with adjacent males. The dominant male may
be limited by sperm depletion or adjacent males
may steal copulations from a preoccupied domi¬
nant male (Rintamaki et al. 1995). Females may
experience difficulties in comparing males and
mistakenly mate with an adjacent, potentially
poorer quality, male. It is not clear whether
territory size or location is a cause or effect of
being a dominant male (Gratson et al. 1991).
It is possible that radio transmitters affected
reproductive performance of prairie-chickens. The
lour radio-marked males were all on the same lek
and included two adults and two yearlings. Only
variable
choice models de^cribimf effwTV C°efru;ients (P,US or m,nus unconditional SE) of standardized variables from discrete
(light gray) and only successful c T c Le^er Prairic'Ch,cken characteristics on obtainment of any copulation attempt
categorical adult or yearling.' DisoUv miTdl (dark.gray) ,n ,he Texas Southern High Plains during 2008 and 2009. Age is
is distance from territory center lo lek - ^ proponjon nl behaviors recorded as each behavior category. Distance
morphological characteristics Frm.- hirc^ ls ,erntory size (minimum convex polygon). Pinnae and mass are
• trro, bars extending outs.de the region 5 to -7 are not shown completely.
Behneyetal. • PRAIRIE-CHICKEN BREEDING BEHAVIOR
103
TABLE 3. Top (A < 10) conditional logit discrete choice models of male Lesser Prairie-Chicken mating success in the
Texas Southern High Plains during 2008 and 2009 incorporating 19 males and 30 successful copulations.
Model-
k
Deviance
AICf
AA1C,
W/
Idle - MCP
2
22.96
27.41
0.00
0.24
Idle + Ase
2
23.10
27.54
0.13
0.22
Idle - MCP + Mass
3
22.06
28.98
1.57
0.11
Idle + Ase - Mass
3
22.34
29.27
1.86
0.09
Idle - MCP + Pinnae
3
22.58
29.50
2.10
0.08
Idle + Age + Display
3
23.01
29.93
2.52
0.07
Idle + Pinnae
2
25.60
30.04
2.63
0.06
Idle + Mass
2
26.35
30.80
3.39
0.04
Idle + Dist + Mass
3
25.15
32.08
4.67
0.02
Idle - Dist + Pinnae
3
25.59
32.5 1
5.11
0.02
Idle
1
30.64
32.78
5.38
0.02
Idle - Display
2
29.63
34.08
6.67
0.01
Idle + Dist
2
30.58
35.02
7.62
0.01
' Ule = proportion of time spent idle; Display = proportion of time spent displaying; Dist - distance from territory center to lek center. MCP territory size
emmum convex polygon); Pinnae and Mass arc morphological measurements; Age = yearling or adult.
one of Ihe radio-marked males mated (a yearling).
Lillie information is available on the effects of
radio transmitters on male grouse reproductive
performance although Boag (1972) reported
radio-marked captive Red Grouse ( Lagopus
lagupus scotica ) were less active than controls.
The small sample of radio-marked males in our
9udy prevented any test of effects.
Territory occupancy stabilized —13 March in
-MK. Males captured after 1 3 March during both
years of study were reobserved on the lek of
capture whereas in 2008, many males captured
Ndore 13 March were not reobserved. In contrast.
Haukos (1988) reported that, within the same
area, territories were unstable and he did not
1 i,serve any copulation attempts on leks whereas
"e observed 91. We suspect this inconsistency
ma.v he due to differences in vegetation on leks
belvveen the two studies. Haukos (1988) reported
fetation on the leks was sparse, if present at all.
and physical structure was frequently altered by
'ind. Our study occurred 20 years later and
accession of vegetation had covered leks with
Sh°rtgrass and small shrub cover.
banded numerous males on leks early in the
-kking season that did not establish territories at
'•se sites. Unfortunately, we did not radiomark
*** individuals. Thus, fate of the males that
^parted their lek of capture and were not
observed is unknown. Hagen et al. (2005) lound
•to some yearling (20%) and adult (8%) males
'Witched leks between years with an average
^ce traveled of 3.3 and 3.1 km. respectively,
was well within our search areas but we failed
lo relocate any of the males at other leks. Haukos
and Smith (1999) observed similar patterns of male
movements and satellite lek formation just prior to
female attendance. Our data, and those of Haukos
and Smith (1999) and Hagen et al. (2005) suggest
that estimates of population size from lek counts
may be biased if these males did not establish
territories on a lek (Walsh ct al. 2010). Research
using early season radiomarking to examine early
season dispersal and inter-lek movements within a
season could prove valuable for understanding lek
dynamics and gene flow, and facilitate bettei
estimates of population size,
ACKNOWLEDGMENTS
Funding was provided by the Texas Parks and Vvildlite
Department. The Department of Natural Resources Man¬
agement at Texas Tech University and the USGS Texas
Cooperative Fish and Wildlife Research Unit also contrib¬
uted resources. This research would not have been possible
without the private landowners who graciously allowed us
to work on their land Wc thank D R. Lucia for assistance
throughout this research as well as N. E. Pinus, A. J.
Teague. C G. Frey. R. T. Sadowski. and C J. Kveton lor
help in the field. Wc also thank D. B Lesmeister for
assistance with discrete choice models. M I Butler. P. B.
Wood. C. A. Hagen. R. M. Gibson, and two anonymous
reviewers provided valuable comments on this manuscript.
T rade name products are mentioned to provide complete
descriptions of methods: the author's and their institutions
neither endorse these products nor intend to discriminate
against products not mentioned.
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The Wilson Journal of Ornithology I24( 1): 106-1 12, 2012
LEK BEHAVIOR OF THE PLOVERCREST
(STEPHANOXIS LALANDI , TROCHILJDAE)
MARCO AURELIO PIZO1
ABSTRACT.—! examined the lek structure and behavior of male Plovercrests ( Stephanoxis lalandi ) at a lek in southern
Brazil. The lek included seven territorial males; the distance between neighboring lek territories was 14.8 ± 6.3 m.
Territory size was 11.4 ± 4.4 nr. Territory size and distance between territories were among the lowest reported for
Trochihnae hummingbirds. Lek attendance by territory owners fluctuated throughout the day. Activity slowly diminished
after an initial period of activity after arrival at sunrise, but increased again between 0900 and 1 500 hrs. All males left their
territories by 1830 hrs. Males sang at a similar rate (74.8 T. 14.5 songs/min) throughout the lekking season, but not
throughout the day. There was no relationship between lek attendance and singing rate, two parameters that potentially
affect mating success in lekking birds. Considerable interspecific variation occurs among lekking trochi lines, indicating that
much remains to be investigated about lek behavior and structure in hummingbirds. Received 11 March 2011 Accepted W
August 20J1.
Lekking behavior has been described for at
least 28 species of hummingbirds (Pizo and Silva
2001), and studies to date have revealed consid¬
erable interspecific variation in the structure and
dynamics of hummingbird leks (Hdglund and
Alatalo 1995, Ramjohn et al. 2003). For instance,
the number of males at leks may vary from two
for Rufous Sabrcwings {Campy lopterus rufus)
(Skutch 1967) to >100 for Long-tailed Hermits
(Phaethornis superciliosus) (Skutch 1964a), Lek¬
king males may be clustered, as with male Broad¬
tailed Hummingbirds ( Selasphorus platycercus)
that remain ~7 m apart (Barash 1972), or form
loose aggregations, as with male Swallow-tailed
Hummingbirds (Eupetomena macroura) that arc
24-120 m apart (Pizo and Silva 2001 ). Activities
at leks may continue throughout the day
( Phaethornis spp.; Ramjohn et al, 2003) or be
limited to a short period such as dawn for
Swallow-tailed Hummingbirds (Pizo and Silva
2001).
Variation may reflect both phylogenetic and
ecological constraints. However, Bleiweiss
(1998) noted the repeated evolution of lekking
behavior among hummingbirds, suggesting that
behavior at leks is not limited by historical or
phylogenetic constraints. Thus, to understand the
relative roles of historical and ecological drivers
in evolution of hummingbird leks, it is essential
to expand our data base to include not only
species representing different clades of the
hummingbird phytogeny, but also to achieve a
' UNESP-Universidad Estadual Puulista,
dc Zoologia, 13506-900 Kio Clam. SP.
pizo@rc.unesp.br
Departamcnto
Brazil; e-mail;
wider geographical sampling that encompasses
contrasting ecological conditions.
My objective was to examine the lek structure
and lek behavior of Plovercrests ( Stephanoxis
lalandi) in a subtropical area in southern Brazil.
Stephanoxis is a monotypic genus of small
hummingbirds (2.2-3.4 g. 8.5-9.0 cm), that occur
in forests and semi-open areas from sea level to
>2.000 m asl, ranging from eastern Paraguay to
northeastern Argentina (Misiones). and southern
ami southeastern Brazil (Schuchmann 1999),
Males of the race .V. /. loddigesii that 1 studied
have long iridescent blue crests with a conspic¬
uous black patch on the underparts, whereas
females are iridescent green with gray below and
with feathers of the head only slightly elongated.
Hummingbirds in the genus Stephanoxis are
known to display at leks (Sick 1997. Sigrist
2006). but details of their lekking behavior are
unreported. Phylogenetically, the genus Stephu-
noxis is placed within the Emerald clade (sensu
McGuire et al. 2007), which includes genera that
exhibit lekking behavior (e.g„ Amazilia and
Campylopterus ) as well as apparently non-lekking
species (e.g.. Thaluraniu and Chlorostilhon)- I
also describe the song and aerial display of
Plovercrests. their seasonal and daily patterns of
activity at the lek. and the relationship between
lek attendance (i.e., time spent in lek territories)
and singing rate.
METHODS
Study Area.— The lek studied was at the edge of
an early secondary forest (sensu Clark 1996)
extending along the margin of a 4.5-km road
connecting Ivoti and Lindolfo Collor (29 35' S,
106
Pizo . LEK BEHAVIOR OF THE PLOVERCREST
107
51 H' W; 130 m asl), two small towns in southern
Brazil. The lek was in the transition area between
ihe forest and an old field, where small trees and
dvnhs ( Plovercrest" is among die lowest reported tor
^hi lines (Table 1 ). An additional reason tor the
Putative preference for edge habitats, pertaining to
lr°chilines, could be the importance ol an
Equate light level for the proper exhibition of
particular patches in the plumage of displaying
birds, as demonstrated for other lekking birds
(Endler 1996). Trochilines, contrasting with the
usually drab colors of hermits, have iridescent
patches in the plumage whose full brightness
depends on the correct light level. One such
iridescent patch in Plovercrests, the male crest, is
conspicuously shown in lekking displays.
The number of male Plovercrests at leks in my
study (2-7) was within the range reported for
othcr Trochilinae hummingbirds, which varies
from two to 20 (Table 1). Territory size and
distance between neighboring territories, howev¬
er. were among the lowest values reported for
trochilines (Table 1 ). Lek size in hummingbirds is
likely influenced by population density, being
negatively correlated with distance between
neiuhboring territories (Snow 1973). Territory
size may also he influenced by vegetation
structure. Stiles and Wolf (1979) noted the
smallest territories of Long-tailed Hermits in
Costa Rica were in very dense thickets, while
the largest territories were in open forest under-
story. The density of woody vegetation at the
main Plovercrest lek was intermediate between a
dense forest understory and an open field.
Provided the observation by Stiles and Wolf
( 1 1)79) can be generalized, Plovercrest leks in
forest interior should have territories closer to
each other than reported in my study,
Seasonal and daily activities at the Plovercrest
lek in my study resembled those ol other
hummingbirds. Activity at hummingbird leks is
either limited to the breeding season (Snow 196S,
1974), with the exception of Swallow-tailed
Hummingbirds that are found at leks throughout
the year (Pizo and Silva 2001), or is greatly
reduced during the non-breeding season (Stiles
and Wolf 1979). Lek activities tor Plovercrests
also coincide with the breeding period (Schuch-
mann 1999, Belton 2003).
The daily activity pattern of Plovercrests was
similar to that described for White-bellied Emer¬
alds (Amazilia Candida ; Atwood et al. 1991). and
Long-tailed Hermits (Stiles and W'olf 1979),
where males left the lek after a period of high
singing rate in the early morning. Singing rates
again increased after this interval, but then
gradually diminished during the hottest hours of
the day. The daily activity pattern at hummingbird
leks as hypothesized by Stiles and Wolf (1979)
likely reflects the need of displaying males to
leave the lek area for foraging.
110
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 1. March 2012
by a> the lek. Parameters used in preparation of the sonogram: Win*.
type-Hamming. n - 324 samples: Time gnd-Overlap 89.8%; Frequency grid-DFT, n = 2,048 samples.
The aerial display of Plovercrests, in which a
displaying bird hovers in front and slightly above
a perched bird, is similar to the shuttle displays of
North American hummingbirds (e.g.. Anna’s
Hummingbird. Calypte anna ; Stiles 1982). The
aerial display of Plovercrests appears to be
similar to those of lekking hummingbirds in the
subfamilies Trochilinae (e.g.. Swallow-tailed
Hummingbirds, Pizo and Silva 2001) and
Phaethornithinac (e.g.. Long-tailed Hermit
Stiles and Wolf 1979). as well as those of son
non-lekking species (e.g., Violet-capped Woo.
nymph [Thai urania glaucopis |; M. A. Pizo. per
obs.). This suggests the aerial display describe
is deeply rooted in hummingbird phylogeny, ar
not restricted to lekking activities. Interspecif
differences in these displays do exist. Hermit
for instance, often display their gape and thro
patterns (Stiles and Wolf 1979), which apparent
does not happen in Plovercrests. However, i
properly evaluate these aerial displays and compiu
jose of different species, recording the display
with video cameras for more detailed analysis w
be necessary. ■
I found no relationship between lek attendance
by male Plovercrests and singing rate in conuast to
White-bellied Emeralds (Atwood et al. 1991)
These authors interpreted singing rates as reflecting
dominance hierarchies among lekking males that
might affect mating success. They noted, however,
the relationship between lek attendance and singing
rate was detected when the three leks studied were
pooled for analysis, but became less clear when
each lek was analyzed separately. Thus, variation
existed among leks of a single species, and
certainly exists in an interspecific comparison.
No relationship between lek attendance and singing
rate was detected for Plovercrests. but singing rates
diltered among males. Relating differences to
possible variation in mating success represents a
challenge lor researchers because copulations are
seldom witnessed even for the best studied lekking
hummingbirds (Stiles and Wolf 1979). A better
understanding of the relationship between lek
behavior and mating success will require a
combination of field effort to locate hummingbird
nests near leks, and laboratory analysis to ascertain
the paternity of nestlings.
Pizo • LEK BEHAVIOR OF THE PLOVERCREST
111
° Mean
I I Mean±SE
F MeaniSD
Males
FIG. 4. Box plots showing lek attendance (A) and singing rate (B) of seven male Plovercrests observed at a lek. Singing
rates and territory attendance for each male were recorded during I - and 15-min periods, respective y. space our y
ObOO to 1800 hrs. Sampling was spread over 20 days from August to December 2006.
TABLE 1. Lek characteristics of Trochilinae hummingbirds. Ranges are presented whenever data for more than one
individual territory and/or more than one lek were available. Species are in alphabetical order. _
Species
Territorial
males/lck
Area of
territories (nr)
Distance between
territories (m)
Perch
height (m)
Source*
^tozilia amabilh
5
15-30
2.4-6
T 1C
6
9
A Candida
A- Kacatl
3-7
2-4
<450
14- 32
15- 22
3-15
2-6
7
14
CmPyIopterits cumpeimis
- ipennis
up to 15
2-10
11. 12
2-4
10
C excellens
2-3
16
4
r- hemileucwvs
4
8
C hrgipennis
2-4
3 3 6
4
c nifus
Petnmeiui mac r our a
Wucharis eliciae
K,ais guimeti
l>na e°chroa cuvierii
2
15
3
4
4
133-266
24-120
<30
15
38
0.3-4.2
5- 13
6- 18
6-12
13
6
2
3
Maspharux platycercus
U'Phanoxis lalandi
3
2-7
9-25
7
9-25
0.8-3.5
5
This study
yaza pella
2-20
10.5
I
‘Sources' l r>n, .losxt ? skutch ( I9S8): 3. Skuich < 1964b): 4. Skuich ( 1967): 5. Barash (1972): 6. Skutch (1972): 7. Skuich ( 1981 ): 8. Hills and Broun
"*6): 9, Atwood «al (1991);’ 10. Winker' e, al. (1992): II. Hayes el al. (1997); 12. Hayes el al. (2000); 13. Pizo and Silva (2001); 14. Hayes (2002).
112
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 1. March 2012
ACKNOWLEDGMENTS
I thank Luiz Pedreiru Gonzaga who prepared the
sonogram, and K. L. Schuchmann, Johan Ingels, and an
anonymous reviewer for critical comments on the manu¬
script. The author was supported by a research grant from
the Brazilian Research Council (CNPq # 303559/2008-0).
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The Wilson Journal of Ornithology 1 24( 1 ): 1 13—1 18, 2012
NEST SURVIVAL, PHENOLOGY, AND NEST-SITE
CHARACTERISTICS OF COMMON NIGHTHAWKS IN A NEW JERSEY
PINE BARRENS GRASSLAND
MICHAEL C. ALLEN1 AND KIMBERLY A. PETERS1 2
.ABSTRACT— We monitored Common Nighthawk ( Chordeilcs minor) nests in a managed grassland in the New Jersey
Pine Barrens in 2009 and 2010. and assessed habitat selection by comparing vegetation characteristics at nests with random
locations. We found relatively high nest survival with an estimated 79% chance of survival through incubation da. y
survival rate = 0.987, n = 16 nests); predation was the most common cause of failure (n — 2). Movements o >ount up o
45 m from the original nest site) were frequent, which introduced uncertainty that prevented us bom estimating surviva
through Hedging. Nest sites had significantly more open ground cover (e.g.. sand, lichen) than random sites, as we as ess
shrub and grass cover, shallower Utter, and lower mean vegetation height. Received 9 May Jill . Aciepit - ugus
The breeding biology and demography of the
nightjars (Caprimulgidae) has been poorly studied
worldwide relative to other groups (Straight and
Cooper 2000, Holyoak 2001. Cink 2002, Brigham
et ah 2011). The Common Nighthawk (C horde ties
minor) is the most widely distributed and best-
studied North American nightjar with a breeding
range extending from Yukon, Canada to Panama
(Brigham et al. 2011), but published data on
reproductive rates, habitat preferences, and nest¬
ing phenology are lacking. Nesting usually occurs
on the ground in a variety of open habitats including
grasslands, gravel rooftops, and disturbed or open
forests (Fowle 1946. Dexter 1952, Kantrud and
Higgins 1992). The species is still common in many
;i,eas. but has exhibited a negative long-term
population decline in the United States (Nebel
etah 2010, Sauer et al. 2011), and has been assessed
« ‘threatened’ in Canada (COSEWIC 2007). and of
conservation concern in several U.S. states (e.g.,
New Jersey; NJENSP 2008).
Only two published studies to our knowledge
l|av'e quantitatively examined nest survival rates
ot Common Nighthawks (Kantrud and Higgins
'"2, Perkins and Vickery 2007), of which only
0ne used modern techniques involving daily
survival rates (Perkins and Vickery 2007). Sim-
llarY rnost data on reproduction by this species
arc from urban rooftop nest sites (Bowles 1921:
Sutton and Spencer 1949; Dexter 1952. 1956;
Weller 1958; Dexter 1961; Armstrong 1965;
Gramza 1967) with relatively few from natural
' New Jersey Audubon Society. Cape May Bird Obser-
v;»°ry. 600 Route 47 North. Cape May Court House, NJ
982 1 0. USA.
Corresponding author;
e*mail; kpeters@massaudubon.org
settings (Fowle 1946. Rust 1947, Kantrud and
Higgins 1992. Perkins and Vickery 2007. Lohnes
2010). The only quantitative data on vegetation
characteristics at nests in natural settings are from
Kantrud and Higgins (1992) and Lohnes (2010).
Data on reproductive rates, timing of nesting
activities, and habitat preferences are important
prerequisites to effect conservation actions for
any species; these arc especially lacking tor the
Common Nighthawk.
We report data from Common Nighthawk nest
monitoring in 2009 and 2010 in managed
grasslands in the Pine Barrens of southern New
Jersey. Our objectives were to: (.1) assess nest
survival ami predation rates lor comparison with
previous studies, (2) quantity nest-site character¬
istics and test whether they differed from those
of surrounding available habitat, and (3) present
location-specific information on clutch size,
behavior of young, and phenology of nesting
activities.
METHODS
Study Area.— Fieldwork was conducted on
the - 3,000-ha Lakehurst section of Joint Base
McGuire-Dix-Lakehurst in New Jersey, USA (40
q-> ' jq 74 ^ 22' W) within the boundaries ot the
Pinelands National Reserve. Approximately
520 ha of the site are actively maintained as
grasslands by mowing, burning, and mechanical
shrub removal. All management activities at the
site occur during winter or early spring which
minimized disturbance to breeding grassland
birds. Grasslands at the site occur in three main
areas embedded within a landscape dominated by
pitch pine (Pinus rigida ) and oak (Quercus spp.)
forests. These are: (1) Test Sile-a 1 70-ha area
surrounding a 3.5-km long runway that is rarely
113
THE WILSON JOURNAL OF ORNITHOLOGY • Voi 124. No. 1. March 2012
1 14
used, (2) Jump Circle-a 1 10-ha circular grassland
used as an air-drop zone, and (3) Westfield-a
240-ha area encompassing two active airstrips.
Fields are dominated mainly by warm-season
grasses (e.g., Schizachyrium spp., Paniciun spp.)
with significant amounts of bare ground (e.g.,
sand, lichens) and early-stage shrub encroachment
(mainly P inus rigida and species in the family
Ericaceae).
Nest Survival and Predation Rates. — Nest
searching occurred within 16 irregularly shaped
plots totaling 257 ha (mean plot size = 16 ha,
range = 9-32 ha). Plot boundaries were delineat¬
ed to provide an ample amount of searchable
habitat (i.e., the maximum deemed feasible to
search) within each of the three grassland areas of
the base. Plot distribution was: six in Test Site
(76 ha), four in Jump Circle (109 ha), and six in
Westfield (71 ha). We searched two to three plots
each weekday for ~2 hrs per plot beginning on 15
April (2009) and 28 April (2010). Searching
involved one to three observers walking parallel
transects and agitating vegetation with 2-m
bamboo poles to flush nesting birds. Plot visits
rotated so that each plot was searched at least
once every 1-2 weeks.
Geographic coordinates of located nests were
obtained using a global positioning system, and
two small pieces of pink flagging were placed on
vegetation 2-3 m from the nest (i.e., creating a
line with the nest at the center). Flagging was
inconspicuous among surrounding vegetation, and
intended to aid in relocation at close range; we do
not believe that it drew the attention of predators.
Nests were generally checked every 2-3 days
until fledging, failure, or until young could no
longer be located. Five check intervals for three
nests exceeded 3 days due to logistical constraints,
four intervals were 4 days and one was 5 days.
Nest searching concluded on 15 July both years,
although all active nests at that time were
monitored until completion.
Young nighthawks arc semi-precocial and te
to move from the original nest site before fledgi
with movements that appear to increase
distance and frequency with age (Fowle 19<
DeXt?rJ952; MCA, pers. obs.). We thorougl
searched the area within -30 m of the nest (or i
last Iocat,0n , which chjcks wcrc ohscrved
in C,,'P,y "CStS- *» follow
in most cases by at least one subsequent sear
during the next nest-check. Typically" young T
days post-hatch were easy to locate as they we
invariably < 1 m from the original nest site, while
older young could not always be found. Thus, wc
calculated nest survival and predation raio.
through hatch-date only (i.e.. success = hatching
This is also the approach taken by Perkins am!
Vickery (2007), who also worked in grassland
habitat. Daily nest survival rates and confidence
intervals were calculated using the logistic nest
survival model within Program MARK (While
and Burnham 1999. Dinsmore et al. 2002). Ths
program was also used to evaluate whether or not
daily nest survival rate varied over the course
of the season. We used the likelihood ratio lest
(Shaffer and Thompson 2007; alpha = 0.05) to
evaluate model performance versus the null : i.e .
constant survival or 'no effect’) model. Nesi
failures were classified as either abandonment or
predation based on timing and evidence at the
nest. Daily predation rates were measured bv
calculating the daily survival rate based on
predation failures only, and subtracting this value
from one.
Clutch Size and Movements of Young.—1 Clutch
size calculations were based only on active nests
that were visited at least twice prior to hatching to
avoid uncertainties associated with mobile young
Observations made during checks after hatching
were used to generalize pre-fledging movements
of young from the original nest site.
Nest -site Characteristics and Habitat Selection
We measured maximum vegetation height (cm),
after finding each nest, at which vegetation touched
a meter-stick at five locations: at the nest and 0.5 n
from it in each of the cardinal directions. Weal?1’
measured litter depth (i.e., unrooted, dead vegeta¬
tion) in 2010 at the same five locations. The mean
value of the five measurements was used "
subsequent calculations and analyses. We visual!)
estimated the percent cover (±5%). alter noai -
attempts were completed, of four vegetation caie
gories within a 1 X 1-nr quadrat centered on tfc
nest: (I) grasses (including rooted live and dc.
grasses), (2) forbs, (3) shrubs (woody perennial-
and (4) open (including sand. lichens, mosses.
lilter). Only nests found prior to hatching were us*
in vegetation calculations, as young found afio
hatching may have wandered from the original "
We also measured vegetation characteristics h
2010 at 80 randomly-generated points within '•
16 plots searched for nests to better assess habiM
preferences. Points were generated in a geograPhK
information system, and constrained to be at k1'1
Allen and Peters • COMMON NIGHTHAWK NESTING BIOLOGY
115
50 m apart to minimize spatial autocorrelation.
Points were not used if they were on a road or other
airfield infrastructure, and were substituted with
the next point on the list so there were five points
completed for each plot. All random vegetation
measurements were performed between 1 5 and 23
June to coincide with the approximate midpoint
of the grassland bird nesting season. Vegetation
measurements were compared between years
(2009 vs. 2010 nests), and between nests and
random locations (2010 only) using nonparametric
Wilcoxon rank sum tests (alpha = 0.05).
Nesting Phenology. — We estimated the date of
nest initiation (first egg laid) to assess nesting
phenology for: (1) nests found during egg-laying
i assuming 1 egg laid/day: Rust 1947), (2) nests at
which the hatch date was known or could be
estimated as the mid-point between two checks
(assuming an 18-day incubation period: Brigham
et al. 2011), and (3) nests found with young
(estimated age based on photographs and field
desenptions of known-age young; Brigham et al.
2011; MCA, unpubl. data). These methods
provide adequate accuracy for estimating nest
initiation (Nur et al. 2004). We acknowledge that
our sample is biased as it excludes nests that were
found and failed during incubation (i.e., egg-
candling or floatation were not used to assign eggs
to age classes), and therefore represents a dis¬
proportionate number of successful nests. We
explicitly tested whether daily nest survival rates
varied over the course of the season to address this
concern.
RESULTS
Nest Survival and Predation Rates— We found
-0 nests during the 2 years of the study: nine in
2009, and 11 in 2010. Four of the 20 nests (all
from 2010) were excluded from nest survival
analyses, including three found during the young
s,age (i.e., post-hatching), and one found during
the incubation stage that was inadvertently
damaged by an observer during a check. We
logged a total of 98 check intervals (median
interval = 2 days) at the remaining 16 nests,
yielding 224.5 exposure-days.
13)111660 of 16 nests included in nest survival
analyses survived to hatching, while three tailed,
two due to predation, and one was abandoned. All
three nest failures occurred in 2010. The aban¬
doned nest apparently had infertile eggs as
incubation was undertaken lor at least 27 days.
The daily nest survival rate for the 16 nests was
0.987 (95% Cl = 0.960-0.996); thus there was
-79% chance (95% Cl = 48-93%) of surviving
an 18-day incubation period (calculated as [daily
survival rate]1*). There was no evidence that
daily nest survival rale varied over the course of
the season (x = 1.1. df = L P = 0.29). The
daily predation rate w-as 0.009, indicating there
was a 15% chance of a nest being depredated
during the 18-day incubation period (95% Cl —
4-47%).
Eggs in 16 nests successfully hatched (including
those found after hatching), and fledging was
confirmed at only three. It is unknown whether
young from the remaining 1 3 nests were predated or
we lost track of them due to movements of young.
The young at one nest were likely depredated by a
northern pine snake { Pimophis mektnoleucus mel-
anoleucus) that was observed ~ 1 m from 0-3 day
old young that were not re-located.
Clutch Size and Movements of Young.— C lutch
size was two at 16 of the 17 nests found prior to
hatching with the other nest containing a single
egg. All three nests found after hatching contained
two young.
We recorded movements of young at 11 of 12
nests visited more than once. The one pair of
young not observed to change locations was
<5 days of age when last seen. Twenty-six
movement events were observed in 42 post¬
hatching checks. Exact distances traveled were
not uniformly recorded, but ranged during a
single check interval (generally 2—3 days) from
0.15 to 6 m. Younger chicks tended to move less.
Young that moved w'ere generally located close
together (within 0.1 m) except for those close to
fledging, which wrere at times — 1-2 m apart. One
of four broods visited on day of hatching had not
moved by the following nest check (2-3 days
later), and three broods had moved only 15-
100 cm. The farthest straight-line distance
recorded to the original nest site over the 14-
day period one pair of young were monitored was
—45 m. In contrast, a pair of 1 1-day old young at
another nest moved only 0.5 m from the original
nest site.
Nest-site Characteristics and Habitat Selection—
Nest sites in both 2009 and 2010 were dominated by
open ground (mean ± SD cover. 58 ± 20%, range
= 5-80%. n = 17), followed by grass ( 18 ± 11%,
range = 5-35%). shrubs (9 ± 13%, range = 0-
40%). and forbs (9 ± 15%, range = 0-45%). Mean
vegetation height at nest sites wus 11 ± 7 cm (range
= 0-50 cm). Vegetation characteristics at nests were
1 16 THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 1. March 2012
Open Grass Shrub
O
O
Forb
FIG. I. Percent vegetative cover at random locations
(white boxplots, n = 80) and Common Nighthawk nests (gray
boxplots, n = 8.) on Joint Base McGuire- Dix-Lakehurst, New
Jersey. USA, in 2010. Open ground included bare sand,
lichens, and matted dead vegetation (litter). Boxplots show
median, interquartile range, and range of data. Open circles
show points >1.5 interquartile ranges above the median.
similar in 2009 and 2010 (Wilcoxon rank sum
tests, IV = 24-43. P > 0.26), but 2010 nests
diftered from vegetation at random locations
(Fig. 1, Table I). Nest sites in 2010 had more
open ground, shorter vegetation, shallower litter,
and less grass and shrub cover than random areas'
Nesting Phenology.— We estimated initiation
dates for 16 of the 20 nests. Four were found
during egg-laying, two were estimated based on
a known hatch date, seven from an estimated
hatch date, and three from the estimated age
of young. The median nest initiation date was
31 May with an interquartile range of 25 May to
11 June, and a range of 18 May to 28 June
(Fig. 2). One nest for which we could not
accurately estimate initiation date was estab¬
lished prior to 17 May, as it was discovered with
a two-egg clutch on this date.
120 1 40 160 180
Julian date
FIG. 2. Estimated initiation dates (first egg Iaidi for
Common Nighthawk nests monitored on Joint Base
McGuire-Dix-Lakehurst, New Jersey. USA, in 20n°
2010. Bins are in increments of 5 days, beginning on I'
May (Julian day 135). Boxplot above shows median,
interquartile range, and range of dates. Asterisks indican
the average start and end dates for nest searches in 200'
and 2010.
DISCUSSION
The lack of data on breeding biology toi
nightjars is a significant obstacle to effective
conservation planning. This is especially relevant
in North America as several species appear to I
experiencing long-term population declines
(Wilson 2008, Nebel et al. 2010. Sauer el al
201 1 ). We found nest survival through incubati"’
to be 79% (0.987 daily survival) which b
considerably higher than reported by Perkins anJ
Vickery (2007) in Florida (28%, 0.932 daily
survival, n = 14 nests). Sample sizes for both
studies were somewhat lower than those general
recommended for daily survival rate estimation
* SE) “ Comm°" nest sites (2009-2010) *1 -
Wilc„r„ raTsUm fLr^n1 P'°‘S “ J°inl Bs“ McGttinr-Dix-Lakehurst. New Jersey. USA.
- afe displayed between the columns: ns, P > 0.05; *, 0.05 > P > 0.01 : **, 0.01 >P>(>'
_Yeg- height (cm)
% Open
% Grass
% Forb
% Shrub
Litter depth (cm)
Nests 2009 (« = 9)
8.6 ± 3.3
53.9 ± 7.9
2LO ± 3.7
7.8 ± 4.3
6-7 ± 3.4
Nests 2010 (n = 8)
ns
ns
ns
ns
ns
9.7 ± 1.8
63.1 ± 4.8
14.4 ± 3.5
10.6 ± 7.0
12.5 ± 5.6
0.3 ± 0.1
**
**
*
ns
Random 20l0^jjy_
21.5 1 14
31.8-24
40.4 - 3-0
3.1 i 1°
29.1 t 3.0
1.2 1 0-1
Allen and Peters • COMMON NIGHTHAWK NESTING BIOLOGY
117
(i.e„ >20 nests; Hensler and Nichols 1981), which
is reflected by the wide confidence intervals around
these estimates (48-93% incubation .survival for
nur study, and 11-68% in Perkins and Vickery
2007). We found apparent nest survival (i.e., %
successful nests) of 81% (13 of 16 nests) in
comparison to 93% in grasslands of the northern
Great Plains (13 of 14 nests [excluding 1 human-
induced failure): Kantrud and Higgins 1992). and
43% in Florida dry prairie (6 of 14; Perkins and
Vickery 2007). Neither Kantrud and Higgins
1 1992) nor Perkins and Vickery (2007) reported
nest abandonment and both concluded that preda¬
tion was the main cause of nest failure.
Published studies of Common Nighthawks have
considered only nest survival through hatching. A
complete picture of nest survival requires data for
the period of young development. Including this
■uage would necessarily result in lower estimates
of overall success, If we assumed, for example,
the same daily survival rate for the period of
young development as we found for incubation,
the expected probability of survival to fledging at
our site would be 62% (assuming 18 days front
hatching until Hedging; Brigham et al. 201 1 ). The
question of whether survival differs substantially
between eggs and pre-fledged young in Ibis
species will likely require telemetry data due to
ihe uncertainties associated with monitoring semi-
precocial young (e.g., Fowle 1946, Rust 1947.
Perkins and Vickery 2007).
Clutch size of Common Nighthawks is similar
across a broad geographic area with two-egg
clutches dominant in Idaho (24 of 27 clutches;
Rust 1947), the northern Great Plains (18 of 21;
Kantrud and Higgins 1992). New Jersey ( 16 of 17;
ihis study), and Florida (13 of 14; Perkins and
Vickery 2007). All other clutches consisted of one
et'g- Perkins and Vickery (2007) argued that some
one-egg clutches could be the result of partial
depredation, and both Rust ( 1947 ) and Sutton and
Spencer (1949) observed eggs rolling from nests
when ihe female flushed, which could be another
source of clutch reduction. We observed one nest
la 2-egg clutch) at which the second egg was not
incubated, but was found •— 1 m distant.
The movements of young we recorded were
similar to previous reports for both rooftop and
non-rooftop sites (Fowle 1946. Rust 1947, Dexter
1952). Fowle (1946) reported single-day move-
ments as far as 15-27 m in a burned clear-cut on
Vancouver Island. British Columbia, compared to
'he maximum of 6 m in 2 days in our study. It is
possible that Fowle’s handling of young for
weighing (not done in our study) contributed to
the farther single-day movements he observed.
Few data exist on the habitat preferences of
Common Nighthawks. However, our finding that
open ground was preferred is not surprising based
on several qualitative accounts (e.g., Fowle 1946,
Rust 1947. Brigham et al. 2011) and two
quantitative studies (Kantrud and Higgins 1992,
Lohnes 2010). Typical nesi sites in our study were
in patches of ‘open’ ground (e.g., sand, lichens,
litter), between warm-season grasses or erica-
ceous shrubs that often provided partial shade.
Lohnes (2010) compared nest sites with random
areas in the Konza Prairie in Kansas and also
found a preference for open ground. Kantrud
and Higgins (1992) noted that over half of 21
Common Nighthawk nests in the northern Great
Plains had 'no vegetation' and they report an
average vegetation height ot 6 cm, considerably
lower than that of other ground-nesting birds in
the area (mean = 33 cm). We found mean
vegetation height at nest sites to be about half that
of random areas (10 vs. 22 cm), a discrepancy at
least partly driven by the higher number of zero
height values at nest sites in open areas.
The pattern of nest- initiation dates observed
in our study appeared to be unimodal (Fig. 2),
although it is possible that increased sample sizes
would reveal a different pattern. Some nests also
may have been initiated before or after nest
searches (15-28 Apr to 15 Jul). This is not likely
to be a significant proportion of nests, however, as
nighthawks do not typically arrive on the study
site until early to mid-May (MCA, pers. obs.) and
fall migration in this species begins in mid-August
(Walsh et al. 1999). The median initiation date we
observed (31 May) was earlier than observed in
the northern Great Plains (24 Jun, n = 8 nests,
Kantrud and Higgins 1992) and northern Idaho
(30 Jun, n = 27; Rust 1947), hut our range (18
May-28 Jun) was within the range observed in
these studies (7 May- 15 Jul).
ACKNOWLEDGMENTS
This study w as funded by the Department of Defense
Legacy Resource Management Program and ihe U.S. Navy
Agricultural Outlease Program. Field work was performed
by Mike Allen. Ron Hutchison. Tamarra Mart/, Kim Peters,
Ben Sandstrom. Katie Schill. I.ena Usyk, and Rachel
Villani. We thank John Joyce of Joint Base McGuire-
Dix-Lakehurst for helpful logistical support.
1 18
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 1. March 2012
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The Wilson Journal of Ornithology 124(1 ):1 19-126. 2012
REPRODUCTIVE LIFE HISTORY TRAITS OF THE YELLOWISH PIPIT
(. ANTHUS LUTESCENS)
MAIKON S. FREITAS1 AND MERCIVAL R. FRANCISCO12
ABSTRACT.— We describe reproductive traits of the Yellowish Pipit (Anthus lulescens) in the Slate of Sao Paulo.
Brazil. We found 32 active nests during three breeding seasons (2008-2010). Domed nests were built exclusively on the
ground where the grass was sufficiently tall to conceal them. Clutch initiation across years occurred from July to October
and average ± SD clutch size was 3.05 ± 0.4 eggs or young. Yellowish Pipits were predominantly single-brooded. Eggs
were pale white with brown spots and blotches that could be more concentrated at the larger end or homogeneously
distributed over the entire surface. Eggs were 18.2 1 0.8 mm in length. 13.7 - 0.3 mm in width, and weighed 1.7 _0.1_g.
Incubation and nestling periods lasted 1 3.03 ± 0.2 and 1 4.5 ~ 1 .0 days, respectively Mean lime incubating/hr was 38 ±
71 min, and incubation recesses averaged 9.4 t 4 nun. Young were provisioned on average 13.3 £ 7.9 Utne. , >
males and females. Estimated overall nesting success using a null model of constant nest survival rates was X e ( - c
36-97*5). Model selection analyses indicated survival was negatively correlated to nest age and time within the breeding
reason. Comparisons of Yellowish Pipit life history traits with northern temperate congeners provided support for the
premises that clutch sizes are smaller and young development is slower in the tropics. The hypothesis that annual fecundity
;an be similar across latitudes due to a negative correlation between clutch size and number of renesting attempts was not
supported. Our data contradicted the commonly claimed, but poorly tested hypothesis, that smaller clutch sizes in the
tropics can he explained by a longer breeding season that permit more opportunities to rencst within the same breeding
reason. Received 14 February 2 Oil. Accepted 15 August 201 1.
Several studies have addressed avian life
history adaptations of northern temperate versus
iropical and southern temperate habitats. Broad
latitudinal patterns of reproductive traits have
been proposed, i.e.. Southern Hemisphere species
have smaller clutch siz.es (Moreau 1944, Lack
1947. Skutch 1949, Murray 1985). lay more
clutches per year (Lack and Moreau 1965,
Ricklels 1969). and have longer incubation and
nestling periods (Skutch 1949). The occurrence of
latitudinal differences in clutch size has been
tested (Yoni-Tov et al. 1994. Young 1994. Geffen
and Yom-Tov 2000, Martin et al. 2000. Ghalam-
bor and Martin 2001). but the claim thal
incubation and nestling periods, as well as number
°l renesting attempts, differ between Northern and
Southern hemispheres is still not accepted (Geffen
and Yom-Tov 2000). Only a few studies have
compared species paired by phylogeny and
ecology, and attempted to isolate the latitudinal
effect from the phylogenetic influence (Yom-
Tov et al. 1994. Marlin et al. 2000, Ghalambor
and Martin 2001, Martin 2002). Passerines of
lfle genus Anthus (Motacillidae) are globally
distributed, and occur on every continent ex-
Cept Antarctica (Ridgcly and Tudor 1994, Tyler
-1*94). This makes them well suited for studying
1-niversidade Federal de Sao Carlos, Campus de
Surocaba, Rod. Joao Lome dos Santos, km 110, Some-aba.
Sp 18052-780. Brazil.
Corresponding author; e-mail: mercival@utscar.br
breeding trail diversification across latitudes.
However, many motacillids have not been studied
in detail, especially those in South America (Tyler
2004).
We present the first comprehensive description
of the reproductive life history traits ot the
South American Yellowish Pipit (A. lutescens).
Our objectives were to: (1) provide information
on phenology and duration ot breeding season,
clutch size, length ot incubation and nestling
periods, nesting success, renesting attempts, and
parental care for a Sao Paulo State population,
southeast Brazil; and (2) compare these life
history traits with data from the literature lor a
set of northern temperate congeners.
METHODS
Study Area. — Observations of Yellowish Pipits
were conducted along the Sorocaba River and
in an adjacent urban park (16 ha), including an
artificial’ lake of 2.8 ha. The study area is in the
suburbs of the city of Sorocaba, State of Sao Paulo
in southeast Brazil (23 28' 99" S, 47 26' 17" W).
The area is characterized by the presence of large
patches of exotic grasses (mainly Zoysia japonica
and Cynodon daetylon). Trees and bushes are
widely spaced and the grass is kept relatively
short by employees of Sorocaba city prefecture,
which provided suitable breeding habitat for
Yellowish Pipits. The climate is tropical with
two well-marked seasons: a humid, hot season
119
120
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 1. March 2012
from October through March (average rainfall =
919 mm. temperatures varied from 15.7 to 32.4
°C) and a dry. cold season from April through
September (average rainfall = 294 mm, temper¬
atures varied from 11.4 to 30.6 C).
Study Species.— The Yellowish Pipit is a
monomorphie passerine widely distributed in
South America from western Panama south to
Uruguay and Argentina (south to La Pampa and
Buenos Aires). It inhabits grasslands, open C'er-
rado. pastures, and cultivated lands often near
water or marshes (Ridgely and Tudor 1994, Sick
1997, Tyler 2004). The Yellowish Pipit is a
common species, but data on its breeding biology
are scattered and many aspects are poorly docu¬
mented. Data on incubation and nestling periods,
breeding phenology, and parental care are present¬
ed here for the first time.
Field Procedures. -Wc conducted systematic
nest searches from July to January during three
breeding seasons (2008, 2009, and 2010). We
searched for nests at least three times per week by
covering 1 km of each margin of the Sorocaba
River and Lhe entire adjacent park. Nests were
located by following adults in their territories
when they were carrying nest material or feeding
young, and were checked every 1-3 days. We
used metal calipers accurate to ±0.01 mm to
measure nests and eggs, and a spring scale
accurate to ± 0. 1 g to weigh eggs.
The incubation period was from the first day
of incubation to the day before hatching, and
nestling period was from hatching day to the day
before Hedging. Observations were performed
daily during the laying stage, and we could detect
females that began incubation before and after the
set of eggs was complete. We also checked if eggs
were warm to detect Lite beginning of incubation.
We did not touch or handle young to avc
shortening the nestling period (Skutch 194‘
Clutch initiation dates were obtained from ne:
found in die construction stage (i.e.. we observ
the first egg in die nests) (n = 15), and by bac
dating for nests for which hatching or fledgi
dates were known, based on mean incubation u
nestling periods (// = 12),
We estimated lhe frequency at which adu
>i '° WM thc Pulton
= 15). Nests were domed with a small side
entrance, often invisible from above. Nests were
exclusively on the ground, where the grass was
sufficiently tall to conceal them, usually in slight
depressions in the soil under dense vegetation
Fourteen nests were on flat terrain, while 18 were
in crevices in the banks of the Sorocaba River.
2-5 m from water. Nest material consisted ot dry
grasses, and the nest chamber was lined with finer
grass leaves and grass stems (Fig. I). Nest
measurements varied (Table 1 ) and one nest had
a tubular entrance ~13 cm in length. Males and
females shared nest building activities with both
carrying and placing nest materials, often one
after the other at similar rates (MSF, pers. obs.).
Adults brought nest materials on average 12.6 ±
8.4 times/hr (range = 4-24) during 7 hrs of focal
observation (n = 6 nests). Time gaps between
visits were 3.6 ± 4.7 min in length (range = 0.1-
25, n = 88 observations). Two nests found at the
beginning of construction took 3 days to
complete.
The earliest clutch initiation dates (laying of the
first egg) varied among years: 20 August 2008, 6
September 2009. and 28 July 2010 (Fig. 2). The
latest clutch initiation was on 19 October 2008,
and the latest nesting activity (the last young
observed in a nest) was on 4 November 2008.
The average breeding season (pooling the 3 yrs
together) spanned almost 5 months, but nests
found in July and November were exceptions
(only I nest each). Laying initiations were highly
concentrated in August and September, and the
average number of active nests was concentrated
in August through October (Fig. 3). However,
clutch initiations were clearly concentrated in
only 1 month (Fig. 2) when each year was
analyzed separately.
The basic egg color was pale white and
markings varied remarkably, even within a single
nest. Some eggs were predominantly white with
pale to intense brown spots and blotches moie
concentrated at the larger end. while others were
heavily spotted over the entire surtace (Fig. 1).
Eggs measured 18.2 ± 0.82 mm in length (range
= 17.1-19.7) and 13.7 ± 0.3 mm in width (range
= 13,3-14.2), and weighed 1.7 ± 0.12 g (range =
1 5-2.0) (n = 16). Clutch sizes were two ( n = 1),
three (n = 18). or four (n = 2) eggs or young
(3.05 ± 0.4), and eggs were invariably laid on
consecutive days (n = 15 nests). Incubation oi 10
observed nests, started on the third day after onset
of laving, even when clutch sizes were two ( n — 1
nest) or four eggs (rt = 1 nest). One egg took
14 days to hatch, but the incubation period was
13 days (29 eggs from 10 nests) (13,03 ± 0.2).
We believe that only females incubated for two
reasons: (1) we did not observe adults taking turns
TABLE 1. Measurements (mm) of Yellowish Pipit nests
length (OL). inside high (IH), inside diameter (ID), entrance
(„ = 1 1 ): outside high (OH), outside width (OW), outside
width (EW), and entrance high (EH).
ow
OL
IH
ID
EW EH
Mean ± SD
Range
88 ± 8.3
71-104
114.4 ± 11.7 130.25 ± 15.6
93-127.5 104.5-157.3
62 ± 8
50.1-74.7
82.4 ± 16.7
55.8-108.5
56 ± 9.9
37.7-68
46.5 ± 98.8
30-58.6
71
122
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124. No. 1. March 2012
w
c
a)
-O
E
12
10
8
6
4
2
0
□ 2008
■ 2009
250
Months
-• Number of clutch initiations of Yellowish Pipits across different months through three breeding seasons (2008.
2009, and 2010), and monthly rainfall.
to incubate; and (2) the non-incubating individual
often remained near the nest singing vigorously,
suggesting it was the male. Males did not feed
females in the nests in 3 1 hrs of focal observations
at nine different nests, bui usually escorted them
during incubation recesses. Females spent from
23.2 to 55.8 min incubating the eggs per hr (38 ±
7.1 min). They left the nests 1-3 times per hr
(2.2 ± 0.6). and incubation recesses were 3.8 to
26.3 min in length (9.4 ± 4, n = 53). When
incubating females were Hushed from nests, they
performed a ‘broken-wing’ display, vocalizing
and dragging their wings along the ground in an
attempt to distract the observers.
Hatching was synchronous (nests were checked
from 0900 to 1000 hrs) in 12 of 16 nests. Nestlings
had yellowish skin and were covered with gray
down at hatching. The bill and swollen flanges
were yellow and the mouth lining was blight
orange. Adults gathered a large number of small
25
20
15
10% (Craig and Enderson 2004:fig. 46). Similar !'
rates varied between 64 and 86% in Washingt1"
TABLE 2. Occupancy rates of Peregrine Falcons at nest-sites in Colorado. Montana, and Wyoming. 2005-2009.
Nest-sites studied
Year
CO
MT
WY
2005
2006
2007
2008
2009
Means
29
36
27
27
44
64
80
86
93
1 12
64
61
54
29
46
Sites with pairs
CO
MT
WY
27
52
64
34
67
61
23
68
51
23
74
29
41
84
41
co
93
94
85
85
93
90
Occupancy ('*)
MT
WY
81
84
79
80
75
80
100
100
94
100
89
97
Enderson et al. • PEREGRINE FALCON NESTING PERFORMANCE
131
TABLE 3. Nest success and reproductive performance of Peregrine Falcons in
Wyoming, 2005-2009.
Colorado. Montana, and
Yea
Number of pairs"
Successful pairsh
Success rale (%)
Number of young
Young per pail"
CO
MT
WY
CO
MT
WY
CO
MT
WY
CO
MT
WY
CO
MT
WY
2005
24
49
64
16
40
45
67
82
70
36
94
99
1.5
1.9
1.5
2006
32
66
61
24
58
44
75
88
72
53
147
101
1.7
2.2
1.7
2007
17
68
51
12
51
36
71
75
71
28
108
75
1.6
1.6
1.5
2008
11
67
29
8
54
19
73
81
66
13
125
45
1.2
1.9
1.6
2009
28
79
41
26
69
28
93
87
68
61
176
58
2.2
2.2
1.4
Totals
112
329
246
86
272
172
191
650
378
Means*3
77
83
70
1.7
2.0
1.5
! Pairs for which reproductive outcome was known.
’ Pairs producing at least one young 28 days of age or older.
c Based on all pairs of known outcome, successful or not. ,
0 Mean success rale based on the total number of successful pairs. 2005-2009, divided by the total number of pairs.
Slate. 1990-2001. with differences between con¬
secutive years as great as 12% (Hayes and
Buchanan 2002:table 4). The USFWS national
monitoring results for 2003 show a rate of 87% for
90 territories in Colorado, Montana. Utah, and
Wyoming (Green et al. 2006), and 81% for 91
territories in the same slates in the draft report for
2006 (M, G. Green, unpubl. data). Occupancy rate
may not be a sensitive indicator of population
change because of considerable between-year
variation.
The vagaries of adverse weather may explain
some variation in nest success. Wet weather, in
-009. probably caused nest failure at three sites in
the Bighorn Mountains of Wyoming, a phenom¬
enon reported elsewhere (Olsen and Olsen 1989).
The nest-sites we studied were distributed across a
•arge region and adverse weather in any year
would not likely affect nesting in all states, or
even in parts of states, to the same extent.
Annual nest success in Washington, in compar¬
ison. varied widely between 40 and 80% (mean —
61%,/? = 460) in 1990-2001 (Hayes and Buchanan
-002). Success may be inflated in that study
because young of all ages were recorded. Annual
nest success in Idaho. 2005-2009, w as between 52
and 83% ( mean = 71%.//= 1 29 ) ( Moulton 2009 );
°nly young —33 days of age or older were
recorded. The success rate for 70 pairs in Colorado.
Montana, Utah, and Wyoming in the 2003 USFWS
monitoring survey was 74% (Green et al. 2006).
and the draft report for 2006 gave a success rate of
70% for 70 pairs (M. G. Green, unpubl. data).
Wide variation in reproduction rate among
years has been reported. Reproduction rate in
Colorado ranged from 1.4 to 2.1 (mean = 1.7)
young/pair (40-70 nesting attempts/year) during
1995-2001 (Craig and Enderson 2004). Repro¬
duction rate for 10 pairs in 2004 averaged 2.1
young/attempt (Enderson 2005). Reproduction
rate in Washington in 1990-2001 varied from 1.0
to 2.2 young/pair, but may have been biased
upwards because voting of all ages were reported
(Hayes and Buchanan 2002). In Washington, 449
young were counted in those years in 679 nesting
attempts (mean = 1.5). Reproduction rates
during annual counts in the same period in Idaho
averaged between 1.0 and 2.5 (6 to 15 nesting
attempts/year) (Moulton 2009). The 2005-2009
average in Idaho was 1.6 young/pair for 129
nesting attempts. The 2003 USFWS national
survey found a reproductive rate of 1.5 young/
pair in Colorado, Montana, Wyoming, and Utah
(Green et al. 2006) and 1.4 in 2006 (M. G.
Green, unpubl. data). The 2000 Canadian na¬
tional peregrine survey reported a mean ol 2.5
young per pair (n — 23) in Alberta south of 58
N latitude, a population where some pairs were
adjacent to those in Montana (Rowell et al.
2003). We conclude that annual reproduction in
the range of 1.4 to 2.0 young/pair on territory
was usual. Wide year-to-year fluctuations were
common, perhaps caused partly by adverse
weather.
Reproduction measured in our study seems
robust, but factors such as adult mortality, age at
first reproduction, and immigration, all usually
unknown, combine to affect population change.
Craig et al. (2004) modeled these components
based on values from Colorado during 1989-
2001. They predicted an average reproduction of
— 1.7 young/pair would yield a population growth
132
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 1. March 2012
rate of 3 to 8% per year, the range resulting from
the actual values accepted for the other compo¬
nents. That prediction coincides with our discov¬
ery of new pairs each year at cliffs where none
had been seen in earlier searches.
ACKNOWLEDGMENTS
This work was supported in part by funds from the U.S.
Fish and Wildlife Service administered by the Montana
Fish, Wildlife and Parks Department, the Wyoming
Game and Fish Department, and the Colorado Division
of Wildlife, and partly by funds arising within these
agencies. K. C Uaynam and Adam Shteading helped with
fieldwork in Montana. Observers in Wyoming included
Terry McFaneaney, D. R. Mutch. S. M. Patla, D. W
Smith, and L, A. VanFlcct. Michelle Cowardin, David
Klute. K. M. Potter, and Michael Reid participated in
Colorado. We arc grateful for their help. We thank Colleen
Moulton for permission to use recent information from
Idaho. Reviews by M. R. Fuller and C. M. White improved
this paper.
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Cade. T J. and W. A. Burnham (Editors). 2003. Return of
the peregrine. The Peregrine Fund. Boise. Idaho, USA.
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biology and management in Colorado. 1973-2001.
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Peregrine Falcon (Falco peregrinus). III. Weather,
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The Wilson Journal of Ornithology 1 24( 1 ): 1 33-1 38, 20 1 2
reproductive success of the creamy-bellied thrush in a
SOUTHERN TEMPERATE ZONE
ANDREA ASTIE1-2 AND NATALIA LUCHESI1
ABSTRACT— We describe ihe breeding biology and reproductive success of a Creamy-bellied Thrush (TWio
i wmrochalinus) population from a southern temperate zone in western Argentina. We tound 236 Creamy-bellied Thrush
nests of which most were predated (67T). The breeding season was from late October to late December and clutch size was
three eggs. Egg survival, hatching success, and fledgling survival of non -depredated nests were quite high <0.6/ - U.U3.
074 ± 0.03. and 0.87 ± 0.04. respectively). The number of eggs in the nest did not affect egg survival or hatching success,
bu! number of nestlings in the nest affected fledgling success. Daily nest mortality was higher during the early and late
nestling period than durina laving, and early and late incubation periods. Highest nest mortality coincided with periods
when activity of parents at' the nest was highest The clutch size was similar to data reported lor thrushes Irom the tropics
and south temperate areas, and lower than reported for thrushes from north temperate areas. This latitu ina Pattem ,s
similar to the general pattem described for passerines in the tropics and southern temperate areas. Recei\e( < e ruary
1011. Accepted 14 September 201 1.
The study of avian breeding ecology in the
Americas has mostly concerned tropical and
northern temperate species. New data from the
Southern Hemisphere suggest life history traits
and behavior of southern temperate species are
more similar to tropical than to northern temperate
species (Martin 1996, Martin et al. 2000,
Robinson et al. 2010). This conclusion is based
on a limned number of southern temperate
locations and species, and more information is
needed on avian life history traits in southern
temperate areas (Robinson et al. 2010).
The Turdidae (true thrushes, Turdus spp.) is a
cosmopolitan group in the tropics, and northern
and southern temperate areas around Ihe world.
Tints, they are an excellent model for study of life
history evolution, breeding biology, and latitudi¬
nal variation among related species occupying
different ecosystems. However, there are only a
comparative studies (Martin et al. 2000,
berretti et al. 2005) and the available information
ls biased to north temperate species. Most
information on breeding biology for species ol
T'irdiis in Argentina comes from studies in the
Eintpas and Yungas (e.g„ Martin et al. 2000,
Suckmann and Reboreda 2003, Ferretti ct al.
2005). There are no studies available tor popula-
lions Irom semi-arid areas of western Argentina
(but see Mezquida and Marone 2001 for other
Passerine species).
The Creamy-bellied Thrush ( Turdus amauro-
' Institute Argcntino de Investigaciones de Zonas Aridas.
•ADIZA-CONICF.T, Mendoza. Argentina.
Corresponding author;
e-mai|; aastie @ mendoza-conicet . gob .ar
chalinus) is widespread in South America, but its
breeding biology has only been recently studied
(Astie and Reboreda 2005, 2006). The objectives
of our study were to obtain information on
breeding biology and reproductive success of a
Creamy-bellied Thrush population from a south¬
ern temperate zone in western Argentina. Specif¬
ically, we examined if number of eggs and
nestlings present in the nest affect reproductive
success during different stages of the nestling
cycle.
METHODS
Study Species.— The Creamy-bellied Thrush is
a monomorphic and monotypic passerine ot the
genus Turdus. This species is widely distributed
from southern Brazil to southern Argentina (Ridge-
|y and Tudor 1989), but little is known about its
breeding biology. Creamy-bellied Thrushes build
open cup nests composed of grasses cemented with
mud and lined with grasses and hairs. They lay
three esgs with a pale greenish background and
spots and blotches of reddish-brown concentrated
at the larger pole (Astie and Reboreda 2005). The
incubation period is 1 1 .5 days and the nestling
period is 12 days (Astie and Reboreda 2005,
2009a). Average adult mass is 55 g (Astie and
Reboreda 2005). This species is heavily parasitized
by the Shiny Cowbird (Molothms bonariensis) in
the study area (Astie and Reboreda 2005, 2006,
2009a, b).
Study Site. — The study was conducted at Guay-
mallen. Mendoza Province. Argentina (32 51' S,
68 42' W) during the 1999-2002 breeding seasons
(Oct-Dec). Mendoza is in the Monte Desert region
of Argentina. The Creamy-bellied Thrush only
133
134
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124, No. 1. March 2012
occupies areas irrigated for agriculture. The study
area was a 1. OOO-ha cultivated field with vineyards,
olives (Olea europaea), and poplar (Papains nigra )
groves.
Data Collection. — We followed the fates of 236
thrush nests which were found by observing adult
behavior and systematic search. Nests were
visited every 1-2 days until nestlings Hedged or
the nest (ailed. We recorded the numbers of eggs
and nestlings during visits. We considered a nest
to have been predated when the complete clutch
disappeared between two subsequent visits.
Data Analyses. — We divided the reproductive
season into groups of 10 days starting with the
first egg laid until the last nest in laying stage was
found. We recorded the frequency of nests that
started in each period and estimated the survival
ol nests (0-1) throughout the season with logistic
regression including a subset of nests found
during building and laying periods (n = 08 nests).
We calculated (mean ± SE) success of eggs
and nestlings in nests in each nesting cycle period
(egg laying, incubation, and nestling) that were
not predated, deserted, or parasitized by the Shiny
Cowbird. Egg survival was calculated as the
proportion of eggs present in the nest at the end of
incubation divided by the number of eggs in the
nest at the start of incubation. Wc only considered
nests found in building and laying stages that
survived until the hatch of the first egg („ = 48
nests). We calculated hatching success as the
proportion of eggs that hatched divided by the
number of eggs in the nest at the end of
incubation. We only considered nests found in
building, laying, or incubation stages where at
least one egg hatched (n = 109 nests). Fledglim-
survival was calculated as the proportion of
fledglings divided by the number of eggs that
hatched. We considered only nests found during
building, laying, or incubation stages that fledged
at least one nestling (n = 44 nests). We used a
Chi-square test to analyze if number of eggs in the
nest affected egg survival (all eggs survived or at
least one disappeared) or hatching success (all
eggs hatched or at least 1 failed), and if fledgling
survival was associated with number of nestlings
(all nestlings survived or at least I died).
We evaluated if nest survival was associated
with adult activity in the nest by subdividing the
the f8 Cyt ? ,mo tivc Peri°ds: laying (laying of
stacel Tavin^ .T"? ^ -VincSon
. Ce me laying of the third egg until d .v 7> ,
incubation ,day S unti, the h«
early nestlings (from the day the first egg hatches
until day 6). and late nestlings (from day 7 unit
the first fledgling left the nest).
Nest mortality risk (m) was calculated for each
period following Mayfield (1975). and the
standard error was calculated as suggested b;
Johnson (1979). Wc compared mortality rates
with a Fisher test of contingence. We compared
each nest mortality period versus every other
period and applied a Bonferroni correction (or
multiplc comparisons (Abdi 2007).
Adult activity in the nest was recorded h
videotaping 20 nests with Hi8 Sony vide,
cameras. Nests were recorded during 4 hr-
beginning at 0700. Cameras were placed 2 m
from the nest and camouflaged with leaves We
recorded two nests during the laying stage, >u
nests during early incubation, two during late
incubation, four with early nestlings, and six w-ith
late nestlings. We obtained latencies (time elapsed
since placement of the camera and the moment m
adult returned to the nest ), frequency of visits per
hour (average number of times an adult entered
the nest in I hr), and nest attentiveness (average
proportion of time an adult stayed in the nest
during I hr) for each video. All statistical tests
were conducted with StatView 5.0 (SAS 1998).
RESULTS
We found 236 nests of Creamy-bel lied Thrush¬
es. 42% during the building and laying period.
5 1 % during the incubation period, and lac during
the nestling period; 18 were found in 1999. 87 in
2000. 91 in 2001. and 40 in 2002. Sixty-seven
percent of the nests were predated. 8C7 were
deserted, and 2.5% were destroyed by strong
winds or rain. Only 22.5% of the nests produced
at least one fledgling. The majority of the nests
(62%) were parasitized by the Shiny Cowbird and
at least one egg in 68% of the nests was
punctured.
Most of the nests (70%, n = 236) found were in
vineyards and in olive trees, and the rest in popL'
and fruit trees. Nest dimensions (mean - SC1
were; 10.5 ± 0.5 cm in external height. 6.1 -
0.3 cm in depth, and 12.3 ± 0.2 cm in externa!
width with an internal diameter of 7.9 ± 03 cm
(n = 20 nests).
The first nest was found on 21 October and the
number of nests in the laying stage increased to a
maximum between 23 and 25 November: the las'
nest in the laying stage was found on --
December (Fig. I ). Nest survival was not associ-
Astie and Luchesi • CREAMY- BELLIED THRUSH REPRODUCTIVE SUCCESS
135
J3
(A
®
C
*-
0
L.
0)
n
E
3
2
Period
FIG I. Number of nests in the laying stage during the reproductive season of the Creamy-bellied Thrush. The
reproductive season was divided into intervals of 10 days.
aied with time in the season when the nest was
initialed: nests that failed or succeeded (0- 1 ) were
independent of the time when they were initiated
(logistic regression: X2 = 1.03, P = 0.31, n = %
nests).
One egg was laid per day and incubation started
witli laying of the penultimate egg (for nests
found during building and laying stages, n = 08).
tgg survival was 0.67 ± 0.03 (/» 48 nests),
hatching success was 0.74 ± 0.03 (n ® 109 nests),
and fledgling survival was 0.87 ± 0.04 (n = 44
nests). The number of eggs present in the nest did
n'« affect egg survival or hatching success (X2 =
m P = 0.09, n = 48 and X2 = 0. 12 ,P = 0.94,
11 ' 109, respectively), hut the number of
ffstlings was negatively associated with fledgling
success (X2 = 16.35. P = 0.001. n = 44). At least
■he nestling died when there were three nestlings
"'58% of the nests (/? = 12 nests), at least one
nestling died in 20% of the nests (n = 15 nests)
' lien there were two nestlings, but only 4% died
" = 17 nests) when there was one nestling.
Bonfenoni correction for multiple com-
P^isons set the significance level at y. < 0.005.
Dai|.v nest mortality was higher during laying
(0-079 ± o.(K)6. n = 39) than during early
,ncubation (0.013 ± 0.002, n = 50, X2, = 8.77,
^ ~ 0.003), but there was no difference with late
incubation (0.017 ± 0.002, n = 53, X:i = 4.62,
■D ~ 0.041), early nestling (0.1 1 — 0.006. n = 50,
= 2.13. P = 0.1 1), and late nestling (0.10 ±
1-013, n = 24, X2, = 4.40, P = 0.022) periods.
We found no differences between early and late
incubation (X2 = 1.09. P = 0.27) nor between
early and late nestling (X2! = 1.02, P - 0.28)
periods. Early incubation was significantly lower
than early and late nestling periods (X2, = 37.66.
P < 0.001 and X2, = 45.99, P < 0.001,
respectively), and late incubation was also
significantly lower than early and late nestling
periods (X2, = 37.54, P < 0.001. and X2, =
45.14, P < 0.001, respectively; Fig. 2)
We had small samples for parental care
behavior and could not perform any statistical
comparisons. Wc observed a trend of increased
latency to return to the nest during the laying
stage. Frequency of visits appeared to be highest
during the nestling stage and time spent in the nest
was highest during the incubation stage (Fig. 3).
DISCUSSION
The Creamy-bellied Thrush in the southern
temperate Monte Desert has several characteris¬
tics typical of tropical birds: low nest survival,
high predation rates, and small clutch size. Nests
at our study site had a low survival rate, as only
22.5 % of the nests produced at least one
lledcling: predation was the major cause ot nest
failure (67%). Nest predation was constant
throughout the season and was not related to the
time a nest was initiated. Nest mortality varied
during the nestling cycle and was highest during
the late nestling period (Fig. 2). Parental activity
during this stage was highest around the nest
136
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 1. March 2012
0,14
Laying Early Inc. Late Inc. Early Nest. Late Nest.
HG. 2. Daily nest mortality (mean ± SE) during laying, early incubation, late incubation, early nestling ami lute
nestling periods of the Creamy-hcllied 1 brush. The number of nests included was 39 in laying, 50 in early incubation. 53 in
late incubation, 50 in early nestling, and 24 in late nestling periods.
(Fig. 3) and suggests that visual predators were
involved. This could be related to attraction of
visual predators when parental activity increased
around the nest (Skutch 1949, Martin et al. 2000,
Martin et al. 2011). An experimental approach
would be needed to rule out other alternative
hypothesis (e.g., older nesllings/nests may pro¬
duce stronger odors that may attract the attention
of predators). We observed that 33% of the eggs
disappeared during the incubation stage. This
could be caused by partial predation or by brood
parasitism, as Shiny Cowbirds puncture eggs in
parasitized and in unparasitized nests (Astid and
Reboreda 2006 ).
Hatching success, and egg and fledgling
survival in successful nests (nests that were not
predated or deserted) was high (74, 67, and 87%.
respectively). Hatching success and egg survival
were not related to number of eggs present in tin
nest. There was a proportion of eggs that did no
hatch (0.26) and this may be caused by infertilit\
or by death of the embryo caused by insufficien
incubation (Davies and Brooke 1988. Svenssoi
et al. 2007). We found that number of egg:
present in the nest had no effect on hatching
success and it is unlikely that insufficien
incubation was the main cause. Nestlings dice
rom starvation more often when they shared the
“rr lhT °ne Sib,ing- siting that
food competition between nestlings was strong
Most of the nestlings survived when only one or
two eggs hatched due to previous egg loss or
hatching failure. However, when all eggs hatched,
at least one nestling died. The brood reduction
hypothesis (Lack 1947, Ricklefs 1965) suggests
that some species lay more eggs than they can rear
nestlings because food supply may vary unpre-
dictably. Thus, parents may lay a large clutch
appropriate for a food-rich year and. in food-poor
years, nestling survival would be mediated by
sibling competition. The brood reduction hypoth¬
esis could be a possible explanation for Creamy-
hcllied Thrush nestling mortality. However, future
studies should evaluate if nests with three
nestlings improve nestling survival in food-good
years.
The clutch size of Creamy-bellied Thrushes at
our study site was small (mean = 3 eggs) and
typical of tropical and southern temperate birds
There is a lack of information of the breeding
biology of most thrushes, but the available data
suggests this group has the same pattern as other
passerines. The clutch size reported for thrusto'
from north temperate areas is 4-5 eggs (Scbnao-
1991, Arheimcr and Svensson 2008. Morton am-
Pereyra 2010), and is 2-3 eggs for thrushes a
tropic and south temperate areas (Lichtensteu
1998. Sackmann and Reboreda 2003. Akinp- ■'
2005, Astie and Reboreda 2005, Halupka and
Greeney 2009). Ours is the first study presenting
data from a Tardus species that inhabits an so
temperate area as far as we know. We did not
Aslie and Luchesi • CREAMY-BELLIED THRUSH REPRODUCTIVE SUCCESS
137
I ~.J
8
7
6
5
4
3
2
1
0
FIG. 3. Latency (time in seconds an adult spent in returning to the nest after we placed the camera), frequency (number
of visiis/hr). and nest attentiveness (percentage of time in the nest during each penod). All data are presented mean _ .
conduct our study in a tropical environment, but
life-history traits of the Creamy-bellied Thrush
are similar to tropical birds. Future research on the
breeding biology of southern temperate thrushes
may offer new understanding of the evolution of
life-history traits.
ACKNOWLEDGMENTS
We thank P. E. Llambias and F. Fernandez Campon for
helpful comments on this manuscript. NL was supported by
a fellowship from Consejo Nacional de Investigaciones
Cientificas y Tecnicas (CONICET). AA is a Research
Fellow of CONICET.
138
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124. No. 1. March 2012
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The Wilson Journal of Ornithology 124(1): 139 145. 2012
FLANGE COLOR DIFFERENCES OF BROOD PARASITIC
BROWN-HEADED COWBIRDS FROM NESTS OF TWO HOST SPECIES
REBECCA CROSTON.' 7 K CHRISTOPHER M. TONRA,2-5
SACHA K. HEATH,2,36 AND MARK E. HAUBER1 4
ABSTRACT— We compared the red. green, and blue color values from digital photographs of the rictal flanges of
nestling Brown-headed Cow-birds (Molothrus ater). a generalist obligate brood parasite, in sympatric Yellow Warbler
iSetopliaga petechia) and Song Sparrow ( Meloxpizu mclojial nests at Mono Lake. C ulifornia. USA. We detected significant
differences in all three color components across nestlings of different species (R: P < U.0001 : G: P < 0.00131. B . P <
0.0001 ). hut differences among cowbird nestlings from the nests of these two hosts were not significant (R : P — 0.543. G.
P = 0.737: B: P = 0.319). Principal components results were mixed: Principal Component I described brightness and
accounted for 84% of the variance. It did not differ among cowbird nestlings front nests of different hosts (P — 0.319).
Principal Component IT described chromaiicity and accounted for \4% of the variance, which differed significantly among
cowbird nestlings from the two different hosts' nests I P = 0.026). Color differences between cowbird nestlings from nests
of different host species may result from selective parasitism by female parasites based on host nestling flange morphology,
or ontogenetic effects on cowbird nestlings reared by different host species. Received 25 January 2011. Accepted 21 July
2011.
Evidence of recognition and discrimination of
parasitic nestlings is relatively rare among hosts
of avian brood parasite species (Redondo 1993;
Grim ct al. 2003; Langmore et al. 2003. 2009;
Schuetz 2005b; Sato et al. 2010; Shizuka and
Lyon 2010). Patterns of parasite chick's visual
and/or acoustic similarity of host nestlings in a
handful of brood parasite lineages ( Anderson et al.
2009, Sato et al, 2010, Langmore cl al. 2011)
imply mimicry to avoid rejection (Langmore ct al.
2003, Payne 2005, Tokue and Ueda 2010,
Langmore et al. 2011). Hosts may discriminate
not only by directly rejecting foreign nestlings,
but by providing belter care or higher quality prey
(Schuetz 2005a. Solcr 2008) for nestlings with
particular attributes (Rothstein 1978, Lichtenstein
2001. Dugas 2009), resulting in variation among
nestlings in growth rale and condition (Hauher
Graduate Program in Biology. Ecology. Evolutionary
biology and Behavior Subprogram, Graduate Center. City
University of New York, NY 10016. USA
Department of Wildlife. Humboldt Slate University,
Areata. CA 95521. USA.
PR BO Conservation Science. Petaluma, CA 94954,
USA.
'Department of Psychology, Hunter College. City
University of New York, NY 10065, USA.
Current address: Smithsonian Conservation Biology
Institute. National Zoological Park. P. O. Box 37012-MRC
5503, Washington, D C. 20013. USA.
Current address: Department of Wildlife. Humboldt
Stale University. Areata. C'A 95521. L SA.
Department of Psychology. Hunter College. 695 Park
Avenue. New York. NY 10065. USA.
Corresponding author; e-mail: RCroston@gc.cuny.edu
and Kilner 2007). Nestling discrimination among
cowbird hosts has been documented for Rufous-
bellied Thrushes ( Turdus rufiventris ) parasitized
by the non-evicting generalist Shiny Cowbird
(Molothrus bonuriensis ) (Lichtenstein 2001), but
is not yet known to occur in any hosts of the
Brown-headed Cowbird (M. titer).
Hosts may recognize parasitic nestlings using
variation in size, color, vocalization, brood size,
and length of time before fledging (Langmore
et al. 2003. Schuetz 2005b, Grim 2007). Variable
coloration of both gapes and rictal flanges may
have a signaling function, conveying nestling
identity, need, health or other indicators of quality
(Thorogood et al. 2008, Dugas 2010), which
would need to be matched by parasitic nestlings
(Nicolai 1974, Payne 2005, Hauber and Kilner
2007). Flange color is typically monomorphic
within species, but Brown -headed Cowbird nest¬
lings appear polymorphic across the species so
that a nestling has either distinctly yellow or white
flanges with lew intermediates (Rothstein 1978).
Polymorphic flange color occurs in only two
phylogenetically distant New World oscine gen¬
era. Geospiza and Molothrus. It is plausible this
polymorphism in cowbirds is the outcome ot
selection for preferential parasitism of certain host
species by female cowbirds to match the host-
specific flange color by the parasitic nestling
(Ellison et al. 2007).
Alternatively, the differences in human-per¬
ceived flange phenotype ol cowbird nestlings
may not result from genetic polymorphism, but
from differences in carotenoid consumption and
139
140
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 1. March 2012
provisioning to chicks across different hosts.
Carotenoid pigments are derived entirely from
diet, and their concentration is known to modulate
nestling mouth color (Thorogood et al. 2008).
Carotenoid concentration is widely hypothesized to
indicate nestling quality, as demonstrated in House
Sparrows ( Passer domesticus) (Loiseau et al. 2008)
and Bam Swallows ( Hirundo rusticci ) (Saino et al.
2000, 2003).
We investigated whether cowbird nestlings
differ in flange coloration when reared by one of
two host species. Song Sparrows (Melospiza
melodia) and Yellow Warblers (Setophaga pete¬
chia) using quantitative measures of coloration.
Birds have a fourth violet- or ultraviolet-sensitive
photoreceptor type, and human color perception is
an insufficient proxy for avian color perception
(Cuthill et al. 2000). We provide the first
objective assessment of cowbird nestling flange
colors based on measures of color using digital
photographs and imaging software (Dale 2000).
However, this remains a preliminary analysis
because imaging software is designed for human
vision and has limited value for avian perceptual
studies (Stevens et al. 2007).
The objective of our study was to test the
hypothesis that rictal flange color of host and
cowbird nestlings varies between nestlings and
parasites of two sympatric hosts. We predicted
measures of flange colors would differ among: ( I )
nestlings of different species (Yellow Warbler,
Song Sparrow, and Brown-headed Cowbird), and
(2) cowbird nestlings in nests of different host
species.
METHODS
Study Site and Species. — This study was con
ducted in the riparian corridors of four tributarie
of Mono Lake (38° 1’ N, 119° 3' W) on th-
eastern slope of the Sierra Nevada, California
USA: Lee Vining, Mill, Rush, and Wilson creeks
We located Song Sparrow' and Yellow Warble
nests and monitored nests during the 200<
breeding season lollowing Martin and Geupe
(1993) and Ralph et al. ( 1993). The ranges of nes
initiation dates for Yellow Warbler and Sonj
Sparrows were similar in 2004 (Tonra et al. 2009)
Nestling Photographs,- We photographed nest
mgs on day 6 (hatching day = day 0) of the
cowbird nestling cycle. This day was chose,
because .t coincided with the age at which
allowed f ^ S"tTicien,i>' ***& to band and
allowed for incorporation of carotenoid pigments
from host-provisioned diet into tissues. Photo¬
graphs were taken with a Hewlett Packard
Photosmart 215 digital camera, set to ISO 200
and 'fine' quality (1,280 X 960 pixels). We
photographed all cowbirds in each nest and. if
hosts were present, we also randomly selected one
individual to photograph. Sixteen Brown-headed
Cowbird. three Yellow Warbler, and three Song
Sparrow nestlings were included in the analysis.
Both cowbird and host chicks were photographed
in two Song Sparrow and two Yellow Warbler
nests, and one Yellow Warbler and two Song
Sparrow nests each contained two cowbird
nestlings. Each photograph was taken of the nght
side of the head against a background of gray
paper with a strip composed of six 1-cnr sections
cut from paint store color sample cards (red. blue,
green, white, yellow, and black) (Home Depot,
Reno. NV, USA) as a color standard, and stored in
a dark box between photography sessions. This
allowed us to make direct comparisons of colors
under varying light conditions in the field. The
photographs were saved and subsequently ana
lyzcd as jpeg images using the histogram function
in Adobe Photoshop Elements 8.0 (Adobe Sys¬
tems Inc.. San Jose. CA, USA). Storing images as
jpeg compresses both image and color data
(Stevens et al. 2007); color compression in this
software obscures rather than enhances differenc¬
es in color and would result in our failure to reject
the null hypothesis (despite its falsehood: Type II
statistical error). Thus, use of jpeg images made
our analyses more conservative.
Flanges were divided into three portions tor
color measurement: A at the apex of the flange,
site B at the fleshy middle, and site C at its most
rostral point. Three replicate measures of red.
green, and blue values were made at each flange
site for each nestling. Red, green, and blue
measures represent the intensity levels (satura¬
tion) for 24-bit color; these measures range in
intensity from 0 (black) to 255 (white, totally
saturated color). Measurements were also made
from the center of the yellow standard present in
each photograph to allow for direct comparison of
the standard and biological colors.
Data Analysis. — We compared red (R). green
(G), and blue (B) values, while accounting lor
variation in light conditions associated with held
work in each photograph, by first scaling
according to the RGB values of the yellow
standard in that photograph i. Thus, F(A| *
where I = R. G, or B value, F, = flange color
Croston el al. • FLANGE COLOR DIFFERENCES OF COWBIRDS
141
ll II 1 1 ll
SOSP YWAR BHCO in SOSP BHCO in YWAR
nest nest
FIG. 1. Differences in flange color saturation values by species and host. SOSP Song Sparrow, YWAR Yellow
Warbler, and BHCO = Brown-headed Cowbird. Bars represent mean saturation values of red. green, and blue across flange
sites and replicates. Error bars represent standard error,
value for i, and Y| = the yellow standard for i.
Repeated measures at each flange site within color
group (R, G, and B) were averaged across
replicates. Data were analyzed using three sepa¬
rate univariate analyses of variance (Mixed
Effects ANOVA), where each color value was
the dependent variable, nestling species (Yellow
Warbler, Song Sparrow, or Brown- headed Cow-
bird) and cowbird nestling host species (Yellow
Warbler or Song Sparrow) were fixed effects, and
nestling metal-band ID and flange site were
random effects. Color variables R, G, and B are
necessarily correlated and we also used principal
components analysis (PCA) to recombine color
variables into uncorrelated scores describing
brightness and chromaticity (following Endler
andThery 1996). Mean PC scores were compared
among host nestling species and cowbird nestling
species groups using ANOVA. All analyses were
conducted in JMP Version 8.0 (SAS Institute Inc..
Cary, NC, USA).
RESULTS
Color values were significantly different among
nestling species in all three univariate analyses of
red. green, and blue color components (R: Fz.ax =
1 * .67, P < 0.000 1 : G: F2.w = 1 1 - 1 4, /* < 0.000 1 ;
B: *2.50 = 16.61, P < 0.0001), but not between
cowbird nestlings of different host species I million birds present. However, 302 birds of eight
species, including passerines, were found dead at the site during 2007-2010. suggesting additional factors were involved.
Most carcasses showed no signs of injury and concentrations of dead birds had accumulated in a few distinctive low pits in
the canyon. Gas samples from these locations showed elevated C02 concentrations in late 2010. Analysis of carcasses
indicated no evidence of blunt trauma or internal bleeding. Volcanic gases accumulating at these poorly ventilated sites mas
have caused the observed mortality, but are temporally variable. Most auklets breeding in the Aleutian Islands do so in
recent lava flows that provide breeding habitat; our study documents a cost of this unusual habitat selection. Received I?
March 2011. Accepted 28 September 2011.
Active volcanoes frequently emit gases such as
carbon monoxide (CO), and carbon dioxide (CO:)
from steam vents, I'umaroles, and gas seeps that are
toxic in sufficient concentrations but odorless and
therefore not repellent to animal life. Ecological
effects of volcanic activity, including gas emissions,
are of interest because of their potential effects on
species at risk or with restricted distributions (e.g..
Short-tailed Albatross | Phoebastria alhatrus | breed¬
ing at Torishima; Einkelstein et al. 2010).
There are 41 historically active volcanoes in
Alaska, including 24 in the Aleutian Islands (Miller
et al. 1998). The Aleutian Islands are also home to
several million nesting seabirds (Byrd et al. 2005)
and many species of land birds, including endemic
subspecies and a vast array of migrants (Gibson and
Byrd 2007). Least ( Aethia pit si I la) and Crested
auklets \. cristate! la) are two of the most abundant
seabirds in Alaska, but most breed in large mixed
colonies at seven sites in the Aleutian Islands— all in
lava flows and associated debris on recently active
volcanoes (Jones 1993a, b). Volcanically active
areas, such as the Aleutian Islands, pose greater
risks to birds than in many other areas. The eruption
of Kasatochi Volcano in the central Aleutian
Islands in August 2008 likely killed thousands of
auklets (Williams el al. 2010), and two dead adult
Fork-tailed Storm-Petrels (Oceanodromu J'urcata)
Deportment of Biology. Memorial University
Newfoundland, St. John’s. NL A IB 3X9, Canada
'usT^' ^ Midd'en'ld R“ad' MC
’Current address; Department of Biology. University
Saskatchewan and Environment Canada I ZoZ
Boulevard. Saskatoon. SK S7N 3H5. Canada
Corresponding author; e-mail: aJex.bond<§>usask ca
were found near a CCL seep one year following the
eruption (J. C. Williams, pers. comm.) indicating
that even non-breeding prospecting individuals are
vulnerable.
There arc few previous accounts of avian mor¬
tality specifically associated with volcanic gases
(Lohkov and Nikanorov 1981. Durand 2007). Large
and small mammals, and numerous bird species
were found in 1974-1979 in a volcanic seep asso¬
ciated with Kikhpinych Volcano, Kamchatka.
Russia. The authors inferred that mammals and
large scavenging birds died of asphyxia alter
entering a gas seep to scavenge smaller prey that
had previously died of asphyxia (Lobkov and
Nikanorov 1981). At least four adult Kelp Gulls
(l aims domimeanus) were likely killed by CCL or
ITS emissions from geothermal vents at Sulphur
Bay. Rotorua on New Zealand's North Island
(Durand 2007). Dead seabirds without visible
external injuries have been found in natural
depressions similar to those on Kiska at Bogoslof
Island, Aleutian Islands, Alaska. (J. C. Williams,
pers. comm.). The objectives of our paper are to: 1 1 1
characterize the gaseous emissions from Kiska
Island, and (2) report the avian mortality observed
from 2007 to 2010. especially that likely related to
volcanic activity.
METHODS
Sirius Point. Kiska Island (52 08’ N. 177 36' E:
Fig. I ) is the site of a large seabird colony with ■>|
million Least and Crested auklets (Sowls et al.
1978). The auklet colony is on the westernmost
active volcano in the Aleutian Islands: Kiska
Volcano. A parasitic lava cone emerged from the
sea adjacent to Sirius Point in 1964-1969. forming
146
Bond et al • AVIAN MORTALITY AT A VOLCANO IN ALASKA
147
60° N
50° N
nc- 1. Kiska Island and Sirius Point, the northern extremity. Aleutian Islands. Alaska The mangie .nd cates
proximate location of the gas seep, the shaded area is the auklet colony, and the crosshairs show the summit
^ Volcano.
a sleep-sided canyon with an older lava flow al the
ll,rnier north coastline (Coats et al. 1961 . Sitrtkin et
1,1 ^81). This canyon continues for > 1 km along
!tie anthem and eastern boundaries of the new lava
^re and varies from 10-20 m depth with near
vertical walls in places. Many living but weak.
Moribund, and dead Least Auklet fledglings (some
"I'h injuries caused by Norway rat | Rattus
norvegicus] predation) were regularly found at
points along this canyon during 2001-2006 (Major
2004; ILJ. pers. obs.). It was previously assumed
these were weak fledglings that, unable to fly,
tumbled into low points in the canyon and. unable
to find their way to the sea. died ol starvation and
exposure. Our research team further investigated
this phenomenon by walking the eastern third ot
148
THE WILSON JOURNAL OF ORNITHOLOGY • Vo/. 124. No. 1. March 2012
TABLE 1.
Birds found dead
in volcanic areas in 2007-
-2010 at Kiska Island. Alaska.
Species
Number found
Totals
Age”
2007
2008
2009
2010
Peregrine Falcon
SY
0
1
0
0
1
Glaucous-winged Gull
ASY
3
0
0
0
3
Least Auklet
HY
80
104
51
67
302
Least Auklet
SY
3
0
2
0
5
Least Auklet
ASY
11
0
0
0
11
Crested Auklet
HY
3
2
2
2
9
Crested Auklet
ASY
3
0
0
0
3
Brown Hawk-Owl
AHY
0
1
0
0
1
Pacific Wren
HY
12
0
0
0
12
Pacific Wren
AHY
4
0
0
0
4
Gray-crowned Rosy-Finch
AHY
3
0
0
0
3
Snow Bunting
AHY
2
0
0
0
2
“ HY: Halch year, SY: Second year, AHY: After hatch-year, ASY: After second-year.
this valley (~200 m) at least once every 6 days
during daylight hours from May to August in
2007-2010. All bird carcasses were identified,
collected, weighed, and measured throughout the
season, and examined for evidence of rat predation
or other causes of death (Major and Jones 2005,
Major ct al. 2007).
Three gas samples from the depressions were
collected at ~ 2-week intervals during June-July
2009. and three additional samples were taken
1 month apart from June to August 2010. Briefly, a
3 to 5-m Tygon tube was lowered into the seep, the
air was suctioned out with a large syringe, and a gas
sample was taken into a pre-evacuated glass
sample cylinder. Samples were sealed and trans¬
ported to the U.S. Geological Survey (USGS) in
Menlo Park, California, for identification and
quantification of the following gases: He. H2. Ar.
02, N* CH4, C02, C2H6. H2S. CO, C,HS“ and
C4H|(|. Gas samples were analysed for bulk
composition by gas chromatography, and the C02
fraction was dried and purified cryogenically,
using methods described by Evans et al. (1988).
A C02 split was analysed for the ratio of nC/l2C at
the USGS Reston Stable Isotope Laboratory usii
methods described by Revesz and Coplcn (200)
The remaining C'02 was reduced to graphite on
Fe catalyst at the USGS laboratory in Restc
Virginia, USA to ascertain the volcanic ai
biogenic fraction of bulk C, and analysed for ti
ratio ol ‘ ‘C/'-c at the Lawrence Livermore Cent
or Accelerator Mass Spectrometry.
,.p ';‘"S.'ICal wcre performed in SPSS 16.0
(SPSS Inc, .008). and results were considere
significant at /» < 0.05. We used analysis c
variance to test differences among years in
deceased Least Auklet wing chord and mass, as
well as differences in gas composition between our
samples and normal atmospheric concentrations.
We used Games-Howell (GH) tests for multiple
comparisons (Games and Howell 1976) of auklet
measurements as variances were not homogeneous
(Levenc I960, Day and Quinn 1989).
RESULTS
Dead birds (mostly fledged juvenile Least
Auklets) were found in the canyon during 2001-
2006. Other species, including passerines, gulls,
and raptors began appearing in the canyon in 2007.
suggesting factors other than natural deaths
associated with a large seabird colony might be
involved (Table 1). Most auklets appeared on 1-
2 days each year: 30 July 2007, 1 August 2008, 2-3
August 2009, and 30 July 2010. Other species
included: Peregrine Falcon ( Falco peregrinus).
Glaucous-winged Gull (Lams glaucescens),
Brown Hawk-Owl ( Nino.x scutulata) (Bond and
Jones 2010), Crested Auklet, Pacific Wren I Trog¬
lodytes pacificus). Gray-crowned Rosy-Finch
(Leucosticte tephrocotis), and Snow Bunting
(Plectrophenax nivalis) (Table 1).
The mass of individual dead Least Auklet
fledglings ranged from 35 to 84 g and differed
among years (FX297 = 79.42, P < 0.001). Past-hoc
tests revealed the mass of dead fledglings differed
each year with 2009 < 2010 < 2008 < 2007 (GH
tests, all P < 0,003). Fifty-six birds in 2007 (69 %),
96 in 2008 (91%), and all birds in 2009 (n = 52)
and 2010 (n = 67) were below the asymptotic
Bond el al. • AVIAN MORTALITY AT A VOLCANO IN ALASKA
149
TABLE 2. Atmospheric composition of gas samples at Kiska Island, Alaska, in 2009 and 2010 (elevated CO, in the
sample from 30 Jul 2010. indicated in bold). Data are presented as the percent composition of samples; gases representing
<0.001% of samples are not included. Normal atmospheric composition is from NASA Global Climate Data Center.
Gas 19 Jun 2009 4 Jut 2009 18 Jul 2009 31 May 2010 30 Jun 2010 _ 30 Jul 2010 _ Air _
At 0.944 0.933 0.913 0.905 0.913 0.890 0.934
0, 21.044 20.875 21.115 21.257 21.083 20.717 20.946
N2 77.974 78.025 77.872 77.759 77.964 77.035 78.084
CO, 0.037 0.166 0.099 0.079 0.039 1-358_ 0.07-9
weight of 73.0 ± 2.2 g reported in a chick growth
study on Kiska by Major et al. (2006).
Flattened wing chord also varied by year (/Ties
= 33.39. P < 0.001) with corpses from 2009 and
2010 having shorter wings than those in 2007 and
2008 (GH, P < 0.001). The mean (± SD) wing
chord in 2007 and 2008 was 91 ± 5 mm and 92 ±
5 mm respectively, while in 2009 and 2010. the
mean was 86 ± 5 mm and 85.5 ± 6 nun. There were
1 (4%>. 3 (37c). 9 (177c). and 13 ( 19%) fledglings
with w ing chords shorter than the mean wing chord
reported by Major et al. (2006) of 80.3 ± 3.4 mm in
2007. 2008. 2009. and 2010. respectively.
Gas concentrations and composition were similar
to normal atmospheric levels in all samples, except
,or slight enrichments in CO,, which reached
1 .358% on 30 July 2010. Elevated CO, was found
on other days, hut quantities were insufficient to
perform isotopic analysis (Table 2). Isotopic anal¬
ysis of this single sample gave a 6 1 'C' of -9.55%n,
within the range of magmatic gas from Aleutian
Arc volcanoes (Symonds et al. 2003). A low UC
"aluc of 0.0399 (Fraction Modern Carbon; 0.052%
cl the total sample volume) of the July 20 1 0 sample
had only a trace component of biogenic CO, wilh
’he remainder ( 1 .306% of the total volume, or 96%
°t (he total C02) volcanic in origin.
DISCUSSION
The 2009-2010 samples from the gas seep on
Kiska Island contained only low levels of C02 and
mostly auklets were found dead (Table 2). We
^peci there is significant intcrannua! variation in
emissions, and that emissions were higher in 2007
and 2008 when larger numbers of small land birds
*ere found dead (Tabic I ). Dead passerine birds
without obvious external or internal injuries, and
no alternative explanations for numerous deaths in
■such a small area over a small temporal scale were
lhe first indication of a possible environmental or
geological cause of death. Toxic gas concentrations
may only be present in lethal concentrations on
certain days with light wind; all our sampling
occurred when average wind speed was >25 km/hr,
typical for the area during summer. Cold gas seeps
that emit nearly pure CO: are known in many
volcanic areas, such as Mammoth Mountain,
California, where emission rates have been shown
to vary on time scales ranging Irom diurnal to
decadal in response to both magmatic unrest and
meteorological forcing (Lewicki et al. 2(X)7).
Nearly all confirmed breeding species at Sirius
Point have been recovered in the valley containing
the pits; exceptions being species that breed in much
lower density in this area of Kiska Island such as
Snow Buntings, which are uncommon local breed¬
ers in alpine areas of the volcano (Bond et al. 2010).
The only vagrant found was a Brown Hawk-Owl
(Bond and Jones 2010).
Many dead Least Anklet fledglings were under¬
weight, yet few had underdeveloped wing feathers
compared to chicks in a growth study on Kiska in
2002 and 2003 (Major et al. 2006). This suggests
they were in poor condition (Oyan and Anker-
Nilsscn 1996) and were likely trapped in the valley.
They could not fly or take off once trapped by the
tall vegetation (mainly Puccinellio spp., Carex spp.,
and Calurnagrostis spp.), while attempting to depart
lo the sea. We believe a combination of starvation,
poor condition, and noxious gases contributed
to anklet deaths. Fledgling ale ids have a natural
inclination to descend while fledging, presumably
an adaptation for nesting on slopes and cliffs
(Gaston and Jones 1998). It is difficult, without
detailed necropsies, to know it (he auklets continued
to descend into the gas-filled depression and died
because they could not emerge to go to sea and feed,
or from asphyxia. In contrast, the large number of
land birds found, and that large numbers of seabirds
were found on only 1 or 2 days each year suggests
that gaseous emissions had a role in avian mortality
in some years.
This gas seep had a weak feed of magmatic CO,
that was only readily detectable in one of six
150
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 1. March 2012
monthly samples. 5,3C analysis of the single sample
with substantially elevated C02 placed the ratio of
l3C/l2C in the range of other Aleutian volcanoes,
and higher than biogenic carbon isotope ratios in
C02 (Ceding et al. 1991. Symonds et al. 2003). Of
the 1.358** C02. 0.052% originated in air/soil, and
1.306% (or 96% of all C02) was magmatic in
origin. It was apparently sufficiently strong to
produce concentrations lethal to birds at certain
times (i.c.. calm winds), even if only for a few days
each year. We conclude that, while these gaseous
emissions do not present an immediate threat to the
large auklet population, birds could be particularly
susceptible in some years, and especially if future
volcanic eruptions occur at this site.
ACKNOWLEDGMENTS
We thank A. U. Igamberdiev for assistance with Russian
translation. C. A. Neal of the Alaska Volcano Observatory
(USGS, Anchorage, AK. USA), for proposing the gas
sampling and analysis, and C. P Brake, E. E. Penney,
D. W. Pirie-Hay, and G. VI . Samson for assistance in the
field. Michelle Willc provided valuable discussions on
avian pathology. The Natural Sciences and Engineering
Research Council of Canada. Alaska Maritime National
Wildlilc Refuge, and Northern Scientific Training Program
of the Department of Aboriginal Affairs and Northern
Development of Canada supported our work in the
Aleutians financially, and the captain and crew of the M/
V Tiglax. and J. C. Williams and G. V. Byrd provided
logistical support. This manuscript was improved by
comments from C. E. Braun, and two anonymous
reviewers. Any use of trade, product, or firm names is for
descriptive purposes only and does not imply endorsement
by the U.S. Government.
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Food Habits of Two Fork-tailed Swifts in Venezuela
Charles T. Collins1,2 and Betsy Trent Thomas'
ABSTRACT. — The aerial arthropod prey of Neo¬
tropical Palm Swifts ( Tachomis squamata) and Lesser
Swallow-tailed Swifts ( Panyptila cayennensis) in Ven¬
ezuela included seven Orders and 60 families of insects
plus spiders and mites. Diptera were the most numerous
prey (>50%) taken by both swifts. Prey size ranged
from 0.5 to 7.9 mm and averaged 2.43 and 2.77 mm.
respectively. Both prey type and foraging habitat
differences of these swills could be interpreted as
mechanisms for resource partitioning. Received (
March 2011. Ac cepted 20 September 2011.
The tails of birds are diverse in both morphology
and function. The size and shape of most tails
reflect their functional aerodynamic properties, bul
many others are highly modified for use in sexual
displays (Thomas 1997). Deeply forked tails are
found in many species including some swifts
(Apodidae). swallows (Hirundinidae), and terns
(Steminae) and may reflect selection for both
aerodynamic and display functions. Forked tails
are thought to provide additional lift, when fanned,
and increased turning agility (Thomas 1997).
Deeply forked tails in aerial foraging inseelivores
may be adaptations for pursuit and capture of more
agile prey or foraging low to the ground and close
to vegetation (Waugh and Hails 1983). Fanning of
the wing and tail feathers is a frequently observed
behavior associated with rapid flight changes
during prey captures by swiftlets (Manchi and
Sankaran 2010). Differences in prey selection
resulting from variable flight behaviors may be
an important isolating mechanism for closely
related species, particularly when in mixed species
foraging flocks (Waugh and Hails 1983).
It is usually difficult to get detailed information
on the prey taken by aerial foraging inseelivores
(Jahn et al. 2010). Direct observation can only detect
or identify larger prey items and remains of smaller
1 Depan ment of Biological Sciences. Qdilbmia Stale Ur
CA lJSA: email: ccdgmOc^
CA^ZT.vTr' Fairbr”k *«• B,
3 Deceased.
and more delicate prey may be undetected in gut
contents or fecal samples. The boluses of arthropod
material collected by swifts allow detailed analysis
of both the prey taxon anti prey size of even small
insects and spiders. However, this infonnation is
only available during the chick-rearing period of the
breeding season and may not be representative of
swift diets at all times of the year. Prey type and
availability may change substantially during the
drier non-breeding season in tropical regions (Hails
and Amimidin 1981, Jahn et al. 2010).
The goals of our study wore to: (I ) describe the
type and size of the prey taken by two neotropical
swifts having deeply forked tails, the Neotropical
Palm Swift {'Tachomis squamata ) and the Lesser
Swallow-tailed Swift ( Panyptila cayennensis );
and (2) look for qualitative differences in prey
taken by other swifts lacking deeply forked tails.
The Neotropical Palm Swift is a widespread
and common resident of lowland sandy soil or wet
savannas throughout its range extending from
eastern Colombia and Venezuela south to eastern
Peru, and Amazonian Brazil (Hilty and Brown
1986. Hilty 2003). it is usually observed circling
al “low to moderate heights” over open areas
where there are palms (Hilty 2003:389). h less
commonly occurs in urban areas where palms
have been planted (Chanlier 2000. this study).
The Lesser Swallow-tailed Swift occurs troin
southern Mexico south to southeastern Peru,
northern Bolivia, and Amazonian and southeastern
Brazil (Hilty and Brown 1986. Sick 1993. Howell
and Webb 1995, Hilty 2003). It is “uncommon and
local in occurrence ... over humid lowland and
foothill forest or partially forested terain (Hilty
2003:389) at elevations of 1.000 to 1.400 m (Hilty
and Brown 1986. Stiles and Skutch 1989. Hilt)
2003). Its characteristic tubular nests occur at
elevations from <100 to >800 m in Trinidad and
Venezuela (pers. obs.), and in urban areas in
Surinam (Haverschmidt 1958).
METHODS
Food samples of the two species ol swifts were
collected as boluses of food being brought to
152
SHORT COMMUNICATIONS
153
nestlings at two locations near Maracay, Estado
Aragua, Venezuela. Seven partial or complete
boluses from Neotropical Palm Swifts were
obtained from adults captured in a mist net on
27 July 1976 as they were entering a nesting
colony in dense dead palm fronds near the base of
a tree on the grounds of the Hotel Maracay ( 10
17' N. 6T 35' W). Boluses were collected from
the mouth of the netted adult or from a cloth on
the ground below the net if the bolus was ejected
by the adult when captured. The exact number of
nests could not be ascertained due to the density
of the fronds but there were 28 captures of adults
at this site. It is unlikely that more than one bolus
was collected from any single individual. A single
complete bolus and one partial bolus were
collected on 16 July 1976 from the mouths of
Lesser Swallow-tailed Swift nestlings in a nest on
a roadside overhanging rock cleft in the lower
portion of Henri Pittier National Park, just north
of El Limon (10 19' N, 67“ 39' W). These two
locations are ±9 km apart. No measurements of
insect abundance in the study area were made as
part of this study. All of the food boluses were
stored in alcohol and later examined under a
dissecting microscope. Identifications were made
to the family level; the two psocopterans were
identified as Caecilius ahtillcmm (Turner 1984).
Body size of prey items was measured with an
ocular micrometer to 0.1 mm from the tip of the
head to the tip of the abdomen excluding antennae
or any caudal appendages.
RESULTS
The 381 prey items obtained from Neotropical
Balm Swifts were distributed among seven Orders
and 62 families of insects in addition to spiders
and mites (Table 1). Diptera (52.2%), Homoptcra
'i8.1%), and Hymenoptera (10.5%) were the
roost numerous insects recorded. The 108 prey
Hems obtained from Lesser Swallow-tailed Swifts
^ere similarly diverse with spiders and five
Orders of insects distributed among 22 families.
D‘Piera (62.2%), Homopteru (17.6%), and Hy-
roenoptera (1.3.9%) were the most numerous
insects recorded (Table 1).
The size of the prey items taken by Neotropical
Balm Swifts ranged from 0.5 to 7.8 mm with a
mean ± SD of 2.43 ± 0.9 mm. The size of the
Prey items taken by Lesser Swallow-tailed Swifts
ranged from 1.1 to 7.9 mm with a mean ± SD of
2.77 ± 1.49 IT,m. There was an abundance of
smaller prey (<4 mm) and few larger prey items
in the boluses from both species (Fig. 1).
DISCUSSION
Both Neotropical Palm Swifts and Lesser
Swallow-tailed Swifts took a preponderance
(>50%) of Diptera in the samples collected.
There are no detailed data on flight characteristics
of most insects, but it has been suggested
(Hespenheide 1975) that Hies are more agile
fliers than representatives of other Orders with the
possible exception of some hymenopterans. There
is some support lor ihe suggestion that deeply
forked tails in these two swifts are adaptations for
pursuit of agile prey. Further support can be found
by examining the prey types taken by three other
Venezuelan swifts which have square or only
slightly forked tails. Diptera comprised only 27-
35% of their diets while Hymenoptera. particu¬
larly slower flying winged ants, made up 28-51%
of their diets (C. T. Collins, unpubl. data).
The food of the Lesser Swallow-tailed Swift in
Costa Rica included (lying ants, temutes, small
beetles, bugs, flies, and wasps (Stiles and Skutch
1989); in Brazil “small ants and termites
comprised about 90% of the diet of both species
(Sick 1993:313). Winged ants and temutes were
rare or absent from the prey identified in our study
(Table 1) but expectedly would occur in their
diets at times when these swarming insects are
temporarily abundant,
Diptera made up 43% of the prey items ol the
White-rumped Swiftlct (Ae rod ramus spodiopy-
gius ) in Fiji (Tarburton 1986b), 24% of the prey
of this species in Queensland, Australia (Tarbur-
lon 1993), and 25.8% of the prey of the Glossy
Swiftlet ( Collocalia esculenta) in Malaysia (Hails
and Amirrudin 1981). Diptera were more com¬
monly taken in open areas than in forested areas in
Fiji, and taken more frequently than their
representation in aerial insect samplings (Tarbur¬
ton 1986b). Diptera averaged 22.1% (range =
5.0-57.2%) of the prey of seven larger swifts in
Europe and Africa (Cucco et al. 1993; Collins
et al. 2009. 2010: Garcia-del-Rey et al. 2010). Only
the Common Swift (Apus apus) had an occurrence
above 50% of the prey items and then in only one
of three separate prey collections (Lack and Owen
1955: C. T. Collins, unpubl. data).
Previous studies have also documenled sub¬
stantial differences in prey taken by individual
species on different days or under differing
weather conditions (Lack and Owen 1955, Hails
154
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 1. March 2012
TABLE 1. Prey Items taken by Neotropical Palm Swifts and Lesser Swallow-tailed Swifts in Venezuela.
Neotropical Palm Swift Lesser Swallow-tailed Swift
Prey taxon % n % n
Araneae
8.6
1.9
Thomiscidae
8
2
Clubionidae
5
Lingphiidae
4
Zoridae
1
Salticidae
7
Ctenidae
3
Sparassidae
Lycos idae
Theridiidae
1
1
3
Coleoptera
7.6
3.7
Curculionidae
10
2
Dryopidae
Histeridae
1
2
Nitidulidae
Scaphidiidae
Anobiidae
Bostrichidae
Chrysomelidae
Lyctidae
1
1
1
1
13
1
Hemiptera
1.1
0
Lygaeidae
Piesmatidae
1
3
Homoptera
18.1
17.6
Aphididae
3
2
Delphacidae
33
13
Cicadellidae
20
4
Psyllidae
8
Membracidae
2
Cixiide
3
Hymenoptera
10.5
13.9
Formicidae
7
2
Braconidae
Chalcididae
1
1
10
1
Eulophidae
2
1
Pteromalidae
Ichneumonidae
3
1
1
Chrysididae
2
Encyrtidae
Torymidae
Cephidae
Sphecidae
5
1
1
1
Agaonidae
7
Cynipidae
Psocoptera
0.2
8
0.9
Pseudocaeciliidae
1
1
Diptera
52.2
62.1
Syrphidae
3
Tephritidae
4
A
Calliphoridae
Muscidae
2
2
3
SHORT COMMUNICATIONS
155
TABLE 1. Continued.
Neotropical Palm Swift
Lesser Swallow-tailed Swift
Prey I aeon
%
n
%
n
Diptera, continued
Sciaridae
8
Dolichopodidae
21
20
Ephydridae
26
2
Lauxaniidae
2
1
Chloropidae
68
21
Chamaerayiidae
1
Agromyzidae
16
3
Drosophilidae
6
1
Stratiomyidae
4
Empididae
1
Phoridae
5
Chironomidae
2
Milichiidae
7
Mycetophilidae
2
Cecidomyiidae
1
Pipunculidae
1
Otitidae
1
Sepsidae
4
Anthomyzidae
13
Trixoscelididae
2
Lepidoptera
0.5
0
Coleophoridae
1
Pyralidae
1
Acarina
1.1
4
0
Totals
381
108
FIG. 1. Distribution of prey sizes of the Neotropical Palm Swift (dark bars) and Lesser Swallow-tailed Swift (shaded bars).
156
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 1. March 2012
and Amirrudin 1981. Waugh and Hails 1983,
Tarburton 198(>b, Garcia-dcl-Rey et al. 2010), in
different parts of their geographic range (Collins
et al. 2009) and in samples taken from the same
population in different years (Collins 2010). Thus,
variation in type of prey captured is difficult to
analyze, particularly when only limited food
samples are available. The size of prey items
tends to be more uniform despite appreciable
differences in prey types taken (Collins 2010).
The mean size and range in size of prey items
taken by the Neotropical Palm Swift and Lesser
Swallow-tailed Swift in this study were highly
similar. There is an abundance of smaller prey
items for bolh species and a lesser number of the
larger items (Fig. 1) as true for other swifts
(Collins et al. 2009, 2010; Garcia-del-Rey et al.
2010). Body weight for a variety of insectivorous
birds, is "a better predictor of the size of prey
taken" than morphological characteristics such as
bill size or shape (Hespenheide 1971:63). Recent
studies of other swifts have shown there is a
significant linear relationship between swift body
weight and mean prey size (Collins et al, 2009).
Thus, the larger Lesser .Swallow-tailed Swift
(mean body weight = 20.9 g, range = 15.8-
23.0 g, n = 5; C. T. Collins, unpubl. data) might
have been expected to take, on average, larger
prey items than the smaller Neotropical Palm
Swift (mean body weight = 10.4 g, range = 9.0-
12.4 g. n = 47; C. T. Collins, unpubl. data). This
is not indicated by the data presented. However,
prey taken by these two swifts may also have been
influenced by their foraging habitat. Neotropical
Palm Swifts, as their name implies, forage almost
exclusively in lowland wet palm savannas where
they “circle at low to moderate heights’* (Hilly
2003:390) and at times low over grassy areas
(C. T. Collins, pers. obs.) where agility would be
important. Other species of swifts are generally
uncommon in this foraging area. Lesser Swallow¬
tailed Swifts are frequently observed flying and
foraging high to very high above the ground
(Stiles and Skutch 1989, Hilty 2003). They are at
times found loosely associated with feeding flocks
of other species of swifts ( Chaeiura spp.), at
which time Lesser Swallow-tailed Swifts appear
to fly and forage well above the others (Stiles and
Skutch 1989; Hilty 2003; C. T. Collins, pers.
o .v). hese swifts, when actively foraging, tend
to fly very jerky erratic manner with many
KqT Shm‘S of (Hilty
2003.389). The tail which is usually closed and
spike-like is widely fanned during abrupt changes
in direction (Stiles and Skutch 1989). Foraging at
higher altitudes may reduce the encounter rate
with larger and slower flying prey such as winged
ants and termites, and require more active pursuit
of smaller and faster flying prey, such as Diptera.
Glick (1939) reported Diptera were nearly three
times more abundant than insects belonging to
any other Order at elevations from 30 to 60 m
while there is a greater proportion of larger and.
presumably, slower flying insects nearer the
ground (Johnson 1969). The low wing loading
and high aspect ratio typical of most swifts and
swallows favors the gliding flight often seen in
these birds as well as their low flight metabolism
(Hails 1979). However, no attention has yet been
given to measuring the energetic cost/benefit ratio
of the different foraging behaviors and their
relationship to aerial prey availability.
The maneuverability or agility of birds is
difficult to quantify for purposes of interspecific
comparisons. Two maneuverability indices have
been proposed: a wing index (the ratio of the wing
length to body weight; Tarburton 1986a) and a tail
index (the ratio of the length of the outer and
longest rectrix to body weight: Hails and Atnimi-
din 1981). The tail index of 6.71 for the
Neotropical Palm Swift is among the highest ot
44 species reviewed by Tarburton (1986a). It is
exceeded only by the 7.79 for the African Palm
Swift ( Cypsiurus pan'us) and the 6.97 for the
Black Saw-wing (Psidoprocne pristoplera). Both
of these species are light bodied and have deeply
forked tails. The tail index for the Lesser
Swallow-tailed Swift is 2.67 (C. T. Collins,
unpubl. data). The Black Saw-wing forages low
across forest and woodland clearings, along forest
tracks, and over tallgrass savanna at an average
height of 7 m hut is often observed skimming the
ground (Turner and Rose 1989, Keith et al. 1992.
Sinclair et al. 1997). Its deeply forked tail, which
presumably increases its agility, would be of great
advantage, and selected for, in habitat' requiring
careful maneuvering.
It is not clear as to whether the forked tail of the
Neotropical Palm Swift is selected for lower level
flight in its more restricted palm savanna foraging
habitat or more for pursuit of agile prey,
particularly Diptera. The forked tail of the Lesser
Swallow-tailed Swift seems more likely to be an
adaptation for capturing agile prey in the an
column at higher altitudes above ground level.
The forked tails of these two swifts seem to be
SHORT COMMUNICATIONS
157
related to their exploitation of habitats and non-
uniformly distributed types of aerial insect prey not
as intensely used by other species. This may he
viewed as forms of resource partitioning allowing
coexistence of otherwise similar species of aerial
insectivores (Waugh and Hails 1983, Collins
2000). Additional attention needs to be given to
the food and foraging of these and other swifts to
confirm the interpretations presented here.
ACKNOWLEDGMENTS
I am grateful to Gonzalo Medina P. for permission to
conduct studies of swifts in Henri Pittier National Park and to
Robert Smice and Robert Waggenstein for identification of
the prey items. Michael K. Tarburton, two reviewers, and the
editor made helpful suggestions which improved an carls
draft of this manuscript. The field portions of this study could
not have been conducted without the participation and
cheerful companionship of the late Betsy Trent Thomas.
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158
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 1. March 2012
The Wilson Journal of Ornithology 124(1): 158-1 61, 2012
Observations on Zugunruhe in Spring Migrating Eared Grebes
Andre Konter1
ABSTRACT. — About 200 North American Eared
Grebes (Podiceps nigricollis califomicus ) at Tule Lake
Refuge in northern California were observed engaging
in successive waves of mass pattering and pattering
flights on 25 May 201 1 Most grebes present in a part of
a canal were involved in this activity. Counts of grebes
on the morning of 26 May suggest an important portion
of the Eared Grebes seen in pattering could have left the
area over night. The behavior was characterized as
zugunruhe. Directed mass pattering of Eared Grebes
may contribute to synchronization of the onward
migration of the birds involved. Received 13 July
2011. Accepted 10 September 2011.
North American Eared Grebes ( Podiceps ni¬
gricollis califomicus) are seldom seen in flight,
except when they migrate (Beni 1919, Gaunt et al.
1990). The migration of the species has been well
studied (Storer and Jehl 1985, Gaunt et al. 1990,
Jehl 1997. Cullen et al. 1999, Jehl and McKeman
2002. Jehl and Henry 2010), Cullen et al. (1999)
indicate migration flights begin around dusk and
end before dawn. Jehl and Henry (2010) note
strict correspondence of departure with near-total
darkness. Grebes tend to gather as the time for
departure nears (Jehl and McKernan 2002). Pre¬
departure activities include group diving, and
submerging and surfacing in near unison. A
unique call is given as grebes prepare to depart
and immediately before actual take-off (Jehl and
Henry 2010).
Daytime flights are possibly observed only
when grebes rebuild their flight muscles prior to
migration when they may perform one or two
short practice flights (Jehl and Henry 2010) or
race across the surface in short practice flights,
often in small groups (Jehl and McKeman 2002). I
was surprised to observe a mix of pattering and
flight by larger groups of Eared Grebes in
Northern California during daylight conditions. I
describe these common pattering flight maneuvers
and discuss their possible meaning.
1 Museum of Natural History, 25, rue Munster. Lux,
bourg L-2IM), Luxembourg; e-mail; podiceps @pt.|u
METHODS
A study of courtship of Eared Grebes was
undertaken at Upper Klamath Lake, Oregon, anti
Lower Klamath Refuge and Tule Lake Refuge,
both in northern California, from 14 to 27 May
2011. This region is known to support thousands
of Eared Grebes each year for nesting, water
levels permitting. The California refuges hosted
7,397 and 3,700 nests, respectively, in 2003 and
2004 (Shuford et al. 2006). Fieldwork was from
0700 to 1700 hrs each day using a car as a blind.
The car was parked at suitable places along roads
near bodies of water and remained immobile for
up to 3 hrs. The behavior and displays of grebes
were documented either by photograph, video
film or immediate voice recording. All observa¬
tions of pattering flights are from Tule Lake
Refuge, part of the Klamath Basin National
Wildlife Refuges, an artificial water impoundment
of mostly open water covering -5,200 ha at an
altitude of 1.200 m and surrounded by croplands.
The observations were in an area called the
English Channel (4F 5 1 ' 202 N, 12L 29' 727 W)
in the central part of the wildlife tour into the
refuge. This is an L-shaped canal. <50 m in
width. It opens at its northern end into large sump
1 A. an open and shallow area of the lake. It takes
a left turn after —1.6 km in a straight line from
north to south (NS canal or NS part of the English
Channel) and continues east for another 0.5 km
(EW canal or EW part of the English Channel)
until ending at a dam-levee that separates it from
the adjacent larger sump IB (Fig. 1). The entire
canal is devoid of emerging vegetation.
1 differentiate between pattering (a grebe with
flapping wings runs with paddling feet or even
partially glides over the water surface, but
remains in constant contact with the water ,
pattering flight (after an initial pattering, a grebe
is airborne for a distance limited to a few meters
during which it does not touch the water surtace),
and real flight (the distance covered while
airborne exceeds 10 m). It is well established that
Eared Grebes use pattering in the retreat display
and during escape/pursuit or more generally
SHORT COMMUNICATIONS
159
Momia
'• English Channel area. Tule Lake Refuge
lia
aggression (McAllister 1958. Cullen et al.
these occurrences are not included. My
J^ives in this paper are to provide a lull
option of pattering and pattering flights by
r numbers of grebes, and to discuss possible
l<**s for their occurrences.
RESULTS
Nervations in ihe southern English C hannel
-5 May started at 0900 hrs. Over 200 Eared
hes were scattered partially in loose groups all
r 'he EW pan of the English Channel around
day when about three quarters ot them
aged in pattering. The grebes did so m
Secutive waves, all into a western direction
the connection to the NS canal. The
den take-off by one or two grebes seemed to
* others in their immediate vicinity and on
their way to move in the same direction. Groups
of 10-30 birds pattered over a short distance (20—
30 ml. some briefly loosing contact with the water
surface in a pattering flight. Grebes getting briefly
airborne possibly did so to avoid collision with
conspecifics that remained stationary on the water
surface. Grebes landed ahead of others that started
similar maneuvers in their wake, perhaps cairying
along some of those that had just stopped
pattering. A few additional waves of pattering
were launched. Some birds dived after landing;
others elevated their necks, remained alert, and
looked around without changing their westward
orientation. Most of the population, including
subgroups closer to the NS canal which were not
observed to patter, was swimming in the direction
of the NS canal. The eastern and central parts ot
the EW canal were rather empty of Eared Grebes
after some 2-3 min. leaving only a few Western
(Aechmoplwrus occidental!* ) and Clark s grebes
(A. clarkii) and a few ducks remaining. Fewer
than 100 Eared Grebes were still swimming in the
western part of the EW canal towards the
connection with the NS canal when they encoun¬
tered about 40 birds swimming in a group to re¬
enter the EW canal. A rough count less than
10 min laler indicated that >200 Eared Grebes
had again spread over this canal.
Pattering and pattering flights started anew only
Jo min after the start of the t.rst genera
movement by the Eared Grebes. Take-off by one
or two Eared Grebes incited others m then
surroundings to join as before. The buds moved
westward in several waves and continued sw.^
mine into the same direction after landing,
grebes left the EW canal where only about 30
remained, all towards Us western t ,1 A fe
group of swimming grebes returned - I >at® .
a" lot^eTperiocf without graup pattering, but
with continuous calling, occasional disp ays and
much surface feeding on phantom midg^ (C/^
Zrus ciysti Minis) followed until -1400 hrs
Individual grebes performed feeding dives, but
no group diving, or submerging and surfacing
near unison was observed. The general patlenng
in waves and westward swimming towards the
connection with the NS canal started again and
most Eared Grebes finally left the EW canal. The
first grebes had turned and swam to return to the
EW canal when a sudden simultaneous eastward
160
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 1. March 20/2
pattering of >50 re-entering grebes occurred.
Two or three more waves by other groups
followed immediately. Five minutes later, 232
grebes were counted inside the EW canal.
Only the continuous and contiguous calls of the
birds were heard for —20 min. Ten birds then
initiated a fourth round of pattering in waves. This
time, the grebes had no common general direc¬
tion. The grebes more in the central part of the
observed area moved towards the dam, those
already closer to the eastern end paltered into a
more southwestward to westward direction. 'The
population present divided into two groups. About
100 grebes were clustered near the dam and
another 100 were scattered over the upper western
third of the EW canal. The space in between both
groups remained mostly empty. The western
group started immediately to swim eastward while
the eastern group slowly dispersed. The groups
soon melted and spread over the empty space that
had separated them.
Perhaps five additional pattering flights of up to
4-5 grebes were observed in between the different
mass pattering and pattering flights. It was not
known whether these were premature attempts to
initiate a wave or whether they were unrelated to
the mass movements.
The observations ended at ~ 1 700 hrs and 257
grebes were counted in the EW canal (26 in the
connecting corner square to the NS canal), 65
were present in the lower half of the NS canal and
347 in the upper half. Only five additional Eared
Grebes were detected at the mouth to sump I A.
Other parts of the sump close to the English
Channel were empty of Eared Grebes. A count of
the birds at 0700 hrs on the following day totaled
exactly 400 individuals, 269 less than the previous
count. Only 77 grebes were observed inside the
EW canal (28 in the connecting corner square)
while the NS canal had 323 grebes. Three hours
later, 126 Eared Grebes were recorded in the EW
canal and 337 in the NS canal. The two counts on
26 May revealed quite differing numbers of
grebes. The EW canal held 131 to 180 grebes
less and the entire English Channel held 206 to
269 grebes less than on the afternoon of 25 May.
Eared Grebes had arrived at Tule Lake Rt
in the course of the previous 2-3 weeks. I as:
that shortly after arrival, their wing muscles
•till in good (light condition on 25 May
intense practicing could not have explained
mass pattering. Most birds were actively courting,
hut the group pattering did not appear to tv
related to pair bonding. There is also no reason to
believe the grebes tried to divert an aerial predate
with common flight activity as several instance*
ol Bald Eagles ( Haliaeetus leucncephalus) ap¬
pearing in High! over the grebes or even trying a
catch in the canal did not trigger much reaction.
Birds pattering to escape a pursuing conspecificor
to flee possible danger incited alarm at the most to
a handful of other Eared Grebes in their
immediate vicinity. The generalized pattering by
larger groups of Eared Grebes observed appeared
unrelated to courtship, aggression, fear or predator
presence. A similar or comparable behavior by
Black-necked Grebes (P. n. nigricoUis) in Europe
has not been reported.
There is comparable agitation in Silvery Grebes
(P. occipitalis) during migration towards breeding
areas. Fjeldsa (1982) noted that Silvery Greks
show high restlessness and form long lines that
move back and forth on a lake from where, in the
subsequent night, at least part of the population
departed. He termed this pre-migratory restless¬
ness. Movements of a group of 70 Silvery Grebes
at Laguna Las Encadenadas, Argentina, in De-
cember 2006, were not limited to swimming, but
included sudden quasi-simultaneous take-offs ol
individuals more at the rear end of the line. Some
flew up, reaching a height of -2 m, possibly to
avoid collision with the birds preceding them.
They landed again in front of the group that was
moving in one direction. The grebes at the rear
end acted similarly. The group changed direction
as it approached the shore, but continued
swimming in a line, and pattering and flying from
the back to the front (Konter 2009).
Eared Grebes at Tule Lake Refuge all swam
actively into the same direction, although they did
not form one line. They showed pattering and
pattering flights in waves and repeated the
directed group movements. .4 priori the compar¬
ison of total counts of grebes inside the English
Channel on the following day strongly sugge'^
least a major portion of the population had leti ihc
area. Zugunruhe seems an appropriate character
ization for the Eared Grebes' behavior. Additional
pre-departure activities at Tule Lake Refuge
including group diving, submerging and surfacing
in near unison as reported by Jehl and Henry
(2010) were not obvious. The grebes' diving and
swimming seemed to be predominantly related to
feeding, except the dives after mass pattering
SHORT COMMUNICATIONS
161
involved only a minority of a group. Active
vocalization may have helped group cohesion, hut
il could not be distinguished from advertising by
solitary birds or from contact calling by partners
momentarily separated.
It is not known to where the departing
grebes flew and whether they targeted breeding
areas in the region or flew a long distance. Eared
Grebes can move to other sites used for breeding,
even after arrival in a breeding area, or emigrate
from the region (Cullen 1998). It is also unknown
whether the grebes departed in flocks from the
English Channel and whether they headed in one
or different directions. 1 assume they were
migrants and the extent of their pattering flight
maneuvers suggests an eagerness to move on.
The counts of 25 and 26 May show that not all
Eared Grebes had left the English Channel over
night. Grebes present in the NS part were not
observed on 25 May and they may not have
engaged in group pattering. The first count on 26
May showed that low numbers of grebes were
present inside the EW canal and the higher later
count suggests that new grebes were continuously
settling there. Over 200 Eared Grebes left the
English Channel during the night and this number
corresponds as an order of magnitude to the
numbers involved in the group pattering. Thus,
most pattering grebes could have left over night
iUltl it is likely their zugunruhe contributed to a
simultaneous departure. They were gradually
replaced by conspecifics moving into the EW
fanal on the following day.
Eared Grebes often do not arrive within a short
lJPse of time inside a breeding region where
numbers generally build up over several weeks.
% synchronize, however, nest establishment
McAllister 1956. Boe 1994). In this context, it is
01 interest to further investigate how a conspic-
uous pre-migratory group pattering as observed at
Tule Lake Refuge may contribute to a coordinated
'inward flight inside a breeding region that would
facilitate simultaneous colony establishment by
•urge numbers of pairs. Unfortunately, the data
from Tule Lake Refuge do not permit any
conclusion to be drawn.
ACKNOWLEDGMENTS
I am grateful to Michele Nuss from the Tulc Lake Refuge
Headquarters who was of great help in the preparation of
my fieldwork. 1 thank J. R. Jehl ,lr and C. E. Braun for
critical review and constructive comments on the first draft.
LITERATURE CITED
BENT. A. C 1919. Life histories of North American diving
birds. Order Pygopodes. U.S. National Museum
Bulletin 107:1-47.
Bor. J. S. 1994. Nest site selection by Eared Grebes in
Minnesota. Condor 96:19-35.
Cue U N. S. A. 1998. Population biology of Eared Grebes in
naturally fragmented habitat. Thesis. Simon Fraser
University. Burnaby. British Columbia. Canada.
Ci i ten, s. A.'. J. R. Jehl, and G. L. Nlechterlhn. 1999.
Hared Grebe. The birds of North America. Number 433.
Fjei dsA. J. 1982. Some behaviour patterns of four closely-
related grebes. Podiceps nigrieollis. P. gallardoi, P.
occipitalis, and P. taczanuwskii, with reflections on
phylogeny and adaptive aspects of the evolution of
displays. Dansk Ornithologi.sk Foremngs Tidsskrift
76:37-68.
Gaunt. A. S., R. S. Hikida. J. R. Jehl Jr., and L. Fenbert.
1990. Rapid atrophy and hypertrophy of an avian flight
muscle. Auk 107:649-659.
Jehl Jk„ J. R. 1997. Cyclical changes in body composition
in the annual cycle and migration of the Eared Grebe
Podiceps nigrieollis. Journal ot Avian Biology
28:132-142.
Jehl Jr., J. R. and A. F.. Henry. 2010. The postbreeding
migration of Eared Grebes. Wilson Journal of
Ornithology 122:217-227.
Jehl. Jr.. J. R. and R. L. McKernan. 2002. Biology and
migration of Eared Grebes at Salton Sea. Hydrobio-
logia 473:245-253.
KONTER, A. 2009. Observations on diving times, on pre-
migratory restlessness and on some displays of Silvery
Grebes Podiceps occipitalis. Regulus Wissenschaf-
lliche Bcrichte 24:67-71.
McAllister, N. 1958. Courtship, hostile behavior, nest-
establishment and egg laying in the Eared Grebe
( Podiceps caspicus). Auk 75:290-31 1.
Shleord. W. D.. D. L. Thomson. D. M. Mauser, and
J. Beckstrand. 2006. Abundance and distribution of
nongame waterbirds in the Klamath Basin of Oregon
and California from comprehensive surveys in 2003
and 2004. PRBO Conservation Science. Petaluma.
California, USA.
Storer. R. W. and J. R. Jehl Jr. 1985. Moult patterns and
moult migration in the Black-necked Grebe Podiceps
nigrieollis. Omis Scandinavica 16:253-260.
162
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 1. March 2012
The Wilson Journal of Ornithology 124(1): 1 62- 165, 2012
Aromatic Plants in Eurasian Blue Tit Nests:
The *Nest Protection Hypothesis’ Revisited
Barbara A. Pires,1 Anabela F. Belo,24 and Joao E. Rabaga3,4,5
ABSTRACT. — The ‘Nest Protection Hypothesis'
suggests that some birds add aromatic plants to their
nests to repel or kill ectoparasites. This behavior has
been described for several species, including the
Eurasian Blue Tit (Cyanistes caeruleus). We studied
the reproductive performance, based on 26 nests (in
nest boxes), of this species in mixed forested areas of
Quercus spp, and Pinas pinea in the Parque Florestal de
Monsanto, the largest park of Lisbon, Portugal. The
frequency of aromatic plants in nests was compared
with frequency of these plants in the study area. The
three most frequent aromatic plants ( Dittrichia vi.scosa,
Lavandula deniata, Calaininrha baetica) in nests were
used more than expected from their availability in the
study area. We could not reject the null hypothesis that
nest survival rale is independent of the presence of
aromatic plants in the nest. Received 17 .lime 2011.
Accepted 17 September 2011.
Some birds use fragments of fresh plants in their
nests different from those used in nest cup construc¬
tion. For example, raptors include fragments of
resinous conifers (Dvkstra et al. 2009)
in their nests and passerines use herbaceous and
shrubby species ("Wimberger 1984. Lambrechts and
Dos Santos 2(XX)). These fragments tire incorporated
into the nest cup (Ontiveros et al. 2007) and several
hypotheses have been presented to explain ihis
behavior (e.g.. Bahbura et al. 1995. Gw inner and
Berger 2006, Mennerat et al. 2009b). The ‘Nest
Protection Hypothesis' (NPH) seems to be the most
plausible explanation for this behavior when the
green material is aromatic. This hypothesis suggests
that sprigs of aromatic plants are added to nests
because of the presence of volatile secondary
' Avenida 5 de Oulubro, 267 2 Dto 1600-035 Lisboa
Portugal.
“Laboratory ol Botany. Department of Biology. Univcr
sity of Evora. 7002-554 Evora. Portugal.
' Laboratory of Ornithology. Department of Biology, Univci
stty of Evora. 7002-554 Evora. Portugal.
4 Mediterranean Ecosystems and Landscapes Research
Group Ins, nute of Mediterranean Agrieul.ural and Environ
menu) Sciences, Ujlrvcrs.ty offivora, 7002-554 Evora, Portugal
Corresponding author; e-mail: jrabaca@uevora pt
chemical compounds (e.g., Wimberger 1984). name¬
ly terpenes (Camacho et al. 2000), to redtiCv
ectoparasite loads. Clark and Mason ( 1 988) explained
that volatile compounds can affect ectoparasite
feeding, even if numbers of ectoparasites in nests
do not decrease with presence of aromatic plants.
The NPH should be more relevant for hoic-
nesting birds which may reuse the same cavil'
for several breeding attempts, thus increasing the
probability of detrimental ectoparasite attack--. This
trail has been documented for European Starlings
( Slttnuis vulgaris) (e.g.. Gwinnerand Berger 2005 1
and Eurasian Blue Tits (Cyanistes caeruleus) (t, g-
Lambrechts and Dos Santos 2000. Mennerat et al
2009b). Female Eurasian Blue Tits, a few days
before egg laying, start to add fresh aromatic plait
material to their nest (Mennerat et al. 2009a) aDd
continue this behavior throughout the reproductive
cycle (Lambrechts and Dos Santos 2000).
Our objective was to examine if Eurasian Blue Tits
nesting in nest boxes use aromatic plains in their nests
more than would be expected according toavailabil
ity of these plants in the study area and. if so. which
species are used. An additional objective can be
established if aromatic plants are better represented m
nests than predicted, indicating a selective plan1
search: does the presence of aromatic planis in the
nests influence Eurasian Blue Til nest survival rate
METHODS
Study Area. — The study was conducted m
Parque Florestal de Monsanto. Lisbon. Portugu1
the largest park in the city with -900 ha. The
park has extensive forested areas dominated bv
Quercus spp. ( Q. robur. Q. saber. 0. cocrifeni. Q
rotundifoUa. Q. faginea, and 0. pyrentdea). Pllul '
pinea . P. balepensis . and Eucalyptus glohune
Four Quercus spp. and Pinus pinea mixed stand'
of —8 ha each were selected as study sites.
placed 484 (121/stand) pine wood nest bov-'
(chamber size: internal height x width X depth
17 X 10.5 x 13.5 cm; entrance hole diameter ~
3.5 cm) attached to a branch with a hook or wire
au'ay from hard substrate, 3 to 6 m above the
SHORT COMMUNICATIONS
163
TABLE I. Breeding
Eurasian Blue Tits using
de Monsanto (n = 26).
parameters (mean ± SD) of
nest boxes in Parque Florestal
Clutch size
6.0 ± 1.6
Eggs hatched
4.6 ± 2.3
Chicks fledged
3.0 ± 12.0
Hatching rate, %
71.9 ± 31.3
Nest survival rate, %
64.0 ± 36.1
Breeding success, %
47.9 ± 30.9
ground and oriented south or east to avoid the
dominant moderate-strong winds from north and
west (e.g.. Lambrechts et al. 2010). Nest boxes
were equally spaced from each other in a grid
arrangement of 25 X 25 m ( 1 nest box/25 X
25 nr). Nest boxes could not be placed at a few
points due to site constraints (lack of trees, ponds,
etc.).
Eurasian Blue Til Breeding Performance —
Fifty nest boxes were randomly selected in each
stand in the 2009 breeding season. We searched
for reproductive events of cavity nesting birds and
monitored the breeding performance of Eurasian
Blue Tits. All occupied nest boxes were checked
weekly from I March to 3 July to ascertain: ( I )
clutch size, (2) hatching rate (percent of eggs
incubated to term that hatched), (3) nest survival
mie (percent of fledglings per number of hatched
eggs), and (4) breeding success (percent of
fledglings per clutch). All nests were removed at
the end J. Casanova. 2006. Essential oil oSOittrichia mars*
ssp. viscosa : analysis b> J3C-NMR and antimicrobial
activity. Flavour and Fragrance Journal 21:324-332.
Bousmaha, L., f. a. Bekkara. f. Tomj. and J
Casanova. 2005. Advances in the chemical eompo
sition of Lavandula dentata L. essential oil from
Algeria. Journal of Essential Oil Research 1 7:292-29^
Camacho, A., a. Fernandez. C. Fernandez.. J- Ativ
rejos. and R. Laurent. 2000. Composition of the
SHORT COMMUNICATIONS
165
essential oil of Dittrichia viscosa (L.). W. Greuter.
Rivista Italiana EPPOS 29:3-8.
Clark, L, \nd J. R. .Mason. 1985. Use of nest material as
insecticidal and anti-pathogenic agents by the Euro¬
pean Starling. Oecologia 67:169-176.
Clark, L. and J. R. Mason. 1988. Effect of biological
active plants used as nest material and the derived
benefit to starling nestlings. Oecologia 77:174-180.
Dykstra, C . J. Hays, anl> M. Simon. 2009. Selection of
fresh vegetation for nest lining by Red-shouldered
Hawks. Wilson Journal of Ornithology 1 2 1 :208-2 1 1 .
Freeman. B. C. and G. A Beattie 2008. An overview of
plant defenses against pathogens and herbivores. The
plant health instructor. Iowa State University, Ames.
USA. http://www.apsnct.org/edcenter/intropp/topics/
Pages/OverviewOfPluntDisenses.aspx
Ci winner, H. 1997. The function of green plants in nests
of European Startings Stimuis vulgaris. Behaviour 134:
337-351.
GwtNNER. H. AND S, Berger 2005. European Starlings:
nestling condition, parasites and green nest material
during the breeding season. International Journal of
Ornithology 1 46:365 -371.
Gwinner. H. and S. BERGER. 2006. Parasite defence in birds:
trie role of volatiles. Acta Zoologiea Sinica 52:280-283.
Hinkle, N. 2010. Animals: pets (companion animals)
external parasite control. Georgia pest management
handbook. College of Agricultural and Environmental
Sciences, University of Georgia, Athens, USA. http://
www.em.uga.edu/pmh/
IHRAHl.M, M.. P. KAINULAINEN, A. Apt ATI Nt, K. Tlll.lK
K ala, and J. Holopainen. 2001. Insecticidal, repel¬
lent, antimicrobial activity and phytotoxicity of
essential oils: with special reference to limonene and
its suitability for control of insect pests. Agricultural
and Food Science in Finland 10:243-259,
Lambrechts. M. M, and A. Das Santos. 2000. Aromatic
herbs in Corsican Blue Til nests: the ‘Potpourri'
hypothesis. Acta Oecologica 21:175-178.
UMBR5CHTS. M. M„ F. AlJRlAKNSfiN, D. R. Ardia. A. V.
Artemyev, F. AtiEnzak, .1. Banbura. E. Rarha.
J.-C. Bouvier, J. Camprodon, C. B. Cooper. R. D.
Dawson. M. Eens, T. Ef.va, B. Faivre;. L. Z.
Garamszegi. A. E. Goodknough. A. G. Gosle.r, A.
Gregoike, S. C. Griffith, 1.. Gl'Stafsson, I.. S.
Johnson. W. Kama. O. Kf.iSs, 1’. E. Llambias. M. C.
Main-waring, R. Mand. B. Mass a. T D. Mazgajski.
A. P. Moli.er. j. Moreno, b. Nabt-Daenzer. J.-A.
Nilsson, A. C. Norte. M, Orf.i.l. K. A. Oitkk. Ch.
R Park, Ch. M. Perrins, .1, Pinowski. J Porkirt. J.
Pom. v. Remes, H. Richner, S. Rytkonen. M.-T.
SH1AO, B. SiLVERIN, T. SLAGSVOLD, H. G. SMITH, A.
Sorace. M. J. Stenning, 1. Stewart. Ch. F.
Thompson, J. TOrOk. P. Tryjanowskl a. j. van
Noordwijk, D. W. Winkler, and N. Ziane. 2010.
The design of artificial neslboxes for the study of
secondary hole-nesting birds: a review of methodo¬
logical inconsistencies and potential biases. Acta
Ornithologica 45:1-26.
Macchioni. K. P. L. Cioni. Ci. Flamini. I. Morelll S.
Macc ioni, and M. ANSALDI. 2002. Chemical compo¬
sition of essential oils from needles, branches and
cones of Pinas pinea , P halepensis , P. pinaster and P.
nigra from central Italy. Flavour and Fragrance
Journal 18:139-143.
MAMOCI. E.. I. CavoSKI. V. SlMEONh. D. MoNDELLl, L. AL-
Ritar, and P. Caboni. 2011. Chemical composition
and in vitro activity of plant extracts from Ferula
communis and Dittrichia viscosa against postharvest
fungi. Molecules 16:2609-2625.
Matos, O. 20 1 1 . The use of plants to fight toxin producers'
pests and microorganisms that cause diseases in animals
and humans via food (in Portuguese). Page 7 in 1 Garcia
do Orta Conference— Medicinal plants. Institute of
Hygiene and Tropical Medicine. Lisbon. Portugal.
Mennlrat. a., P. Per RET, and M. M. Lambrechts. 2009a.
Local individual preferences for nest materials in a
passerine bird. PLoS ONE 4t4):c5104. DOL10. 1371/
journal, pr.ine.0005 104
MeNNILRAT. A.. P. PF.RRET, P BOURGAIXT. .1. Bl.ONDEL, O.
Gimenez, D. W. Thomas, P. Heeb. and M. M.
LAMBRECHTS. 2009b. Aromatic plants in nests of Blue
Tits: positive effects on nestlings. Animal Behaviour
77:569-574.
moura. L. G. Wunderlich, m. Uhrig. A. Couto, V.
Peres. A. KatZIN, and E. Kimura. 2001. Limonene
arrests parasite development and inhibits isoprenyla-
tion of proteins in Plasmodium falciparum. Antimi¬
crobial Agents and Chemotherapy 45:2553-2558.
NHWCOMBE. R. G. 1998. Two-sided confidence intervals for
the single proportion: comparison of seven methods.
Statistics Medicine 17:857-872.
Ontiveros. D.. J. Caro, and J. M. Plegtiezuelos. 2007.
Green plant material versus ectoparasites in nests of
Bonelli's Eagle Journal of Zoology 27:99-104.
PETIT, C.. M. Hossaert-Mgkey. P Perret. J Blondel,
and M. M. Lambrechts. 2002. Blue Tits use selected
plants and olfaction to maintain an aromatic environ¬
ment for nestlings. Ecology Letters 5:585-589.
WiMBERGER. P. H. 1984. The use of green plant material in
bird nests to avoid ectoparasites. Auk 10:615-618.
166
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. I. March 2012
The Wilson Journal of Ornithology 1 24(1): 166- 1 69, 2012
Nesting of the Cinereous Warbling Finch ( Poospiza cinerea) in
Southeastern Brazil
Uschi Wischhoff,1’2 Fernando Marques-Santos,1 and Marcos Rodrigues'
ABSTRACT. — We describe a nest and nesting
activity of the Cinereous Warbling Finch (.Poospiza
cinerea I in Paredao da Semi do Curral City Park, State
of Minas Gerais in southeastern Brazil. Little is known
about the reproductive biology of this globally vulner¬
able species, The nest was built with fragments of grass
spikes in an Australian pine (Casuarina equisetifolia).
The clutch consisted of three eggs. We describe
courtship feeding behavior of the Cinereous Warbling
Finch and brood parasitism of the nest by the Shiny
Cowbird ( Molothrus bonaritnsis). Received 2 January
2011. Accepted 28 August 201 /.
Plain-tailed Warbling Finch ( P . alticola) and
Rusty-browed Warbling Finch ( P . enthropltr d
are scarce or unavailable. Little is known about
reproduction of the Cinereous Warbling Finch.
Lopes el al. (2010) reported two individuals
carrying nest construction material near degraded
pastures and orchards in Fortaleza de Minas CO
53' S, 46 42' W; 900 m asl) in October 2006, Wc
present the first detailed description of the nest
of the Cinereous Warbling Finch in southeastern
Brazil.
The genus Poospiza (Emberizidae) is wide¬
spread across South America and the Andes
Mountains (Ridgely and Tudor 1989); it in¬
cludes two endangered Andean species and one
vulnerable species in Brazil (BirdLife Interna¬
tional 2010). The Cinereous Warbling Finch
(Poospiza cinerea) is endemic to the large
savannah-like biome known as Cerrado in
central South America (Silva and Bates 2002).
This species may have been extirpated in three
of the five Brazilian states where it originally
occurred (BirdLife International 2010) and its
population is believed to be diminishing in the
other two states (Minas Gerais and Goias).
Habitat loss is considered the main cause of the
‘vulnerable' designation (BirdLife International
2010).
We searched the literature for reproductive data
on the clade in Poospiza which includes the
Cinereous Warbling Finch (Lougheed et al. 2000).
Data are available for Black-capped Warbling
Finch (P. melanoleuca) (Di Giacomo 2005),
suggested to be conspecific with the Cinereous
Warbling Finch (Ridgely and Tudor 1989). and
Ringed Warbling Finch ( P. torquata) (Mezquida
and Marone 2003). Reproductive data for the
1 Laboratory de OmitoJogia. Dcpartamento de Zoolog
» * Mi"“ e™*- c*» m
j l . 2 70-9U I , Belo Horizonte, Brazil
2 Corresponding author; e-mail: uschiw@gmail.com
METHODS
Study Area. — We began studying the basic
biology of a small population of Cinereous
Warbling Finches in May 2010 in the Paredao
da Serra do Curral City Park (19° 57' S, 43' 54'
W) in Minas Gerais, southeastern Brazil. The park
borders Belo Horizonte, a city of s2 million
residents. The climate is dry in winter and rainy in
summer (Cwa in Koppen’s system of classifica¬
tion; Peel et al. 2007), typical of tropical
highlands of Minas Gerais. The vegetation in the
area is classified as campo sujo with small
portions ol campo cerrado (Oliveira-Filho and
Ratter 2002). It is heavily degraded by urbaniza¬
tion. exotic and ornamental species (e.g.. Pwo
spp. and Eucalyptus spp.), frequent illegal '^ge¬
lation burning, and intensive mining.
The Cinereous Warbling Finch is frequently
seen in small groups of two to four members
loraging in typical plant species of Cerrado as
well as in exotic species. We observed a small
group with the aid of 8 x 40 binoculars and found
a nest being constructed. The nest was monitored
at a distance and its contents were verified when
the female spontaneously left the nest.
The gender of the individuals at the nest site
was assigned based on morphological, behavioral,
and vocalization characteristics (FMS and IJVV
unpubl. data). Measurements were taken with a
spring scale with 0. 1-g precision, a caliper with
0. 1 -mm precision, and a measuring tape.
SHORT COMMUNICATIONS
167
HG. I. (A) Shiny Cowbird egg oil the left. Cinereous Warbling Finch egg on the right; (B) nest with these two eggs
measured on 25 October 2010; (C) nest with three Cinereous Warbling Finch eggs plus one Shiny Cowbird egg on 24
October 2010; (D) nest supported by Australian pine branches.
RESULTS
We observed nest construction activity by
( inereous Warbling Finches on 17 October
2010. The nest (Fig. I ) was under construction
and both male and female were seen building the
nest, although another female member of the flock
stayed with the pair passively until the first egg
"as laid.
The nest was I m from a paved street adjacent
'o the Park at 1,179 m asl (19 57' S. 43 55' W).
rite nest was not a completely symmetric cup
and Ottow (1964) and Post and Wiley 1
Nest abandonment suggests this is a strategy used
to evade parasitism by the Shiny Cowbird a
strategy also reported for the Black-capped
Warbling Finch (Hoy and Ottow 1964).
ACKNOWLEDGMENTS
This work was supported by the Brazilian Re*‘lp-:i
Council (CNPq) and ‘Funda^ao O Boticdrio de fVeaV' J
Natureza'. MR received fellowships from t-NPq "Kl
FAPEMIG (PPM). FMS received an undergraduau-
scholarship from CNPq. We thank the administration
Mangabeiras City Park and the Belo Horizonte
Foundation for permission to work in Paredao da Setra “
Corral City Park. We also appreciate the reviews by Diemch
SHORT COMMUNICATIONS
169
W. Wischhoff and Fabio V. Vione, and the valuable
comments of C. E. Braun and two anonymous referees.
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United Kingdom, www.birdlife.org
Dr La Pena. M. R. 2006. Guia de lotos de nidos. huevos y
pichones de aves argentinas. L.O.L.A. — Literature of
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Pages 201-465 in Historia natural y paisaje de la
Reserva El Bagual. Provincia de Formosa. .Argentina.
Invemario de la fauna de vertebrados y de la flora
vascular de un area protegida del Chaco Hiimcdo (A. G.
Di Giacomo and S. F. Krapovickas, Editors). Tcmas dc
Natumleza \ conservation 4. Aves Argentinas/Asocia-
ucin Ormtologica del Plata, Buenos Aires, Argentina.
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Cowbirds and thetr hosts. Proceedings of the Western
Foundation of Vertebrate Zoology 2:226-302,
Hov. G. and J. Oitow. 1964. Biological and oologicul
studies of the molothrine eowbirds (Ictcridae) of
Argentina. Auk 81:186-203.
Hovt, D. F. 1979, Practical methods of estimating volume
and fresh weight of bird eggs. Auk 96:73-77.
Lores, L. E.. G. B. Malacco. E. F. ALtkff, M. F.
Vasconcelos, D. Hoffmann, and I.. F. Sii.vi.ira.
2010. Range extensions and conservation of some
threatened or little known Brazilian grassland birds.
Bird Conservation International 20:84 94.
I.ouciheed, S, C.. J. R. Frp.ih.AND. P. IIandhdkd. ami P. I .
Boac. 2000. A moleculur phylogeny of Warbling Finches
(Poospiza): paraphylv in u neotropical cmlvri/id genus.
Molecular Phylogenetics and Evolution 17:367-378.
Mezquida, E. T. and L. Makoni 20OV Comparison of the
reproductive biology of two Pooxpka warbling-linches of
Argentina in wet and dry years, Arden 91:251-262.
0nvr.ikA-Fii.HO, A. T. AND .1. A. Ra ITER. 2002. Vegetation
physiognomies and woody flora of the Ccrrado Biome.
Pages 91-120 in The cerrados of Brazil: ecology and
natural history of a neotropical savanna (P. S. Oliveira
and R. J. Marquis, Editors). Columbia University
Press, New York. USA.
PF.EL. M. C., B. L. Fini.ayson, and T. A. McMahon. 2007.
Updated world map of the Koppen-Geiger climate
classification. Hydrology and Earth System Sciences
11:1633-1644.
Post, W. and J. W. Wiley. 1977. Reproductive interac¬
tions of the Shiny Cowbird and the Yellow-shouldered
Blackbird. Condor 79:176-184.
R IDG ELY, R. S. AND G. TUDOR. 1989. The birds of South
America: the oscine passerines. University of Texas
Press, Austin. USA.
Rodrigues, M., L. M. Costa. G. H. S. Freitas. M.
Cavalcanti, and D. F. Dias. 2009. Ninhos e ovos de
Emherizoides herbicala. Emberizoides ypiranganus e
Enibemugra longicauda (Passeriformes: Emberizi-
dae) no Parque Nacional da Serra do Cipo. Minas
Gerais. Brasil. Revista Brasileira de Ornitologia
17:155-160.
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hospedantes del Renegrido (Mrdothrus bonariensis)
(Aves. Ictcridae). Historia Natural 4:121-130.
Santana. O. A. and J I. Encinas. 2008. Lcvantamento
das espccics exoticas arboreas e seu impacto nas
espccies nativas ein areas adjacentes a depositos de
residuos domiciliarcs. Biotemas 21:29-38.
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77ie Wilson Journal of Ornithology 124(1): 169- 173, 2012
Description of Eggs, Nest, and Parental Care ot the Smoky Bush Tyrant
(Myiotheretes fumigatus) from Ecuador
Tadeusz Stawarczyk,1,3 Marta Borowiec,1 Harold F. Greeney, and Jose T. Simbaha
Museum of Natural History, University of Wroclaw,
Sienkiewicza 21. 50-335 Wroclaw. Poland.
Vanayacu Biological Station and Center for Creative
Studies. Napo Province, Cosanga. Ecuador, c/o Foch 72 1 y
Amazonas. Quito. Ecuador.
Corresponding author; e-mail: stawar@biol.uni.wroc.pl
ABSTRACT. — We report the first nest of the Smoky
Bush Tyrant ( Myiotheretes fumigatus) which was found
on 1 1 October 2009 at the Yanayacu Biological Station.
Napo Province in Ecuador. The nest was a shallow open
cup. 2 m above ground on the side of a dead stump
covered in epiphytes. The nest was 12 cm wide by
6.5 cm in height; internally, the cup was 7 cm wide by
170
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124, No. 1, March 2012
4 cm deep and was lined predominantly with scales
from the tree-fern (Cyathea spp.), but included a few
small sticks and brightly colored feathers. Both eggs
were predominantly white with a few small, widely
dispersed, chocolate brown spots, predominantly around
the fattest area. They measured 24.0 X 18 and 23.0 X
17.5 nun. and weighed 3.6 and 3.5 g, respectively. The
first fully feathered fledgling left the nest on 2
November and the second on 3 November, for a
nestling period ol 16—17 days. We noted the presence of
a third bird (besides the pair) which remained within the
territory through the entire nesting period, at times in
close association with the breeding pair. Received 4
March 2011. Accepted 15 July 2011.
adult. Unexpectedly, a third adult appeared hut
seemed to elicit no reaction from the already-
present adults. We did not search for the nest that
evening as darkness was approaching. We re¬
turned the following morning and observed an
adult entering the nest in a dead stump.
Nest. — The nest was a shallow open cup. 2 m
above ground on the side of a dead stump covered
in epiphytic mosses, ferns, orchids, and bromeli-
ads (Fig. 1 A). The supporting trunk was 3 tn rail
in a re-growing pasture 30 m from the forest edge
The nest was sunk into naturally growing tiros*
and its exact outer dimensions were difficult to
Bush tyrants are a group of four New World
flycatchers (Tyrannidae) which, together with
>20 other genera, belong to subfamily Fluvico-
linae (Fitzpatrick 2004, Ohlson et al. 2008, Tello
et al. 2009). The Smoky Bush Tyrant ( Myiother -
etes fumigants) occurs on both slopes of the
Andes from western Venezuela and northern
Colombia to Peru. The nominate subspecies,
fumigants , occurs in nonhem Ecuador, while
ssp. cajamarcae occurs in southern Ecuador and
adjacent Peru, mostly from 2.000 to 3,200 m asl
(Ridgely and Greenfield 2001, Fitzpatrick 2004).
Ridgely and Greenfield (2001: 511) stated the
Smoky Bush Tyrant “generally remains inside
forest,"' but reponed this species to be most
frequent in the subcanopy of humid montane
forest edges and shrubby slopes or grassy regions
with scattered trees. We conducted our studies in
the vicinity of the Yanayacu Biological Station
and Center for Creative Studies. 5 km west of
Cosanga. Napo Province. Ecuador, at an altitude
of —2,100 m asl. The habitat in the area is
dominated by montane cloud forest, interspersed
with several small, semi-open clearings. One pair
of birds occupied a small natural clearing
dominated by Chttsquea bamboo surrounded by
high trees; another pair was observed in a larger
area of Clui.se/uea bamboo with scattered low
trees. A third pair, which was attending a nest,
was in a pasture with scattered bushes and small
trees.
OBSERVATIONS
We flushed an adult Smoky Bush Tyrant on t
afternoon of 1 1 October 2009 from a dead stun
Z:,rStUK ,heh,'ni1 th= ^ Station T
adult gave alarm calls as it changed perch,
several times, and was soon joined by asecon
measure; it was — 12 cm wide by 6.5 cm in height
The egg cup measured 7 cm wide X 4 cm deep
The outer portion of the cup was constructed
principally of moss intertwined with sparse
rootlets. The cup was lined predominantly with
scales from the tree-fern ( Cyathea spp ). bui
included a few small sticks and brightly colored
feathers (Fig. IB).
EgRS- — The nest on first inspection (12 Oct .
contained two well-incubated eggs. Both eggs
were predominantly white with a few (~lOl
small, chocolate brown dots, widely dispersed amt
predominantly around the thickest pan (Fig. K)
They measured 24 X 18 and 23 X 17.5 mm and
weighed 3.6 and 3.5 g. respectively. Both eggs
hatched on 1 7 October.
Incubation. — A HOBO temperature logger was
placed in the nest on 12 October. The logger
recorded temperature, once every minute, in the
nest lining below the eggs and simultaneously in ;•
protected location within the epiphytes 1 m below
the nest. We used the relative differences >n
temperature between these readings to record adult
presence or absence from the nest. The nest wa*
filmed most days from 15 October to 3 November
w ith u tripod-mounted digital video camera placed
1 5 nr from the nest. We used video records ol
adult presence to help interpret changes in nest
temperature and to identify daily incubation
rhythms. Mean daily attendance was 69 ± 5rr l'!
daylight hours during the final 6 days of incubation
(including day of hatching). Mean periods o! udu t
absence during the entire observation period were
18 ± 9 min (n = 58). while mean periods of
attendance were 41 ±31 min (n = 53).
Nestlings. — We examined the nestlings oil
October, the day of hatching. They had yellow
pink skin, were blind and mainly naked but with
quite dense, fawn-colored natal down ~10 mm
SHORT COMMUNICATIONS
171
FIG. 1. (A). Smoky Bush Tyrant nest in open shrub
habitat. October 2009. Yanayacu Biological Station. Napo,
Ecuador. (B). Nest with eggs of Smoky Bush Tyrant
'Photograph A and B by T. Stawarczyk). (C). Egg of
Smoky Bush Tyrant (Photograph by J. Simbana).
Ic,ng on the coronal, occipital, and dorsal tracts
1 pterylography follows Wethcrbee 1957). The
young weighed 5.0 and 3.6 g. respectively. We
weighed the nestlings on 23 October, when they
weighed 21.7 and 19.2 g. respectively and on 26
October when they weighed 27.7 and 24.4 g.
respectively. The first fully feathered fledgling
toft the nest on 2 November and the second on 3
November, for a nestling period ot 16-17 days.
Parental Care— Adult Smoky Bush Tyrants do
not show sexual dimorphism and were not
individually marked; we were unable to describe
the role of the male and female in parental care.
However, two adults took part in incubation, as in
three cases both birds were visible simultaneously
while changing places at the nest. Similarly, both
parents cared for the nestlings, occasionally
arriving simultaneously at the nest with food.
Adults did not fly straight into the nest when
approaching but stopped at a few preferred
perches for 10-30 sec. apparently surveying the
area surrounding the nest. We saw adult Smoky
Bush Tyrants aggressively pursuing a Tropical
Kingbird (Tyr annus inelancholicus) on three
occasions and twice chasing a Pale-edged Fly¬
catcher (My ia r chus cephalotes). when these
species approached to within 15-20 m of the
nest. The bush tyrants began calling on one
occasion when two Inca Jays (Cytmocorax yncas)
passed nearby. We observed no aggressive
behavior towards oiher bird species passing
through the Smoky Bush Tyrant territory.
The third bird, first seen on the day of the nest’s
discovery, was later observed on several othei
occasions. It was not seen closer than 15-20 m
during incubation. The third bird was observed
closer to the nest after nestlings hatched, but was
not recorded carrying food or feeding nestlings. It
visited the nesting site on one occasion when both
parents were within 1.0-1. 5 m ot the nest. It was
fully tolerated by both parents and was not chased
as with other intruders.
An adult brooded for 70.3% of the observation
period during the first 2 days after hatching
(7.3 hrs of filming), remaining in the nest for an
average of 34 min per brooding bout (n ~ 9, range
= 14_74 min). An adult brooded for 62.9% in the
next 3 days (16.7 hrs of filming) and stayed in the
nest for an average of 1 1 .8 min per brooding bout
(„ = 78, range = 2-39 min). The parents brooded
for only 5% of daylight observation periods
during the second week ol observation and
stopped brooding entirely in the third week.
Adults provisioned young at a rate of 0.6 times
per nestling/hr (9 trips in 7.3 hrs), when the
nestlings were 1-2 days of age but. during the
next 3 days (nestlings = 3-5 days of age), they
provisioned at a rate of 2.3 times per nestling/hr
(n = 78 trips in 16.7 hrs). The provisioning rate
increased to 4.0 times per nestling/hr (/i = 1 67 trips
in 21 hrs) during the second w'eek, whereas in the
third w'eek the provisioning rate was 4.3 times per
172
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124, No. 1, March 2012
nestling/hr (n = 136 trips in 14.2 hrs). The parents
delivered 415 food items during 59 hours of
filming, across the entire observation period.
DISCUSSION
The breeding biology of Myiotheretes bush
tyrants is poorly known. There is only one
species. Streak-throated Bush Tyrant (M. striati-
collis), for which the nest is described as “a
messy cup under bridge or overhanging structure"
(Fitzpatrick 2004: 389). The breeding period of
this species was in January-June in Colombia and
nestlings were reported in early March in
Venezuela (Fitzpatrick 2004).
Some details of breeding biology of the Rufous-
webbed Bush Tyrant ( Polioxohnis rufipennis ) are
known, a species now placed in a separate genus
but which is closely related to Myiotheretes
(Oh Ison et al. 2008. Tcllo et al. 2009). Vuilleumier
(1994) originally described the nest as belonging to
Myiotheretes rufipennis. The two described nests
of this species were at elevations -4,000 m asl in
northern Peru. Both were in open areas near the lop
of the giant bromeliad (Puya raimondii ) (Brome-
liaceae), 2.5-2. 8 m above the ground. These nests
were open cups made of twigs and grass stems, and
lined predominantly with pieces of Puya seed
down and a few feathers ( Vuilleumier 1994: 4-5).
The nest of the Smoky Bush Tyrant was in similar
open habitat, at a similar height above the ground,
and was similarly constructed. The nest, however,
was better concealed among epiphytes. Fjeldsa
(1990: 27) described the nest of the Rufous- webbed
Bush Tyrant as "a rather flimsy and open cup of
stalks and thin twigs placed just below the top of
5 m tall Polylepis tree overhanging a stream”. It
remains to be learned how much variability of nest
placement and structure occurs within this group of
species. Both nests of the Rufous-webbed Bush
Tyrant in Peru were found in late October, when
young were neatly ready to fledge (Vuilleumier
1994). Thus, the nest we observed agrees more
with an October-November breeding season for
the Rufous-webbed Bush Tyrant than for the
Streak-throated Bush Tyrant breeding from Janu¬
ary to June. Nesting during the drier months in our
™ me oreeamg cycles of most hi
Andean species in eastern Ecuador (Greeney ei
^UII) and With most tyrannids at our study
(e.g Greeney et al. 2005, Greeney 2007) 7
melees Other species nesting in similar habi
^smoke-colored Pewee (Omopus fumigm
(Dyrcz and Greeney 2010); Pale-edged Flycaici
(Dyrcz and Greeney 2011); and Cinnamon Fly¬
catcher ( Pyrrhomyias cinnamotneus) (H I
Greeney, unpubl. data).
The described eggs correspond well to nnw
fluvicoline flycatchers which have white eggs
with scattered, small reddish to blackish spots
(Sehonwetter 1971). Allocation of the natal down
of young seems to be typical as for some other
open cup nesting tyrannids (Wetherbce 1957.
Collins and Keane 1991).
The presence of a third adult which remained m
close association with the breeding pair, through¬
out the entire nesting period is of interest. Mostoi
our observations were through a camera, and -u-
could not tell the birds apart. Thus, it cannot be
excluded that eggs were incubated by the third bird,
which would suggest helpers at the nest. Fitzpatrick
(2004) reported that juveniles of tyrant flycatcher.'
stay for many months with their parents. He
mentions only one example, a Cliff Flycatcher
( Hirundinea ferruginea ), where three birds were
observed attending a single nest in Argentina More
recently, Dyrcz and Greeney (2011) observed
fledgling Pale-edged Flycatchers remaining with
their parents for >3 months at our study site. This
is one of the least-studied aspects of parental care
for tropical tyrannids, and it is unknown if long
post-fledging dependency periods are normal.
ACKNOWLEDGMENTS
We thank both reviewers and the editor tor stimulating
remarks which helped us improve this manuscript.
LITERATURE CITED
Collins. C. T. and K. Klane. 1991. Natal pierylosu a
phoebes. Wilson Bulletin 103:300-303.
Dyrcz. A. and H. F. Greeney. 2010. Breeding ecology
the Smoke-colored Pewee ( Cant opus hmupano 1
northeastern Ecuador. Omitologia Neotropic-1
21:489-195.
Dyrcz. A. and H. F. Greeney. 2011. Breeding biolop yi
Pale-edged Flycatcher ( Myiarchus ccphaloiesi in ""r v
eastern Ecuador. Ornitologia Colonibiana 11: In pit"
Fitzpatrick. J. W. 2004. Family Tyrannidae iTvrjm
flycatchers). Pages 1 70-462 in Handbook of the birds
of the world. Volume 9. Colingas to pipits u
wagtails (J. del Hoyo, A. Elliott, and D. A Christie
Editors). Lynx Edieions, Barcelona. Spain.
FjeldsA . J. 1990. Geographic variation in the Kn
webbed Tyrant Polioxohnis rttfipennvi. with deso1 ■■
tion of a new subspecies. Bulletin of the Bntish
Ornithological Club 110:26-31.
greeney, H. F. 2007. Observations on nesting biolog'
and natural history of Slaty-backed Chat-Tyraf'
( Ochthoeca cinnamomeiventris) with a description ot I
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nestling growth and plumage development. Boletin de
la Sociedad Antioqucha de Omitologia 17: 10-16.
Greekey. H. F.. R. C. Dobbs, F. R. Martin. K. Hai.upka,
and R. a. Geus. 2005. Nesting and foraging ecology of
the Rufous-crowned Tody-Flycatcher < Poecilotrieeus
mficeps) in eastern Ecuador. Omitologia Neotropical
16:427-432.
Gkeeney, H. F.. P. R. Martin. R a. Gf.i.is. A. Solano-
Ugai df. F. Bonier, B Freeman, and E. T. Miller.
2011. Notes on die breeding of high Andean birds in
northern Ecuador. Bulletin of the British Omilholog
ical Club 131: In Press.
Ohlson, J.. J. FjeldsA. and P. G. P. Ericson. 2008. Tyrant
flycatchers coming out in the open: phylogeny and
ecological radiation of Tyrannidae (Aves. Passeri¬
formes). Zoologica Scripta 37:3 1 5-335.
Ridgely, R. S. and P. J. Greenfield. 2001. Tlie birds of
Ecuador. Cornell University Press. Ithaca, New York, USA.
SchOnwitvlk, M. 1971. Ilatulbuch dcrOologic. Volume 2.
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Tello, J. G., R. G. Moyle. D. J, Marchcse, and J.
Cracraft. 2009, Phylogeny and phylogenetic classifi¬
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their allies (Aves: Tyratinides) Cladistics 25:1-39.
Vi'lLLEUMlER, F. 1 994 Nesting, behavior, distribution and
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( My iol hemes , A vim is, Neoxolmts, Agriornis and
Muscisaxlcota). Omitologia Neotropical 5:1-55.
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The Wilson Journal of Ornithology 1 24( 1 ): 1 73-176. 20 1 2
Nest, Eggs, and Nest Placement of the Brazilian Endemic Black-bellied
Seedeater (Sporophila melanogaster )
Cristiano Eidt Rovedder' and Carla Suertegaray Fontana12
ABSTRACT. — We present the first detailed description
of the nest and eggs of the Black-bellied Seedeater
( Sporophila melanogaster) based on observation of 64 nests
in three areas of grassland in southeastern Santa Catarina and
northeastern Rio Grande do Sul states, Brazil. The nests
were found from November tlirough Match. The nest has
tin. shape of a shallow basket, constructed with portions of
dned grasses and strung with spider webs. Half of the nests
were constructed in Ludwigiit sencea (Onagraceae), and the
other half were in 15 other plant species. Of these, the most
nnpnrtant were Eupatonum polystuchyiwi (10%) and
Wi yrocline vauthiericaut (6%) (Asteraceae). Only the
female constructs the nest. The eggs are ovoid and colored
whitish with brownish-purple spots near the wider portion.
Clutch size was two eggs, rarely three. Received 23
''member 2010. Accepted II October 20! I .
The Black-bellied Seedeater ( Sporophila mela-
nugaster) is endemic to Brazil (Sick 1997). where it
is listed as endangered (MMA 2003). Globally, it is
considered a near-threatened species (IUCN 2010).
The entire population in the breeding season is
Uhorutorio de Omitologia. Museu de Ciencias e Tecnolo-
g'a. Prngrama de Pds-Graduaqao cm Zoologia. Faculdadc
800 m asl with small
patches of Araucaria forest and wetlands or
natural drainages (Klein 1981, Rambo 2000.
Porto 2002).
Nest searches were conducted from October
through March during three breeding seasons
(2007/2008. 2008/2009, and 2009/2010) in three
areas: (1) wet grasslands of the Ague Branca
Stream (28 35' S, 50° 24' W: Bom Jesus, Rio
Grande do Sul), (2) wet grasslands of the Santana
River (28 29' S, 50 43' W; Bom Jesus, Rio
Grande do Sul), and (3) grasslands of Coxi/ha
Rica (28' 18' S, 50 ; 16' W; Lages, Santa
Catarina),
We collected data on the supporting plant for
64 nests. Fifty nests were in the area of Agua
Branca Stream, eight nests w'ere in the grasslands
of Coxilha Rica , and six nests were in the wet
grasslands of the Santana River. We collected
data on nest plant composition of 54 nests and
measured 49. as nests were predated or destroyed
during the nesting period, or immediately after
fledging. Classifications of nests followed Simon
and Pacheco (2005). Nests were collected after
they were measured, and deposited in the
Collection of Birds at the Museu de Ciencias e
Tecnalogia da Pontifuia Universidade Catdlica
do Rio Grande do Sul (PUCRS).
Plants that supported nests were measured in
the field, and some were collected for identifica¬
tion. Measurements taken were based on Ralph et
al. (1996): height of the plant, minimum and
maximum diameter of the crown, and stem
thickness (at the height where the nest was
attached). Nests, supporting plants, and eggs were
measured with metal calipers (accurate to
0.02 mm) and a millimeter ruler. We used
descriptive statistics (mean ± SD) to compare
measurements. The color of the eggs followed
Smithe (1975). Mass of eggs was not measured.
Direct observations of six nests found in the
construction stage were conducted to record adult
behaviors during nest construction.
rvc.su 1. 1 s
Nests were small cups, classified as low c
fork (fork basket placed low). They w
constructed of thin plant fibers, mostly Eragro.
airoides, and small portions of PasP alum notati
Bnza umolae. and Eustachys uliginose, (
Poaceae) (F,g. 1). These fibers were conned
FIG. I. Nest of the Black-bellied Seedeater in Eupa-
toriam betoniciiforme (Ilsi Boldrini, pers. comm.), Vacaria.
Rio Grande do Sul, Brazil. (Photograph by Cristiano
E. Rovedder).
by large amounts of spider webs, which also
ad fixed the nest to the supporting plant.
Sixteen different plant species were used to
support nests. Most often used species were
Ludwigia sericea (Onagraceae) with 50% of the
total nests (n = 32), followed by Eupatorium
polysiachyum (Asteraceae) with 10.9% (// = 7).
and Achyrocline vauthieriana (Asteraceae) with
6.2% (n - 4). Other less used plant species were:
Andropogon lateralis (n = 3). Erechtites hier-
aciifolius ( n = 3), Bacckaris coridifolia (n - ->•
Eupatorium betoniciiforme (n = 2). Pteridium
aquilinum ( n = 2), and Vemonia spp. (« = -)•
Baccltaris caprariifolia, Erechtites valerumfolm.
Eupatorium bupleurifolium, E. candolleanum.
and Paspalum exaltation were each recorded once
supporting nests. Two species of supporting planb
were not identified. Plant measurements taken
were: height =■ 81 ± 25.3 cm (range = 38-170:
n = 49). stem thickness = 5.9 ± 3.31 mm (range
= 1-20.9: n = 49), largest crown diameter = 41.4
± 23.7 cm (range = 9-11.2; n = 48). and
smallest crown diameter = 31.1 ± 10.1 cm (range
= 7-69; n = 48). Nests were built next to the
main trunk in 81% of the records ( n = 49). Tire
distance from the nest to the edge of the plant was
12.4 ± 9.16 cm (range = 2-42: n = 22).
Nest construction started at the beginning
of November, and only females were recorded
constructing the nests (n = 6 nests; 14.4 hrs of
observation). Females laid two (88.6%: n = 39)
to three eggs per clutch (11.4%; n = 5). The
eggs were ovoid with background color ranging
from white to beige. Irregular brownish-purple or
SHORT COMMUNICATIONS
175
FIG. 2. Egg of Sporophila melanogaster. (Photograph
by Cristiano E. Rovedder).
yellowish blotches and stripes (Sepia 219 and
Burnt umber 22 [sensu Smithe 19751), as well as
smaller spots were generally more concentrated at
the larger end (Fig. 2). Egg measurements (n = 8)
were: length = 17.5 ± 0.43 (range = 16.9-18.3)
and width = 12.2 ± 0.35 min (range = 11.7-
12.8). Nests had little variability in shape and
measurements, especially in the internal chamber.
However, height above the ground was variable
which could be the result of the need to elevate
the nest above the water level in the wetlands
(Table 1).
DISCUSSION
Nests of S. melanogaster resemble those of its
congener S. hypoxantha in shape, structure, and
measurements (Di Giacomo 2005, Franz and
Fontana 2010); the two species are sympatric in
Part ol their breeding ranges and both use similar
nest-support plants, including Eupatorium poly-
stachyum and Baccharis capra riifolia (Franz and
Fontana 2010). However, our data indicated that
N melanogaster preferred Ludwigia sericea for
nest sites. Nest construction is by the female, as for
other species of Sporophila (e.g.. S. leucoptera .
S. hypoxantha, S. lineola). The number of eggs laid
per clutch is also similar (Di Giacomo 2005,
Francisco 2009, Franz and Fontana 2010, Oliveira
et al. 2010).
The literature indicates Sporophila mekmogas-
ter breeds only in wetlands (Machado et al. 1998,
Bencke ct al. 2003, Machado et al. 2008). despite
a lack of specific studies on the nesting behavior
of the species with one exception (Rovedder
201 I ). However, this species can nest in dry and
natural portions of steep fields (using Eupatorium
polystachyutn bushes) near drainages or wetlands
where use by cattle or people is infrequent. This
could be an adaptation to loss of wetlands and
conversion to crops; human stresses, such as live¬
stock grazing or agriculture could create inappro¬
priate habitats for Black-bellied Seedeaters.
Nesting-plant species preferences by 5. mela¬
nogaster are suggested based on the proportion of
the first and the second most frequently used
plant, and also by quantitative studies (Rovedder
and Fontana in prep.). This knowledge, as well as
detailed description of the nest and eggs of the
Black-bellied Seedeater, is important for devel¬
opment of new studies on the species’ life history
to benefit conservation of this threatened endemic
Brazilian species.
ACKNOWLEDGMENTS
We are grateful to 1 I. Boldrini and staff (UFRGS) for
assistance in identifying plant species; Ismael Franz. Jonas
Rosoni, Marcio Repenning, and Mariana L. Gongalves for
field assistance; two anonymous reviewers and C. E. Braun
for manuscript improvement: the Fundacao Grupo Boti-
cario de Protegao a Namreza and Neotropical Grassland
Conservancy for financial support to the project; CNPi] for
a scholarship to C. E. Rovedder; and the Museu de C iencias
e Tecnologia da PUCRS for logistical help.
LITERATURE CITED
Bencke. G. A., C. S. Fontana. R. A. Dias, G. N.
Mauricio. and J. K. F. Mahler Jr. 2003. Aves.
TABLE 1. Measurements (cm) of 48 nests of the Black-bellied Seedeater ( Sporophila melanogaster) in Brazil.
Variables
Mean
SD
Min
Max
Largest external diameter
6.55
0.57
5.5
8
Smallest external diameter
6.13
0.45
5.3
7.3
Largest internal diameter of chamber
4.55
0.37
3.9
5.5
Smallest internal diameter of chamber
4.24
0.33
3.5
5
Eternal height
5.14
0.57
3.5
6.8
Internal height (depth)
3.34
0.42
2.3
4.1
Height above ground (« = 54)
31.5
10.83
15
60
176
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 1. March 2012
Pages 189-479 in Livro vermelho da fauna amea9ada
de extin^o no Rio Grande do Sul (C. S. Fontana.
G. A. Beneke. and R. E. dos Reis, Editors). Porto
Alegre. Rio Grande do Sul. Brazil.
Boldrini, 1. I.. L. Eggers. L. a. Mentz, S. T. S. Miotto,
N. I. Ma lzenbacher, H. M. Longhi-Wagnkk. R.
Trevisan, A. A Schneider, and R. B. SeiObal.
2009. flora. Pages 40-94 in Biodiversidade dos
Campos do Pianalto das Araucarias (1. I. Boldrini.
Editor). Brasilia, Brazil.
Di Giacomo. A. G. 2005. Aves de la Reserva el Bagual. Pages
201-465 in Historia natural y paisa je de la Reserva El
Bagual, Provincia de Formosa, Argentina. Asociueion
Oniilologica del Plata (A. G. Di Giacomo and S. F.
Krapovickas, Editors). Buenos Aires. Argentina.
F acchinetti. C., A. Cl. Dt Giacomo, and J. C. Reboreda.
2008. Parental care in Tawny-hellied (Sporophila
hypoxantha ) and Rusty-collared (.S', collarix) seedcai
ers, Wilson Journal of Ornithology 120:879-883.
Font ana, C. S„ C. E. Roveddbr, M. Repenning, and
M L. GonCalves, 2008. Estado atual do conheci-
mento e conserv^nu da uvifauna dos Campos de Cinia
da Serra do sul do Brasil, Rio Grande do Sul e Santa
Catarina. Revista Brasileira de Ornilologia 16:281-307.
Franc isco. M. R. 2006. Breeding biology of the Double-
collared Secdealer (Spompliila caerulescens). Wilson
Journal of Ornithology I 18:85-90.
Francisco. M. R. 2009. First description of nests and eggs
of the White-bellied Seedeater (Sporophila leucop-
tera). Wilson Journal of Ornithology 121:628-630.
Franz, 1. and C S. Fontana. 2010. First data on the
breeding biology of the Tawny-bellied Seedeater
(Sporophila hypoxantha ) in south Brazilian high
altitude grasslands. Proceedings of the International
Ornithological Congress 25:753.
1UCN. 2010. ILCN Red List of threatened species. Version
2010. 3. Gland, Switzerland, w ww.iucnrcdlisl.org/apps/
redlist
Jacobs. F. P., J. Vizenttn-Bugoni. M. A. A. Coimbra,
and R. A. Dias. 2010. Breeding biology of the Marsh
Seedeater (Sporophila palustris ) in southern Brazil
Proceedings of the International Ornithological Con¬
gress 25:760
Klein, R. M. 1981. Fisonomia. importancia e recursos da
vcgeta9ao do Parque Estadual da Serra do Tabuleiro
Sellowia 33:5-54.
Machado, A. B. M.. G. M. Drlmmond, and A. P. Paglia.
2008. Livro vermelho da fauna brasileira amea9ada de
extinjao. MMA, Funda9»o Biodiversitas, Bclo Hor¬
izonte, Brasilia, DF.
Machado. A. B. M.. G. A. B. Fonseca, R. B. Machado.
L. M. S. Aguiar, and L. V. Lins. 1998, Livro
vermelho das espticies amea9adas de extinyikida taur^
de Minas Gerais. Funda9ao Biodiversitas, Bel
Horizonte, Brasilia, DF.
Ministe.kio IX) Meio Ambiente (MMA), 2003. Lisu di-
espdeies da fauna brasileira ameuyadas de extinyar
Normative Instruction Number 3. 27 May 2003
Didrio Oftcial da Repuhlica Federativa do Rgm
Brasilia. DF.
Oliveira, L. s. de, l. m. s. Sousa. P. v. Davaho. ani
M. R. Francisco. 2010. Breeding behavior of tic
Lined Seedeater (Sporophila lineola ) in southeastern
Brazil. Ornilologia Neotropical 21:251-261.
Porto. M. L. 2002. Os compos sulinos-sustentabiDdatic e
manejo. Revista Ciencia e Ambiente 24:1 19-1)8
Ralph, C. J.. G. R. Gbupel. P. Pyle. T. E. Martin. D. F
Desantp. and B. MilA. 1996. Manual de meado- de
campo p«a d monitoreo de aves terrestres. USDA, Rust
Service. General Technical Report PSW-GTR- 159. P.-.fw
Southwest Reseatth Station, Albany, California. ISA.
Ramho, P. 2000. Fisionomia do Rio Grande do Sul— cnsiio
de uina monografiu natural. Third Edition. I’NISI-
NOS, Silo Leopoldo, Brasil.
RlDOELY, R. S. and G. Tudor. 1989. The birds of South
America. Volume I . The oscine passerines. University
of Texas Press, Austin. USA.
RosArio, L. A. DO. 1996. As aves cm Santa Catarina
Distribuivao geografica e meio ambiente. FATMA—
FltndufSo de Antparo a Tecnologia e ao Meio
Ambiente, Floriuntipolis. Brasil.
ROVhDDER, C. E. 2011. Histdria natural de SporophihJ
melanogaster (Pelzeln 1 870) (Aves: Emberizidae1 coot
enfase em sua biologja reprodutiva. Dissertate de
mestrado. Pontiffcia Univcrsidade Catdlica do Hio
Grande do Sul, Porto Alegre, Brasil.
Rovedder. C. E. and C. S. Fontana. In prep. Selection o;
nesting sites by Black-bellied Seedeater (Sparophtio
melanogaster ) in southern Brazil (preliminary title1
(Abstract submitted to IX Neotropical Ornithology-
Congress |NOC| and VIII Peruvian Ornithological
Congress |COPJ. Cuzco, Peru).
Sick. H. 1997. Ornilologia Brasileira. Nova Fronteira. Rto
de Janeiro. Brasil.
StMON, J. E. and S. Pacheco. 2005. On the Standardization
of nest descriptions of neotropical birds. Revista
Brasileira de Ornilologia 12:143-154.
Smithe. F. B. 1975. Naturalist’s color guide. American
Museum of Natural History . New York. ISA.
SHORT COMMUNICATIONS
177
The Wilson Journal of Ornithology 1 24(1): 1 77- 179, 2012
Breeding of the Brown Creeper (Certhia americana) in Central America
Carlos Funes,1 Oscar Bolanos,1 and Oliver Komar1-23
ABSTRACT— We report the first nesting record of
the Central American population of Brown Creeper
( Certhia americana) in the La Montanona pine-oak
(Pinus-Quercus) forest of Chalatcnango Department,
nnnhem El Sahador. The nest was in a cavity in the
trunk of a pine \ Pouts oocarpa) tree. Most insectivorous
birds in this region breed during the rainy season when
insects are generally most abundant; however, nesting
of the Brown Creeper occurred at the height of the dry
season, during January and February'. Received IV. April
-Oil. Accepted 15 August 2011.
The avian breeding season in the tropics is less
well defined than in temperate zones, where
bleeding is constricted by climate. Avian breeding
in tropical areas can extend over a longer period;
some species, especially columbids, may breed
year-round. Nectarivores such as hummingbirds
(Trochilidae) and tlowerpiercers (Dig I ossa spp.)
typically breed during the dry season, when many
plants are in flower. Most insectivorous birds lime
their breeding to match hatching with the onset of
the rainy season, when insect abundance greatly
increases (Sketch 1950). El Salvador, in northern
Central America, has extremely marked wet and
dry seasons. Most hatching of insectivorous birds
occurs in May and June, similar to the breeding
season in North American temperate zones
'Dickey and van Rossem 1938).
The Brown Creeper ( Certhia americana) is an
insectivorous bark gleaner, distributed from North
America to Mexico, and through mountainous
areas of Guatemala and Honduras to northwest
Nicaragua (Hejl et al. 2002). The species has been
lound since 1999 in all major pine-oak (Pinus-
Quercus) forests of El Salvador along the northern
border near Honduras between 1 . 1 75 and 1 .850 m
elevation (Komar 2002; OK, unpubl. data).The
population resident in the mountains of eastern
fn 'grama de Ciencias para la Conservation, SalvaNA-
Tf RA.Colonia Flor Blanca, 33 Avenida Sur #640. San Sal -
vador, El Salvador.
Present address: Instituto Regional de Biodiversidad.
Zamnrano University. Km 33. Carretera a Danlf. Francisco
Moraztm, Honduras.
Corresponding author; e-mail; okomar@zamorano.edu
Guatemala, Honduras, northwestern Nicaragua,
and presumably El Salvador, is known as Certhia
americana extima. one of 13 recognized subspe¬
cies (Hejl el al. 2002). Hejl et al. (2002) report
nesting in U.S. and Canada from April through
July, and Land (1962) collected a male in Sierra
de las Minas in eastern Guatemala with partially
enlarged testes on 5 March.
We encountered an active nest ot Brown
Creeper during field work on the ecology of
wintering birds in pine-oak forests. We observed
the nest briefly during 2 days, documenting it with
measurements and photographs, and observing
behavior of the adults and nestlings.
OBSERVATIONS
Nest observations occurred during 1130-1230
and 1520-1625 hrs on 5 February 2010 at the La
Montanona Forest, a protected natural area. We
returned to photograph the nest and nestlings on 6
February 2010. This site is in the central part of
Chalatenango Department. El Salvador, near the
Honduras border. The specific site ol the nest
observation was 14 08' 39" N, 88 54' 25" W at
1,470 m elevation in the La Laguna municipality.
The natural area contains -2,500 ha of pine-oak
forest, ranging from 900 to 1,600 m elevation.
An active Brown Creeper nest was located in a
natural cavity ~5 m above ground in the trunk of
a 25-m pine (Pinas oocarpa ), in somewhat open
pine-oak forest. The cavity had a single entrance
(Fig. 1 A). The nest cavity was 28 cm high, from
the nest cup at its base to the cavity roof, and
13 cm deep. Cavity width ranged from 2 to 5 cm.
The nest cup, constructed mostly of dry pine
needles, beard lichen (probably Usnea sp.), and
mosses, measured ~5 cm in diameter (Fig. IB).
Wc observed two adults taking turns feeding three
nestlings and removing fecal sacs from the nest. The
adults, often together, visited the nest every 2 to
30 min (n = 8. mean ± SD = 10.1 ± 9.5 min). A
passing Ivory-billed Woodcreeper (Xiphoriiynchus
flcivigaster) extracted one of the nestlings while we
watched, and flew away with the nestling hanging
from its bill, dropping the nestling before disappear¬
ing. some 50 m distant near a ravine.
178
THE WILSON JOURNAL OF ORNITHOLOGY • Vo/. 124. No. 1. March 2012
FIG l. Single-entrance cavity with Brown Creepei
■n El Salvador (A) Adult Brown Creeper amving at c
necdlcTZmTr ? ' A" 0pen nest CUP constructed of dry
cav1v .rfrh "Che,I: and mos“* ^ « the bottom o
cavity . (C) The nestlings climbed up the cavity will ,
researchers measured 1,0 **. PhotoA* by Ab*
DISCUSSION
The timing of breeding in the middle of the dry
season, when insectivores generally arc noi
nesting and populations of visiting migratory
birds are high, is of interest. We found nestlings.
— 1 week of age. on 5 February. Given an average
incubation period of 15 days for Brown Creepers
( He jl et al. 2002). and laying of one egg per day.
we estimate that egg-laying in El Salvador began
~I2 January. Most other insectivorous bad.
gleaners in Central America are reported to breed
later in the year (Table I). The only other
insectivorous bird species in Central Amenca
reported to breed in January or February iSkutch
1969) is the Lineated Woodpecker (Dnwopus
lineatus) which occupies a similar feeding niche
(tree bark) as the creeper, hut is more than
times heavier. Some Golden-fronted Woodpeck¬
ers (Mekmerpes aurifrons) may also begin egg-
laying in early February (Skutch 1969).
We do not have evidence that creepers or an)
other birds breed regularly or frequently during
the dry season in the pine-oak forest ecosystem :n
El Salvador. We searched the La Montanona pine-
oak forest for birds during 5 days each winter
from 2007 to 2010, and invested equal efforts at
three similar sites in El Salvador where Brown
Creepers also were found. We spent 16 weeks
observing the drv-season bird communities in
pine-oak forest of El Salvador. The only indica¬
tion of nesting behavior of any bird species other
than the nest reported here was the observation ot
a pair of Lineated Woodpeckers widening a
potential nest hole in December 2008. Bird
monitoring data from a mist-netting station m
pine-oak forest at Montecristo National Park
provided no indication of insectivorous birds in
breeding condition during January or February,
despite 5.600 net hrs during those month'
(SalvaNATURA. 2003-2009. unpubl. data).
One Brown Creeper at Montecristo National
Park, captured on 10 April 2008 and classified as
second year, was molting contour feathers and
still retained heavily worn juvenile flight feathers-
this is consistent with hatching during February
2007. The bird had a completely ossified skud
(confirming it was likely born the previous year',
and no fat, consistent with a resident, non-
migratory individual. The bird w as not in breeding
condition. We have heard Brown Creepers singing
from February to July at Montecristo National
Park. Singing is suggestive of breeding behavior.
SHORT COMMUNICATIONS
179
T4BLE 1. Reported nesting season for selected Central American bark-gleaning insectivorous bird species.
Species
Earliest repotted egg dales
References
Ivory-billed Woodcreeper < Xiphorhynchus flavigaster)
Spot -crowned Woodcreeper ( Lepidocolaptes ufftnis)
Streak-headed Woodcreeper l L souleyetii)
Golden-tfonted Woodpecker ( Melanerpes aurifnm )
Lineatcd Woodpecker ( Dryocopus lineatus)
Hairy Woodpecker i Pieoide s villosus)
Apr
Apr
Late Mar
Early Feb
Jan (possibly late Dec)
Apr
Dickey and van Rossem 1938.
Vega Rivera et al. 2003
Skutch 1969
Skutch 1969
Skutch 1969
Skutch 1969
Skutch 1969
although migratory birds in more northern win¬
tering areas occasionally sing during the non¬
breeding season (OK. pets. obs.).
Winter nesting in Central America raises
questions about the ecology of Brown Creepers.
The species is assumed to be a permanent resident
in Central America, but the observation of nesting
in winter raises the possibility that northern
populations migrating to Mexico or as far south
as Central America (which has not been docu¬
mented) could conceivably encounter resources
sufficient for double nesting, which has been
reported recently for other migratory species
(Rohwer et al. 2009). Early nesting in Central
America also may indicate the local subspecies is
on a separate evolutionary track from more
nonhern subspecies and may eventually evolve
phonological barriers to gene flow.
ACKNOWLEDGMENTS
National Park as pari of the Permanent Bird Monitoring
Program conducted by SulvaNATURA. We are grateful to
C. E. Braun. Knut Eisermann. and Steven Latta. for
comments that improved the manuscript.
LITERATURE CITED
Dickey. D. R. and A. J. van Rossem. I93S. The birds of El
Salvador. Field Museum of Natural History. Chicago.
Illinois, L'SA.
Hcjl. S. J.. K. R- Newxon, M. E. Mcfadzen, J. S. Young,
and c. K. Ghalambor. 2002. Brown Creeper (Cenliia
amencana ). The birds of North America. Number 669.
Komar, O. 2002. The birds of Montecristo National Park.
Ornitologia Neotropical 13:167-193.
Land, H. C. 1962. A collection of birds from the Sierra de
las Minas, Guatemala. Wilson Bulletin 74:267-283.
Rohwer. S.. K. A. Hobson, and V. G. Rohwer. 2009.
Migratory double breeding in neotropical migrant
birds. Proceedings of the National Academy of
Sciences of the USA. 106:19050-19055.
Sketch. A. F. 1950. The nesting season of Central
American birds in relation to climate and lood supply.
This study was conducted while undertaking monitoring
«ork funded by Texas Parks and Wildlife Department with
funds from the U.S. Fish and Wildlife Service. The Ministry
°f Environment and Natural Resources of El Salvador
provided the research permit. Local lodging and land access
was granted by the Comitd Representativo de Bencl'iciarios
de La Montanona (CORBEL AM). Roselvv Judrez collected
data from a captured Brown Creeper al Montecristo
Ibis 92:185-222.
SKETCH, A. F. 1969. Life histories of Central American
birds. 111. Pacific Coast Avifauna 35:374-547.
Vega Rivera, J. H.. D. Ayala, and C A. Haas. 2003.
Home-range size, habitat use, and reproduction of the
Ivory-billed Woodcreeper ( Xiphorhynchus flavigaster)
in dry forest of western Mexico. Journal of Field
Ornithology 74:141-151.
The Wilson Journal of Ornithology 124( 1): 179-183. 2012
Effects of Parasitism by Brown-headed Cowbirds May Persist
into Post-fledging
Sean M. Peterson.1-2-3 Henry M. Streby,1-2 and David E. Andersen1-2
Department of Fisheries. Wildlife, and Conservation Bio¬
logy. University of Minnesota, 200 Hodson Hall. St. Paul. MN
55108, USA.
2 U.S. Geological Survey, Minnesota Cooperative Fish
and Wildlife Research Unit, 200 Hodson Hall. St. Paul. MN
55108. USA.
ABSTRACT. — Brood parasitism by Brown-headed
Cowbirds ( Molothms ater) typically decreases the number
of host juveniles that fledge: however, little information
J Corresponding author:
e-mail: sean.michael.peterson@gmail.com
180
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 1. March 2012
exists regarding the effect of cowbird parasitism during the
post-fledging period. We monitored 115 Ovenbird
( Seiurux itumcupillit ) nests in 2006-2008 in northcentral
Minnesota, six of which were parasitized. We used
radiotelcmctry to monitor movements of 36 Ovenbird
fledglings (9 additional fledglings depredated <24 hrs
after fledging were excluded from the movement analysis)
from non-parasitized nests and one fledgling from a
parasitized nest. Clutch sizes and produetiv ity were lower
in parasitized Ovenbird nests than non-parasitized nests,
similar to populations at other locations. The fledgling we
tracked from a parasitized nest ( in 2008) died after 2b days.
It was the only fledgling in our study that died (n = 20)
with no sign of predation and an empty stomach. That
fledgling look 12 days to travel 50 m from its nest and
25 days to travel >100 m from its nest. Fledglings from
non-parasitized bruods tracked tor >25 days during 2008
(n = 16) took 4.1 ±0.71 anil 9.5 1 1 .14 days to travel the
same distances. Our observations suggest that negative
effects of brood parasitism may persist into the post-
fledging period, possibly confirming observations of
cowbird-only survival compiled from the literature.
Received 6 March 2011. Accepted 22 July 201 1.
Brood parasitism by Brown-headed Cowbirds
(Molotlirus ater, hereafter cowbirds) has numerous
negative effects on productivity of nesting migrant
passerines (Rothstein 1990. Robinson et al. 1995,
Ortega 1998, Lorenzana and Sealy 1999). Egg
replacement by female cowbirds significantly
decreases number of Ovenbirds ( Sei tines auroca-
pilla) fledged in parasitized nests (llann 1937.
Donovan et al. 1995. Hersek et al. 2002). Cowbird
parasitism significantly increased nest abandonment
by California Gnatcatehers ( PolioptiUi califomicci)
(Braden et al. 1997) and delayed nesting of Yellow
Warblers {Seiophaga petechia) that bury parasitized
clutches (Guigueno and Sealy 2010). Nest predation
of parasitized songbirds is also influenced by the
presence of cowbird nestlings. Predation of Amer¬
ican Redstart (S. ruticilla) nests was 16-19% higher
in parasitized nests than in nests not parasitized by
cowbirds (Hannon et al. 2009). Begging behavior in
nestling songbirds is a significant factor contributing
to nest predation (Haskell 1994) and cowbirds beg
significantly more than nestlings of host species
(Payne 1991). Experimental nests at which cowbird
begging calls were broadcast were significantly
more likely to be depredated than nests at which
Indigo Bunting (Passerine) cyanea) calls were
broadcast (Dearborn 1999).
Substantial attention has been given lo effects of
cowbirds on nesting success, but less is known about
how cowbird nest parasitism impacts host broods
during the post -fledging period. Smith (1981)
monitored marked Song Sparrows ( Melospiza melo-
dia) and found that fledglings experienced no
significant reduction in survival due to brood
parasitism. However, juvenile indigo Buntings from
parasitized nests were 82% less likely to return to
natal areas ii their second year than juveniles from
non-parasitized nests (Payne and Payne 1997).
Rasmussen and Sealy (2006) reported that adult
hosts of parasitized broods, in 97 of 102 observations
involving 42 species of hosts, were observed feeding
cowbird fledglings, but not their own young. Airola
(1986) found that parasitized family groups in the
Sierra Nevada contained 76% fewer host fledglings
than non-parasitized groups. These authors suggested
the discrepancy in parental care may cause increased
mortality ofhost fledglings in the early post-fledging
period. The post-fledging period is a time of high
mortality for many songbirds without additional
stresses Iron cowbird parasitism (Ricklcfs 1968.
King el al. 2006. Berkeley et al. 2(K)7).
Cowbird fledgling activity occurs in four main
phases: inactive, active, superactive. and indepen¬
dent (Woodward 1983). The inactive and active
phases cover the first 1 1 days after leaving the
nest when ihe cowbird develops the ability to fly.
but generally does not actively beg or follow the
host parent*. The superactive phase occurs 13 to
23 days after fledglings leave the nest and is
characterized by fledglings following host adults
and near-ecnslant begging. The superactive period
is followed by independence. 25 to 30 days after
leaving the nest. Thus, cowbird-induced parental
neglect of offspring may affect host fledgling
survival up to 30 days into the post-fledging
period.
We slutied a population of Ovenbirds in
northcentral Minnesota to assess the effects ol
forest maragement practices on reproductive
success. Ovenbirds generally do not remove
cowbird eg«s or abandon nests at high frequencies
in response to parasitism, but are capable of
successfully raising cowbirds and their own young
through the nesting period (Hann 1937. Hersek
et al. 2002i. However, little is known about the
effects of hood parasitism on Ovenbird fledgling
survival. 50 m J
12.0(1)
4.1 ± 0.71 (16)
Days to >100 m b
25.0(1)
9.5 ± 1.14 (16)
Adult carec
3/9 (0.33)
105/155 (0.68)
1 Dm 10 irarel >50 m from nest.
1 Days to travel >100 m from nest,
Proportion of days adults were present during observations of fledglings during the cowbird supcractivc phase (Days 13-23).
mixed northern hardwood-coniferous forests in the
Chippewa National Forest. Itasca County. Minne¬
sota. USA (47 26' N. 93 40' W). We visited nests
every 4 days to monitor condition and contents, and
visited nests more frequently as the estimated
fledge dale approached. We observed nests remote-
0 wnh binoculars when possible and took different
paths to and from nests to avoid developing trails
leading to nesis. We recorded clutch or brood size
and presence of cowbird eggs and nestlings during
each observation. We weighed and banded Oven-
ford nestlings with standard aluminum U.S. Geo¬
logical Survey leg bands 1 or 2 days before we
expected nestlings to fledge. We attached radio
transmitters to one (rarely 2-3) Ovenbird nestling in
each nest, using a figure-eight harness (Rappole and
Tipton 1991), Radio transmitters lasted —60 days,
had a 0.5- 1.0- km signal range during ground-based
telemetry', and were 4. 3-4.9% of nestling mass at
hmeot attachment, decreasing to 3 .0-3. 5% as birds
'cached maturity. We monitored fledglings daily
and recorded location, activity, adult presence, and
fledgling status (alive or dead). We recorded
locations of nests and fledglings using handheld
Global Positioning System units ( 100 points aver-
aged per location) and derived distances from
fledglings to the nest from which they Hedged using
Geographic Information System software. We
^corded parental activity as present or absent and
noted if parents were feeding fledglings during each
JS-20-min observation of the fledgling. Proportions
01 observations when parents were present were
h^sed on 95% confidence intervals. We visually
inspected remains of dead fledglings for signs of
predation and identified stomach contents when
stomachs were recoverable. We compared clutch
sRc. hrood size, and number of Hedged young
between parasitized and non-parasitized nests using
Mann-Whitney U- tests. We report the number of
days required for fledglings to travel >50 and
>100 m from nests as means ± SE.
RESULTS
We monitored 1 15 Ovenbird nests during 2006-
2008. six (5%) of which were parasitized by
cowbirds (each with I cowbird egg). One parasitized
nest was abandoned during the laying stage, one was
depredated during the nestling stage, one fledged
one Ovenbird with the cowbird egg unhutched, and
three Hedged at least one Ovenbird and one cowbird.
Parasitized nests contained smaller Ovenbird clutch¬
es (4/ = -3.8 \,P <0-001) and broods (£/= -2.92,
P < 0.003), and Hedged fewer Ovenbird young ( U
= -2.65, P < 0.008) than non-parasitized nests
(Table 1).
Two of the three Ovenbird fledglings tracked
from parasitized broods lost their transmitters
within 2 days of leaving the nest and their fates
were unknown. The third fledgling was in a brood
with two other Ovenbirds and one cowbird. The
mean mass of the three Ovenbirds when banded
was 14.7 g. 1.2 g more than the mean mass of all
Ovenbird nestlings weighed. The Hedgling with
the transmitter weighed 15.5 g. 1.0 g more than
the mean mass of all Ovenbird nestlings to which
we attached transmitters. We monitored that
Ovenbird Hedgling for 26 days, and 36 Ovenbird
fledglings from 31 non-parasitized broods for 1
to 49 days each. Twenty-six days after Hedging,
the fledgling from the parasitized brood was
dead, but there was no evidence of predation. Its
stomach was empty. All stomachs recovered
from fledglings of non-parasitized broods (n =
4) contained multiple intact and partial insects
(Coleoptera and Lepidoptera), and one also
contained a snail (Pulmonata) and a seed. All
fledglings recovered from non-parasitized nests
had signs of predation.
182
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 1. March 2012
We did not observe the fledgling from the
parasitized brood >50 m front the nest until
12 days after fledging and it did not move >100 m
from the nest until 25 days after fledging.
Fledglings front non-parasitized broods tracked
for at least 25 days (n — 16) were observed >50 lit
front nests 2-10 days (.v = 4.1 r 0.71) after
fledging, and >100 m from nests 3-16 days (.v =
9.5 ± 1.14) after fledging We observed host
adults with the fledgling front the parasitized
brood during three (33%) of nine observations
during the cowbird fledgling superaclive phase
(days 13-23). We observed adults present with
fledglings from non-parasitized broods during 105
(68%) of 155 observations during that period
(difference = 0.35; 95% confidence interval =
0.034-0.666).
DISCUSSION
Cowbird parasitism reduced Ovenbird clutch
size, brood size, and number of young fledged in
northcenlral Minnesota. These findings are similar
to results of studies of Ovenbird populations in
other regions (Hann 1937. Hersek et al. 2002). Our
observations of apparent parental neglect and
starvation of a fledgling from a parasitized brood
is consistent with claims by Rasmussen and Scaly
(2006) that effects of cowbird parasitism likely
extend beyond the nesting period. Rasmussen and
Sealy (2006) suggested that host adults spend most
of their time provisioning cowbird fledglings,
thereby neglecting their own offspring. The host
fledgling we monitored was accompanied by adults
less often than any fledgling from a non-parasitized
brood during the cowbird superaclive phase (days
13 to 23), and was the only fledgling to apparently
starve (i.e., empty stomach and no sign of
predation). This fledgling also remained closer to
its nest than any other fledgling we monitored,
suggesting the cowbird fledgling may have reduced
brood movement. We acknowledge that inference
from our post-fledging observations is speculative
because of the small sample siz.e. It is possible the
fledgling’s mortality may have been caused by
adult mortality or by disease. However, adult
Ovenbird survival is high during the post-fledging
period (Bayne and Hobson 2001 ). and we observed
no signs of additional stressors (e.g., blowfly
infection or heavy tick load). Brood" parasitism
could significantly impact reproductive success in
populations with high incidence of nest parasitism
it our observations arc representative of fledglings
in broods with cowbirds.
Ovenbirds renest up to five times (more
commonly once or twice) after nest failure t Harm
1937, Podolsky et al. 2007). However, pairs rarely
double brood (Hann 1937, Zach and Falls 1976,
Podolsky et al. 2007). The presence of cowbirds in
successfully- fledged broods may reduce seasonal
reproductive success more than cow bird- induced nest
failure. On average, an adult Ovenbird has two
nesting seasons (Hann 1937). Thus, if cowbirds
reduce the survival ot host fledglings, a single
cowbird fledgling could substantially reduce the
lifetime reproductive success of an average Ovenbird.
Models of songbird reproductive success typically
rely on estimates of nest success and assumptions
about fledgling survival. Our observations suggest
brood parasitism may decrease reproductive success
by decreasing nest productivity and by reducing
survival of young fledged from parasitized nests
Each of these influences could result in overestimates
of reproductive success if all successful nests are
treated equally. Wc recommend further investigation
of the relationship between cowbird brood parasitism
and host fledgling survival, especially in areas where
brood parasitism is relatively common.
ACKNOWLEDGMENTS
These data were collected during a project funded by the
U.S. Geological Survey and the US. Fish and Wildlife
Service through Research Work Order 73 at the Minnesoi;.
Cooperative Fish and Wildlife Research Unit with in-kind
suppon from the U.S. Forest Sen ice. We handled, banded,
and attached radio transmitters to birds following Priutvol
#0806A3576 1 , approved by the University of Minnesota
Institutional Animal Care and Use Committee We dunk
D. D. Robinson. A. C. Edmond. E. S. Michel. A. P-
Monroe. T. L. Eisenhauer. J. L. Hammers. J. M. Rcfsnider.
and K. J. Iknayan for assistance in field data collection
Brian Scholtens for assistance with dissection and stomach
content identification, and L. I. Berkeley and S. R Loss lot
helpful comments on the manuscript.
LITERATURE CITED
Airola. D. A. 19X6. Brown-headed Cowbird parasitism
and habitat disturbance in the Sierra Nevada. Jouni "
of Wildlife Management 50:571-575.
Bayne, E. M. and K. A. Hobson. 2001. Movement
patterns of adult male Ovenbirds during the P0-’
fledging period in fragmented and forested bm-t
landscapes. Condor 103:343-351.
Berkeley, L. I.. J. P. McCarty. andL. L Wolfenbakcix
2007. Postfledging survival and movement in Diclais-
sels (Spiza amaricema ): implications for habitat man¬
agement and conservation. Auk 124:396-409.
Braden. G. T.. R. L. McKernan, and S. M.
1997. Effects of nest parasitism by the Brown-head
SHORT COMMUNICATIONS
183
Cowbird on nesting success of California Gnatcatcher.
Condor 99:858-865.
DEARBORN. D. G 1999. Brown-headed Cowbird nestling vo¬
calizations and risk of nest predation. Auk 1 16:448-457.
Donovan, T. M., F. R. Thompson 111. J. Faabokg, and
J. R. Probst. 1995. Reproductive success of migratory
birds in habitat sources and sinks. Conservation
Biology 9:1380-1395.
Gwcueno. M. F. and S. G. Seai.Y. 2010. Clutch
abandonment by parasitized Yellow Warblers: egg
burial or nest desertion? Condor 1 12:399-406.
Hann. H. W. 1937. Life history of the Oven-bird in
southern Michigan. Wilson Bulletin 49:145-237.
Hannon. S. J.. S. Wilson, and C. A. McCallum. 2009.
Does cowbird parasitism increase predation risk to
American Redstart nests? Oikos 1 18:1035-1043.
Haskell D. 1994. Experimental evidence that nestling
begging behavior incuts a cost due to nest predation.
Proceedings of the Royal Society of London. Series B
257:161-164.
Hfrsek, M. J.. M A. Franked, J. A. Ciu.ia.no, and F. E.
Washerman. 2002 Brown-headed Cowbird parasitism of
Ovenbirds in suburban forest fragments. Auk 1 19:240 243,
King. D. I., R. M. Degraaf, M. L. Smith, and J. P.
BlonACCORSI, 2006. Habitat selection and habitat-
specific survival of fledgling Ovenbirds {Seiurus
aurocupllla). Journal of Zoology 269:414-421.
I-ORENZANA. J. C. and S. G. Seai.Y, 1999. A meta-analysis of
tltc impact of parasitism by the Brown-headed Cowbird
on its hosts. Studies in Avian Biology 18:241 253,
Okiega, C. 1998. Cowbirds and other brood parasites.
University of Arizona Press, Tucson, USA.
Payne, R. b. 1991. Indigo Bunting (Passerina cyanea).
The birds of North America. Number 4.
Payne, R. B. and L. L. Payne. 1998. Brood parasitism by
cowbirds: risks and effects on reproductive success
and survival in Indigo Buntings. Behavioral Ecology
9:64-73.
Podolsky, A. L. T. R. Simons, and J. A. Collazo. 2007.
Modeling population growth of the Ovenbird ( Seiurus
iwmcnpilla) in the southern Appalachians. Auk 124:
1359-1372.
Rappoll. j. II. AND A. K. Tipton. 1991. New harness
design for attachment of radio transmitters to small
passerines. Journal of Field Ornithology 62:335-337.
R asmussen, J. L. and S. G. Sf.aly. 2006. Hosts feeding only
Brown-headed Cowbird fledglings: where are the host
fledglings? Journal of Field Ornithology 77:269-279.
RiC'KLEES. R. E. 1968. The survival rate of juvenile Cactus
Wrens. Condor 70:388-389.
Robinson, S. K.. S. I Roihstein. M. C. Brittingham.
L. J. Petit. AND J. A. Gr/yboWSKJ. 1995. Ecology and
behavior of cowbirds and their impact on host populations.
Pages 428-460 in Ecology and management of neotrop¬
ical migratory birds (T. E. Martin and D. M. Finch,
Editors). Oxford University Press. New York. USA.
ROTHSTEIN. S. I. 199(1. A model system for coevolution:
avian brood parasitism. Annual Review of Ecology
and Systematic* 21:481-508.
Smith, .1. N. M 1981. Cowbird parasitism, host fitness, and
age of the host female in an island Song Sparrow
population. Condor 83:152-161.
Woodward. P. W. 1983. Behavioral ecology of fledgling
Brown-headed Cowbirds and their hosts. Condor
85:151-163.
Zach, R. and J. B. Falls. 1976. A second brood in the
Ovenbird, Seiurus aurocapillus. Canadian Field-Natu¬
ralist 90:58-59.
The Wlson Journal of Ornithology 1 24( I ): 1 83- 1 85, 20 1 2
Evidence of Double Brooding by Black-bellied Whistling-Ducks
J. Dale James,1 2 Jonathan E. Thompson,1 3 and Bart M. Ballard1 1
ABSTRACT. — We report the first observation of
double brooding by Black-bellied Whistling-Ducks
IDendrocygna autumnal is). We monitored 151 nest
k°Xcs on the Rob and Bessie Welder Wildlife Refuge in
H»uth Texas during 1998 and 1999 and uniquely marked
' Caesar Kleberg Wildlife Research Institute. Texas A&M
University — Kingsville, V1SC 218. Kingsville. TX 78363.
USA.
Current address: Ducks Unlimited Inc., 193 Business
f.»k Drive, Suite E. Ridgeland. MS 39157. USA.
Current address: Ducks Unlimited Canada. #200. 10720-
'^8 Street, Edmonton. AB T5S 1 J 3, Canada.
Corresponding author; e-mail: bart.ballard@tamuk.edu
all incubating pairs of Black-bellied Whistling-Ducks
using these nesting structures. We color-banded a pair ol
Black-bellied Whistling-Ducks in May 1999 that was
incubating a clutch of 21 eggs, Irom which 18 young
eventually Hedged. The same pair later Incubated a second
clutch of 15 eggs in July and August 1999. of which 12
hatched. Double brooding is apparently not a common
reproductive strategy for Black-bellied Whistling-Ducks
in south Texas, but could be facilitated through biparental
investment in most aspects of reproduction, including
incubation and brood rearing, and a relatively long
potential breeding season in most of this species' breeding
range. Received 9 Max 20 J I. Accepted 22 July 201 /.
184
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 1. March 2012
Black-bellied Whistling-Ducks (Dendrocygna
autumnal is) typically raise one brood per breeding
season, although they may renest if the first clutch
is destroyed or their first brood is lost early in
brood-rearing (Delnicki 1973). Currently, the
Wood Duck (Aix sponsa) is the only North
American duck species know n to commonly raise
two broods in a single nesting season (Haramis
1990). Double brooding has been documented less
frequently in several other species of dabbling
ducks including White-cheeked Pintail (Anas
bahamensis) (Sorenson ct al. 1992). American
Black Duck (A. rubripes ) (Benson and Foley
1962). and Mallard (A. platyrhynchos) (Olsen ct
al. 2003). The growing season in south Texas is
>300 days (Tunnel 2002), and ample time may
exist for Black-bellied Whistling-Ducks to pro¬
duce two broods provided adequate habitat
conditions are available. Johnson and Barlow
(1971) possibly observed a pair of Black-bellied
Whistling-Ducks with a second brood in the same
breeding season, but the pair was not marked and
the observation could not be confirmed. Other
researchers that studied the breeding ecology of
Black-bellied Whistling-Ducks found no evidence
of double brooding (Bolen 1967, Delnicki 1973).
Delnicki (1973) speculated that a female Black-
bellied Whistling-Duck may be physiologically
incapable of double brooding. Our observation is
the first confirmed documentation of a Black-
bellied Whistling-Duck successfully producing two
broods in a single breeding season.
METHODS
We studied the reproductive ecology of Black-
bellied Whistling-Ducks on the Rob and Bessie
Welder Wildlife Refuge near Sinton, Texas in
1998 and 1999 (28° 07' N, 92 22' W). We
monitored nesting activity in 151 nest boxes at the
refuge. We captured all incubating pairs of Black-
bellied Whistling-Ducks in their nest box during
late incubation during the 1998 and 1999 breeding
seasons. We marked captured birds with an U.S.
Geological Survey aluminum band on the right
tarsus and a uniquely coded, plastic band on the
left tarsus in accordance with U.S. Geological
Survey (Permit #10360) and Texas A&M Uni¬
versity — Kingsville Institutional Animal Care and
Use Committee protocols (Approval #1-97-34).
OBSERVATIONS
We discovered a clutch of six eggs on 16 April
799 in nest box A near a small windmill pond.
Seven days later on 23 April 1999, the clutch was
being incubated and we left it undisturbed Wc
captured the female (WB49) on 18 May 1999
while she incubated 21 eggs. W'e captured her
male mate (YB03) while incubating the clutch on
21 May 1999. We observed this pair of birds on
24 May in the nest box with young and the next
morning 18 ducklings exited the nest box and
were observed with the marked pair. Thirty-eight
days later on 1 July 1999 we observed the marked
pair with 13 fully-feathered ducklings on Paloma
Tank, -2.5 km from nest box A. We discovered a
clutch of three eggs on 1 3 July 1999 in nest box B
at Paloma Tank and on 20 July we flushed the
same marked pair and 13 recently fledged Black-
bellied Whistling-Ducks from the shoreline of
Paloma Tank. The clutch in nest box B contained
nine eggs on this visit (20 July). By 26 July, we
discovered that female W'B49 was incubating a
second clutch of 15 eggs in nest box B. The male
(YB03) and previously fledged young were no!
observed. We captured female WB49 on 10
August 1999 and male YB03 the next day while
incubating the second clutch in nest box B. Wc
revisited nest box B on 21 August 1999 and found
12 hatched and three unhatched eggs. Neither ot
the two broods was observed again.
DISCUSSION
We documented that Black-bellied Whistling-
Ducks are capable of double brooding. This is a
single observation, but there are several aspects of
Black-bellied Whistling-Duck ecology that could
increase the propensity for double brooding. First,
their potential breeding season is long relative to
other species of waterfowl because they breed
primarily in subtropical and tropical regions. Tire
growing season in south Texas is >300 days
(Tunnel 2002), and a breeding season of this length
provides ample opportunity to lay, incubate, and
raise two clutches when habitat conditions are
favorable. Second, both males and females share n
incubation and brood-rearing duties (James aiw
Thompson 2001). Biparental care in these aspect
of reproduction may allow females to maintain a
positive nutrient/energy balance throughout ne>
ing and brood rearing, reducing the time ber^ei. 1
fledging their first ducklings and laying the seconu
clutch. Black-bellied Whistling-Ducks may al*1
rely largely on exogenous versus endogenous
nutrients for egg production, as these birds to 1
readily feed on high-energy waste grains at sioe
yards, grain mills, and sorghum fields during e
SHORT COMMUNICATIONS
185
breeding season (Bolen 1967; JDJ, pers. obs.). This
may enhance the ability of some females to meet
the high nutrient demands of producing two
clinches and rearing these young.
Similar to geese. Black-bellied Whistling-Ducks
often remain in family groups through late summer
after young are Hedged (Bolen 1967). and possibly
irough the first winter (Cottam and Glazner 1959).
How double-brooding behavior affects family group
dynamics and other life history strategies of this
species remains unknown. Further understanding
reproductive strategies, including the advantages of
biparental incubation and brood rearing and the role
o! nutrient reserves in reproduction, are avenues for
luture research in this species.
ACKNOWLEDGMENTS
We are grateful lo the Rob and Bessie Welder Wildlife
foundation lor research support and access lo the study site.
We also thank the Caesar Kleberg Wildlife Research
ioslimte for additional logistical support and K. G. Erwin
''c'd assistance. This is publication #609 of the Welder
Wildlife Foundation and #11-120 of the Caesar Kleberg
Wildlife Research Institute.
LITERATURE CITED
RtsNSON, 1). and D. D. Foley. 1962. Hatching dates of
waterfowl in New York. New York Fish and Game
Journal 9:73-92.
Rolen, e. G. 1967. The ecology of the Black-bellied Tree
Duck in southern Texas. Dissertation. Utah State
University. Logan. USA.
Cottam. C. and w. C. Glazner. 1959. Late nesting of
water birds in south Texas. Transactions of the North
American Wildlife Conference 24:382-395.
DhLNK’Kl. D. 1; 1973. Rencsting. incubation behavior, and
compound clutches of the Black -bellied Tree Duck
in southern Texas. Thesis. Texas Tech University,
Lubbock. USA.
HARAMIS. G. M. 1990. Breeding ecology of the Wood
Duck: a review. Pages 45-60 /// Proceedings of 1988
North American Wood Duck Symposium (L. H.
Fredrickson, G. V. Burger. S. P. Havera, D. A. Graber,
R E. Kirby, and T. S. Taylor. Editors). St. Louis,
Missouri. USA.
James, J. D. AND J. E. Thompson. 2001. Black-bellied
Whistling-Duck ( Dendrocygna autumnal is). The birds
of North America. Number 578.
Johnson, A. R. and J. C. Barlow. 1971. Notes on the
nesting of the Black-bellied Tree Duck near Phoenix,
Arizona. Southwestern Naturalist 15:394-395.
Olsen, R. E.. T. Yerkes. and J. W. Simpson. 2003.
Occurrence of second broods in Mallards in the
Midwest. American Midland Naturalist: 150:302-307.
Sorenson, L. G.. B. I.. Woodworth, l. M. Rett an, and
F McKinney. 1992, Serial monogamy and double
brooding in the White-checked (Bahama) Pintail Anas
babamensis bohamensis. Wildfowl 43:156-159.
Tunnel Jr., J w. 2002. Geography, climate, and hydrog¬
raphy. Pages 7-27 in The Laguna Madre of Texas and
Tamaulipas (J. W. Tunnel Jr. and F. W. Judd, Editors).
Texas A&M University Press, College Station, USA.
The Wilson Journal of Ornithology 1 24( I ): 1 85- 1 87, 20 1 2
First Case of Renesting after Brood Loss by a Greater Prairie-Chicken
Lance B. McNew12 and William J. White'
ABSTRACT. — Production of a second brood, or
^'“ble brooding, by a single female in one breeding
'cason has not been reported for any species of grouse
111 ^orth America. We describe the hreeding history of
"ncof55 radio-marked female Greater Prairie-Chickens
1 Tmpanuchus cupido) that successfully renested after
losing a |,roo[| from a pirM nesting attempt during the
-hi I breeding season in Kansas. Observations of double
brooding by grouse might only he possible in areas like
lile Him Hills of Kansas, where populations have a long
breeding season in combination with a high rale of
Division of Biology. Kansas State University. Manhat-
Utn- KS 66506. USA. ’
'Corresponding author; e-mail: lbmcnew@k-state.edu
brood loss. Received 15 August 201 1. Accepted 2R
October 2011.
Double-brooding has been defined as the pro¬
duction of two broods from two separate nesting
attempts by a single laying female in one breeding
season, but may or may not result in two broods
Hedging (Fredrickson and Hansen 1983). Theo¬
retically. the production of second broods should
increase the lifetime productivity and fitness of
short-lived species of birds. However, the poten¬
tial for birds to produce multiple broods in a sin¬
gle season is limited by the length of the nesting
season, duration of a breeding attempt Irom clutch
186
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 1. March 2012
initiation until offspring are independent, age of
the nesting female, and food availability (Olsen
et al. 2003). The production of multiple broods
within a breeding season has been previously
unreported for North American grouse (subfamily
Tetraoninae). although common in other avian
taxa (Labranche and Walters 1994, Guthery and
Kuvlesky 1998, Morrison 1998. Pope and Craw¬
ford 2001. Olsen et al. 2003. Ortego 2004,
Monroe et al. 2008, Mulvihill et al. 2009, Sandor
and Moldovan 2010).
Greater Prairie-Chickens ( Tympanuchus cu-
piclo) are a ground-nesting prairie grouse with an
extant distribution ranging from Oklahoma to
North Dakota (Johnson et al. 201 I). Populations
in the southern extent of their distribution in
Kansas arc characterized by having long breeding
seasons, high nesting propensity, large clutch
sizes, and high rates of renesting after failure of
first nests (McNew et al. 2011). Chicks fledge and
can achieve short flights at 14 days of age but are
not independent until 40-85 days of age (Johnson
et al. 2011. McNew et al. 201 1 ). We report on the
breeding history of a radio-marked female Greater
Prairie-Chicken in Kansas that successfully
hatched a nest and then renested after losing the
brood from her first nesting attempt.
METHODS
We placed necklace-style radio transmitters
(Model A3950, Advanced Telemetry Systems,
Isanti. MN, USA) on 55 female Greater Prairie-
Chickens captured at 13 leks during 1 1 March-
5 May 201 1 in Chase. Greenwood, and Morris
counties. Kansas (UTM Zone 14 N: 0717451 E,
42661 17 N) as part of a study evaluating prairie-
chicken ecology within the intensively-grazed
Flint Hills ecoregion. Annual spring burning of
residual vegetation over large extents of native
tallgrass prairie is common and cattle grazing is
the dominant land use in the Flint Hills (McNew
et al. 2011).
OBSERVATIONS
We captured and equipped a female Greater
Prairie-Chicken on 4 April 201 1 with a uniquely
numbered aluminum leg band (#1249) and radio
transmitter. The radio-marked female was moni¬
tored >3 times per week from vehicles during the
nesting and brood-rearing period (Apr-Aug). The
female was Hushed on 10 May and had a nest
with 12 eggs. We estimated, via floatation and
back-dating from day of hatch, the clutch was
initiated on 21 April. Nest attendance by the
female was monitored remotely by telemetry
every 1-3 days throughout the incubation period.
The last date the female was known via telemetry
to be incubating her first nest was 27 May. anil
she was first detected to be away from her nest on
28 May. On 29 May, we visited the nest site and
confirmed via eggshell remains that all 12 eggs
successfully hatched on 27 May. On 29 May. the
female was discovered to have moved 3.2 km
from her location the previous day. suggesting
potential total brood loss of the newly hatched am!
flightless young. We Hushed the hen on 13 June
when her chicks should have been 16 days of age,
and conducted a thorough search for chicks: finding
none. We conducted a second flush count tin
following day and again counted no chicks
confirming her first brood had been lost sometime
during the pre-fledge period ( likely prior to her long
movement on 29 May when chicks were 2 days of
age). We continued to monitor the female by
telemetry and on 22 June we discovered this female
incubating a second nest of eight eggs. We
estimated with egg flotation that the second nest
was initiated on 10 June, indicating 13 days between
the time when her first brood failed arid when she
began laying her second clutch. The distance
between her first and second nest was 2.9 km, The
female’s second clutch successfully hatched all
eight chicks on 15 July. We conducted a flush count
at 14 days post hatch (29 July) and found the second
brood failed during the pre-fledging period. 3
second flush of female 1249 was conducted on .4)
July to confirm the absence of chicks.
DISCUSSION
The production of multiple broods is though'
to be an adaptive life history' strategy lor some
populations of birds where survival and tuture
breeding effort is not diminished (Perrins 19 4).
Boer-Hazewinkel 1987). Low occurrence of
second broods has been reported for other species
of gallinaceous birds in North America: Northern
Bobwhite (Col inns virginiamts; Sandereock et al.
2008). Mountain Quail (Oreortyx pictus. Pope and
Crawford 2001), Wild Turkey (Meleagris gallo-
pavo; Keegan and Crawford 1993). and Ring-
necked Pheasant ( Phasianus colchicus : Gate'
1966. Dumke and Pils 1979). Renesting after
loss of a brood has only been documented in one
other species of grouse, the Scottish Red Groan
( Lagopus lagopus scoticus ; Kirby and Smith
SHORT COMMUNICATIONS
187
2005). Selection has not favored production of
multiple broods by gallinaceous birds due in part
;o limited benefit of this strategy for increasing
productivity (Guthcrv and Kuvlesky 1998, San-
dercock et al. 2008). Our observation may not be
considered true double-brooding, as two success¬
ful broods were not produced, but our field re¬
port is the first case of a female prairie grouse
producing tw'o broods in the same breeding
season. Occurrence of double-brooding is likely
extremely rare in prairie-chickens because
females provide uniparental care during incuba¬
tion and brood-rearing, and juveniles are attended
by females for 60-85 days after hatch (Johnson ct
al. 2011. McNew et al. 2011). Only one of our six
radio-marked hens which lost their first broods
before chicks fledged was known to have renested
following brood loss in this study, and previous
research did not document second broods for any
or 47 cases in which radio-marked female Greater
Prairie-Chickens lost their first broods prior to
fledging (McNew et al. in press). Double-
brooding may be more common in (he Flinl Hills
ecoregion than other portions of the species' range
because the breeding season is long and brood
mortality is high during the pre-flcdging period
(>70%; McNew et al. in press). However,
production of a second brood is likely limited to
females which lose their first broods early due to a
l°ng brood-rearing period and relatively high
survival of juveniles from fledging to recruitment
' -0.5; McNew et al. in press).
ACKNOWLEDGMENTS
thank J. W. Doggett. K. D. Lunsford, and M. K.
Kiicluc for Held assistance and U. K Sandercock for
reviewing the manuscript. Wc thunk The Nature C'onser-
ianc-v- f-'S. National bark Service, and -12 private
rind.'wners for access to their properties This study was
1 ' inied by Kansas Federal Aid in Wildlife Restoration
Pmject W-67, Kansas State University, and the Kansas
Department of Wildlife. Parks, and Tourism. Field methods
"ere approved by Kansas State University's Institutional
‘nimal Care and Use Committee (Protocol t/2962).
LITERATURE CITED
b,)hr-Hazewinki;l. J. 1987. On the costs of reproduction:
parental survival and production of second clutches in
'he Great Tit. Ardea 75:99-1 10.
Dcmkf.. R. t. AND C. M. Pils. 1979. Renesting and
dynamics of nest site selection by Wisconsin pheas¬
ants. Journal of Wildlife Management 43.705-716.
Fredrickson, L. H. and J. L. Hansen. 1983. Second
broods in Wood Ducks. Journal of Wildlife Manage¬
ment 47:320-326.
Gates, J. M. 1966. Renesting behavior in the Ring-necked
Pheasant. Wilson Bulletin 78:309-315.
GlTHF.RY. F- S. AND W. P. KUVLESKY. 1998. The effect of
multiple-hrooding on age ratios of quail. Journal of
Wildlife Management 62:540-549.
Johnson. J. A.. M. A. Si hrokdkr. and L. A. Robb. 2011.
Greater Prairie-Chicken ( Tympanuvhus cupido ). The
birds of North America. Number 36.
Kixgan. T. W and J. A. Crawford. 1993. Renesting by
Rio Grande Wild Turkeys after brood loss. Journal of
Wildlife Management 57:801-804.
Kirby, A. D. and A. A. Smith. 2005. Evidence of re-nesting
after brood loss in Red Grouse Lagopus lagopus
scoiicus. Ibis 147:221.
LabraNCHE. M. S. and J. R. Wai ters. 1994. Double
brooding in Red-cockaded Woodpeckers. Wilson
Bulletin 106:403—408.
McNew. L. B.. A. J. Gregory. S. M. Wisely, and B. K.
Sandercock. 201 1 Reproductive biology of a southern
population of Greater Prairie-Chickens. Pages 209-221
in Ecology, conservation, and management of grouse
(B. K Sandercock. K. Marlin, and G, Scgelbacher.
Editors). Studies in Avian Biology Number 39.
University of California Press. Berkeley. USA.
McNew. L. B. A. J. Gregory. S. M. Wisely, and B. K.
Sandercock. In Press. Demography of Greater
Prairie-Chickens: regional variation in vital rates,
sensitivity values, and population dynamics. Journal
of Wildlife Management
Monroe, A. P„ K. K. Haeunger, R. L. Brasso, and D. a.
Cristol. 2008. Occurrence and implications of double
brooding in a southern population of Tree Swallows.
Condor 11 0:382-386.
Morrison, J. L. 1998. Effects of double brooding on
productivity of Crested Caracaras. Auk 1 15:979-987.
Mulvihiel. R. S.. S. C. LA-nA. and F. L, Newell. 2009.
Temporal constraints on the incidence of double brooding
in the Louisiana Waterthrush. Condor 1 1 1:341-348.
Olsen, R. E.. T. Yerkes. and J. W, Simpson. 2003.
Occurrence of second broods in Mallards in the
Midwest. American Midland Naturalist 150:302—307.
Ortego, J. 2004. A possible case of double brooding of
Eagle-Owls (Bubo bubo) in Spain. Journal of Raptor
Research 38:378-379.
PERRINS, C. M. 1970. The liming of birds' breeding
seasons. Ibis 112:242-255.
Pope, M. D. AND J. A. Crawford. 2001. Male incubation and
bi parental care in Mountain Quail. Condor 103:865-870.
Sandercock, B K.. W. E. Jensen, C. K. Williams, and
R. D. Applegate. 2008. Demographic sensitivity of
population change in Northern Bobwhite. Journal ot
Wildlife Management 72:970-982.
Sandor, A. D. and I. Moldovan. 2010. A possible case
of double brooding of Pharaoh Eagle Owls ( Bubo
ascalaphus Savigny. 1809) in Egypt. African Journal
of Ecology 48: 1 1 29-1130.
188
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 1. March 2012
The Wilson Journal of Ornithology 1 24(1): 188- 1 90. 2012
Do Sora Nests Protect Red-winged Blackbirds from Marsh Wren Predation?
Leanne A. Grieves1-2 and Scott Forbes1,3
ABSTRACT. — We report an apparent protective
effect of neighboring Sora {Porzana Carolina) nests on
Red-winged Blackbird {Agelaius p/weniceus) nests in
an experimental study. We suggest that quail eggs used
in Sora nests acted as a supernormal stimulus drawing
Marsh Wrens (C is tot horns palustris), the main predator
in the system, from Red-winged Blackbird nests.
Received 16 August 2011. Accepted 6 January 2012.
Nest predation is the most significant source of
mortality in many populations of nesting Red-
winged Blackbirds (Agelaius phoeniceus) (Cacca-
mise 1976, Martin 1988, Pieman et al. 1988.
Westneat 1992; reviewed in Beletsky 1996,
Weatherhead and Sommerer 2001). These black¬
birds often nest with a variety of other species in
their wetland habitats and an obvious question is
whether the presence of interspecific neighbors
affects rates of predation by providing additional
cues for predators. Our logic was that once
predators are in the area, they are more likely to
locate a blackbird nest. We tested this hypothesis
by performing an artificial nest experiment that
placed Sora ( Porzana Carolina) nests near black¬
bird nests at randomly assigned locations within
study marshes. We chose Sora as the interspecific
neighbor as their nests are common on our study
site (near Winnipeg in southern Manitoba), and
they do not cooperate with blackbirds in any
obvious way to deter predators (e.g., mobbing).
We knew from field work at this site since 1993
(Forbes 2010) that nests of both blackbirds and
Sora are often robbed by a variety of avian and
mammalian predators. Our expectation was that if
Sora nests provided a conspicuous cue for
predators, nests of blackbirds with nearby nests
of Sora would experience higher rates of preda¬
tion; we did not expect to find the opposite effect.
Department of Biology, University of Winnipeg, 51'
Portage Avenue. Winnipeg. MR R3B 2E9, Canada.
.. De(fa"menl of Biology, McMaster University, 1280
Main Street West, Hamilton. ON L8S 4KI. Canada
Corresponding author; e-mail; s.forbes@uwinnipeg.Ci
METHODS
The study area consisted of three artificial
wetlands in Rosser, Manitoba, Canada (49 57' N,
97 19' W) which we refer to as the Northwest
(NW), Northeast (NE). and Southeast (SE!
marshes with nesting populations of Red-winged
Blackbirds and Sora. The sites were excavated
during construction of a highway overpass,
creating relatively shallow and uniform Typlta
spp. marshes used by a variety of nesting birds.
We used old. abandoned or flooded Red-winged
Blackbird nests as experimental nests. These nests
were removed from their original locations and
placed on bamboo tripods 0.5 m above the ground
or water. We obtained experimental eggs for ihe
blackbird nests from two sources: flooded nests
and unhalehcd eggs collected from nests during
routine surveys. We had limited availability ol
blackbird eggs, and used Brown-headed Cowbird
(Molothrus ater) eggs to complete clutches of
three eggs (2 blackbird, I cowbird) in nine of 66
experimental clutches. This mimics the natural
situation as Brown-headed Cowbirds are Irequent
brood parasites in this system (Glassey and Forbes
2003, Royie et al. 2011). The modal clutch size in
this population is four, but clutches of three are
common in the study population (Forbes 2019).
Thus, with a limited supply of Red-winged
Blackbird eggs available, a dummy clutch o:
three allowed us to increase our .sample size. Sora
were used as an interspecific model and Japanese
Quail ( Cotumix japoniea) eggs purchased com
mercially were used to mimic their eggs following
Pieman et al. (1988). We used both nests that had
been abandoned during flooding and artificially-
constructed nests from mounds of Typha spp. tor
the experimental Sora nests. Experimental Sora
nests were placed at ground level and tilled with
three quail eggs to remain consistent with the
number of eggs used in the blackbird nests,
although the average clutch size for Sora i>
between eight and II (Bent 1926, Lowther
1977, Kaufman 1989).
The three marshes were subdivided into 20 X
20-m quadrats (69 quadrats in NW. 59 in NE, and
SHORT COMMUNICATIONS
189
TABLE 1. Number of experimental Red-winged
Blackbird nests that survived (no predation) or failed
(depredation) when an experimental Sora nest was present
or absent
Locution
Sora nesi
Falc of Red- winged Blackbird ned
Survived
Failed
Northwest
Present
8
1
marsh”
Absent
9
9
Northeast
Present
4
3
marsh*1
Absent
3
11
Southeast
Present
4
1
marsh'
Absent
9
4
‘ Fisher exact lest P = 0.0912.
. Fisher exact lest P = 0.1564.
1 Fisher exact test P = 1.000.
44 in SE). The experimental nests were placed in
ihe marshes at the center of randomly chosen
quadrats between 7 and 30 June 2010, spanning
the period of peak nesting activity and extending
io the end of the nesting period for most
blackbirds in the study population (Forbes
2010). Three eggs were placed in each nest and
were removed 48 hrs later. Nests were checked
daily for the occurrence of predation. Red- winged
Blackbirds and Sora nested in all three marshes.
Marsh Wrens ( Cistothonis palustris) and their
nests were observed in the NW and NE marshes
bui not in the SE marsh. Evidence of egg
predation consistent with Marsh Wrens was found
in NW and NE marshes but not in the SE marsh.
OBSERVATIONS
Between 28 and 67% of experimental Red-
winged Blackbird nests were depredated, consis-
,enl with estimates of nest predation in active
blackbird nests (reviewed by Beletsky Id96).
Avian predators were responsible for most preda¬
tion of experimental nests in all three study sites.
Twenty-nine (44%) of the 66 experimental black¬
bird nests placed into the marshes were depredated:
-8 ot 29 depredated nests were due to avian
predators, and at least 16 of the 28 nests (57%)
were depredated by Marsh Wrens based on the
Presence of punctured eggs in the nest (Pieman
i^77). There was no obvious relationship between
nest fate of experimental blackbird and Sora nests
'Tisher exact test, two-tailed: P = 1.00).
We used two-tailed Fisher exact tests to
examine the effects of interspecific neighbors
(Sora) on nest predation of blackbirds. The results
for individual marshes were not statistically
significant (Table 1). However, when data for
the two marshes (Northeast and Northwest) where
nesting Marsh Wrens were present were com¬
bined. a significant effect was observed (Table 1;
Fisher exact test. P = 0.031). Conversely, in the
one marsh where nesting Marsh Wrens were
absent, no effect of a Sora nest on the likelihood
of predation on a blackbird nest was observed
(Table 1; Fisher exact test, P = 1.00).
We found no obvious effect of the presence of
an active Red-winged Blackbird nest in the same
quadrat as a dummy nest on predation. There were
active blackbird nests in most quadrats at the
beginning of the season, but the attrition of active
nests both due to predators and Hedging meant
that few of our dummy nests overlapped with
active blackbird nests. Further, some dummy
nests were placed in quadrats with active Marsh
Wren nests with no obvious effect. We suspect
this was not because the proximity to Marsh
Wrens was unimportant, but rather because the
spatial scale of quadrats and territories was
dissimilar. We observed Marsh Wrens ranging
widely in the NW and NE marshes, but they were
not present in the SE marsh.
We examined the likelihood of predation on
active Red-winged Blackbird nests in relation to
distance from a Marsh Wren nest in the NE marsh
where the location of all Marsh Wren nests was
known. We found a positive but non-significant
effect: 10 of 11 nests within 20 m of a Marsh
Wren nest were depredated, compared to 23 of 34
nests >20 m from a Marsh Wren nest (Fisher
exact test, P = 0.24).
DISCUSSION
Red-winged Blackbird nests in marshes with
Marsh Wrens, placed near Sora nests, were less
likely to be depredated than solitary blackbird nests.
This result was unexpected. Rather than attracting
additional predation as we initially expected, the
presence of a Sora nest appeared to confer some
level of protection to a blackbird nest. The effect
was not due to group defense by blackbirds as only
artificial nests were used and there were no adults
associated with the experimental nests.
The behavior of Marsh Wrens seems most
likely to account for the observed results. Marsh
Wrens were the main predator in the NW and NE
marshes but were absent from the SE marsh. We
suggest that quail eggs in the experimental Sora
nests acted as a supernormal stimulus, distracting
the Marsh Wrens from the neighboring blackbird
190
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 1. March 2012
nests and explaining reduced predation when Sora
nests were present in the marshes with breeding
Marsh Wrens. Previous experimental work by
Pieman (1977) showed that Marsh Wrens are not
able to destroy quail eggs; thus, the stimulus
presented by these eggs remained for the duration
of our 48-hr trial period.
We had expected corvids and mammals to be
significant predators of blackbird and Sora nests
in addition to Marsh Wrens based on many years
of work at Ihis site. We may have overestimated
the importance of crows and ravens (Corvus spp.)
because ihey arc observable. Mammalian preda¬
tion tends to be intermittent but widespread.
Common raccoons ( Procxon lotor) in particular
have decimated entire Red-winged Blackbird
colonies in one or two nights.
Our experimental design contained one unavoid¬
able element that may have contributed to lower
predation of blackbird nests in the presence of Sora
nests. As artificial nests were used, there were no
attending adult blackbirds or Sora. A female Sora or
Red-winged Blackbird would be in nearly constant
attendance at the nest during incubation under natural
conditions (Kaufman 1989, Beletsky 1996) and, for
blackbirds, the territorial male would defend against
Marsh Wren intrusions (Beletsky 1996). Marsh
Wrens are known to attack Sora nests (Allen 1934)
and it is possible that in the absence of adult Sora,
Marsh Wrens had greater than normal access to the
experimental nests. However, nests do remain
uncovered during egg-laying before the onset of
incubation by both blackbirds (Beletsky 1996) and
Sora (Kaufman 1989) and a 2-day exposure of the
eggs as in our experiment would not be unusual.
ACKNOWLEDGMENTS
Funding was provided for this project by the Natural
Sciences and Engineering Research Council of Canada
(NSERC) and the University of Winnipeg. We thank two
anonymous reviewers and C. E. Braun for helpful
comments on the manuscript.
LITERATURE CITED
At-LEN, A. A. 1934. The Virginia Rail and the Sora. Bird
Lore 36:196-204.
BELETSKY. L. 1996. The Red-winged Blackbird: the
biology of a strongly polygynous songbird. Academic
Press, San Diego, California. USA.
Beni. A. C. 1926. Life histories of North American marsh
birds. U.S. National Museum Bulletin 135
CACCAM1SL. D. F. 1976. Nesting mortality in the Red
winged Blackbird. Auk 93:517-534.
Forbes, S. 2010. Family structure and variation in
reproductive success in blackbirds. Behavioral Ecolu-
gy and Sociobiology 64:475-483.
Glassey. B. and S. Forbes. 2003. Why Brown-headed
Cowbirds do not influence Red-winged Blackbird
parent behavior. Animal Behavior 65:1235-1246.
Kaufman. G. W. 1989. Breeding ecology of the Sora,
Porrana Carolina, and the Virginia Rail, Ratlin
limicola. Canadian Field-Naturalist 103:270-282.
Low i her, J, K, 1977. Nesting biology of the Sora at
Vermillion, Alberta. Canadian Field-Naturalist 91:63-
67.
Martin, T. hi. 1988. Processes organizing open-nesting
bird assemblages: competition or nest predation’
Evolutionary Ecology 2:37-50.
PlCMAN, J. 1977. Destruction of eggs by the Long-hilled
Marsh Wren ( Telmatodytes palusiris palustris). Cana¬
dian Journal of Zoology 55:1914-1920.
Picman. J.. M. Leonard, and J. Horn. 1988. Antiprcda-
lion role of dumped nesting by marsh-nesting ReJ-
winged Blackbirds. Behavioral Ecology and Sociobi-
ology 22:9-15.
Royle, N. J.. M. E. Hall. J. D. Blount. and S. Forbes.
201 1. Patterns of egg yolk antioxidant co-variation a:
an avian brood parasite-host system. Behavioral
Ecology and Sociobiology 65:313-323.
WEATHERHEAD. P. j. and S. J. Sommerer. 2001. Breeding
synchrony and nest predation in Red-winged Black
birds. Ecology 82:1632-1641.
Westneat, D. F. 1992. Nesting synchrony by female Red-
winged Blackbirds: effects on predation and breeding
success. Ecology 73:2284-2294.
The Wilson Journal of Ornithology 124(1): 191- 197. 2012
Ornithological Literature
Margaret A. Voss. Book Review Editor
BIRDS OF HAWAII. NEW ZEALAND AND
THE CENTRAL AND WEST PACIFIC. By Ber
van Perlo, illustrated by the author. Princeton
University Press, Princeton. New Jersey. USA.
2011: 256 pages. 95 numbered color plates, and
numerous unnumbered text figures and range
maps. ISBN: 978-0-691-15188-5. $29.95 (soft
cover).— As the senior author and illustrator of A
field guide to the birch of Hawaii and the tropical
Pacific (Pratt el al. 1987). which is still in print
Irora the same publisher (second edition in
preparation; www.hdouglaspratt.com), I am not
an unbiased reviewer of this book, but I will strive
lo be objective. The two books cover the same
geographical area except that van Perlo adds New
Zealand, This is the latest of a series of what the
publisher calls “illustrated checklists". However,
the first sentence of van Perlo’s preface reads
1 his book should be regarded and treated as a
held guide in which the necessary information,
needed to identify a bird at the moment you
observe it, is given in condensed form.” so 1 will
evaluate it as a field guide.
Coverage is said to be up-to-date as of 2009.
but (he book includes some records that have yet
t0 be published (Vice et al. in prep.) and misses
others that were published well before 2009
(Ramon and Jones 2005; VanderWerf et al.
2(K)6. 2008). The taxonomy follows Clements
(2007) and is not as up-to-date as the species list.
Newell's Shearwater (Puffinus newel li ) is men-
c°ncd only in the Endnotes as a recent split from
^lanx Shearwater ( P . puffinus), yet the book
includes a full account for Townsend’s Shearwa-
ler (P. auricularis ), which occurs in the region
°nly as the subspecies I1, a. newelli. Species such
a* (Western) Yellow Wagtail (Mntacilla Jlava).
Oreat Reed Warbler (Acrocephahis arundinct-
(t-us), Black-headed (Tricolored) Munia (Lonch-
ura malacca), and Black-tailed (Grey) Waxbill
Ihstrildu perreini) that have never been reported
l,r established in the region are included appar¬
ently because of confusion with other included
Species: respectively Eastern Yellow Wagtail
(V. tschutschensis); Oriental Reed Warbler (A.
orietualis)’. Chestnut (Black-headed) Munia
(L. atricapilla); and Black-ramped Waxbill (E.
troglodytes). |For clarity, the previous sentence
uses van Perlo' s English names (from Clements
2007) with alternatives from Gill and Donsker
(2011) in parentheses. 1
The Introduction includes a cogent description
of plate tectonics and island formation, and rather
broad overviews ol island habitats and the
regional avifauna. The last begins with a brief
discussion of how island avifaunas form, a short
paragraph ahout island extinctions, and a rather
arbitrary listing of some of the phenomena
demonstrated by island birds. It says little about
historical causes of island extinctions, ongoing
conservation problems, endangered species, or
potential new threats to island birds. A series
of maps of the main island groups, with bird-
significant islands numbered for cross-referencing,
accompany illustrations of the endemic species
for each group (the Tinian Monarch [Monarcha
takatsukasae ) and the two megapodes [Megapodius]
have the wrong illustrations).
The main body of the book comprises num¬
bered color plates with facing-page species
accounts. Nearly all accounts, even those for
single-record vagrants, include tiny thumbnail
distribution maps (some compress the entire
tropical Pacific into 2 cm!). I found most of them
too small to be useful, hut for widely distributed
seabirds, shorebirds, and migratory waterfowl,
they provide an informative regional overview.
Accounts also include a list ol the political entities
in which the species lives, sometimes with
numbers for particular islands as shown in the
Introduction. Crowding and small overall size
would not allow direct labeling on the plates, but
the numbers, letters, and heavy use of abbrevia¬
tions make for a lot of annoying cross-referencing.
The author/illustrator defends his simplistic
painting style with comments such as “painting
each individual feather will give too much
information unless the feathers form a pattern”
and criticizes other illustrators for including too
much detail. But even cartoonish illustrations can
be very effective, and require no defense if well
executed. Van Perlo’s style differs strikingly from
my own. but succeeds for an illustrated checklist,
if not always for field guide purposes. A few poor
191
192
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124, No. 1. March 2012
drawings notwithstanding, I found his illustrations
to be accurately drawn, and 1 much prefer an
accurate drawing painted with less detail to a
highly detailed rendering of a bad initial drawing.
If the basic drawing is poor, no amount of detail
will make it better. Van Perlo succeeds best with
birds he knows, either from observation or
photographs, so most New Zealand birds are well
drawn, while those from Micronesia or Hawaii are
less so and uneven. Still, few of the drawings are
seriously misleading.
Coloration is another matter. Throughout the
book, the colors are overly bright to the point of
being garish (possibly more the fault of the printer
than the illustrator). But the user cannot assume that
everything is too bright generally because the almost
fluorescent Orange Fruit Dove (Ptilinopus victor) is
disappointingly dull. Within a plate, colors often are
more dissimilar than they are in life. The Todir-
amphus kingfishers are shown as either rich blue or
olive green above, even though all are subtle shades
of greenish blue. Among the large pigeons, several
are too blue above, the New Zealand Pigeon
( Hemiphaga novaeseelandiae) grotesquely so. The
Nicobar Pigeon ( Caloenas nicobarica), which looks
black in the field, Pohnpei Fantail (Rhipidura
kubaryi). and Mao ( Gymnomyzja samoensis) are so
colorful as to be unrecognizable.
Comments on identification are very brief, and
rely heavily on the illustrations. Most are barely
adequate, but many are far too brief. Of the
Nukupuu (Hemignathus lueidus), van Perlo simply
says "unmistakable in range" when nothing could
be further from the truth (Pratt and Pyle 2000),
especially given his very inaccurately colored
female. 1 found numerous outright mistakes, the
most obvious of which include: long wavy, rather
than stiff, tail streamers on the Red-tailed Tropicbird
0 Phaethon rubricauda): black, rather than chestnut,
thighs on the Great Blue Heron (A idea he radios)-,
reversal of the illustrations of the two megapodes
( Megapodius spp.); a contrastingly pale tail on the
misleadingly named Grey-tailed Tattler (Tringa
brevipes ); a barred belly on the nonbreeding
Wandering Tattler (T. incana): badly garbled
subspecies of Whimbrel (Numenius phaeopus), with
hudsonu us wrongly said to resemble variegatus,
and the illustration of the latter actually representing
the former; the statement that the two Phalaropus
phalaropes are identical rior.sally with images that
compound the. error; dusky orange feet (should be
w excepl ,he Hawaiian Islands,
ere they are bright orange) and dark tail (paler
than rest of dorsum in all Pacific forms) on the Black
Noddy (Anous minutus ); wrong subspecies of
Eastern Yellow Wagtail (A/, t. tschutschensis rather
than M. t. simillima ); blue rather than silvery white
‘spectacles’ on the Chinese Hwamei (Gurrulax
canorus)-, a white band on the underside of the tail of
the male Common Cicadabird ( Coracina tenuiros-
tris ); wrong map for the Black-faced Cuckooshnke
(C no vaehol landiae); immature Northern Mock¬
ingbird (Mimus polyglottos) with an unstreaked
breast; pink rather than red undertail coverts of the
Red-whiskered Bulbul (Pycnonotus jocosux); a
sharp crest on the Palau Flycatcher {Mmgru
erythrops), which shows hardly any crest, and no
ca*st on the Azure-crested Flycatcher (A/, a:\ireo-
capilla), which has a pronounced one: incorrect
distribution and misleading coloration of the
Samoan form of Fiji Shrikebill ( Clytorhynchiis
vitiensis powelli); the more widespread gray, rather
than the much darker Palau form of White-breasted
Woods wallow (Artemius teucorynchus)-, prominent
wing bars on Maui female Hawaii Amakihi
(Hemignathus virens ); and misspellings of Niua-
fo' ou and Matsuduira. The brief habitat descriptions
are often inappropriate to the region. For example,
the Little Ringed Plover (Charadrius dubius), a rare
winter visitor to the small islands and atolls of
Micronesia, is said to inhabit “sparsely vegetated
fiats at shallow inland waters”, clearly a reference to
continental rather than island habitats.
Van Perlo based his voice descriptions on study
of published recordings rather than on field work
with the unfortunate result that voices of Micro-
nesian and many Polynesian birds are not
described at all. even though all have been well
described in the literature and are readily
available in sound archives. Perplexingly. the
accounts include some vocalizations that are not
heard in the region (i.e.. those of nonbreeding
visitors that vocalize only in breeding areas) 1
found van Perlo' s transliterations inscrutable and
often downright misleading, and he makes no
comparisons among syntopic species that would be
helpful to birders. For example, many of the "little
green” Hawaiian honeycreepers sing trills that are
easily compared (Pratt et al. 1987). Van Perlo
accurately describes the voice of the Hawaii
Amakihi (H. virens) but fails to compare it to the
songs of eight other species with similar songs. Hi-
description of the homologous song
the Kauai Amakihi ( H . kauaiensis) as a “high.
3-noted, slightly descending tjeutjewjew or reed-
warbler-like series’’ is incomprehensible and must I
ORNITHOLOGICAL LITERATURE
193
have been based on the wrong recording. He makes
Du mention of the mewing gnatcatcher-like calls of
the three Amakihis although they are among the
ini st frequently heard sounds in Hawaiian forests.
The Endnotes deal briefly with last-minute
axonomic and nomenelalural changes made by
:e organizations that oversee such matters, and
provide a few additional notes on identification.
The lists of national and international organizations
and the references overlook nearly all important
American-affiliated agencies and publications.
Finally, an Appendix, with too many errors of
nomenclature and orthography to detail here, lists
species that have gone extinct since 1800.
Ber van Perlo’s book clearly suffers from the
amhor/il lustrator' slack of personal familiarity with
the region and its birds. He acknowledges that he
owes '‘everything to the artists and writers who are
my predecessors in creating field guides” and the
statement is no exaggeration. Except for the
descriptions of published recordings of vocaliza¬
tions. the entire content of this book is derivative, a
repackaging of previously published (but unallrib-
Wcd) information, none of which was produced by
'be author himself, Consequently, this hook should
never be considered a primary source. As a quick
and handy illustrated list, it is adequate, but is
hardly the kind of field guide most birders demand.
However, the general nature -oriented traveler may
!|nd the book's compact size and abbreviated text
helplul in organizing a trip through this vast ocean
L’gion and in identifying its most common birds. —
H. DOUGLAS PRATT, Research Curator of
Birds Emeritus, North Carolina State Museum
of Natural Sciences, 1 1 West Jones Street.
Raleigh, NC 27601, USA; e-mail: dprattl4@nc.
R.com
LITERATURE CITED
Clements, J. F. 2007. The Clements checklist of the
birds of the world. Cornell University Press,
Ithaca, New York, USA.
C" L. F. and D. DONSKER (Editors). 2011. IOC World
Bird Names (Version 2.9). Princeton University-
Tress, Princeton, New Jersey, USA. http:/ /www.
'vorldbirdnames.org/
PRatt, h. d., p. l Bruner, and D. G. Berrett. 1987. A
field guide to the birds of Hawaii and the tropical
Pacific. Princeton University Press, Princeton, New
Jersey, USA . ,
Pratt, T. K. and R. L. Pyle. 2000. Nukupu'u in the
Twentieth Century: endangered species or phan¬
tom presence? 'Elepaio 60:35-41.
Rauzon, M. ]. AND H. L. JONES. 2005. First record of
the Kelp Gull and significant records of the
Glaucous-winged and Laughing gulls for the
central Pacific. Western Birds 36:296-302.
VandEKWerf, E. A., G. J. Wiles, A. P. Marshall, and
M. KNECiiT. 2006. Observations of migrants and
other birds in Palau, April-May 2005, including the
first Micronesian record ol a Richard s Pipit.
Micronesica 39:11-29.
VanderWerf, E. A., B. L. Beckfr, j. Fjizenga,
AND H. EtIZENGA. 2008. Nazca Booby Sulci grand
and Brewster’s Brown Booby Sula leucogaster
brcu'Xteri in the Hawaiian Islands and Johnston
and Palmyra atolls. Marine Ornithology 36:67-
71.
Vice, D. S., C. Kessler, D. L. Vice. G. J. Wii.es, H. D.
Pratt, J. Flores, P. Radley, N. Johnson, and C.
ACUON. In prep. New and noteworthy bird records
for the Mariana Islands, 2004-2010.
THH ATLAS OF BIRDS. DIVERSITY. BE¬
HAVIOR AND CONSERVATION. By Mike
Unwin. Princeton University Press, Princeton,
New Jersey, USA. 2011; 144 pages; many
unnumbered photographs and maps. ISBN; 978-
q_69 | . 14949-3. S22.95 (paper).— This was not the
book 1 anticipated from the title. We now have
a remarkable new perspective of the geography
of birds from geographic information system-
generated maps of bird habitats, large-scale bird
atlas and roadside survey projects, and migratory
tracks of individual birds equipped with satellite
transmitters. This information can be used to
delineate biodiversity hotspots (including those
that span international borders); document range
expansions and contractions that may or may not
be driven by climate change; and identity critical
migratory routes and stopover sites. Synthesizing
this information into a single book would make a
major contribution to our understanding ot the
status and vulnerabilities of birds. Although some
of this information is included in The Allas oj
Birds , such as maps of migration routes based on
satellite tracking or Sooty Shearwaters (Puff urns
griseus) and an Osprey {PandUm haliaetus), this
is not a major focus of the book.
The Adas of Birds is filled with maps, but these
are primarily the traditional types ol maps one
finds in ornithology textbooks or other general
books on ornithology. The goal is to provide an
overview of the biology, distribution, and conser¬
vation of birds throughout the world. Maps
illustrate the distribution of all bird Orders and a
few select families, the location of protected and
194
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 1. March 2012
unprotected Important Bird Areas (IBAs), and the
approximate location of major migratory fly ways.
Other maps serve as backdrops to show the
locations for particular examples that are de¬
scribed in capsule summaries illustrated with
photographs arrayed around the map. The maps
showing the distribution of Orders and families
are attractive and easy to read, but the IB A maps
are too small to provide more than a general sense
of the distribution of IBAs on each continent.
Many of the maps and examples were provided
by Birdlife International, providing a rich source
of information on global distribution of birds.
Many of the examples emphasize the importance
of IBAs and the conservation work of Birdlife
International and its partners. The information
typically is derived from sources in particular
countries, and the book emphasizes comparisons
of number of bird species, endemic species. IBAs,
and threatened species in different countries.
Comparisons among nations are frequent in the
text and maps, and there is an Appendix dedicated
to statistics for each country. These comparisons
are presented without sufficient discussion of how
the data may reflect the number of active birders
and ornithologists in each country, and the history
and level of support for the IB A program in
different regions. For example, the United King¬
dom may have more recorded bird species than
any other European country because of a large
number of experienced birdwatchers who fre¬
quently detect rare birds rather than because it
supports a particularly diverse array of birds.
The author was successful in achieving his
primary goal, which apparently was to produce
a well-illustrated overview of’ bird biology and
conservation, not to develop a book incorporating
new sources of geographical information on birds.
Many of the basic concepts of ornithology and
bird conservation are discussed in an accessible
and engaging style. In describing differences in
courtship displays among different species of
birds. Mike Unwin writes that “each species has
its own routine” (page 72). and he succinctly
describes passerines as “small birds that sing”
(page 60). Ravens iConms spp.) aside, that is an
accurate and memorable definition, particularly
when it is followed with a succinct description of
the passerine syrinx. Key topics such as the
evolutionary history of binds; the structure and
adaptations of leathers; and the effect of imro-
sucdtd7art'SPCCieS °n birds are summarized
•succinctly. Each topic is covered in a short essay
on a single page, complemented by a facing page
with select examples illustrated by photographs.
This provides a useful introduction to bird biology
and conservation for anyone with a general interest
in birds, and this book might be an appropriate text
for an informal course or workshop in ornithology.
It is not sufficiently comprehensive to be used as a
text in a more advanced course. Some important
topics arc not covered or are only briefly men¬
tioned. Theories about how birds navigate over
great distances are summarized in a single, brief
paragraph (page 79), and complex communal
social groups with cooperative breeding are briefly
mentioned in a single example.
The concise discussions of major areas of
biology require some simplification. This is not a
problem, but there are occasional minor mistakes.
Bird migration is almost certainly older than “the
end of the last Ice Age" (page 78). “AnisodactyT
is defined incorrectly on page 60, but correctly
on page 66. The “semi-plume (contour)" feather
illustrated on page 18 appears to be a contour
feather with a downy base, not a semiplume feather
with only downy barbs. Careful editing of the
manuscript would have caught these and other
minor problems. Careful review would have also
prevented mislabeling of some illustrations. The
photographs of “African Spoonbill" and "Sacred
Ibis” on page 49 appear to be photographs ot
Roseate Spoonbill ( I* law lea ajaja) and White Ibis
(Eudocimus a I has), respectively.
Mike Unwin deftly manages the complexities ot
shifting avian taxonomy resulting from molecular
studies, describing the status of particular taxo¬
nomic groups (such as New World vultures) in both
traditional and revised taxonomies. The discus¬
sions of different Orders of birds include this
perspective except for the section on passerines,
which docs not mention molecular evidence ot
convergent evolution of distantly related passerine
lineages in Australia and on other continents. The
complexities of passerine taxonomy are probably
beyond the scope of this book, however.
The final chapters on global threats to bird- and
international efforts to save birds and then
ecosystems provide a good overview lor anyone
interested in setting personal priorities lor bird
conservation. The descriptions of conservation
success stories (pages 122-123) are particularly
effective. The sections on bird conservation, along
with the accessible introduction to some basic bird
biology, makes the book worthwhile for amatem
naturalists and conservationists. — ROBERT A
ORNITHOLOGICAL LITERATURE
195
ASKINS, Katherine Blunt Professor of Biolo¬
gy. Connecticut College, New London. CT
06320, USA: e-mail: raask@conncoll.edu
THE COMPLETE GUIDE TO FINDING THE
BIRDS OF AUSTRALIA. Second Edition. By
Richard Thomas. Sarah Thomas, David Andrew,
and Alan McBride. CSIRO Publishing, Col ling-
wood, Victoria, Australia. 2011: 463 pages, 28
black-and-white and 64 color photographs, and 77
maps. ISBN: 978-0-643-09785-8. USD 42.95
(paperback). — This excellent book is an expanded
and updated version of the book by Richard and
Sarah Thomas published in 19% (Frogmouth
Publications. Oakington, England. 280 pages), which
'Ct the standard for bird finding in Australia. This
new edition with its added two highly experienced
birdwatcher authors will once again set die standard.
The book has a section entitled ‘States and
Territories’ that presents hireling sites by state starting
with Victoria in southeastern Australia, then proceeds
tunher south to the island-state of Tasmania and then
continues counterclockwise through New South
Aales, the Australian Capital Territory, Queensland,
Northern Territory, Western Australia, and South
Australia. This edition has an added chapter with site
guides to ‘Australia's islands and external territories.'
which include such far Hung places as Lord 1 lowe,
Christmas, and Macquarie islands.
The coverage of each stale begins with a map of
die state with the areas covered demarcated (e.g.. for
Victoria: Melbourne area. Southwestern Victoria,
«e,i and numerical reference to each site discussed
"i the text. The introductory material includes a list
"* endemic species and bird specialties of the state.
Then follows a detailed examination of each site, in
many eases including a map. Each site section
includes a list of key species, and in the text the bird
names are printed in bold face, w hich makes finding
a particular species in the text easy. The site guide
descriptions provide names, telephone numbers,
e-mail addresses, or web sites of landowners or
government offices that need to be consulted prior to
' •siting and, where prudent, warn of potential threats
le-g» at Fogg Dam Conservation Reserve in the
Nonhem Territory: “(beware of crocodiles and
‘makes)’' (page 120). Directions arc clear and
fonci.se. For the areas that 1 know best (Tasmania,
pans ot Western Australia, and the Alice Springs
•trea) I found the directions excellent. 1 here is also a
chapter on pelagic hireling w ith internet sites, e-mail
addresses, and phone numbers provided to facilitate
lining up pelagic trips. A substantial portion of the
book (pages 201-393) is a section entitled ‘Bird
Finder Guide.’ which includes a section of 64 color
photographs of Australian birds. The photographs
really make you want to drop everything and head
for Australia. The bird finder guide text presents a
paragraph (some short, some long) on each ol the
70IH- species that occur in Australia (excluding
vagrants and introduced species, which are covered
in appendices).
The species are presented in taxonomic order
and for each family there is a brief presentation of
interesting features of its Australian species. Each
species account includes the range and status, and
in many cases references the relevant sections ot
the site guides. Appendices include, in addition to
vagrants and accidentals and introduced species,
a glossary of vegetation, landscape, and more
general terms such as 'platelet,' a circular scrape
made by buttonquail ( Turnix spp.) while feeding
in litter. A final appendix is a directory that deals
with planning a trip, timing, arranging transport,
accommodations, climate, and various hazards, as
well as equipment such as CDs and field guides
and important telephone numbers and web sites in
each stale that might be useful. The three indices
cover common names, scientific names, and sites.
This book is loaded with essential information for
anyone planning to soil out Australian birds on their
own, or planning research on a specific group ol birds
or in a particular area. Much has changed in the world
of bird watching in Australia in the 1 5 years since the
first edition of this book originally became available.
The increase in communications and the ease of
retrieving information due to advances in internet,
cell phones, and global positioning system technol¬
ogy has expanded the horizons of bird watching and
facilitated field research. The intensifying of Hoods
and droughts in recent years, presumably a result
of global wanning, has changed many Australian
landscapes. The tw-o new authors of this edition have
revisited 90% of die original sites and many of the
changes that have occurred are reflected in this new
edition. This is a comprehensive guide, well-written
and well-illustrated. 1 cannot imagine planning a trip
to Australia and not having a copy ot this book.
WILLIAM E. DAVIS JR., Professor Emeritus.
Boston University. 23 Knollwood Drive, East
Falmouth. MA 02536. USA; e-mail: wedavisl 1 @
gmail.com
196
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 1. March 2012
ECOLOGY, CONSERVATION, AND MAN¬
AGEMENT OF GROUSE. Edited by Brett K.
Sandercock, Kathy Martin, and Gemot Segelhacher.
Studies in Avian Biology Number 39. University of
California Press, Berkeley, USA. 2011: xvi and 358
pages. ISBN 978-0-520-27006-0. S70.00 (cloth). —
This attractive Volume resulted from the 1 1"‘
International Grouse Symposium held in 2008 in
Whitehorse. Yukon, Canada. Forty-three manu¬
scripts were submitted of which 25 survived peer
review (61 reviewers are identified). The material is
presented in 25 chapters (76 different authors)
separated into four sections (Spatial Ecology,
Habitat Relationships, Population Biology, and
Conservation and Management). Eight species of
grouse (Tctraoninae) are included: four species of
prairie grouse, three ptarmigan, and one forest
grouse. Only two chapters originate outside of
North America (France) and the Volume is not
overly representative of grouse species throughout
their Holarctic distribution. Compounding the
limited view of the distribution of grouse to North
America, five papers originate from work in
Kansas, three each from Idaho and Nebraska, (wo
each from California and the Dakotas, and one each
from Alaska. Alberta, British Columbia/Manitoba,
Colorado, Nevada, Oklahoma, Texas, and one is an
overview ot habitat models for prairie grouse. This
is mostly a synopsis of grouse research in western
North America. Despite the locus on prairie grouse
(19 of 25 chapters) in North America, the subject
material is quite broad and the papers use a wide
range of modem methodology.
Modeling was explicitly used in 18 chapters as
was radiotelemetry while implants of testosterone
(# 14), molecular genetics (# 21), stable isotopes
(# 21). and transplants (# 22) were used in one
chapter each. Response to hunting is reported in
three chapters (#s 23, 24, and 25) and Adaptive
Harvest Management was examined in one (# 25).
Etfects of anthropogenic disturbances, not includ¬
ing hunting, are mentioned in three chapters (#s 5,
19, and 20). Thus, there is ample reference to
well-tested techniques and exploration of evolv¬
ing approaenes.
The Volume is heavily slanted toward rese
on Greater Prairie-Chicken (Tympanuchus
P'do) and Greater Sage-Grouse (Centroce
urophasiamts), each with eight separate chap
his probably reflects recent and current resea
Distant second place with two chapters each
rZTp Pra,"c'Chickcn ('/: pallidicinctus)
Rock Ptarmigan (Lagopus muta). Only Gre;
Sage-Grouse and Lesser Prairie-Chicken are ol
major immediate conservation concern as both an
Candidates for T or E listing in the United State*
while the former has been listed as Endangered
in Canada. However, grouse as a group with sev
eral exceptions have been generally negative!}
impacted by habitat fragmentation and loss acres*
their collective distribution.
The information in Studies in Avian liiolog \
Number 3V has general application for a variety
of species dependent upon native prairies and
sagebrush (, Artemisia spp.) steppe. The impor¬
tance of landscape scale is emphasized in the
section on Spatial Ecology while how habitat
affects nest success and brood survival is explored
in the section on Habitat Relationships. These are
important issues for maintenance of grouse
populations.
It is difficult to focus on all chapters in this
Volume hut the chapter by Kalerand Sandercock
on success of a transplant of Evermann's Rock
Ptarmigan (L. in. evermanni) to an isolated island
in the Aleutian Archipelago where the species had
been extirpated should be of interest to population
biologists. The behavior (and nest success and
production of young) of newly translocated hens
was similar to that of established hens resulting
from transplants in prior years. This work
suggests that translocations of non-migratory land
birds to former habitats on isolated islands, once
causes of local extirpation have been resolved,
can be successful and have great potential using
wild-trapped stock. Many populations ot grouse
are non-migratory and. because of habitat loss and
fragmentation, may have been extirpated from
former habitats. Provided suitable habitat can be
secured and managed, it is possible that popula¬
tions can he re-established.
The reality of grouse biology is that habitat
(mentioned in at least 18 of 25 chapters) is most
important followed by nest success and survival
of chicks to recruitment into the subsequent
breeding population. These factors are nicely
covered and new data are presented. I was also
impressed with the discussion ot hunting
although the data from California and Nevada
do not nicely mesh. Hunting can be addin-e
mortality or the effects can he compensatory of
not be adequately measured. Clearly, hunting i'1
October can affect and depress grouse popula¬
tions. Use of Adaptive Harvest Managetnen'
(AHM) has been used for waterfowl under th.u
specific name and for changes in hunting
ORNITHOLOGICAL LITERATURE
197
regulations for grouse without being labeled as
AHM. Trial and error comes to mind.
The chapter by Oyler-McCance ct al. on global
climate change using White-tailed Ptarmigan (L
leucum) as a vehicle is novel and explores new
approaches. The data are presently unclear and it
is not known which of several variables arc
inrolved with the apparent changes over a 70+
;.earpenod. It is of interest that population size in
ihe area studied over this period has not changed
drastically.
I was unable to attend the 1 1th International
Grouse Symposium and now wonder what I missed
in the presentations (papers) that did not make it
into Studies in Avian Biology Number 39. Research
on species of grouse has contributed to science on
many fronts. As this volume demonstrates, grouse
remain ideal research subjects to explore a wide
variety of topics important to ornithologists. 1
recommend this Volume to everyone interested in
grouse or emerging techniques for examining
processes that affect population biology. It is
remarkably well organized and free of obvious
errors.— CLA1T E. BRAUN. Grouse Inc., 5572
North Ventana Vista Road, Tucson. AZ 85750
USA; e-mail: sgwtp66@gmail.com
THE WILSON JOURNAL OF ORNITHOLOGY
Editor
CLAIT E. BRAUN
5572 North Ventana Vista Road
Tucson. AZ 85750-7204
E-mail: TWILSONJO@comcast.net
Editorial Board
RICHARD C. BANKS
JACK CLINTON EITNIEAR
SARA J. OYLER-McCANCE
LESLIE A. ROBB
Editorial
Assistant
NANCY J. K. BRAUN
Review Editor
MARGARET A. VOSS
Penn State Erie
The Behrend College
4205 College Drive
Erie, PA 16563, USA
E-mail: mavl l@psu.edu
GUIDELINES FOR AUTHORS
Please consult the detailed "Guidelines for Authors” found on the Wilson Ornithological Society web site
(http://www.wilsonsociety.org). All manuscript submissions and revisions should he sent to Clait E. Braun.
Editor. The Wilson Journal of Ornithology , 5572 North Ventana Vista Road. Tucson. AZ 85750-7204. USA.
The Wilson Journal of Ornithology office and fax telephone number is (520) 529-0365. The e-mail address is
TWilsonJO@comcast.net
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Notify the Society immediately if your address changes. Send your complete new address to Ornithological
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should be sent directly to the Editor.
MEMBERSHIP INQUIRIES
Membership inquiries should be sent to Mark E. Deutsch lander. Department of Biology, Hobart and William
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THE JOSSELYN VAN TYNE MEMORIAL LIBRARY
The Josselyn Van Tyne Memorial Library of the Wilson Ornithological Society, housed in the University ol
Michigan Museum of Zoology, was established in concurrence with the University of Michigan in 1930. Until
1947 the Library was maintained entirely by gifts and bequests of books, reprints, and ornithological magazines
from members and friends of the Society. Two members have generously established a fund for the purchase
of new books; members and friends are invited to maintain the fund by regular contribution. The fund is administered
by the Library Committee. Jerome A. Jackson, Florida Gulf Coast Univeristy, is Chairman of the Committee. The
Library currently receives over 200 periodicals as gifts and in exchange for 77 te Wilson Journal of Ornithology. I or
infonnation on the Library and our holdings, see the Society's web page at http://www.wilsonsociety.org. 3Vith the
usual exception of rare books, any item in the Libraiy may be borrowed by members of the Society and will he sent
prepaid (by the University of Michigan) to any address in the United States, its possessions, or Canada. Return
postage is paid by the borrower. Inquiries and requests by borrowers, as well as gifts of books, pamphlets, repnntv
and magazines, should be addressed to: Josselyn Van Tyne Memorial Library-. Museum of Zoology, The University
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be sent to the Treasurer.
This issue of The Wilson Journal of Ornithology was published on 14 March 2012.
Continued from outside back cover
119 Reproductive life history traits of the Yellowish Pipit ( Anthus lutescens)
Maikon S. Freitas and Mercival R. Francisco K
127 Nesting performance of Peregrine Falcons in Colorado, Montana, and Wyoming, 2005-2009
James H. Enderson, Robert J. Oakleaf, Ralph R. Rogers, and Jay S. Sumner
133 Reproductive success of the Creamy-bellied Thrush in a southern temperate zone
Andrea Astie and Natalia Luchesi
139 Flange color differences of brood parasitic Brown-headed Cowbirds from nests of two host species
Rebecca Croston, Christopher M. Foma, Sacha K Heath, and Mark E. Hauber
146 Avian mortality associated with a volcanic gas seep at Kiska Island, Aleutian Islands, Alaska
Alexander L. Bond, William C. Evans, and Ian L. Jones
Short Communications
152 Food habits of two fork-tailed swifts in Venezuela
Charles T. Collins and Betsy Trent Thomas
158 Observations on Zugunruhe in spring migrating Eared Grebes
Andre Konter
162 Aromatic plants in Eurasian Blue Tit nests: the ‘Nest Protection Hypothesis’ revisited
Barbara A. Fires, Anabela F. Belo, and Jodo E. Rabaga
166 Nesting of the Cinereous Warbling Finch ( Poospiza cinerea) in southeastern Brazil
Uschi Wischhoff, Fernando Marqucs-Santos, and Marcos Rodrigues
169 Description of eggs, nest, and parental care of the Smoky Bush Tyrant {Myiotheretes fumigatus )
from Ecuador
Tadeusz Stawarczyk, Marta Borowiec, Harold F. Greeney, and Jose T. Simbana
1 3 Nest, eggs, and nest placement of the Brazilian endemic Black-bellied Seedeater
( Sporopbila rnelanogaster)
Cristiano Eidt Rovedder and Carla Suertegaray Fontana
1 7 Breeding of the Brown Creeper ( Certhia americand) in Central America
Carlos Funes, Oscar Bolafws, and Oliver Komar
' l) Effects of parasitism by Brown-headed Cowbirds may persist into post-fledging
Sean M. Peterson, Henry M. Streby, and David E. Andersen
183 Evidence of double brooding by Black-bellied Whistling-Ducks
J. Dale James, Jonathan F.. Thompson, and Bart M. Ballard
' 85 First case of renesting after brood loss by a Greater Prairie-Chicken
Lance B. McNew and William J. White
'88 Do Sora nests protect Red-winged Blackbirds from Marsh Wren predation?
LeanneA. Grieves and Scott Forbes
' -'1 Ornithological Literature
Margaret A. Voss, Book Review Editor
The Wilson Journal of Ornithology
(formerly The Wilson Bulletin)
Volume 124, Number 1 CONTENTS March 2012
Major Articles
1 The Northern Black Swift: migration path and wintering area revealed
Jason R Reason . Carolyn Gunn, Kim M. Potter, Robert A. Sparks, and James W. Fox
9 Duration and rate of spring migration of Kirtland's Warblers
David N. Ewert, Kimberly R. Hall, Joseph M. Wunderle Jr., Dave Currie, Sarah M. Rockwell.
Scott B. Johnson, and Jennifer D. White
1 5 A new area of endemism for Amazonian birds in the Rio Negro Basin
Sergio H. Borges and Josi M. C. Da Silva
24 Grassland bird community response to large wildfires
Anthony J. Roberts, Clint W. Boal, David B. Wester, Sandra Rideout-Hanzak, and Heather A. Whitlaw
31 Arthropod abundance and seasonal bird use of bottomland forest harvest gaps
Christopher E. Moorman, Liessa T. Bowen, John C. Kilgo, James L. Hanula, Scott Horn, and
Michael D. Ulyshen
40 Seasonal variation in shorebird abundance in the State of Rio Grande do Sul, southern Brazil
Angelo L Scherer and Maria V. Retry
51 Plasticity of habitat selection by Red-backed Shrikes ( Lanins collurio) breeding in different landscapes
Federico Morelli
57 Territory distribution and habitat selection of the Serra Finch ( Embernagra longicauda) in Serra do
Cip6, Brazil
Guilherme H. S. Freitas and Marcos Rodrigues
66 Foraging over Sargassum bv western North Atlantic seabirds
Mary L. Moser and David S. Lee
73 Male Common Loons signal greater aggressive motivation by lengthening territorial yodels
John N. Mager III, Charles Walcott, and Walter H. Riper
81 Territorial fidelity to nectar sources by Purple-throated Caribs, Eulampis jugularis
Vinita Gowda, Ethan J. Temeles, and W. John Kress
87 Breeding and foraging variation of the Plush-crested Jay (Cyanocorax chrysops) in the Brazilian
Atlantic Forest
Angelica Maria Kazue Uejima, Andrea Larissa Boesing, and Luiz dos Anjos
96 Sexual selection and mating chronology of Lesser Prairie-Chickens
Adam C. Behney, Blake A. Grisham, Clint W. Boal, Heather A. Whitlaw, and David A. Haukos
1 06 Lek behavior of the Plovercrest ( Stephanoxis labtndi, Trochilidae)
Marco Aurelio Pizo
1 13 Nest survival, phenology, and nest-site characteristics of Common Nighthawks in a New Jersey Pine
Barrens grassland
Michael C. Allen and Kimberly A. Peters
Continued on inside back cover
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ONTISPIECE. Fledgling Northern Pygmy-Owls ( Glaucidium gnoma ) recently provisioned with a shrew {Sore x sp.),
Feton County. Montana, USA. Northern Pygmy-Owls exhibit bi-parental care during the early post-fledging period. Males
attend young for 3 1 to 34 days after fledging, whereas females attend young for shorter and more variable lengths of time (9
to 30 days after fledging). Photograph courtesy of © Daniel J. Cox/NaturalExposures.com
'The Wilson Journal
of Ornithology
Published by the Wilson Ornithological Society
VOL. 124, NO. 2 June 2012 PAGES 199-428
The Wilson Journal of Ornithology 124(2): 199-207, 2012
POST-FLEDGING ECOLOGY OF NORTHERN PYGMY-OWLS IN THE
ROCKY MOUNTAINS
GRAHAM G. FRYE1 - 1 AND HARRY R. .IAGEMAN2
ABSTRACT. — We investigated the post- Hedging ecology of the Northern Pygmy-Owl ( Glaucidium gnoma ) at two study
areas in the Rocky Mountains of Montana and Idaho from 2002 to 2009. Wc observed 16 successful nesting attempts that
fledged from two to seven young. Fledging dates ranged from I 8 June to 5 August and all nests were vacated within a 2-day
period. Post-fledging behavioral data were collected regularly from Hedging through initiation of natal dispersal from five
radiomarked family groups and opportunistically from three additional family groups Post-Hedging movement data were
collected from eight family groups and two males that were suspected of nesting. Adults attended broods for 9 to 30 days
(females) and 31 to 34 days (males) postfledging, after which they were not observed associating with their young. Young
remained within the natal territory fur I to 10 days following departure of adult males, after which they abruptly initiated
natal dispersal. Areas used by family groups during the post fledging dependency period ranged from 34.6 to 94.5 ha.
Family groups were active throughout the day, hut activity was notably more intense during crepuscular periods. Our
earliest observations of young hunting occurred 9 days after Hedging and 47% of all fledgling hunting attempts observed
(» - 75) were successful. Adults and fledglings used vocalizations in contexts consistent With previous descriptions with
the exception of an undcscribcd two-note vocal i/at inn that appeared to function as a contact call preceding prey deliveries.
Received 6 August 2011. Accepted 0 December 2011.
The post-fledging period is a crucial stage in
the life history of birds. Fledglings develop the
skills necessary for foraging (Weathers and
Sullivan 1989. Bustamante 1993), (light (Busta¬
mante and Hiraldo 1989. Bustamante 1993), and
predator avoidance (Weathers and Sullivan 1989)
during this period, as well as acquire the energy
reserves necessary for migration or dispersal
Rocky Mountain Front Institute of Natural History . 226
6" Avenue NE. Choteau. MT 59422. USA.
Department of Fish and Wildlife Sciences. University of
Idaho. Moscow. ID 83843. USA.
Current address: Department of Biological Sciences.
Boise State University, Boise, ID 83725, USA.
4 Corresponding author; e-mail: ggfrye@rmf-inh.org
(Wood el al. 1998). Adults provide fledglings
with food (e.g.. Buitron 1988. Ogden and Stutch-
bury 1997) and protection from predators (e.g.,
Greig-Smith 1980. Sergio and Bogliani 2001),
w'hile serving as models for adaptive behavior
(Galef and Laland 2005).
Relatively few forest-nesting bird species have
been studied during the post-fledging period
because of the difficulty of collecting data from
mobile family groups in forested environments
(Ogden and Stutchbury 1997. Tarwater and
Brawn 2010). Most post-fledging investigations
have focused on estimating mortality, which can
be an important factor in recruitment anil is often
high (Lack 1954). For example, the mortality rate
of fledgling Burrowing Owls (Athene cunicu/aria)
199
200
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 2. June 2012
was 43% during the post-fledging period, ac¬
counting for two-thirds of all mortality observed
in the first year of life (Davies and Restani 2006).
Similarly, post-fledging mortality of Ferruginous
Pygmy-Owls ( Glaucidium hrasilianum ) was 37%
(Proudfoot and Johnson 2000). However, mortal¬
ity is only one aspect of the post-fledging ecology
of birds. The developmental and behavioral
components of a species' post-fledging strategy
also have direct implications on individual fitness.
For example, extent of parental investment affects
survival and recruitment of offspring, as well as
survival and future reproduction of the parents
(Williams 1966. Trivers 1972, Roff 1992). Simi¬
larly, tradeoffs involved in learning to forage
independently while avoiding predators place
strong selective pressure on fledglings during the
post-fledging stage (Lack 1954. Arnold and Wade
1994). Post-fledging strategies vary among species,
but their characteristics are seldom explicitly
described.
The Northern Pygmy-Owl is among the least
studied of North American strigids and little is
known about the post-fledging ecology of the
species. Our objectives were to describe: (I)
behaviors, (2) movements, and (3) developmental
patterns of family groups of the Northern Pygmy-
Owl from fledging through initiation of natal
dispersal.
METHODS
Study Areas. — We conducted research on two
study areas in the Rocky Mountains of Montana
and Idaho. One study area was in the Lewis and
Clark National Forest adjacent to the Rocky
Mountain Front in northern Montana (47 52' N,
112 41' W). and encompassed the western
portions of Teton, Pondera, Lewis and Clark,
and Glacier counties. Elevations ranged from
~ 1,300 to 2,500 m and topographic relief
was extreme. Average annual precipitation at the
nearest station of record (Gibson Dam; 1,399 m
asl) was 43.2 cm and average annual snowfall was
185.4 cm. The average daily high and low
temperatures in January were 0.4 and -10.8 C,
respectively. The average daily high and low
temperatures in July were 26.1 and 8 2 C
respectively (NOAA 2011). Vegetative ’ cove^
was predominately lodgepole pine (Pinas con -
tortd) and Douglas-fir (Pseudotsaga menriesii )
forest interspersed with stands of quaking aspen
(/ opulus tremuloides). Engelmann spruce (Picea
engelmannii) was common in more mesic areas.
and subalpine fir ( Abies lasiocarpa) occurred at
higher elevations. Riparian vegetation was pre¬
dominately black cottonwood ( Populus tricho-
ctirpa ), willow {Salix spp.). alder (Alnus spp.), and
silverberry ( Elaeagnus commutata).
The second study area was in north-central
Idaho (46 49' N, I 16 54' W) and included
portions of Latah, Benewah, and Clearwater
counties. Ownership was —50% federal (Clear¬
water National Forest) and 50% state and private
industrial forest lands (mostly Potlatch Corpora¬
tion). Elevations ranged from -500 to 1.600 m.
The study area was transitional foothills between
the Palouse Prairie to the west and the Rocky
Mountains to the cast, and had more moderate
topography than the Montana study area. The area
was wanner and more mesic than the Montana
site with mixed mesic forests predominating.
Average annual precipitation at the nearest station
of record (Potlatch; 84 1 .2 m asl) was 62.2 cm and
average annual snowfall was 1 14.8 cm. The
average daily high and low temperatures in
January were 2.2 and -6.1 C, respectively. The
average daily high and low temperatures in July
were 28.2 and 7.6 C, respectively (NOAA 201 1).
Grand fir ( Abies grand is) was the dominant
conifer, but Douglas-fir and western larch (Larix
occidcntalis) were common stand associates on
xeric south-facing aspects. Riparian communities
were dominated by western red cedar (Thuja
plicata), alder, and willow.
Field Procedures. — We recorded fledging date
and brood size at all successful nests located during
the study (n 1 6). Fledging was directly observed
at one nest, occurred within a I -day period between
visits at 13 nests, and was estimated based on
developmental stage of fledglings at two nests. We
used tail length and flight ability of fledgling1' as
criteria for estimating developmental stage. Obser¬
vations of known-age fledglings indicated that at
5-6 days after fledging rectrices were —25-30% of
full length and flight ability was markedly
improved relative to the first day after fledging,
rectrices were -50% of full length at 10 days, and
rectrices were full grown by 18-20 days. Brood
size was estimated based on counts 1-2 days prior
to fledging at four nests, within I day after fledging
at 10 nests, and within 8 days after fledging at two
nests. Brood reductions could have occurred prior
to counts; therefore, brood sizes are minimum
estimates.
We attached radio transmitters to both adults
from each of four family groups occupying
Frye and Jageman • NORTHERN PYGMY-OWL POST-FLEDGING ECOLOGY
201
TABLE 1. Reproductive data and post-fledging observation effort for Northern Pygmy-Owl family groups in the
Rocky1 Mountains of Montana and Idaho.
Family group"
Year
Observation (hrs)
Radiomarked owls
Breeding status
Fledging date
Brood size
MT-I
2004
26.5
Male, female, two young
Breeding
28 Jun
7
MT-2
2003
45.6
Male, female, two young
Breeding
8 Jul
4
MT-3
2006
46.7
Male, female, one young
Breeding
15 Jul
3
MT-4
2005
38.1
Male, female
Breeding
5 Aug
5
MT-5
2005
0
None
Breeding
8 Jul
4
MT-6
2005
0
None
Breeding
18 Jul
4
MT-7
2002
0
None
Breeding
10 Jul
3
MT-8
2003
0
None
Breeding
25 Jul
6
MT-9
2006
0
None
Breeding
5 Jul
6
MT-10
2002
0
None
Breeding
23 Jul
3
MT-I 1
2005
0
None
Breeding
28 Jul
5
ID-1
2008
14.4
Male
Breeding
1 Julh
3
ID-2
2008
4.9
Male, female
Breeding
24 Jun
4
ID-3
2009
7.5
None
Breeding
28 Jun
5
ID-4
2008
0.9
Male
Breeding
1 Julb
3
ID-5
2007
0
Male
Breeding
18 Jun
2
ID-6
2007
0
Male
Suspected
Unknown
Unknown
ID-7
2007
0
Male
Suspected
Unknown
Unknown
a MT = Montana. ID = Idaho.
Fledging date estimate based on developmental stage of young when first observed.
distinct breeding territories in Montana (MT-1,
MT-2, MT-3, MT-4; Table I). One fledgling was
radiomarked in one of these family groups (MT-3;
Table 1) and two fledglings were radiomarked in
each of two family groups (MT I and MT-2;
Table I). Both adults were radiomarked in one
family group in Idaho (ID-2; Table I). The adult
male from three additional family groups (ID I,
ID-4. ID-5; Table 1) and two adult males
suspected of breeding (ID-6. ID-7; Table 1 1 were
also radiomarked. We assigned ‘suspected breed¬
ing’ status to ID-6 and ID-7 based on the spatio-
temporal location patterns of these owls. Both of
these owls began concentrating their space use at
approximately the same time as locations of pre¬
nesting owls in Idaho were concentrated near nest
areas. The timing and duration of use for these
areas (hereafter 'concentrated-use areas’), which
were similar in size to the breeding season home
ranges of ow ls known to be nesting (HRJ. unpubl.
data), coincided with the timing and duration of
the nesting/post-fledging periods for owls known
to have nested. We did not radiomark fledglings
in Idaho. Fledglings that were not radiomarked
were located by listening for vocalizations.
Family groups were randomly selected for this
investigation, but previously monitored individu¬
als and territories were excluded from the
selection process. Each radio-marked family
group was tracked for one breeding season
between 2003 and 2009 (Table 1).
We captured owls with mist nets, balcha-tri
traps, bow nets, or by hand at nest cavities. Adults
were captured and radiomarked during or prior
to nesting. Young were radiomarked within 6 days
after fledging. Very High Frequency (VHF) trans¬
mitters weighing 1. 4-2.2 g (<3% body mass;
Holohil Systems Ltd.. Carp, ON. Canada and
Wildlife Materials Inc., Carbondale, IL, USA) were
affixed using back pack-style harnesses constructed
of braided Dacron cordage. All owls studied in
Montana were also marked with color bands to aid
in individual identification.
We regularly observed five family groups (MT-
1. MT-2, MT-3. MT-4, ID-1) for periods ranging
from 0.25 to 5.25 hrs (x = 2.03 hrs, n = 91)
during at least three visits per week from date of
fledging until young began to disperse from their
natal territory'. Observation periods were stratified
so that morning (30 min before sunrise to 1000
hrs), mid-day (1001 to 1600 hrs), and afternoon/
evening (1601 hrs to dark) were approximately
evenly sampled. Additional behavioral data were
gathered opportunistically from three family
groups (ID-2, ID-3. ID-4: Table 1). Behavioral
data were obtained by observing owls through
binoculars (from -10-80 m distant) and record¬
ing descriptions, times , and durations of activities
202
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 2. June 2012
TABLE 2. Timing of post-fledging events, estimated size of post-fledging range, and maximum distance from nest for
Northern Pygmy-Owl family groups in the Rocky Mountains of Montana and Idaho. Blank spaces indicate insufficient data.
Family group-
Last female
anendaneeh
Last male
attendance6
Male return to
nest stand’1
Female return
to nest stand'1
Initiation of
natal dispersal1’
Post-fledging
range (nl
Max diu
lo nest
MT-1
12
32
39
45
42. 42
91.8 ha (24)
1.967 m
MT-2
22
34
45
57
35, 37
92.5 ha (23)
3.340 m
MT-3
19
34
50
38
40.2 ha (28)
2.522 m
MT-4
10
31
37
42
34.6 ha (21)
943 m
ID-1
30
34
Did not return
e
38.8 ha (23)
1,200 m"
ID-2
9
40
ID-4
48
MT = Montana. ID = Idaho.
Number of days after fledging.
d Maximum distance that family groups were observed front nest sites,
‘ Exact nest location unknown; location approximated on basis of first location that young were observed
Male moved to new area at end of post-fledging period and did not return to nest stand during life of transmitter.
in notebooks. We monitored five adults and two
fledglings throughout the night for 1-3 nights
each (10 nights total). We recorded owl locations
every 2 hrs on those occasions.
Data Analysis. — Date ranges (number of days
after fledging) represent the earliest and latest dates
on which specific events or behaviors were
observed. The observation dates prior to and
following an event were averaged to approximate
the actual date il an event occurred between visits
from an observer (mean lime between observation
periods = 2.27 days, n = 78), Distances were
measured in ArcMap 9.3.1 (ESRI 2008). We
calculated the size of areas used by family groups
between Hedging and initiation of natal dispersal
(hereafter ‘post-fledging ranges’) in ArcMap 9.3.1
with the Home Range Tools extension (100%
Minimum Convex Polygon-Fixed Mean method:
Rodgers et al. 2007). We use ‘males’ in reference
to breeding males and ‘females’ in reference to
breeding females. Gender of adults was classified
on the basis ot behavior (vocalization and copula¬
tion) and presence/absence of brood patch. We did
not classify gender of young due to the lack of non-
invasive criteria for the species (Pyle 1997).
RESULTS
Movements and Family Group Association
Fledging dates in Montana ranged from 28 June
5 August (// = 1 1 ). Fledging dates in Idaho rani
from 18 June to 1 July (n = 5). We direc
observed young exiting the nest cavity at one ne
* of seven ow|s 1,1 'ha* brood left the nest cav
within a 6.5-hr period. The seventh owl did r
leave the nest cavity until 23-29 hrs after the fir
Brood size ranged from two to seven (median
n — in).
Young owls remained within —100 m of each
other from the time of Hedging until the end of the
dependency period, and were observed in groups
with individuals spaced 0 to 30 m during 69% of
observation periods (n = 91). Allopreening was
observed between young during three observation
periods, and between adults and young during
four observation periods.
Adult females attended young for 9 to 30 days
after Hedging (Table 2). Females provisioned
young with prey items that were delivered by
males and prey they captured (54 and 46% of
temule prey deliveries, respectively, n = 41).
Males most often delivered prey to females and
only rarely delivered prey directly to young
during this period (88 and 12% of male prey
deliveries observed during female attendance,
respectively; n = 25).
Females left their family groups 9 to 30 days
after Hedging and were not observed associating
with the young again. Family groups were 225 to
1.178 m from nests when females terminated
association with them. Females moved within
their home ranges independently after departing
family groups. Females used areas that did not
overlap those used by the remaining family group
members during this period with the exception of
one female for a 3-day period. We did not
observe this female associating with the remain¬
ing family group in that instance. We generally
observed males within 200 m of family groups
after females departed and prior to male depar¬
ture (84% of locations for which proximity was
known, n = 37). Males continued to attend
young until 31-34 days after fledging (Table 2).
after which they were not observed associating
with young again.
Frye and Jageman • NORTHERN PYGMY-OWL POST-FLEDGING ECOLOGY
203
Five radio-marked males (MT-1, MT-2, MT-3,
MT-4, ID-4) returned to the nest stand (850-
3,171 m distant) within 6-16 days (37-50 days
alter Hedging; Table 2). All females with active
transmitters (MT-1. MT-2, MT-4, ID-2) returned
to the nest stand 31-35 days after departing family
groups (40-57 days after fledging; Table 2).
Females relumed to the nest stand 5-12 days
later than males within territories (Table 2). Wc
observed mated pairs together shortly after
females returned to the nest stand at all but one
of these territories.
Five males that were eilher confirmed or
suspected to be breeding (ID-1. ID-2, ID-5, ID-
6. ID-7) exhibited a different movement pattern
after the post-fledging dependency period. These
males made relatively abrupt movements of 1.5-
3.2 km to areas not previously used during the
nesting season. We did not observe any of these
males returning to the nest stand (or the
concentrated-use area for the males suspected of
breeding) following their departure, but they were
only tracked for 1 to 16 days after leaving the
breeding territory because of limited transmitter
battery life.
Post-fledging ranges varied in size, as did the
maximum distance family groups were observed
from nests (Table 2). One family group (ID-1)
moved in a roughly circular pattern around the
nest site, reaching a maximum distance of
1.200 m. but returning to within 500 m. Another
family group (MT-4) was a maximum of 943 m
from the nest, but returned to within 200 m.
Family groups, with these two exceptions, moved
progressively farther from the nest during the
post-fledging period.
Independence and Dispersal. — Radio-marked
young began to move farther from brood mates I
to 8 days after males ceased associating with
family groups. It was not possible to document
complete disassociation of fledglings with certain¬
ty because of the limited number of young with
transmitters. However, the highly vocal nature of
young pygmy-owls reliably facilitated detection of
unmarked young throughout the post-fledging
period, even after males ceased attending young.
Thus, w'hen observation periods failed to yield
aural or visual evidence of additional owls, w'e
assumed fledglings had ceased associating with
one another. Radio-marked young remained within
their natal territories for I to 10 days after departure
of males (35-42 days after fledging; Table 2).
At that point, either transmitter signals were lost
( n = 2). or we documented young moving outside
of adult home range boundaries (n = 3).
Behavior and Development. — The earliest ob¬
servations of successful hunting by young occurred
9 days after Hedging. Two of six (33%) hunting
attempts during the observation period on that date
resulted in successful capture of small unidentified
Lepidoptera. Hunting attempts by young were
observed during 59% of observation periods > I hr
in duration after 12 days postfledging (n = 46).
Young used exaggerated head movements while
concentrating on potential prey and perches, at
times turning Iheir heads nearly upside dowm. The
first successful capture of vertebrate prey (a
southern red-backed vole | Clethnonomys gap-
peri |) by young was observed 14 days after
Hedging. Fledglings were successful during 47%
of observed hunting attempts (// = 75).
Young were not observed to cache prey items,
although they procured prey from adults they did
not immediately consume during 6% of prey
deliveries ( n = 80). Adults cached prey during
5% of prey deliveries ( n = 80), apparently
because fledglings did not respond to delivery
calls. The young became highly vocal, excitedly
converged on the adult, and rapidly consumed
prey during 74% of prey deliveries (n = 80).
Adults provisioned fledglings with arthropod,
avian, and mammalian prey.
The young were active during 90% of diurnal
observation periods (n = 91). Activity was
notably less intense from late morning through
mid-afternoon than during early morning and
evening hours, consisting primarily of intermittent
vocalizations and short movements (< 100 m).
Young were only observed to remain silent and
inactive >1 hr during 1 1% of observation periods
lasting SI hr (n = 72). Fledgling activity
increased during crepuscular periods. Young
made longer and more frequent movements within
or among stands in the early morning and
evening. Seventy-seven percent of hunting at¬
tempts by young In = 75) were observed during
crepuscular periods. Observations during all
nocturnal observation periods (n = 10) indicated
that owls remained in the same tree until
approximately dawn.
Fledgling vocalizations were limited to the
begging call (described by Holt and Peterson
2000), which was given repeatedly during all
observation periods in which young were active
(// = 82). The vocalizations of one fledgling often
caused others to vocalize. Periods of vocalization
204
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 2. June 2012
within a brood at times exceeded 1 hr in duration,
punctuated only by brief intervals of silence.
Adults used the ‘chitter call’, primary song (Toot
song’), and Trill calf (described by Holt and
Peterson 2000) when in the vicinity of fledglings.
An alarm call (described by Frye 2005) was also
observed on five occasions in association with
avian predators near young. A two-note call
composed of notes resembling those of the
primary song, but the second note often slightly
higher in pitch than the first, was used by males
preceding prey deliveries. Spacing between the
two notes was similar to that between notes of the
primary song, but repeated calls were spaced by at
least 8-10 sec and at times 1 min or more. These
two-note vocalizations were often given repeat¬
edly for several minutes, at limes accompanied by
trill calls, before males began using the chitter
call. The chitter call was used by both adults
during prey deliveries. We observed increased
male vocal activity (the primary song and trill
call) after return to the nest vicinity (37-50 days
after fledging; Table 2).
DISCUSSION
Synchronous or nearly synchronous Hedging
appears to be typical of Northern Pygmy-Owls.
Giese and Forsman (2003) observed all young
exiting nest cavities within a 6-hr period at four
nests on the Olympic Peninsula, Washington. Holt
and Norton (1986) observed a brood of six owls
fledge over a 2-day period in Montana. Rashid
(1999) reported a brood of three owls leaving the
nest within a 2-day period in Colorado. Fledging
was directly observed at only one nest during our
study, but observations prior to and following
fledging indicated that all successful nests for
which fledging duration was known (n = 14) were
\acated within 1-2 days of the first ow l leaving the
cavity. Nesting phenology was more advanced in
Idaho than in Montana. The Idaho study area had
milder climate with less snow cover than the
Montana site. The influence of these differences on
prey availability may explain the observed differ¬
ences in nesting phenology, as birds are thought to
time nesting to coincide with seasonal peaks in
r“lity (LaCk l954)' FledSinS ‘>“urred
rj en Junc and 1 7 July in Washington (n ~ 9;
G.ese and Forsman 2003), 5 and 6 June in western
and m '* H0lt and Norton l986>’ u"d 12
d 13 July in Colorado (n - I; Rashid 1999)
and SrSh°Ciat,‘.ln Individuals within family groups
and the role of breeding adults in attending
dependent young vary among species of forest
owls. Both adults attend Ferruginous Pygmy-Owl
broods during the post-fledging period (Proudfoot
and Johnson 2000). Flammulalcd Owls (Otto
Jlcwimeolus) exhibit brood partitioning, the young
separating into two groups, each of which is
attended by one adult (Linkhart 1984. Goggans
1986, Linkhart and Reynolds 1987). Northern
Saw-whet Owl (Aegolius acadicus) broods remain
loosely associated as a family group after fledging
and are provisioned primarily by the male and
occasionally by the female (Cannings 1993).
Female Eurasian Pygmy Ow ls (Glaucidium pas-
serinum) care for young alone for the first week
after fledging, after which the male returns and
assists in provisioning young. Eventually, the
female departs, leaving the male to attend young
alone for the remainder of the post-fledging
dependency period (Konig et al. 1995, 1999).
The attendance strategy of adults that we
observed most closely resembles that of the
Eurasian Pygmy Owl, the difference being that
both Northern Pygmy-Owl adults attended broods
prior to female departure. We observed this
strategy in all family groups for which the role
ol the female was known (n — 6). However, it is
possible that both adults attend some broods
throughout the post- fledging period. For example,
some Spotted Owl ( Sirix occidentalis) broods are
attended by both adults and some by a single adult
during the post-fledging period (Gutierrez et al.
1995). The variation that we observed in duration
o! female attendance supports this possibility. One
female attended a brood for -88% (30 days) of
the post-fledging dependency period, whereas
another attended a brood for only -21% (9 days).
Previous information on family group proxim¬
ity to nests during the post-fledging period is
limited. Holt and Peterson (2000) reported a brood
ol six young roosting 75 m from the nest 8 days
after fledging. Rashid (1999) observed two of
three fledglings from a brood in Colorado -270 in
Irom the nest 18 days after fledging. Post-fledging
movements Irom the nest varied greatly among
family groups in our study. All family groups
were substantially farther than 75 m from the nest
8 days after fledging (300-670 m). Proximity to
nests after 1 8 days was more varied (200-
2,400 m).
No previous information is available on inde¬
pendence and dispersal timing for Northern
Pygmy-Ow'ls. Our observations of provisioning
and attendance by males indicate young achieve
Frye and Jageman • NORTHERN PYGMY-OWL POST-FLEDGING ECOLOGY
205
independence simultaneous with or only slightly
before they begin to disperse from their natal
territory. Similarly, young Flammulated Owls
become independent of adults only slightly before
initiating natal dispersal (independence at 25 to
32 days after fledging, dispersal at 30 to 35 days
after fledging; Linkhart and Reynolds 1987).
Eurasian Pygmy Owl fledglings become indepen¬
dent from adults at 27-34 days (Marks et al. 1 999),
which coincides with the range of independence
dates we observed for Northern Pygmy-Owls (31 —
34 days; Table 2). Ferruginous Pygmy-Owls
disperse from their natal territory 7-8 weeks after
fledging, the young often traveling >1 km in the
first day (Proudfoot and Johnson 2000). Similarly,
our observations indicate abrupt initial dispersal
movements, assuming that signal losses were not
due to transmitter failure in our study (an
assumption we believe to be justified on the basis
of expected battery life). Young either made abrupt
movements of 965 to 2.015 m upon apparent
initiation of natal dispersal, or their transmitter
signals were lost.
Our observations of abrupt movements to new
areas by five males immediately after the post-
fledging dependency period indicate variability in
movement patterns after males stop attending
young. Radiotelemetry data collected in our study
areas between February and November suggest
large abrupt movements are uncommon for adults
during most of the year, but can occur for males
both before and after the nesting season (unpubl.
data). We hypothesize that some males shift home
ranges seasonally to facilitate breeding with more
sedentary females. Differential seasonal move¬
ments have been documented for other species of
owls. Female Boreal Owls (Aegolius funereus),
for example, will often move nomadically post-
breeding, whereas associated males remain in the
breeding territory (Wallin and Andersson 1981,
Solheim 1983. Korpimaki 1986. Ldfgren et al.
1986, Hayward et al. 1993).
Previous descriptions of diel activity patterns
during the post-fledging period are lacking, but
increased crepuscular activity of adult Northern
Pygmy-Owls has been noted during acoustical
surveys (Nobel 1990, Sateret al. 2006) and during
nest observations (Holt and Norton 1986, Rashid
1999). We observed increased vocal activity and
movements (including foraging) during morning
and evening hours. It is possible the nearly
persistent diurnal activity of young during obser¬
vation periods was stimulated by the observer’s
presence, but we do not believe that was the case.
Calls of fledglings were heard from a distance as
observers approached family groups on most
occasions, indicating they were active before our
arrival. Previous reports suggesting that Northern
Pygmy-Owls arc exclusively diurnal and crepus¬
cular were based on a lack of observed nocturnal
activity (Holman 1926, Holt and Norton 1986,
Noble 1990), rather than observed nocturnal
inactivity of radio-marked owls. Our observations
of nocturnal inactivity are consistent with previ¬
ous reports suggesting Northern Pygmy-Owls are
primarily or exclusively diurnal and crepuscular.
Contexts of most vocalizations observed in our
study u'ere consistent with those described by
Holt and Peterson (2000) and Frye (2005).
However, to our knowledge, the use of the two-
note call has not been described previously. This
vocalization appeared to function as a contact call
preceding prey deliveries.
We were unable to estimate post- fledging
mortality rates because of the limited number of
young with transmitters. We suspected mortality
of one fledgling in each of three family groups
(MT-1. MT-4, ID-3) on the basis of reduced brood
counts, but fates of those owls were unconfirmed.
Estimating rates and sources of mortality during
the post-fledging period should he a priority for
future Northern Pygmy-Owl investigations.
The patterns in post-fledging movements,
behaviors, and development we documented
advance our understanding of the ecology of this
poorly studied species. Results from our two study
areas, separated by >325 km and characterized by
different forest composition, were highly consis¬
tent. Our sample sizes were small, but the size of
post-fledging ranges, maximum distances that
family groups were observed from nests, and
estimated durations of post-fledging dependence
should aid managers in minimizing impacts on
Northern Pygmy-Owls during this critical life
history stage.
ACKNOWLEDGMENTS
We thank those who made this project possible, but
whose long list of names is impractical to include. We
especially thank volunteer field assistants T. L. Gray. S. M.
Westberg. K. K. Rogers, E. E. Fairbank. and S. L. Hahn for
long hours in helping to capture owls and collect data.
Funding was provided by the Rocky Mountain Front
Institute of Natural History. Conservation Research Foun¬
dation. Wilson Ornithological Society. Nnormss Wildlife
Foundation. University of Idaho Kvale and Norbcre/
Meiners awards. Pa/ouse Audubon Society, Clearwater
206
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 2. June 2012
National Forest. Idaho Fish and Game-Region 2, and
Potlatch Corporation. Materials and/or logistical support
were provided by W. C. Maples and the L'SFS Rocky
Mountain Ranger District. Lewis and Clark National Forest.
Marmot's Edge Conservation, and the Owl Research
Institute. G. A. Proudfoot provided valuable advice on
affixing radio-transmitters to pygmy-owls. GGF thanks
R. P. Gerhardt for inspiring a research interest in pygmy-
owls. J. L Aycrigg. C. E. Braun, E. O. Gallon. D. W. Holt.
J. A. Manning. J. S. Marks. K. L. Nicholson, G. A.
Proudfoot. K. M. Slrickler. A. G. Wells, and an anonymous
reviewer provided helpful comments and criticism on
previous versions of the manuscript.
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The Wilson Journal of Ornithology 1 24(2);208 -2 1 6, 2012
CLIMATE CHANGE DOES NOT AFFECT PROTANDRY IN SEVEN
PASSERINES IN NORTH AMERICA
LISA BAUBOCK.1 ABRAHAM J. MILLER-RUSHING,' - RICHARD B. PRIMACK,1
TREVOR L. LLOYD EVANS,- AND FRED E. WASSERMAN1 4
ABSTRACT.-Recent studies have suggested climate change could amplify the differences between arrival dates of
male and female passerines. We investigated the generality of this finding and additional questions related to protandry by
analyzing years of banding data for seven species of migratory passerines. Six species exhibited significant protandrv
with males amv.ng on average between 2 and 6 days earlier than females. Only Baltimore Orioles (Icterus galbula) did not
have significant differences between average arrival dates or males and females. The magnitude of protandrv did not
change in response to warming spring temperatures during the period of study, and none of the ecological variables
examined explained variation in the amount of protandry. Males of all species studied were significantly larger than
cmales. However, the magnitude ol size difference also did not explain the amount of protandry observed. Arrival dates of
males and termites within each species tended to follow similar trends over time and sex ratios did not change overtime for
any spec.es. Changes m sex ratios of Mourning Warblers (Geothlypis Philadelphia)- more females in Wanner years-
significantly related to mean temperature in the year of migration. Protandry may remain fairlv consis.cn. K
,m,m maKh & n“ded w f ** !»««■ 201, .
Evidence shows that male passerines tend to
arrive earlier each spring than females of the same
species, a phenomenon known as protandry
(Rubolini et al. 2004). The generality of this
pattern is still uncertain and mechanisms under¬
lying this difference have not been definitively
established although several hypotheses exist
(Morbey and Ydenberg 2001, Coppaek and Pulido
2009, Saino et al. 2010, Spottiswoode and Saino
2010).
Recent studies have suggested that climate
change could amplify the difference between male
and female arrival dates, because male and female
migratory birds may respond differently to
warming climate (Moller 2004. Spottiswoode et
al. 2006; but see Rainio ct al. 2007). Males may
be under selection to arrive as early as possible
(Crick 2004) while, for females, it may be
advantageous to remain in wintering areas until
conditions have improved (Spottiswoode et al.
-006). Thus, males could gain an advantage over
other males by arriving earlier in warmer spring
conditions, allowing them to secure better territo¬
ries. This theory leads to the prediction that highly
territorial birds should increase in protandry as
022P5°uIa Department' Bos,on University, Boston.
search c^nf1 ** ?***• Schoodic Education and
Harbor. ME 0^9 USA ^ P ° B“
a
. u. Hn.x 1770, Manomet, MA 0214S USA
Corresponding author; e-mail; few@bu.edu
temperatures warm because males may be under
greater selection to arrive earlier.
Another potential effect of changing environ¬
mental conditions is a change in sex ratios.
Observations of changing sex ratios at bird¬
banding stations may be due to changes in
wintering areas or migration routes of males and
females, particularly for species such as the
American Redstart ( Setophaga ruticilla). in which
males and females winter in different locations
(Marra el al. 1993. Nebel and Ydertherg 2005).
Differential mortality between males and females
could also cause changes in sex ratios at a given
location. Ibis could be caused by variation in
climate or other environmental changes including
habitat loss.
Our objective was to use a long-term record of
bird observations at a banding station to test three
primary hypotheses: ( 1 ) males arrive earlier than
females in spring. (2) timing of migration of
males changes faster in response to climate than
that ot females, and (3) sex ratios change in
association with changes in climate. We also
tested whether several ecological variables, in¬
cluding territoriality, habitat, wintering and breed¬
ing ranges, and number of’ clutches per season
could explain variation in the magnitude ot
protandry. the effects of climate change on arrival
times of birds, and changes in sex ratios.
METHODS
Bin! Data. The staff at the Manomet Center
(ot Conservation Sciences made observations of
208
Baubock et al. • CLIMATE CHANGE DOES NOT AFFECT PROTANDRY
209
bird arrival dates at the Center, which is on the
western side of Cape Cod Bay. Plymouth County.
Massachusetts. USA (4U 50' N. 70 30' W). This
coastal migratory route is characterized by brushy,
second growth deciduous woodland 7-10 m in
height, dominated by oak ( Quercus ) tree species,
encaceous shrubs, and thorny greenbrier (Smilax
spp.) vines. It is bordered on the cast and south by
a steep, eroding coastal bluff and on the west and
north by brushy wetlands. Average annual tem¬
perature during the period of study was 9.7 C.
and annual precipitation was 1 29.5 cm.
The Center operated between 45 and 50 nylon
mist nets ( 12 X 2.6 m, 4 panels. 36 mm extended
mesh) annually from 1970 to 2002, inclusive.
Less complete coverage and imprecise records
regarding capture effort expended were available
during the first 4 years of the observatory's
existence (1966-1969) and we excluded these
years from analysis. Each bird captured was
marked with a unique identification band, which
prevented double counting of individuals. Nets
were kept at fixed locations throughout the study.
Nets were generally operated from 0.5 hr prior to
sunrise to 0,5 hr after sunset, except for closures
during adverse weather conditions. Thus, 50 nets
open for 12 hrs equals 600 net hrs per day.
Sampling was conducted from 5 to 7 days per
week during the spring (15 Apr-15 Jun) migration
period.
The staff banded 205,454 individuals of 159
species during the study years. We considered
only passerines for which males and females
could be reliably distinguished (n = 7 species)
(Table I). We considered the first capture of a
bird as that individual's arrival date — i.e., we did
not consider repeat captures for individual birds.
We did not consider locally breeding birds,
which we identified on the basis of well-
developed brood patches or cloacal protuberanc¬
es; we did not consider spring captures of
hatching-year individuals.
The data we analyzed represented birds cap¬
tured and banded during spring migration. Indi¬
viduals from each species did not necessarily
belong to a single breeding population. Thus, w-e
reler to our data as representing migration
cohorts— i.e.. groups of birds that passed through
Manomet during spring migration. The banding
data are a subset of those used in a previous study
of migratory responses to climate change (Miller-
Rushing et al. 2008).
Climate Data. — We calculated mean monthly
temperatures for Manomet. Massachusetts by
averaging data from five weather stations within
a 20-km radius. We avoided possible microcli¬
matic anomalies that may occur at a single station
by averaging temperatures from several weather
stations (Pielke et al. 2002). Mean temperatures in
March. April, and May were significantly corre¬
lated from Wilmington. North Carolina north to
Manomet (P < 0.05 for all correlations). We
calculated the mean arrival date for each bird
species and averaged the previous 2 months’
temperatures to obtain the relevant mean temper¬
ature index for each bird. Wc obtained the
monthly minimum and maximum temperatures
from the Plymouth- Kingston weather station in
Plymouth, Massachusetts.
We obtained annual indices for North Atlantic
Oscillation (NAO) and the El Nino Southern
Oscillation (ENSO) from the National Center for
Atmospheric Research (Boulder. CO. USA; www.
cgd.ucar.edu/). These indices integrate many
climate variables over large regional areas.
Positive NAO index values correlate with south¬
erly winds in the eastern United States (Hurrell
1995). while negative values correlate with
increased precipitation in (he eastern United
States (Mauget 2006). Positive ENSO index
values correlate with relatively warm tempera¬
tures during winter and spring in the southeastern
United States, and with relatively cool tempera¬
tures in Central America, southern Caribbean, and
much of South America (Trenberth and Caron
2000). Positive ENSO index values also correlate
with relatively dry years in the southeastern
United States and with relatively wet years in
Central America, southern Caribbean, and north¬
ern South America (Trenberth and Caron 2000).
March-May temperatures at Manomet were not
correlated with NAO (/■ = 0.03, P = 0.89) nor
ENSO (/- = 0.03, P = 0.86).
Data Analysis.— Wc converted all arrival dates
from calendar dates to days after the vernal
equinox. This transformation avoided biases in
Julian or calendar dates caused by changes in
timing of the vernal equinox. We calculated the
mean arrival date separately for males and
females of each species in each year, differences
between male and female arrival, number of
males and females banded in each year, and the
ratio of males to females. A small number of birds
ol the earliest or latest arriving species may have
arrived prior to 15 April or after 15 June in
210
THE WILSON JOURNAL OF ORNITHOLOGY • Vo/. 124. No. 2. June 2012
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Baubock el al. • CLIMATE CHANGE DOES NOT AFFECT PROTANDRY
21 1
unusual years. However, for nearly all species,
less than 2°/c of birds were captured on the first 3
or last 3 days of banding. The exception was the
American Goldfinch ( Spinas tristis) for which 5c7c
of birds were caught within the last 3 days of
banding, indicating that we may have missed the
tail end of migration for this species. We believe
this is unlikely to have substantially influenced
the results.
We used linear regression to characterize
temporal changes in mean arrival dates for males
and females of each species, difference in mean
arrival dates between males and females, and
the ratio of females to males. These regressions
indicated whether males or females arrived
earlier, later, or no differently over time, and
whether the amount of protandry or the ratio of
females to males changed over time.
We used reverse stepwise regression to test the
relationships of the mean arrival dates of males
and females, differences in mean arrival dates,
and the female-to-male ratio of each species with
three climate variables: (1) mean temperature in
Manomet, Massachusetts in the 2 months prior to
the average arrival date for each species, (2)
the NAO index, and (3) the ENSO index. We
included a lagged temperature term (the temper¬
ature in the 2 months prior to migration during the
previous year) when analyzing changes in lernalc-
to-male ratios as a way to test the effect of the
previous year's temperature on sex ratios.
We rated the seven species according to
several ecological characteristics, including num¬
ber of clutches, territoriality, feeding and breed¬
ing behavior, breeding habitat, and length of
migration (Table I). Our categorizations were
based on banding data at Manomet Center for
Conservation Sciences (population changes,
mean arrival date, female-male ratio, average
arrival, and average wing-chord length) and a
review of relevant literature. Wc also calculated
the average size of males and females of each
species based on measurements of wing length,
and calculated the difference between males and
females. We evaluated the importance of these
(actors by grouping species by each characteristic
and used ANOVA to compare the effect of each
v ariable on each group. We considered all results
w here P < 0.05 to be statistically significant. Wc
used sequential Bonferroni correction to guard
against Tvpe-I error (Rice 1989) in cases of
multiple tests.
RESULTS
Protandry. — Six of seven species studied had
significant protandry; males arrived earlier than
females by 3.6 days on average each year (paired
/-test, two-tailed P < 0.001) (Table I). Only
Baltimore Orioles had no significant difference
between the average arrival times of males and
females (paired /-test, two-tailed P = 0.57).
However, the amount of protandry varied widely
among the species studied: male American
Redstarts arrived 2.1 days earlier than females
on average (paired /-test, two-tailed P < 0.001),
whereas male Black-and-white Warblers ( Mnio -
til la vuria) arrived 5.S days before females on
average (paired /-test, two-tailed P < 0.001).
None of the ecological variables examined-
winlering range, breeding range, number of
clutches per season, population status, average
sex ratio, and mean difference between male and
female arrival dates significantly explained vari¬
ation in the amount of protandry observed. We
tested whether males have significantly longer
wings, and are larger, than females. Males were
significantly larger than females in all species
studied (paired /-test, two-tailed P < 0.001)
(Table I). However, the magnitude of size
difference did not explain the amount of protandry
observed l / = 0.30, P — 0.52).
Migration Times. — Neither males nor females
of any of the species we examined arrived
significantly earlier over time as measured by
linear regression after correcting for the number
of tests (// = 14). The difference in arrival times
between males and females also did not change
significantly over time for any species during the
period studied (Fig. 1).
Male American Redstarts, after correcting for
multiple tests, were the only group for which
arrival dales w'ere significantly related to any
climate variable with males arriving earlier in
warmer years (reverse stepwise regression. P =
0.002) (Table 2). However, prior to correcting for
multiple tests, seven of 14 tests had relationships
with P < 0.05. which is unlikely to have been
caused by chance alone (y2 - 59.7. df = 1, p <
0.001). suggesting the sequential Bonferroni cor¬
rection may he overly conservative. Five of the
seven species, before the correction, had a pattern
where arrival dates for one sex were related to a
climate variable, while arrival dates of the other sex
were unrelated to climate i Table 2). Despite these
differences, the arrival dates of males and females
212
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 2. June 2012
Black-and-white Warbler Mourning Warbler
Common Yellowthroat
Eastern Towhee
American Goldfinch
Baltimore Oriole
American Redstart
circles and the dashed trend line; males am amres nT^h ^ C*Ch Spec.ie* studied versus time- Females are represented b
significant protandry (paired /-test two-tailed P < 0 001 /onT? 'hC*°l,d trend lme' Six of seven sPecies studied ha
average arrival times of males and females (paired , -test. twwaUedT =^71 had "° Significant difference 1,1
Baubock et al. • CLIMATE CHANGE DOES NOT AFFECT PROTANDRY
213
TABLE 2. Relationships of mean arrival dates of males and females with climate variables as measured by reverse
stepwise regressions that included three climate variables: mean temperature (Mean T), NAO index, and ENSO index.
Slopes arc shown as days/ C for Mean T and days/index unit for NAO and ENSO. The P-value indicated in bold is
significant after sequential Bonferonni correction in = 14 tests). However, seven of the 14 tests hud relationships with P <
0.05. which is unlikely to have been caused by chance alone
0.05 for all species). However, after correcting for
the number of tests (n = 7), changes in the
female/male ratios of Mourning Warblers were
significantly related to mean temperature in the
year of migration with more females in years with
higher temperature (reverse stepwise regression,
P = 0.002) (Table 3). Variation in sex ratios
among species was not explained by any of the
ecological variables we tested, nor was it related
to the average arrival date of the species or the
average sex ratio as measured by ANOVA.
DISCUSSION
All species we examined demonstrated protan¬
dry, except Baltimore Orioles. Protandry did not
change over time, nor did it change in response to
any climate variables that we tested. This result
contrasts with a previous finding that protandry
increased in Barn Swallows ( Hinindo rustica) in
Europe in response to climate change (Moller
2004), but supports a study of protandry in other
European bird species (Rainio et al. 2007).
Our finding that protandry is common among
the sexually dimorphic species we examined
confirms previous results (Rubolini et al. 2004).
However, our results do not appear to support any
of the hypotheses explaining the development of
protrandy in birds. Males were larger than females
in all study species (Table 1). but there was no
correlation between size and amount of protandry
observed, as would be predicted by the ‘differen¬
tial susceptibility’ hypothesis, which suggests
larger males may be less affected by adverse
conditions than smaller females and can therefore
arrive earlier (Morbey and Ydenberg 2001. Saino
et al. 2010. Spottiswoode and Saino 2010). In
addition, male Baltimore Orioles, which arrive
simultaneously with females are. on average,
larger than females similar to the other species
we examined. Thus, it is unlikely that greater
susceptibility to adverse conditions is preventing
females from arriving as early as males. Further,
males are not arriving earlier by virtue of a more
northerly wintering area. American Redstart
males and females, for example, winter near each
other on Jamaica (Stpdds and Marta 2005) but
still had significant differences in timing of
arrival. Different wintering areas may be pari or
all of the cause of protandry for American
Goldfinches — a species in which males winter
further north than females (Prescott and Mid¬
dleton 1990) — but this explanation does not
appear to account for protrandy in the other
species studied.
Another group of hypotheses explaining pro¬
tandry suggest males gain a fitness advantage over
females by arriving earlier and. thus, will arrive
early despite non-ideal early spring conditions.
Moller (2004) and Spottiswoode et al. (2006)
found that more fit males arrive earlier, and that
early arrival is correlated with improved second¬
ary sexual characteristics. Thus, males gain a
reproductive advantage by arriving earlier via the
'mate choice' hypothesis: male arrival date
214
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 2. June 2012
Black-and-white Warbler
£ 70
r
| -» -« -» -4 -J -2 -1 0 1 J 1 «
Southern Oscillation Index
Common Yellowthroat
.£ 7S
I
Mean temperature (-CJ
Mourning Warbler
North Atlantic Oscillation Index
Eastern Towhee
Mean temperature («C)
American Goldfinch
Baltimore Oriole
Mean temperature in the previous year («C)
American Redstart
for the species. Females are represented hv dntl ,ulialcs each species studied versus the most important climate variable
trend line. Only the mean tempemtu^ V* « represented by crosses and the solid
on the x-axis refers to current year mean tcmnemhf * W C" corre,atlon was to a temperature variable. Mean Temperature
Redstarts were the only group lor which ,rriv.l • cxceP‘. 1,1 the case of the American Goldfinch. Male American
earlier in warmer years. * • a cs were significantly related to any climate variable with birds arriving
Baubock et al. • CLIMATE CHANGE DOES NOT AFFECT PROTANDRY
215
TABLE 3. Relationship between sex ratios and climate variables for each species as measured by reverse stepwise
regression. Climate variables tested were mean temperature in the year of migration (Mean T). mean temperature in the
year prior to migration (Lagged mean T). NAO index, and ENSO index. Slopes are for femalcstmales per C. Only changes
in the sex ratios of Mourning Warblers were significantly related to mean temperature in the year of migration (reverse
stepwise regression, P = 0.002). after correcting for the number of tests {« - 7). The significant P values reported for
Black-and-white Warblers and Baltimore Orioles disappear after correcting for multiple tests.
Clini car.
Black-and-white
Warbler
Mourning. Warbler
Common
Yellowihmai
Lustcin Towhec
American
Goldfinch Ballimore Oriole American Redstart
Mean T
Mean T
None
None
None Lagged mean T None
Slope
0.22
0.77
0.17
R-
0.14
0.29
0.21
P
0.035
0.002
0.010
reflects male quality and females are able to
choose the best males based on secondary sexual
characteristics. The ‘rank advantage’ hypothesis
(Morbey and Ydenberg 2001. Coppack and Pulido
2009. Saino et al. 2010) suggests earlier arriving
males may be able to secure better territories,
which makes them more attractive to females.
However, we did not find that extent of protandry
was related to strength ot territoriality. Males of
one of the two non-territorial species we studied,
American Goldfinches, still arrived significantly
earlier than females. Thus, it seems unlikely that
territoriality and mate choice are the exclusive
reasons for protandry.
A last hypothesis is that earlier arriving males
gain an advantage because they can breed earlier
or more frequently; the 'mate opportunity’
hypothesis (Morbey and Ydenberg 2001, Coppack
and Pulido 2009. Saino et al. 2010). However, this
hypothesis docs not explain why males should
arrive earlier than females. Females must also be
arriving earlier for earlier arriving males to mate
more frequently. /Ml the birds studied are serially
monogamous (Poole 2005) and it is unlikely that
earlier arriving males gain an advantage by being
able to have more mates.
It is not clear why our results contrast with those
of Moller (2004) who found that protandry
increased for Barn Swallows in Europe as a result
of climate change. We found no increase in
protandry in any of the species we examined. It is
possible males may gain an advantage from arriving
early relative to females, but females may also gain
an advantage if they arrive early with respect to
other females. Early arriving females may be able to
choose among more potential mates, or perhaps take
advantage of better environmental conditions, such
as better nesting sites, or benefit from maintaining
synchrony with their preferred food sources. The net
effect would he that both males and females advance
their arrival times as much as possible or necessary,
leaving the original difference in migration times
intact. Our Finding suggests that protandry may
remain fairly consistent as the climate changes.
Female/male ratios did not change over time for
any species and only the fcmale/male ratios of
Mourning Warblers were significantly related to a
climate variable, mean temperature. The sex ratios
for three species (Black-and-white Warbler,
Mourning Warbler, and Baltimore Oriole; Ta¬
ble 3) that reflected a relationship to a climate
variable, were associated with the temperature
metrics of ihe current year or to the temperature
metrics of the previous year. The relationship w'as
positive, indicating more females in years with
higher temperature, or in the year following warm
years (Table 3). This is the opposite of the
prediction of the ‘differential susceptibility’
hypothesis of protandry (Morbey and Ydenberg
2001, Saino et al. 2010), in which one would
expect males to have greater mortality in cold
years, as they arrive earlier and are more exposed
to poor conditions such as low temperatures and
lack of food. Another possibility is that males and
females migrate along different routes depending
on the temperature.
We found the extent of protandry is not
changing in response to climate change, contrast¬
ing with previous findings in Europe (Mpller
2004). We suggest researchers continue exploring
the occurrence and magnitude of protandry, and
the response of protandry to climate change to
examine it our results are general or whether the
eflects of climate change on protandry vary
substantially across species and locations.
Additional studies of birds on breeding areas
could provide more information about the cause
of protandry and effects of climate change.
216
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124, No. 2. June 2012
Studies occurring along migration routes may
misrepresent populations, because different age or
sex groups may migrate along different routes.
ACKNOWLEDGMENTS
We thank the staff at the Manomet Center for
Conservation Sciences for their generosity and cooperation
in sharing their data. The findings and conclusions in this
paper are those of the authors and do not necessarily
represent the views of the funding agencies and organiza¬
tions.
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The Wilson Journal of Ornithology 124(2):2 17-229, 2012
COMPARISON OF MIGRANT SONGBIRD STOPOVER ECOLOGY ON
TWO ISLANDS IN THE GULF OF MAINE
REBECCA W. SUOMALA,1 M SARA R. MORRIS.' AND KIMBERLY J. BABBITT1
ABSTRACT. — We compared migrant Bird recapture rate, stopover time, mass gain, and fat class between Star Island.
New Hampshire and Appledore Eland. Maine during spring and fall migration in relation to differences in relative species
abundance between the islands: and examined potential movement of migrants between the islands. The average recapture
rate in spring was 5.7% on Star Island and 3.6% on Appledore Island. Five species were recaptured more frequently on Star
Island and one species more frequently on Appledore Island. There was no difference in mean minimum stopover time
during spring <2.4 days on Star Island; 2.5 days on Appledore Island! and fall (2,‘> days on Star Island: 3.2 days on
Appledore Island). Three species had a longer mean stopover time on Appledore Island than Star Island. The island w ith the
greater percentage of recaptures and longer stopover had more captures lor a given species. Mass gains were significant for
six species during spring (27.3% ) and 10 during fall (38.5% l on Star Island, and live 1 22.7%) during spring and L3 (50.0%)
during fall on Appledore Island. Five species had a difference in rate of mass gain between the islands. The between-island
difference in species abundance was not reflected in between-island differences in mass gam. except lor Red-eyed Vireo
[Vireo olivuceus 1 during fall. There was no clear pattern in species differences in fat levels and differences in captures,
stopover length, or mass gain between the islands. The fat-class and mass-gain results suggest habitat use. as measured by
relative abundance, is not based on the ability to gain mass at the time of stopover. The notable tall mass gains for Red-eyed
Vireo illustrate the availability of food resources for some species on both islands. Only 42 of 1U.437 migrant birds banded
moved from one island to the other. There was little evidence of movement between islands in a seasonal ly-appropriate
direction for continued migration, or evidence indicating a shift between islands after initial capture. Received 21 April
2010. Accepted II November 201 1.
Stopover sites provide migrants with an oppor¬
tunity to replenish critical energy supplies (Moore
et al. 1995), reorient (Baird and Nisbet I960),
escape adverse winds and weather, recover from
muscle fatigue or injury, evade predators (Moore
et al. 1992. Cimprich el al. 2005), and avoid the
dehydration ol daytime flight (Moore el al. 1992).
Lack of suitable stopover habitat may increase the
risk of mortality during migration (Bairlein 1992,
Moore et al. 1992, Hutto 1^98) contributing lo
population declines (Moore 2000, Petit 2000).
Measuring the importance of a given stopover
site and site variables (i.e., habitat type, vegetation
structure, food, etc.) to migrant songbirds is
challenging. Variability in weather, wind direc¬
tion. and an individual’s energetic condition result
in variability of stopover site use in any given
year, making it easy to view stopover sites as
interchangeable and dismiss any given site as
unimportant to passerine populations (Moore el al.
1992. Hutto 1998). Migrants may choose specific
1 Department of Natural Resources and the Environment.
James Hall, University of New Hampshire. Durham. NH
03824. USA.
Canisius College. Department of Biology. 2001 Main
Street. Buffalo. NY 14208. USA.
Current address: New Hampshire Audubon Society; 84
Silk Fanil Road. Concord, NH 03301. USA.
'Corresponding author: e-mail:
bsuomala@nhaudubon.org
stopover sites or may use stopover sites different¬
ly based on available resources, environmental
conditions, and priorities.
Star and Appledore islands in the Isles of Shoals
on the New England coast, USA. provide a unique
opportunity to examine migrant stopover patterns.
Large numbers of songbirds stopover during spring
and fall migration (Mortis et al. 1996) and the
islands arc <1 km apart, eliminating weather as a
factor in between-site comparisons. They are on the
edge of the Gulf of Maine, and most migrants
travel along the coast, south or southwest during
fall (Drury and Keith 1962. Drury and Nisbet 1964,
Richardson 1978) and northeastward during spring
(Dairy and Keith 1962). Thus, the islands are not
necessarily the first or last stop for a migrant before
a long flight; and stopover due to extreme
physiological stress is less frequent than at many
other ecological barriers.
We previously (Suomala el al. 2010) found
differences in ihe relative abundance of migrant
species between Appledore and Star islands.
These differences were most closely related to
dilferences in habitat structure and area between
the islands. Interspecific differences in island use
during migratory stopover were most closely
related to the species' breeding habitat. Star
Island has lower scrub-shrub vegetation and more
closely resembles a typical scrub-shrub habitat.
Species that breed in scrub-shrub or open habitat
217
218
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 2. June 2012
were more common on Star Island. Appledore
Island is larger and has more trees and taller
vegetation. Species more common on Appledore
Island were primarily area-sensitive, forest-breed¬
ing species. Suomala at al. (2010) present
complete habitat and species abundance data for
Appledore and Star islands.
The differences in species distribution patterns
between Appledore and Star islands (Appendix)
provided an opportunity to compare mass gain,
recapture rate, and stopover time between the
islands in relation to species distribution differ¬
ences. We hypothesized that if habitat use during
migratory stopover is related to foraging oppor¬
tunities we should expect higher mass gain on the
island where they are more abundant
The proximity of Star and Appledore islands
and their approximate north-south alignment
suggest potential patterns of movement between
the islands. Morning flights for habitat exploration
prior to settling at a stopover site (Hutto 1985,
Moore ct al. 1990, Wiedner el al. 1992) should
lead to habitat shifts from lower quality habitat on
one island to more suitable habitat on the other
island; those species more numerous on a given
island should be most likely to crossover to that
island. Alternatively, onward migration during
morning flights (Bingman 1980, Wiedner et al.
1992), would lead to seasonally directed same-day
movement between the islands.
Our objectives were to: ( J ) compare recapture
rate, stopover time, mass gain, and fat class
between the islands in relation to differences in
relative species abundance between the islands;
and (2) examine potential movement of migrants
between the islands in relation to these factors.
We hypothesized that differences in frequency
and duration of stopover and mass gain among
migrants would correspond to differences in
species distribution between the islands. We
predicted that birds would move between Star
Island and Appledore Island in a seasonally-
appropriate direction during morning flights and
be captured on both islands.
METHODS
Study Sues.— Out study sites were on Star and
^P'e^^eJslands in the I^es of Shoals
(42 58 N, 70 36 W) in the Gulf of Maine. This
group of nine small islands and several ledges is
AnnSj °T / nearest Polnt of the mainland.
ppledore Island. Maine is the largest of the
islands at 33.6 ha and Star Island, New Hampshire
is 13.4 ha. The minimum shore-to-shore distance
between Star and Appledore islands is ~0.7 km
and the study sites were 1.6 km apart.
Bird Surveys. — Mist netting was conducted
simultaneously on both islands in 1999 and 2000
during spring ( I I May-8 Jun 1999. 10 May-8 Jun
2000) and fall (16 Aug-30 Sep 1999 and 2000)
migration. Nets (6 X or 12 X 2.6 m. 4 shelves.
30 mm mesh) were operated from sunrise to sunset,
and checked every 30 min. Up to five nets were
operated on Star Island and up to 10 nets were
operated on Appledore Island. Nets were placed in
similar, representative habitat types for each island
(habitat data in Suomala et al. 2010). Captured
birds were brought to a central location on each
island and banded with USGS aluminum hands.
'The following data were recorded for each bird
captured: age, sex, degree of skull pneumatization
(scale of 0-3) during fall, unflattened wing chord
(0.5 mm), fat class (scale of 0-4), tail length
(0.5 mm), tarsus length (0.1 mm), and mass
(0.01 g). Birds recaptured on subsequent days were
treated the same as initial captures. Both banding
stations used identical protocols following Morris
et al. (1994, 1996).
1 he fat classification system initially followed
Morris et al. (1996) but was condensed (6 to 2
categories) during analysis. This provided an
approximate separation of birds with some fat
present (categories I -4, 1 = fat lining lurcula to
4 - lat extending over pectoralis; presumably
sufficient tat for continued flight.) and birds
without lat (categories 0 and 0.5, none to a trace).
Data Analyses. — The analyses included only
those species that do not breed on the Isles ol
Shoals; thus, all individuals were considered
stopover migrants. We used Systat Version 10
(SPSS Inc. 2000) for statistical analyses. We did
not use Bonferroni corrections in the analyses to
reduce the chance that real differences or relevant
patterns would be missed (Jones et al. 2002.
Gotelli and Ellison 2004). There is a risk of Type I
error, hut there is also a risk of missing relev ani
patterns when Bonferroni corrections are used
(Gotelli and Ellison 2004). overlooking important
biological differences.
Species recapture percentages were analyzed
foi each sampling period to learn if there were
differences between seasons and years. We did
not statistically adjust recapture analyses for the
different number of nets between the islands
because the Star Island nets occupied a much
higher percentage of available habitat than nets on
S non i a la el at. • MIGRANT STOPOVER ECOLOGY ON ISLANDS
219
Appledore Island, increasing recapture likelihood
and compensating for the increased chance of
recapture due to greater netting effort on Apple¬
dore Island.
We analyzed spring and fall separately. We
pooled data within a season from 1999 and 2000
for mass gain/loss analysis to better represent
typical conditions (Dunn 2000); data from Morris
et al. ( 1996) also showed similarities in mass gain
on Appledore Island between years. We used the
same pooling of data for stopover time and fat
class analyses so the results could be compared to
the mass change results. We compared differences
in fat class between islands using a Chi-square test
and analyzed only those species with 20 or more
individuals captured on each island.
We compared the number, stopover length, and
mass change of recaptured birds for those
migrants that stayed for a minimum of one night,
and were recaptured at least I day after their
initial capture. Migrants recaptured only on the
day of initial capture were not included in the
analyses of recaptured birds. We compared the
number of individuals recaptured between islands
using Fisher's exact test (Zar 1999). We calculated
the minimum length of stopover by subtracting
the init ial date of capture from the date of the last
recapture for each individual (Cherry 1982,
Moore and Kerlinger 1987, Morris el al. 1994).
and compared differences in mean minimum
stopover length between islands using a two
sample /-test. We analyzed only those individual
species with 20 or more individuals banded on
each island and five or more recaptured on at least
one island for both tests.
We calculated mass change during stopover for
each recaptured individual by subtracting mass at
first capture (initial mass) from mass at last
capture (final mass) (Morris et al. 1994, 1996).
We used a Chi-square test to compare the number
of birds gaining and losing mass during stopover
between islands and analyzed only those species
with 10 or more recaptured individuals on each
island. We calculated percent mass change during
stopover as (final mass-initial mass)/initial mass
x 100 (Bairlein 1985; Morris el al. 1994, 1996).
We used a two sample /-test to compare mean
percent mass change for all recaptures between
the islands and analyzed only those species with
five or more recaptured individuals on each
island. We did not adjust the mass of recaptured
individuals to a standard time of day following
Bairlein (1985) and Winker et al. (1992). We also
analyzed mass gain for the same species on each
island individually using paired /-tests to compare
initial mass and final mass.
We analyzed hourly mass change by analyzing
mass al first capture of all birds captured using a
linear regression of mass on time of day (Winker
et al. 1992, Morris et al. 1996, Dunn 2000). We
conducted a multiple regression analysis of mass
on lime of capture with w ing length included as an
independent variable (Dunn 2000). Time of
capture was measured in hours since sunrise.
Wing length outliers were removed if outside the
range for that species in Pyle (1997). We used
ANCOVA to compare regressions from each
island to examine if there w-as a significant
difference in hourly rate of mass gain or loss
between islands. Only those species with a
minimum total of 20 captured (1999 and 2000
combined) were analyzed.
RESULTS
Birds. — We banded 1,572 migrants during
spring and 2.261 during fall on Star Island and
3,240 migrants during spring and 3,364 during fall
on Appledore Island. Scientific naines of species
and numbers captured are in the Appendix. The
majority of birds captured during fall W'ere young
(hatching year; Star Island, 87.2%; Appledore
Island, 93.0%).
Fat Class of Birds Captured. — Appledore Is¬
land had consistently higher percentages of birds
with some fat for all species combined; this dif¬
ference was significant for both spring and fall
(spring: x’ = 29.141, df = 1, P < 0.001; fall: f
— 5.803, df = 1. B = 0.016). Two species had a
greater percentage of individuals with some fat on
Star Island, both during fall; 13 species had a
greater percentage with fat on Appledore Island,
six during spring and seven during fail (Table 1).
Recapture Rates. — The average recapture rate
in spring was 5.7% (91 individuals) on Star Island
and 3.6% (116 individuals) on Appledore Island.
Star Island had a higher recapture rate than
Appledore Island in both spring sampling periods
but the difference was only significant in 1999 (P
— 0.001; 2000, P = 0.160, Fisher's exact test).
The average recapture rate in fall was 9.7% (215
individuals) on Star Island and 12.3% (411
individuals) on Appledore Island. Appledore
Island had a higher recapture rate than Star Island
in both fall sampling periods but the difference
was only significant in 2000 (1999. P = 0.325:
220
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 2. June 2012
TABLE I. Comparison of fat class of birds captured on Star Island (SI) and Appledore Island (AP) in spring and fall
using Chi-square analysis (df = 1 for all tests). Some fat is defined as those individuals with a fat class of I or more; n is the
number of birds captured on each island. Island is the location with the significantly greater percentage of individuals with
some fat. Based on banding data from 1999 and 2000.
n % with some fal
Species
Season
SI
AP
SI
AP
Eastern Wood-Pewee
Spr
39
76
15.4
10.5
Yellow-bellied Flycatcher
Spr
37
75
43.2
53.3
Fall
24
64
4.2
25.0
Traill’s Flycatcher
Spr
82
75
6.1
25.3
Fall
52
49
36.5
38.8
Least Flycatcher
Spr
29
49
20.7
36.7
Fall
41
47
31.7
31.9
Blue-headed Vireo
Fall
28
31
35.7
38.7
Philadelphia Vireo
Fall
23
46
26.1
47.8
Red-eyed Vireo
Spr
88
320
51.1
59.1
Fall
185
583
55. 1
61.6
Red-breasted Nuthatch
Fall
32
96
43.8
40.6
Golden-crowned Kinglet
Fall
85
120
7.1
20.0
Ruby-crowned Kinglet
Spr
63
33
46.0
75.8
Cedar Waxwing
Fall
49
58
18.4
22.4
Spr
36
21
50.0
33.3
Fall
132
1 19
5 1 .5
5 1 3
Northern Waterthrush
Fall
165
361
80.0
63 2
Black-and-white Warbler
Spr
28
128
57.1
68.8
Nashville Warbler
Fall
47
138
59.6
61 6
Fall
42
61
35 7
54 1
Mourning Warbler
Fall
23
28
56 5
46 4
American Redstart
Spr
109
271
53.2
54.2
Northern Parula
Fall
Spr
1 18
36
304
135
28.0
72.2
38.2
83.7
Magnolia Warbler
Fall
Spr
24
296
20
510
37.5
60.1
40.0
60.2
Blackburnian Warbler
Chestnut-sided Warbler
Blackpoll Warbler
Fall
Spr
Spr
Spr
80
21
32
78
85
29
50
194
23.8
28.6
46.9
74.4
24.7
65.5
44.0
90.2
Black-thr. Blue Warbler
Fall
Spr
26
23
106
99
40.5
39.1
36.0
57.6
Yellow-rumped Warbler
Fall
Spr
26
50
106
26
1 1.5
66.0
14.2
69.2
Black-thr. Green Warbler
Canada Warbler
Wilson's Warbler
Fall
Spr
Spr
Spr
343
24
21
48
66
31
94
28
27.1
45.8
4.8
73.5
25.8
71.0
29.8
69.0
Yellow-breasted Chat
Fall
Fall
71
51
46.5
29.8
Lincoln’s Sparrow
Swamp Sparrow
White-throated Sparrow
Spr
Spr
Spr
J7
23
71
68
31
37
48
132
81.4
87.0
71.8
60.3
67.7
83.8
81.3
79.5
Baltimore Oriole
Purple Finch
Fall
Fall
Fall
121
36
42
145
55
30
28.9
41.7
19.0
10.3
63.6
66.7
X P bland
0.569
0.451
1.009
0.315
4.861
0.027
AP
1 1.193
<0.001
.AP
0.054
0.817
2.202
0.138
0.000
0.983
0.056
0.812
3.005
0.083
AP
1.773
0.183
2.430
0.119
0.097
0.756
6.670
0.010
AP
7.776
0.005
AP
0.266
0.606
1.496
0.221
0.002
0.968
14.872
<0.001
SI
1.393
0.238
0.060
0.806
3.378
0.066
AP
0.515
0.473
0.033
0.855
3.866
0.049
.AP
2.463
0.117
0.029
0.865
0.000
0.986
0.021
0.886
6.650
0.010
AP
0.065
0.799
11.375
<0.001
AP
0.372
0.542
2.557
0.110
0.121
0.728
0.081
0.776
0.052
0.820
3.561
0.059
AP
5.700
0.017
AP
0.182
0.669
3.684
0.055
SI
2.106
0.147
0.112
0.738
1.379
0.240
8.439
0.004
AP
14.919
<0.001
SI
4.242
0.039
AP
16.698
<0.001
AP
Suomala et al. • MIGRANT STOPOVER ECOLOGY ON ISLANDS
221
TABLE 2. Comparison of number of birds recaptured by species between Star Island (SI) and Appledore Island (AP)
using Fisher's exact test. Island is the location with lire significantly greater percentage of recaptures for that species; n is
the number of birds recaptured on that island. Based on banding data from 1999 and 2000.
Number captured
Recaptured 111%)
Species
Sampling period
SI
AP
SI
AP
p
Island
Traill's Flycatcher
Fall 00
34
34
1 (2.9)
6 (17.6)
0,105
Red-eyed Vireo
Fall 99
69
230
7(10.1)
61 (26.5)
0.005
AP
Fall 00
116
354
10 (8.6)
59 (16.7)
0.035
AP
Red-breasted Nuthatch
Fall 99
32
94
3 (9.4 1
19 (20.2)
0.190
Ruby-crowned Kinglet
Spr 99
47
28
5 (10.6)
0 (0.0)
0.150
Cedar Waxwing
Fall 99
56
70
5 (8.9)
1 (L4)
0.088
SI
Northern Waterthrush
Fall 99
66
133
13 (19.7)
23 (17.3)
0.698
Fall (X)
100
228
12(12.0)
35 (15.4)
0.496
Black-and-white Warbler
Fall (X)
33
93
1 (3.0)
10(10.8)
0.286
American Redstart
Spr 99
67
133
4 (6.0)
1 1 (8.3)
0.777
Fall 99
34
96
1 (2.9)
12 (12.5)
0.182
Fall 00
85
208
15 (17.6)
45 (21.6)
0.524
Magnolia Warbler
Spr 99
137
258
1 1 (8.0)
2 (0.8)
<0.001
SI
Spr (X)
159
254
8 (5.0)
3 (1.2)
0.026
SI
Fall 00
57
61
9 (15.8)
3 (4.9)
0.068
SI
Yellow-rumped Warbler
Fall 99
199
47
39 (19.6)
1 (2.1)
0.002
SI
Fall (X)
145
20
12(8.3)
0 (0.0)
0.364
Lincoln's Sparrow
Spr 00
21
28
3 (14.3)
6 (21.4)
0.714
White-throated Sparrow
Fall 99
95
119
12(12.6)
5 (4.2)
0.039
SI
Purple Finch
Fall 99
42
31
8 (19.0)
1 (3.2)
0.069
SI
2000, P ^ 0.001 ; Fisher’s exact test). No migrants
were recaptured between years.
Twenty-eight species were recaptured on Star
Island and 28 species were recaptured on
Appledore Island during spring; 17 were recap¬
tured on both islands. Forty species were recap¬
tured during fall on Star Island and 42 species
were recaptured on Appledore Island; 31 were
recaptured on both islands. Five species were
recaptured more frequently on Star Island: Cedar
Waxwing, Magnolia Warbler, Yellow-rumped
Warbler, White-throated Sparrow, and Purple
Finch. Only the Red-eyed Vireo was recaptured
more frequently on Appledore Island (Table 2).
Minimum Stopover Time.— There was no dif¬
ference (spring; t = 0.158, df ^ 205, P = 0.875;
lull: 1 = 1.460. df = 624, P = 0.145) in mean
minimum stopover time between islands during
spring (2.4 days on Star Island, n = 91; 2.5 days
on Appledore Island, n = 116) or fall (2.9 days on
Star Island, n = 215; 3.2 days on Appledore
Island, n = 411). Five migrant species were
recaptured in sufficient numbers to compare
stopover time between islands, Three species
had a longer mean minimum stopover lime on
Appledore Island: Red-eyed Vireo in fall (but no!
spring), American Redstart in spring (but not fall),
and Northern Waterthrush in fall (but not spring)
(Table 3).
Mass Change— There were no significant
differences between islands in number of recap¬
tured birds that gained or lost mass during either
spring or fall stopover for all species combined.
Three species (Red-eyed Vireo, American Red¬
start, Northern Waterthrush) were recaptured in
sufficient numbers (fall only) to compare mass
gain between islands. A higher percentage of each
species gained mass on Appledore Island, but the
difference between islands was not significant
(spring: f = 0.139, df - I, P = 0.709; fall: f =
0.206. df = I ,P = 0.650).
The difference between islands in mean percent
mass change of all recaptures was not significant
for either spring or fall (Table 4). Only the Red¬
eyed Vireo had a difference in percent mass
change in either season with a greater increase on
Appledore Island during fall (Table 4).
Thirty-three species were captured in adequate
numbers to analyze mass change using multiple
regression of all birds captured (Table 5). We
analyzed 15 species during both spring and fall.
1 1 during fall only, and seven during spring only.
The majority of species gained 11ms (72.7%
during spring and 76 .9% during fall on Star
222
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124, No. 2, June 2012
TABLE 3. Comparison of stopover times by recaptured birds between Star Island (SI) and Appledore Island (AP) using
a /-test. Mean stopover time is the average minimum stopover time in days for recaptured individuals; n is the number of
recaptured birds analyzed on that island; and Island is the location with the significantly greater mean stopover time for that
species. Based on banding data from 1999 and 2000.
Species
Season
Mean Stopover (days)
SI
±SD (a)
AP
p
Island
Red-eyed Vireo
Spr
3.5 ± 1 .8 (6)
2.3 ± 2.0 (6)
0.304
Fall
2.0 ± 1.6 (17)
3.3 ± 2.6 (120)
0.039
AP
Northern Waterthrush
Fall
2.8 ± 2.3 (25)
4.1 ± 3.1 (58)
0.011
AP
American Redstart
Spr
1.4 ± 0.5 (7)
2.6 ± 1.6 (14)
0.085
AP
Fall
2.4 ± 1.8 (16)
3.1 ± 2.8 (57)
0.367
Magnolia Warbler
Spr
2.1 ± 1.4 (19)
2.0 ± 1.4 (5)
0.941
Fall
2.6 ± 2.4 (10)
1.8 ± 1.3 (5)
0.498
White-throated Sparrow
Fall
5.6 ± 3.8 (13)
3.7 ± 3.4 (6)
0.296
Island; 72.7% during spring and 84.6% during fall
on Applcdore Island). Mass gains were significant
for six species during spring (27.3%) and If)
species during fall (38.5%) on Star Island, and
five (22.7%) during spring and 13 (50.0%) during
fall on Applcdore Island (Table 5). Significant
mass loss occurred only during spring: Black-
throated Green Warbler on Star Island, and Red¬
eyed Vireo and Cedar Wax wing on Appledor
Island. Five species had a difference in the rate c
mass gain between islands (Table 5). Philadelphi
Vireo. Red-eyed Vireo. Cedar Waxwing, an.
Purple Finch had a larger rate of mass gain durin
fall on Appledore Island and Lincoln’s Sparrov
during the spring (Table 5).
Inter-island Movement.— Only 42 individua
migrants moved from one island to the othei
Seven (0.44%) of 1.572 migrants banded on Sta
Island during spring and 23 (1.02%) of 2.26
migrants banded during fall were recaptured oi
Appledore Island. FJght (0.24%) of 3.240 mi
grants banded on Appledore Island during sprint
and tour (0.12%) of 3.364 migrants banded during
fall were recaptured on Star Island.
Six ot 15 spring crossovers were same-da)
recaptures (3 to Star Island and 3 to Appledore
Island) and live of 27 fall crossovers were same-
day recaptures (all to Appledore Island). The
majority of crossovers were recaptured within
3 days of initial banding (32 of 42) hut. during fall
1399. seven individuals were recaptured 4 or more
days after banding, including a Northern Water-
thrush recaptured 10 days after banding and a
Purple Finch recaptured 24 days after handing.
The most numerous (3 or more occasions)
NorthOVerJPeC',eS Were Red-*yed Vireo and
Northern Waterthrush (Table 6).
DISCUSSION
We expected those species captured more
frequently on one island to be recaptured more
frequently and stop longer on the same island
Differences in percent recaptures and stopover
time were consistent with this hypothesis. The
island with the greater percentage of recaptures
and longer stopover was the one with more
captures (Appendix). However, there were a
number of species that did not have significant
differences in recapture rale or stopover time
despite a difference in captures between the
islands. Our results showed no clear pattern
between differences in fat levels and differences
in captures, stopover length, or mass gain. This is
consistent with other studies that found little
relationship between these factors (Moore and
Kerlinger 1987. Kuenzi et al. 1991, Wang et al.
1998).
The bet ween -is land difference in species abun¬
dance (Suomala et al. 2010) was not reflected in
between-island differences in mass gain, except
for the Red-eyed Vireo during fall. The fat-class
and mass-gain results suggest habitat use, as mea¬
sured by greater relative abundance on a given
island, w'as not based on the ability to gain mass.
Species more common on one island did not gain
mure mass or lat on that island, as would be ex¬
pected if they chose that island because there was
more food. Red-eyed Vireo and Yellow-rumped
Warbler lost mass in the spring, even on the island
where they were most abundant. Our mass gain
results were similar to those of Rappole and
Warner ( 1976) who found the majoritv of species
and individuals at a stopover site did not use the
local food resources, but a small percentage
Suomala et al • MIGRANT STOPOVER ECOLOGY ON ISLANDS
223
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remained longer and gained mass. However, there
was wide variation between species, seasons, and
individuals, similar to that found by Morris et al.
(1996) over 10 years on Appledorc Island.
Caution should be used in interpreting the mass
change results of the ANCOVA analysis. This
analysis measures differences in the rate of mass
gain that might indicate differences in food
supplies and quality, but is based on the assumption
of equal foraging lime for all birds (i.e.. arrive at or
before dawn). Thus, mass measurements represent
changes that occurred at the stopover site (Dunn
2000). Birds that stray to the east of the Isles of
Shoals over the Gulf of Maine may have to
continue flying past sunrise (Baird and Nisbet
I960), arriving well after sunrise in a fat-depleted
condition. Their condition would be unrelated to
stopover habitat quality and represents a confound¬
ing factor in the analysis. This phenomenon may
contribute to the small number of species with
significant mass gains estimated by regression
analysis on either island, as suggested by Morris et
al. (1996). However, the results of our regression
and recapture analyses were consistent. This
suggests the ANCOVA analysis was not affected
by large numbers of fat-depleted birds arriving
later in the day or that Star and Appledore islands
were similarly affected and a between-island
comparison is valid, although the slope of the
regression may be flattened. Small sample size
may also be a factor in the lack of significant trends
in the mass-change regression analysis due to high
individual variation in condition (Winker et al.
1992. Winker 1995a, Dunn 2001).
The general lack of significant differences
between the islands in percent mass change
among recaptures, percent of recaptures gaining
mass, and diurnal mass gains of all species
provides a strong indication that factors other
than food availability, as measured by the ability
to increase mass, influence stopover at the Isles of
Shoals. Winker (1995b) also found that capture
rate did not correspond with mass gain and
abundance did not correlate with use of food
resources as measured by fat deposition (Winker
et al. 1992). suggesting that food availability is
not the only factor in site selection. We
hypothesize that migrants may select stopover
sites based on habitat structure that is similar to
familiar breeding habitat, regardless of the actual
food availability at that site (Suomala et al. 2010).
The islands may also function ns an important
stop for rest . reorientation, muscle repair, or water-
224
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124, No. 2. June 2012
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Suomala et al. • MIGRANT STOPOVER ECOLOGY ON ISLANDS
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balance (e.g.. Kuenzi et al. 1991 , Moore et al. 1995,
Ahorn and Moore 2004). Competition for resources
occurs among migrants (Moore and Wang 1991)
and the ability to gain mass may be related to the
ability to obtain a transient feeding territory
(Rappole ami Warner 1976). Predation can be a
significant risk during migration (Moore et al. 1990)
and migrants may prefer locations with fewer
predators or dense vegetation to better escape
raptors. Merlins (Fcilco lolumburitts), the most
common raptor at the Isles of Shoals, are seen more
frequently on Appledore Island than Star Island
(SRM and RWS. unpubl. data). Raptors are also
known to perch on isolated trees and watch for prey
during migration (Moore et al. 1990). a behavior
seen for Merlins on Appledore Island but Star Island
lacks suitable perches (RWS and D. W. Holmes,
pers. obs.).
There w as little evidence of movement between
islands in a seasonally-appropriate direction for
continued migration. Nor was there evidence
indicating a shift between islands after initial
capture, as would be expected if birds were
exploring habitat prior to settling for the day. If
birds were searching available habitat, we would
expect those that landed in low quality habitat on
one island would move to the island with more
suitable habitat and be recaptured there. Our data
suggest that decisions regarding stopover habitat
at the Isles of Shoals were made without apparent
exploration and were unrelated to the ability to
gain weight. This is consistent with Winker’s
1 1995b) observations and suggestion that birds are
able to rapidly select habitat with no observable
exploration.
Cedar Wax wing and Purple Finch crossover
results were consistent with both species roving
among the Isles of Shoals for several days to follow
food supplies and crossing to Appledore Island
where there was a better chance of mass gain. Both
were more numerous on Star Island but gained
significantly more weight on Appledore Island in the
fall. These species are highly frugivorous in fall and
have irregular migration patterns that vary with local
food sources ( Wootton 1996. Winner el al. 1997).
The two Red-eyed Vireos that crossed during fall
from Star Island to Appledore Island (the island with
more initial captures and greater mass gain) may also
have moved to gain more mass. However, so few
birds crossed over that it is difficult to gain any
insight into the relationship of crossovers to species
distribution at initial capture or mass gain differences
between the islands.
226
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 2. June 2012
TABLE 6. Birds captured on cither Star Island (SI) or Appledore Island (AP) and recaptured on the other island. Based
on banding data from 1999 and 2000.
Species
Spring
Fall
Totals
North
SI to AP
South
AP to SI
North
SI to AP
South
AP to SI
Northern Flicker
1
1
Eastern Wood-Pewee
1
1
Traill's Flycatcher
1
1
1
3
Eastern Phoebe
1
1
Blue-headed Vireo
1
1
2
Red-eyed Vireo
1
1
4
6
Blue Jay
1
1
Red-breasted Nuthatch
1
1
Cedar Waxwing
1
2
3
Northern Waterthrush
2
2
4
Black-and-white Warbler
I
1
Nashville Warbler
1
]
•>
American Redstart
1
2
7
Northern Parula
I
1
1
J
Blackpoll Warbler
|
1
J
1
Yellow-rumped Warbler
1
2
7
Yellow -breasted Chat
1
I
Indigo Bunting
2
1
7
Purple Finch
7
—
a
Totals
7
8
23
4
j
42
Limited crossover was most consistent with
movements to reorient at sunrise and regain land
(Wiedner et al. 1992. Murray 1976). compensate
for wind drift (Baird and Nisbet I960. Moore
1990), or avoid crossing water (Baird and Nisbet
1960. Wiedner et al. 1992, Gellin and Morris
2001). Northward crossovers from Star Island to
Appledore Island in lall were consistent with
other northward daytime flights reported at many
locations on the Atlantic seaboard (Baird and
Nisbet 1960. Murray 1976. Wiedner et al. 1992)
CeUin and Morris (2001) found significant
northward and westward movement of birds
banded on Appledore Island in the fall.
CONSERVATION IMPLICATIONS
The notable tall mass gains for Red-eyed Vi
m this study and on Block Island. Rhode Isl;
(Parrish 1997), illustrate the availability of ft
resources for some species on coastal islands. R
eyed Vircos did not maintain a threshold wei
dunng fall stopover on Lake Erie in Canada (Dt
-001) where there was suitable habitat for inse
but no mention of fruit. The coastal habitat, wh
remains Irost-free later into the fall and conta
many fruit-bearing shrubs that provide a mi
reliable and less energetically ■expensive' so"!
of food than insects during the fall (Punish 2000).
may be important to survival of young birds during
their first migration. The availability of habitat
where migrants can meet other physiological needs
may be as critical as habitat for feeding dining
stopover (Abom and Moore 2004). The aggrega¬
tion ot many sites may provide the critical
resources coastal migrants require.
There are few studies with notable mass gains
in passerines during migration (e.g., Rappole and
Warner 1976. Winker et al. 1992. Winker 1995b.
Dunn 2001, this study) and researchers often
attribute a lack of measurable gains to small
sample si/.e. high variation in individual condi¬
tion. and other factors such as age and sex ot
individuals (Winker et al. 1992, Winker 1995b.
Dunn 2001). These factors influence our ability to
detect gains, but we raise the question of whether
the typical stopover ecology of these broad front
migrants contributes to inherently low mass gain.
It is unlikely that a single location could provide
adequate resources for all birds with so many
individuals passing through in a short time. Thus,
the gradual loss of stopover habitat may have a
gieater cumulative impact on migrant populations
than can be easily measured or observed at
individual stopover sites.
Suomala el al • MIGRANT STOPOVER ECOLOGY ON ISLANDS
227
ACKNOWLEDGMENTS
This project was made possible by support from the Star
Island Corporation and New Hampshire Audubon, grants from
die Eastern Bird Banding Association and the University of
New Hampshire Graduate School, and the generous donations
of many individuals. This effort would not have been possible
without help of volunteers at New Hampshire Audubon, the
Star Island banding station, and the Appledore Island
Migration Banding Station, supported in pan by the Shoals
Marine Laboratory. This paper is contribution #17 of the
Appledore Island Migration Banding Station and contribution
# 1 54 of the Shoals Marine Laboratory.
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I-™' A™. H :s"^ut'0n °f mi8ram SWIM used in the comparison analysis of birds captured on Slat
and StlST h h s’ ,n T and 200°- Th' i" » column is the total birds captured on each
differeL in U^sof,> I, a"'""'?' “5Cd in individu“' varies. A - in More captures indicates no
The Zd reUh mre c a T6 c "" be,W“" ,hc isla"d« “ *** &*#««* numbers were insufficient for anal, sis
tne island with more captures ,s trom Suomala (20051 and Suomala ct al (2010)
n
Scientific name
Season
SI
AP
More captures
Northern Flicker
Eastern Wood-Pewee
Colaptes auratus
Contopus virens
Fall
Spr
27
39
60
76
Yellow-bellied Flycatcher
Empidonax flaviventris
Fall
Spr
16
37
26
75
-
Willow/Alder Flycatcher
E. traillii/E. alnorum
Fall
Spr
25
82
64
75
SI
Least Flycatcher
E. minimus
Fall
Spr
52
29
49
49
SI
Eastern Phoebe
Blue-headed Vireo
Sayomis phoebe
Vireo solitarius
Fall
Fall
Spr
41
17
12
47
31
51
AP
Philadelphia Vireo
Red-eyed Vireo
V. philadelphieus
V. olivaceus
Fall
Fall
Spr
28
23
88
31
46
320
SI
AP
Blue Jay
Red-breasted Nuthatch
Cyanocitta cristata
Silt a canadensis
Fall
Spr
Spr
185
5
9
584
21
17
AP
Brown Creeper
Certhia americana
Fall
Fall
32
9
96
49
AP
Suomala et al. - MIGRANT STOPOVER ECOLOGY ON ISLANDS
229
APPENDIX. Continued.
n
Species
Scientific name
Season
SI
AP
More captures
Golden-crowned Kinglet
Re gulus satrapa
Fall
85
120
-
Ruby-crowned Kinglet
R. calendula
Spr
63
33
SI
Fall
49
58
SI
Veer)-
Calharus fuscescens
Spr
9
22
-
Fall
6
27
AP
Swainson’s Thrush
C. ustulatus
Spr
15
73
AP
Fall
11
29
-
Cedar Waxwing
Bombycilla cedrorum
Spr
36
21
SI
Fall
132
120
SI
Ovenbird
Seiurus aurocapilla
Spr
17
171
AP
Fall
9
56
AP
Northern Waterthrush
Parkesia noveboracensis
Spr
18
96
AP
Fall
166
361
AP
Black-and-white Warbler
Mniolilta varia
Spr
28
128
AP
Fall
47
138
AP
Nashville Warbler
Oreothlypis ruficapilla
Spr
18
30
-
Fall
42
61
-
Mourning Warbler
Geothlypis philadephia
Spr
15
46
AP
Fall
23
28
-
American Redstart
Setophaga ruticilla
Spr
109
271
-
Fall
1 19
304
AP
Northern Parula
S. americana
Spr
38
136
-
Fall
24
20
-
Magnolia Warbler
S. magnolia
Spr
296
512
SI
Fall
80
85
SI
Blackburnian Warbler
S. fusca
Spr
21
29
-
Chestnut-sided Warbler
S. pensylvanica
Spr
33
50
-
Fall
9
25
-
Blackpoll Warbler
S. striata
Spr
78
194
-
Fall
74
102
-
Black-thr. Blue Warbler
S. caerulescens
Spr
23
99
AP
Fall
26
106
AP
Yellow'-runtped Warbler
S. coronata
Spr
50
26
SI
Fall
344
67
SI
Black-thr. Green Warbler
S. virens
Spr
24
31
-
Fall
19
25
-
Canada Warbler
Cardellina canadensis
Spr
21
94
AP
Fall
14
36
-
W'ilson's Warbler
C. pusilla
Spr
50
29
SI
Fall
71
57
SI
Yellow-breasted Chat
Icteria virens
Fall
59
31
SI
Savannah Sparrow
Passerculus sandwichensis
Spr
23
7
SI
Lincoln's Sparrow
Melospiza lincolnii
Spr
23
37
-
Fall
21
5
SI
Swamp Sparrow
M. georgiana
Spr
71
48
SI
Fall
24
6
SI
White-throated Sparrow
Zonotrichia albicollis
Spr
68
133
_
Fall
123
145
SI
Rose-breasted Grosbeak
Pheucticus ludovicianus
Spr
12
41
Indigo Bunting
Passerina cyanea
Spr
7
5
Fall
4
6
Baltimore Oriole
Icterus galbula
Spr
12
21
Fall
36
55
Purple Finch
Carpodacus purpureus
Spr
8
2
SI
Fall
42
31
SI
The Wilson Journal of Ornithology 124(2):230-244, 2012
A NATION-WIDE STANDARDIZED BIRD SURVEY SCHEME
FOR VENEZUELA
GUSTAVO A. RODRIGUEZ.1 JON PAUL RODRIGUEZ,1-3
JOSE RAFAEL FERRER-PARIS,'-2 AND ADA SANCHEZ-MERCADO' 2
ABSTRACT.— We developed a field survey protocol based on the North American Breeding Bird Survey to evaluate the
efficiency and reliability of a bird monitoring scheme in the Neotropics, known as NeoMaps. A team of 21 amateur and
professional ornithologists conducted bird counts at 27 locations distributed throughout Venezuela between March and
Apnl 2010. Locations selected followed a stratified spatial sampling design derived from environmental aid
biogeographical variables. Two complementary survey protocols were implemented in consecutive davs along 404m-
long roads.de transects. Three-minute point counts were performed at 50 stops. 800 m from each other on dav 1.
Cumulative Spec.es lists were recorded a. a selection of 10 stops sampled for 9 min each, divided into three consceuuw V
PT'^ "" ‘Jay,,2 We rccorded W species at the 27 sites combined, representing 57% of the 1.033 potential species, ur
43 /e ot all known \ ene/uelnn species. An additional 83 species were recorded outside of the formal point counts, for a total
° .. . spi-‘clcs d^(-'ted, Groups such as hummingbirds and most waterbirds had unusually low numbers of both species and
: pr<“y du" to an abnormally dry year. Our survey me.hods appear to be appropriate for surveying most
k owT nO;rC0,°n,al rCleS- Th,S iS thC r,rst »“*•■«*. *y«ematic bird Su.cv in Venezuela '
knowledge, in any other Iropical country. Received Id March 2011. Accented 20 November 20/ 1
or. lo our
Adequately quantifying bird species richness
and abundance is one of the basic prerequisites of
any sound wild bird conservation and manage¬
ment program (e.g., Robbins et al. 1986. Ralph et
al. 1993, Herzog et al. 2002, Vorisek et al. 2010).
Long-term monitoring programs, such as the
Breeding Bird Survey (BBS) of North America
and the United Kingdom, and the Pan-Europcan
Common Bird Monitoring Scheme (Vorisek
et al. 2010), rely on a variety of bird surveying
techniques that have been extensively tested and
validated, to monitor bird populations in temper¬
ate countries (Ralph and Scott 1981, Ralph et al
1993, Wunderle 1994, Ralph et al. 1995, Buckland
2006, Dawson and Efford 2009. Vorisek et al.
2010). Relatively little has been done to develop
adequate and cost-effective bird survey techniques
in tropical countries, particularly in the Neotropics,
where the highest species richness is concentrated
(Orme et al. 2005). The global Wild Bird Index for
example, has been estimated only from mean
population trends of European and North American
birds, while the data used for the more general
iving Planet Index are overwhelmingly from
cion^nr° d!,EC0l°ei'a' Ins,itul° Venez°lano de Invest,
Venezuela" US' 2°632’ Caracas 1(»^
Venetian f/?*05. BoIdni<™ y Agro fores tales. Instil
ca,,c * -
developed regions (Butchart et al. 2010. Pereira
et al. 2010).
At least four major challenges need to be
overcome lo develop baseline data sets to monitor
change of neotropical bird populations. (1) Survey
techniques developed and applied in temperate
regions (e.g., BBS) need to be widely tested
against the higher levels of species and ecosystem
diversity at tropical latitudes (Myers et al. 2000.
Orme ct al. 2005). (2) Neotropical birds exhibits
variety ol behavioral patterns, such as leking.
permanent occupation of territories, decreased
levels ol singing, overlap or home ranges, and
nomadic or highly mobile behavior in search for
mobile (e.g.. army ants) or spatially patchy (e.g..
fruits) food resources. These patterns depart from
the typical breeding behavior of temperate
species, lor which most survey techniques have
been developed, and many of its assumptions (i.e -
synchronized breeding and song produced by
males only) may not be met in tropical habitats
( Karr 1971, 1981; Poulsen et al. 1997; Herzog et
al. 2002). (3) Developing countries frequently
have severe financial constrains, making it
difficult to plan and conduct efficient research,
surveying, and monitoring programs (Margules
and Redhead 1995). (4) Neotropical nations have
a marked deficit of trained personnel for biodi¬
versity research and monitoring (Rodrieuez et al.
2005).
There have been several important efforts to
develop standardized techniques for surveying
tropical birds adapted to different bird groups and
230
Rodriguez el at. • VENEZUELAN BIRD SURVEYS
231
Caribbean Sea
Colombia
NorthCoast
| NWCordilleras
Llanos
[ | Guayana
Brazil
FIG. I. Venezuela showing location and identification number of the 27 study cells. NeoMaps numbers, names, and
ecoregions are in Table 1.
behaviors (e.g., Karr 1971, 1981: Terborgh el al.
1990: Wunderle 1994; Casagrande and Beissinger
1997; Poulsen el al. 1997; Herzog cl al. 2002;
Rompre el al. 2007). These techniques lend lo be
designed for monitoring populations intensively at
particular locations with high costs in terms of
time, effort, and funds, making them impractical
for monitoring over large tropical regions (Mar-
gules and Redhead 1995). Past and recent efforts
in Venezuela have included bird inventories, but
most have focused either on a single location or a
unique taxon or guild (e.g., Casagrande and
Beissinger 1997, Terborgh et al. 1997, CJiner F
2001. Lasso el al. 2006. Martinez 2008, Seharis et
al. 2008, Lentino et al. 2009, Sanz et al. 2010,
Vilella el al. 2010), and none has been conducted
at the country scale.
Rodriguez et al. (2007) used three different
combinations of numbers of points and count
duration as part of the Neotropical Biodiversity
Mapping Initiative, NeoMaps (Rodriguez and
Sharpe 2002, Ferrer-Paris et al. 2011) with the
goal of testing and adapting the BBS protocol to
the tropics; they concluded the combination of 50
3-min point counts also appeared to be the most
efficient in the tropics. Our objective was to
develop and test the performance of a large-scale
survey in characterizing the avifauna of Vene¬
zuela necessary for a systematic, quick and
low-cost method for obtaining reliable data on
bird richness and abundance at the country level.
METHODS
Sampling Design. — Our sampling design was
based on the stratified spatial sampling design
proposed by the NeoMaps Initiative (Rodriguez
and Sharpe 2002, Ferrer-Paris et al. 2011). We
first superimposed u 0.5 X 0.5 degree grid over a
map of Venezuela (~5() km on a side, or
—2.500 knr/cell). The sampling universe was
defined as 177 from a total of 377 cells that had a
minimum of 90 knr accessible by secondary
roads (at least by 4-whecl drive vehicles). We
applied a principal component analysis (PCA)
within this sampling universe, based on 14
environmental variables to define three orthogo¬
nal environmental axes (physical -climatic, forest
cover, and drought intensity). A subset of 27 cells
was selected to represent the range of environ¬
mental variation in the PCA within the major
biogeographical regions in the country (Rodriguez
2003; JRF, unpubi. data) (Fig. I ).
Sampling Transects.— We identified a 40- km
section of a secondary or tertiary road in each of
27 cells. We tried to avoid urban centers and roads
in poor condition, which would make driving
during the surveys difficult or slow. This was not
completely possible, as in some cells there was
232
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124. No. 2. June 2012
only one adequate road available. We marked 50
stops separated by 800 m from each other using a
Global Positioning System (GPS). Transects were
selected to cover the largest possible environmen¬
tal gradient within the cell.
Sun-ey Teams. — A team of 21 professional and
amateur ornithologists from Venezuela and
abroad was assembled and trained in methods to
be used during I week in early March 2010. The
group was divided into seven survey teams with a
team leader (main observer) and two assistants.
Each team was assigned several study transects,
typically within a single ecorcgion. Team leaders
were professional ornithologists or bird-watchers
with thorough knowledge and experience in
identifying the birds in their region. Most surveys
occurred between 12 and 28 March (-2 weeks)
but, due to unexpected problems, two transects
were surveyed between 6 and 10 April. The short
survey period was designed to minimize the effect
of time of year or season, as well as to keep costs
of training and administration low.
Bird Suneys. — Bird surveys were conducted
along the marked transects, following an adapta¬
tion of the methods of the North American BBS
(Bystrak 1981, Robbins 2000, Rodriguez ct ul.
2007). Our survey protocol consisted of a main
survey (Survey I or SI) based on unlimited radius
point counts, and a complementary survey
(Survey 2 or S2) based on cumulative species
lists, applied on consecutive days (Rodriguez el
al. 2011). The team leader was the primary
observer, as the assistants in most cases did not
have sufficient experience to identify all species
m the region and were occupied recording the
information, organizing the sheets, and perform¬
ing logistical or road safety tasks. However, in
cases when the assistants detected and positively
identified a species not reported by the team
leader during the count time, it was recorded by
making a note of the observer who detected it
Records from the team leader and assistants were
pooled for the results and analyses presented in
this paper. Surveys started at first light which,
depending on the habitat and weather was
between 0 and 20 min before sunrise. We
expected surveys to last no more than 5 hrs but
m some locations, they were longer mostly due to
poor conditions of the roads or obstacles on the
way Counts started upon arrival at each stop to
try to avoid delays. All 50 stops in SI were
indivvf /'L U, 3’min C°Um al each stop. All
ldividual birds seen or heard were recorded and
notes were made for birds detected >100 m. large
birds flying high overhead (mostly raptors or
parrots), and the number of individuals detected
by sight or sound. Birds not safely identified to
species were recorded as unidentified and not
included in the results and data analyses. S2
covered a selection of 10 points and cumulative
species lists were made for three 3-min penods
without counting individuals. We traveled tran¬
sects for S2, whenever possible, in the opposite
direction as for SI to sample individual stops
along the transect at different times of the
morning, as bird activity for most species usually
decreases dramatically after the first 3-4 hrs after
sunrise. S2 was intended to be complementary to
the data of S I ; thus, the selection of points to lx
sampled for S2 was made after SI was conducted.
Point selection was somewhat subjectively direct
cd to cover the diversity of habitats within
transects, giving priority to stops with forested
habitats or water bodies or where it was easier or
safer to stop the vehicle. All data collected during
a day were entered into a data base on a laptop
computer during the afternoon. The team leader
also kept an extended list of all bird species seen
or heard, either during the surveys or not
(hereafter called ‘checklists'). No special effort
was made to seek other species than those
recorded in the surveys.
Sampling Effort. — Total fieldwork time was
-243 person-days (3 days/location X 27 locations
X 3 persons). Bird sampling occupied —729 person-
hrs (mean — 4.5 hrs/day x 2 days/location X 27
locations X 3 persons). The total effective sampling
effort, il we exclude driving time and consider that
mostly only one person made the observations
(—4% of all observations were not detected by the
main observer), was 108 person-hrs (27 locations X
1 2.5 hrs of SI + 1.5 hrs of S2] X 1 person).
Potential Species Lists. — The total number of
species for the country w'as taken from Hilt)
(2003). 1 he list of potential (expected) species for
each ecorcgion was estimated by compiling
several local bibliographic sources (Lentino and
Goodwin 1991, Goodwin and Lentino 1992.
Lentino el al. 1996. Sharpe 1997, Rodriguez
2000. Hilly 2003, Ascanio and Garcia 2005. Sanz
el al. 2010) and from the lead author's unpub¬
lished field observations (GAR). Common and
scientific names of all species mentioned follow
Gill and Donsker (201 1 ).
We classified all potential species into two
categories: ‘common’ and ‘uncommon or rare'.
Rodriguez el cd. • VENEZUELAN BIRD SURVEYS
233
TABLE 1.
Ecoregion. two-digit NeoMaps code, altitudinal range.
and habitat of locations considered in this study.
NeoMaps
Location
Ecoregion
Altitudinal range (in)
Predominant habitat
01
Rio Tocuyo
NorthCoast
400-700
Desert scrub
02
Paraguana
NorthCoast
0-100
Dessert scrub, coast
03
Quebrada Arriba
NorthCoast
500-860
Dry scrub and forest,
farmland
05
Perija
NorthCoast
0-600
Savanna, farmland,
moist forest
07
Sur del lago
NWCordilleras
0-1,100
Farmland, moist second
growth
08
Altagracia
Llanos
200-300
Savanna, dry scrub and
forest
09
Araya
NorthCoast
0-150
Desert scrub, farmland
14
San Tome
Llanos
0-200
Savanna, pine
woodland, palms
16
Otopun
Llanos
100-250
Farmland, savanna,
forest patches
18
Navay
Llanos
200-780
Farmland, savanna,
moist forest
19
Capitanejo
Llanos
100-200
Farmland, savanna, dry
forest
21
Kavanayen
Guayana
1,200-1,350
Savanna, moist forest
22
El Manteco
Guayana
300-400
Savanna, rainforest
patches
23
Paraytepuy
Guayana
900-1.200
Savanna, moist forest
24
Guri
Guayana
100-200
Savanna, rainforest
patches
25
Yacambu
NWCordilleras
800-1.900
Cloud forest, scrub
26
Jaji
NWCordilleras
1 ,700-2,800
Cloud forest, farmland
34
Gavil&n
Guayana
50-200
Savanna, scrub,
rainforest
36
Isla de Guara
Llanos
0-50
Farmland, moist forest
patches
45
Paria
NorthCoast
0-280
Dry scrub and forest,
farmland
57
Pinango
NWCordilleras
2,800-4,300
‘Paramo’ (high Andean
tundra)
66
Macanao
NorthCoast
0-50
Desert semb,
mangroves, coast
75
Caicara
Guayana
40-80
Savanna, moist forest,
palms
80
Colonia Tovar
NWCordilleras
0-2,300
Cloud and moist forest
90
La Escalera
Guayana
500-1,450
Rain and cloud forest,
savanna
93
Anacoco
Guayana
100-200
Rainforest, second
growth
96
Corral i to
Llanos
50-150
Savanna, dry forest
patches
Common birds were subjectively defined as
conspicuous species that could be found in most
parts of the country in relatively high numbers,
and represented 17% of the total potential species.
Ecoregions.— We divided locations into four
ecologically similar regions or ecoregions (Ta¬
ble I. Fig. I). (I) The NorthCoast covers all the
coastal and dry/desert scrub, dry forest, and
savanna locations in northern Venezuela, and the
Maracaibo Lake area, up to 860 m asl. (2) The
NWCordilleras includes all mountainous locations
in the Andean and Coastal ranges with prevalence
ol moist and cloud forest in western and northern
Venezuela, up to 4.300 m asl. (3) The Llanos
includes the lowlands in central Venezuela, most
seasonally flooded, with prevalence of savannas.
234
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 2. June 2012
farmlands, and dry forest, up to 780 m asl. (4) The
Guayana includes all Guayanan and Amazonian
lowland and highland locations, south of the
Orinoco River, up to 1,450 m asl. Most rainforests
are in this region.
Data Analysis.— We pooled data from SI and
S2 (which we refer to as 'SI + S2') for most
analyses but, for those that required numbers of
individuals, we used data from SI only. Check¬
lists were used only occasionally for selected
cases.
Data analyses were performed with R statistical
software with the packages ade4. vegan, lahdsv. ,
and cluster (CRAN.R. Project 2011). We com¬
puted national-level species richness estimates,
using the Chaol estimator based on abundance
(numbers of individuals) of detected species with
data from SI. The Chaol estimator is defined as:
c _ c , "I ("I - 0
‘h’ ~ *0 + -t: - —rr ,
2(a2 + 1 )
where Sn is the number of observed species and a,
and a2 denote the number of species with one or
two individuals, respectively. We used the Chaol
estimator based on frequency of detections
(number of sites at which a species was observed)
with data from S 1 and from SI + S2. The Chaol
estimator is:
Sn — Sq +
“i(«i ~ 1)
2(7/2 + !) ’
where a, and a2 are the number of species present
m one and two records, respectively (Chao 1987).
We computed another estimate of species
richness assuming the relationship between SI
and real species richness (Sp) is similar to the
proportion of species detected in the first 3 min of
at X j2ii _
jl-3|
S2«l
where SI is the number of species detected in S
b2n_3] ,s the number of species delected in S2 (;
three 3-min periods), and S2, , , is the number
spec.es detected in the first 3-min period.
We used the moments-based uncondition
estimator and its standard deviation for interpol
ion o a species accumulation curve based on 5
r S’ " aL 2004> ■ We funher fitted
^cumu 'r e" rurmul“ 10 e'"-upola.e tf
accumulation curve and to estimate its asymptol
(Tjorve 2003):
S = R
(K+e)
where S is the expected number of species for a
value of sampling effort e , R is the total estimated
richness (asymptote), and K is the effort necessary
to reach half the value of R. Asymptote species
richness values were estimated for the curve of the
observed number of species (SI + S2 data) and the
curve of the values estimated by the Chaol
estimator, as both estimates are influenced by the
number of sampling locations. The resulting curve
was further extrapolated to 100 transects to
predict the expected number of species with
increasing sampling effort.
We used a cluster diagram of species compo¬
sition per transect with data from SI + S2 to
examine regional groupings of species. We first
calculated a matrix of pairwise similarity distanc¬
es among transects based on the Sarensen index,
defined as:
D = 2a/(2a + b),
where a is the number of shared species between
two transects, and h is the number of species
present in only one transect. We then applied an
agglomerative nesting (agues) algorithm to the
resulting matrix (Kaufman and Rousseeuvv 1990).
We further compared the number of species
detected per family in SI + S2 and the checklists
in all transects against the expected numbers. We
applied a ■/' goodness of fit to test for the null
hypothesis that observed values had the same
distribution as those expected. Some families had
only one or a lew species and we pooled families
with less than three expected species to perform
this test. /J-values were computed using a
MonteCarlo simulation with 2,000 replicates.
Means (e.g.. species numbers, percentages) are
reported with their standard deviation (— SD*.
while richness estimates (Chaol. Chaol. and
accumulation curves) are reported with their
standard error (± SE).
RESULTS
Species Richness.— About one-half to two-
diirds ol all potential species were detected by
the surveys (45-65%), representing between a
third and one-half (34-49%) of all known
Venezuelan birds (Table 2). SI and S2 were
obtained through independent counts that totaled
Rodriguez el al. • VENEZUELAN BIRD SURVEYS
235
TABLE 2. Number of species observed using the data obtained through Survey 1 . Survey 2, both surveys combined (SI
+ S2) and the checklists, indicating the proportion (%) of all potential species in the 27 transects ( 1 ,033 spp.) and all known
Venezuelan birds (1,383 spp.) that they represent.
Method
Observed
% potential
% Venezuela
Survey 1
526
51
38
Survey 2
465
45
34
SI +S2
593
57
43
Checklists
676
65
49
150 and 90 min, respectively. SI + S2 pooled
species detected on SI and S2 at each transect
: 240 min of observation) and checklists contained
additional opportunistically detected species.
Thus, the highest species numbers corresponded
lo the checklists, followed by SI + S2, SI. and S2,
respectively (Table 2).
The Chaol estimate of total richness based on
SI data, considering number of individuals per
species, was 608 ± 22 species, while the Chao2
estimate using SI + S2 data, based on detections/
transect (n = 27), was 788 ± 36 species. A mean
of 64.2 ± 6.3% of the species from S2 was
detected in the first 3 min and our corrected
estimate of species richness for S 1 is 828.2 ± 95.5
species.
The SI + S2 species accumulation curve
reached an asymptote value at 785 ± 1 1 species
(K = 9.48 ± 0.35) (Fig. 2), while the asymptote
based on Chao2 was 879 ± 1 1 species ( K =
3.47). These asymptotic values represent 76 and
85% of all potential species, and 57 and 64% of
all known Venezuelan birds, respectively. The
extended extrapolated curve shows the number of
new species detected in the survey would decrease
dramatically beyond the sampled 27 transects, i.e..
>
a>
o
0
CL
co
co
o
Number of transects
FIG. 2. Accumulation curve from data of Survey 1 and 2 (SI + S2) (the area shaded around the line is the 95%
confidence interval), and extended extrapolated curve (dotted) from the sampled 27 to 100 transects The asvmDtote of
observed values is 785 species (K = 9.48), and that for the Chao2 estimator is 879 species (K = U 7)
236
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 2. June 2012
v NorthCoast
The^y*axis indicates /!!• s^ec'e^ compos‘tion ,mo,8 all 27 transects with symbols indicating the four ecoregit*.
o™ tTi„ “ " ,ndiVidl,al tra"SeCIS or The ‘-wer the value, the closer two transects
ui groups are in terms of species composition.
the curve tends to flatten beyond this point
(Fig. 2).
SI lasted an average of 5.5 hrs with five
transects lasting >6 hrs. due mostly to unexpected
logistic delays. On average, 39% of the species
were detected during the first hour of the survey,
after which detection of new species continuously
decreased: 64 to 97% of the species were detected
during the first 4 hrs. The last 2 hrs allowed
detection of >20% of the species for 9 of ?7
transects.
Species Composition.— The survey sites 1
each region clustered together or in groups
biological significance, the Llanos being
clearest example (Fig. 3). The avifauna of Gu
nan locations in northern Bolivar (Caicara. C
and El Manteco) had higher affinity with
Llanos, as savanna vegetation in north
Guayana is similar to that «>r the southern Lla
he remaining Guayanan locations, predomin
Nwn “ afeaS’ c,uslered lo8cther. '
WCord.lleras locations clustered together
rth ^ Lag0> Which dusicmd wi.
subset of NorthCoast sites: Rosario de Perija ,
Quebrada Arriba, and Pifiango, which appears
completely isolated from the rest of the transects.
NorthCoast locations were the most diverse,
forming three subgroups: Paria-Araya, Maracaibo
Lake Basin (Rosario de Perija and Quebrada
Arriba), and thorn scrub coastal ecosystems
(Macanao, Paraguana, and Rio Tocuyo).
Sixty-four of 71 potential (expected) avian
families were recorded either by the surveys or
in the checklists (Table 3). Most unrecorded
families were monospecific (6 of 7). and their
species were either nocturnal (Tytonidae. Stea-
tornithidae, Nyctibiidae) or associated with
habitats poorly covered by roadside surveys
(Heliornithidae. Phoenicopteridae, Psophiidae,
Cincilidae). There was no significant difference
between observed and expected species composi¬
tion by family, i.e., the proportion that each
family contributed to the total number of species
(X2 = 57.025. P = 0.153 based on 2,000 Monte
Carlo simulations). We detected a mean of 6^%
o( the expected number of species/family, al¬
though there was some variability, especially ter
families with low numbers of species (Table 3).
Rodriguez el id. • VENEZUELAN BIRD SURVEYS
237
Abundance. — The total number of individual
records during the surveys was 12,109 (8,573
from SI and 3,536 from S2) and the total
individuals recorded (only from SI) was 15.114
(Table 4). There was a mean of 1,76 individuals/
record and 28.73 individuals/species (from SI).
The proportion of common species detected was
27% (37-56% in the different ecoregions)
(Table 4). Most ‘common’ species were recorded
>50 times whereas most uncommon or rare
species were recorded <25 times (Fig. 4). A
large proportion of the species sampled were
uncommon or rare (Fig. 4): —95% of species
were below the 15th prevalence percentile, while
128 species (24%) were recorded only once (from
SI ). On average, we obtained 318 records/transect
(min = 95, max = 479) and 6,4 species/3-min
count (min = 0. max = 18) (from SI). We
observed a mean of 560 individuals/transect (min
= 177, max = 1,379) and 1 1.2 individuals/3-min
count (min = 0. max = 237) (from SI ). The most
abundant species was Western Cattle Egret
(Bubulats ibis) with 823 individuals (data from
SI) and the species with the highest number of
records was Tropical Mockingbird (Mini us gilvus )
with 291 records from SI or 360 from SI + S2.
DISCUSSION
Our survey recorded 57% of all potential
species in the 27 transects and 43% of all known
Venezuelan birds (Table 2) in a little over 2 weeks
of field work using 108 person-hrs of effective
bird sampling. However, 6-8 months were
devoted to planning and logistics prior to the
survey. We suggest that organizing and executing
a survey of this type, in a fairly large tropical
country with an adequate road network but limited
scientific expertise, can be done in <1 year at
relatively low costs. The amount of data generated
and the funds required for implementation
(—$150,000 US including field equipment, plan¬
ning. salaries, and survey costs), is clearly a
modest effort when compared to long-term
programs such as the North American UBS and
the Christmas Bird Counts (Bock and Root 1981,
Bystrak 1981 . Robbins et al. 1986. Robbins 2000).
We believe our objective of developing and
testing a rapid and cost-efficient nation-wide bird
survey for Venezuela was achieved.
We were also able to obtain reliable richness
estimates and visualize the composition pattern in
addition to achieving our cost-efficient objective.
The highest species richness was in Guayana,
closely followed by NWCordilleras, which are the
two ecoregions that include highlands and have
the widest elevation gradient (Table 4). This is
not a surprising result, as the wider elevation
range provides w'idor variety of habitats that host a
larger diversity. NorthCoast. a lowlands region
with predominance of dry or desert scrub, had the
lowest species richness (Table 4), a common
pattern in arid regions (Stotz et al. 1996.
Rodriguez- Ferraro and Blake 2008).
The cluster diagram (Fig. 3) shows that groups
of locations belonging to the same ecoregion are
related due to their large number of shared
species. There are, however, several cases show¬
ing a different pattern. The three northwestern
locations south of the Orinoco River in Bolivar
Slate (Caicara, Guri, and El Manteco) appear
closer to locations in the Llanos than the rest of
Guayanan locations (Fig. I ). This is probably due
to a high number of typical savanna species, the
predominant habitat in the Llanos and present in
northern Bolivar (Huber and Oliveira-Miranda
2010). There has been extensive deforestation in
this area in the last 25 years. At least 2,000 knr of
rainforest were lost to logging and burning in
Bolivar State between 1988 and 2010 (Oliveira-
Miranda et al. 2010: 1 25). leading to savannization
in what formerly were forested locations (i.e., El
Manteco, No. 22; Fig. I ).
The NorthCoast appears to be split into three
groups, two of which appear closer to the Llanos.
Species shared between these (Perija, Quebrada
Arriba. Araya and Faria) and the proper Llanos
transects are mostly those of farmlands and dry
scrub, tw'o habitats shared between these two
ecoregions. whereas the other NorthCoast group
(Macanao, Paraguana, and Rio Tocuyo) share
most species typical of desert scrub, the predom¬
inant habitat in these three transects and the entire
ecoregion. The Sur del Lago transect in the
western Andean foothills, due to its wide altitude
range, was problematic in terms of ecological
classification. It included mostly Andean foothills
(part of the NWCordilleras ecoregion) but also
pan of the Maracaibo Lake lowlands and overlaps
with the NorthCoast region with which it shares a
number of species. A transect (# 57) that appears
completely isolated (Fig. 1 ) with a binomial index
close to 1, is Pinango. despite its ecological and
geographical relation to the NWCordilleras re¬
gion. This location had the lowest number of
species (only 22 in the surveys) but the highest
percentage of endemism and of unique species, a
238
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124, No. 2, June 2012
TABLE 3. Number of species by family (following Hilty 2003) observed in surveys (S 1 + S2) and checklists, compared
to the expected values in all cells combined. Families present in Venezuela but with no species expected in the study cells
were omitted.
Observed
Family
Surveys
Tinamidae
4
Podicipedidae
2
Sulidae
1
Pelecanidae
1
Phalacrocoracidae
1
Anhingidae
1
Fregatidae
1
Anhimidae
1
Anatidae
2
Phoenicopteridae
0
Ardeidae
12
Threskiornithidae
8
Ciconiidae
2
Cathartidae
5
1
Pandionidae
Accipitridae
24
Falconidae
12
Cracidae
5
Odontophoridae
3
Rallidae
8
Heliomithidae
0
Eurypygidac
1
Aramidae
1
Psophiidae
0
Burhinidae
I
1
Charadriidae
Haematopodidae
1
Recurvirostridae
1
1
Jacanidae
Scolopacidae
5
Laridae .
Columbidae
17
Psittacidae
26
Cuculidae
10
1
Opisthocomidae
Tytonidae
n
Strigidae ,
Steatomithidae
o
Nyctibiidae
o
Caprimulgidae
0
Apodidae
8
Trochilidae
Trogonidae 7
Cerylidae 4
Momotidae 1
Galbulidae 4
Bucconidae ^
Ramphastidae ■ ->
Picidae 1 ^
Fumariidae j g
Dendrocolaptidae |
Thamnophilidae
Formicariidae
6
Checklists
Expected
% Observed
5
8
50
2
2
100
1
I
100
1
1
100
1
1
100
1
1
100
1
1
100
1
1
100
6
12
17
0
1
0
15
21
57
8
8
100
2
3
67
5
6
83
1
1
100
25
36
67
12
14
86
7
13
38
3
3
100
9
10
80
0
I
0
1
1
100
1
1
100
0
1
0
1
1
100
5
8
13
1
1
100
1
1
100
1
1
100
12
21
24
8
12
33
17
18
94
29
43
60
1 1
14
71
I
1
100
0
1
0
3
13
8
0
1
0
0
3
0
8
14
0
8
11
73
41
83
40
8
10
70
4
6
67
1 100
49 51
13 46
Rodrigue: et al. • VENEZUELAN BIRD SURVEYS
239
TABLE 3. Continued.
Observed
Family
Surveys
Checklists
Expected
% Observed
Rhinocryptidae
2
2
3
67
Tvrannidae
80
86
138
58
Pipridae
II
11
16
69
Cotingidac
9
11
22
41
Vireonidae
9
9
13
69
Corvidae
4
4
5
80
Hirundinidae
10
1)
II
91
Troglodytidae
14
15
19
74
Cinclidae
0
0
1
0
Polioptilidae
2
2
2
100
Turdidae
12
14
20
60
Mimidae
1
1
1
100
Motacillidae
1
1
2
50
Parulidae
15
17
29
52
Emberizidae
21
23
38
55
Thraupidae
53
60
84
63
Cardinalidae
1 1
11
13
85
Icteridae
17
18
23
74
Fringillidae
4
4
4
100
Mean
65
typical pattern of high Andean locations (Fjeldsa
and Krabbe 1990, Stotz et al. 1996).
A reassuring finding was that species compo¬
sition by families did not differ significantly from
that expected (Table 3). There were several
families that diverged considerably from the mean
proportion of species per family. Nocturnal
families such as nightjars (Caprimulgidae), potoos
(Nyctibiidae). and owls (Strigidae); some water-
birds including ducks (Analidae). plovers and
lapwings (C'haradriidae). and shorebirds (Scolo-
pacidae): and hummingbirds (Trochilidae) had
proportions lower than expected (Table 3). We
believe the lower proportion of these families in
the surveys was for two different reasons. (I)
Roadside surveys, as has been proposed for the
BBS (Robbins et al. 1986, Robbins 2000). tend to
be adequate for most common and diurnal species,
but inadequate for rare, nocturnal or colonial
species. Our surveys began around dawn and most
nocturnal species were not detected: no nightjars
and only one owl (Ferruginous Pygmy Owl
[Glauiidiwn brasiliiuwrn\ , which is also partly
diurnal) were observed. (2) The low number of
waterbird and hummingbird species was probably
not due to the survey method, but reflected their
actual low abundance. The period between May
2009 and April 2010 corresponded to one of the
‘El Nino-Southern Oscillation’ (ENSO) episodes,
whose most obvious effect was severe drought,
diminished water bodies, and overall dry vegeta¬
tion throughout the country (Ropelweski and
TABLE 4. Number of species, individuals, records, and proportion of 'common' species for the four ecoregions in
Venezuela and all 27 study locations combined.
Ecoregion
Species*
Species1,
Individuals1
Records1
% 'common'*
NonhCoast
199
227
3.488
2.347
56
N'WCordilleras
302
351
2.506
1.197
41
Llanos
238
271
5.560
2.673
53
Guayana
339
375
3.560
2.356
37
All combined
593
676
15.114
8.573
27
Based on daia from Survey I and Survey 2 combined.
’ Raced on data from Ihe checklists.
c Based on data from Survey I .
240
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 2. June 20/2
FIG. 4. Abundance distribution (number of records)
from data of Survey I (SI). Dark gray points correspond to
common species, while light gray correspond to 'uncom¬
mon or rare'.
Halpert 1987. NOAA 2011). Only two species of
ducks, for example, were recorded in the surveys
and six in the checklists of the potential \2
species. In addition, numbers were unusually low,
especially in the Llanos, where whistling ducks
(■ Dendrocygna spp.) in an average year can reach
the thousands (Dallmeier 1991, Vilella ct al.
2010). The average proportion by family of
expected species detected in the surveys increases
from 65 to 73% il waterfowl, shorebirds.
nocturnal families, and hummingbirds (Anatidac.
Charadriidae. Scolopacidae, Tvionidae. Strigidae.
Steatornithidae. Nyctibiidae, Capri mulgidae, and
Trochilidae) are removed.
This relative limitation of our survey methc
for sampling nocturnal, colonial or rare species
possibly outweighed by the prospect of rapid I
producing systematic, large-scale abundance dat
for common species that could be of great use fc
monitoring programs. A high proportion r
common species (27%) was found in the stud
cells, similar or higher than the expected propoi
tion (17%). This is an indication that our survey
represent the actual abundance, at least fc
common, more conspicuous species (Fig. 4).
The largest number of individuals (5,560) am
records (2,673) was recorded in the Llanos
despite being third in rank of species richnes
among the lour ecoregions (Table 4). Thest
numbers would have probably been much large
a more typical year when thousands o,
waterbirds gather in the water bodies (Vilella el
al. 2010). Not surprisingly, the Llanos region also
had a high proportion of common species (53%
compared with 27% for the entire country),
although the highest value corresponded to the
NorthCoast with 56% (Table 4). This higher
proportion of common birds in the lowlands is
one of the reasons why species composition of
some transects from Guayana and NWCordilleras
(such as Sur del Lago) tend to overlap partly with
these two lowland ecoregions, producing the
regional ’blending’ (Fig 3).
Our estimated values, all between 785 and 82S
species, were below' the potential species richness
of 1,033 (Fig. 2). However, that number is
probably unrealistic since it includes all species
that have ever been recorded in the study area, bur
not necessarily present during our surveys, as well
as colonial and nocturnal species. An important
pattern observed is that the accumulation curve
tends to flatten beyond the sampled 27 transects
with an increase of only 1 10 new species from
593 species (57% of the potential 1.033 species)
at 27 transects to 703 species (68% of (lie
potential) at 81 transects. Thus, only 18% more
now species would be reported with 200% more
sampling effort (Fig. 2). Therefore, these 27
transects, a number obtained from the NeoMaps
sampling design, appear to be the breakpoint ol
optimal cost-effectiveness. A similar species
accumulation pattern was obtained by Vilella et
al. (2010) through waterbirds roadside counts in
Venezuela Llanos, where the curve tends to
llattcn after the first 10 of 54 sampled transects.
The field techniques we used were based
mostly on the North American BBS (particularly
SI), a set ol techniques that has been developed,
tested, and improved over the past 45 years
(Bystrak 1981. Robbins et al. 1986. O'Connoret
al. 2000, Robbins 2000). Some neotropical
habitats may host bird diversities four or five
times higher than in temperate zones, whereas
individual species densities may be up to 10 time>
lower, and most of these species, common or
scarce, have low detection rates (Terborgh et al.
1990). I his is a major challenge when censusing
tropical birds by this technique, as the high
number of species at each count site may be
difficult to cover, especially early in the morning
Rodriguez et al. (2007) hinted, after the NeoMaps
pilot test, that a second survey (S2 in our study),
conducted u day after the main survey (SI ) might
prove useful for at least two reasons. First, it
Rodriguez el al. • VENEZUELAN BIRD SURVEYS
241
would provide a higher chance to detect rare
species (Fig. 4). which are well known to
represent a large proportion of species in a bird
community (Preston 1962, Gaston 1994). A larger
number of species detected would, in turn, allow
us to generate more accurate estimates of total
species richness. Sixty-seven (11%) of the 593
species detected during the surveys were recorded
only by S2. and 20 only during the third count
period. Second. S2 can be used to estimate
detection (Alldredge el al. 2007), although this
topic will be addressed elsewhere. We cannot
conclusively say yet that conducting two inde¬
pendent surveys at each location (SI -t- S2) is cost
effective, and presently would recommend per¬
forming only one (SI) if time, funds or personnel
were constrained; but encourage exploring alter¬
native schemes (S2) whenever possible. Our
second survey (S2) was able to increase the total
species detected by 1 1%, plus it allows us to later
examine biases during the surveys (such as those
generated by time of day) and estimate species
detection. Further research should be conducted to
identify the most efficient strategy for a second
day of surveys.
Our main survey (SI) lasted an average of
5.5 hrs. which is I to 1.5 Ins longer than an
average BBS route (Bystrak 1981) with the same
sample effort (50 3-min point counts). This was
mostly due to poor road conditions for most
transects, even after selecting the 'best' available
secondary road in each cell. Other minor delays
due to logistic problems, roadside obstacles,
w'eather conditions, etc., could probably be
avoided in an optimized survey scheme. However,
we believe the average survey time could hardly
be <5 hrs in Venezuela or other neotropical
developing countries. We kept registering new
species (up to 20% of the total) in the last 2 hrs of
the survey on about one-third of the transects,
which indicates these last hours were actually
necessary and that bird activity did not decease as
drastically as is normal in BBS counts, at least for
a moderate proportion of the transects.
One main difference between NeoMaps and the
BBS is that NeoMaps is conducted during the dry
season (typically Nov to Mar), when most
Venezuelan birds are not breeding (Hilry 2003).
The main reason for choosing the dry season is
logistical, minimizing potential field days lost to
rain It is also when up to 135 species of boreal
migrants are present as wintering birds (Hilly
2003); this allows us to quantify this important
component of our avifauna. Synchronizing Neo¬
Maps surveys to a breeding season would not be
possible, as avian breeding in the Neotropics is
not synchronized (Karr 1981), and species dis¬
tribute themselves along the 7-month long rainy
season (Hilty 2003).
Our methodology has both strengths and
weaknesses: once a team of people has been
trained, it is useful to perform quick inventories
with rather low costs, yielding reliable results for
a large number of common diurnal species. It is
not useful to accurately assess nocturnal, colonial
or rare species. Poor road conditions or total lack
of roads may be an important hindrance in
producing reliable census results in some pails
of many neotropical countries by either making
die surveys too long ( >5 hrs) or leaving important
areas completely undersampled. Further experi¬
mentation with the survey methodology is desir¬
able.
AC KNOW LEDGM ENTS
This research work was supported by the lnstituto
Venezolano de Investigaciones Cientfficas and TOTAL
Venezuela S.A. We are grateful to our field team leaders:
Jose Clavijo, Anthony Crease, Marieta Hernandez, Jose G.
Leon, Curtis Marantz, and Alejandro Nagy; our field
assistants: Rudy Badiu. Lorenzo Calcano. Diana Esclasans.
.lose L. Garzon, Paul Granado. Karen Lopez, Gonzalo
Medina, Vili.su Moron, Jessica Ortega, Juan Papadakis,
Alfonso Frisco, Haydee Sturhahn. Judit Szabo, Ivan
Tepedilio; and Pio Colnienares. Helios Martinez, Monica
Nunez, Ana M. Perez, and Chris .1. Sharpe for their support
ami collaboration throughout the project. The manuscript
was greatly improved by comments from C. John Ralph, W.
Douglas Robinson, and Clait E. Braun.
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The Wilson Journal of Ornithology 1 24( 2 ):245 252, 2012
POPULATION SURVEY OF LEACH’S STORM-PETRELS BREEDING
AT GRAND COLOMBIER ISLAND, SAINT-PIERRE AND
MIQUELON ARCHIPELAGO
HERVE LORMEE,14 KARINE DELORD,1 2
BRUNO LETOURNEL,- AND CHRISTOPHE BARBRAUD2
ABSTRACT. — The Si Pierre and Miquelon Archipelago hosts the only French Leach’s Storm-Petrel ( Oceanodroma
Irucorhoa ) colony. We conducted a survey during the 2008 breeding season to estimate the breeding population size on
Grand Colombier Island. This survey included an estimation of burrow detection probability using a double-observer
approach. We estimated that 3 % of 1 .each's Storm-Petrels nests had failed before we stalled the survey. Nest occupancy
probability was neither affected by slope nor vegetation type and was 0.546 ± 0.029. Burrow density was positively
affected by slope and, consequently, was much lower on the plateau than on island slopes. Burrow detection probability was
neither affected by observer nor by habitat anil was 0.89 ± 0.01. Wc estimated the population to be 363.787 [95% Cl =
295.502—432.072] breeding pairs, which is among the largest Leach's Storm-Petrel colonies in the northwestern Atlantic
Ocean. Received 10 May 2011. Accepted IV November 2011.
Questions associated with the population dy¬
namics of colonial seabirds arc of intrinsic interest
to biologists and managers of protected areas.
Answers to basic questions about population
estimates and trends are often needed, as seabirds
are recognized as monitors of marine ecosystems
and act as indicators of marine environmental
changes (Cairns 19X4; Monteveechi 1993; Mon-
tevecchi and Myers 1995a. b; Piatt el al. 2007;
Einoder 2009). Breeding surveys arc particularly
relevant for burrow-dwelling species such as
storm-petrels as a decline could go unnoticed in
these inconspicuous species, even for decades.
These species may also be highly vulnerable to
introduced predators or soil erosion in breeding
colonics (Brooke 2004). Population estimates and
trends must rely upon rigorous standardized
protocols that should be developed throughout
the range of species or population of concern
(Walsh et al. 1995).
Monitoring programs have two important
sources of variation that must be considered in
monitoring design: spatial variation and detection
rate (Thompson 1992. Lancia et al. 1994. Nichols
et al. 2000. Pollock et al. 2002). Spatial variation
arises when the observer cannot monitor the entire
1 ONCFS-CNERA Avifaunc Migralrice-Station dc Chize.
Candour dc la Canauderic 79360 Villiers en Bois. France.
CLBC-CNRS, l PR 1934. Carrcfour dc la Canaudcne
79360 Villiers en Buis. France.
ONCFS-Service dc la collcctiviid territorialc de Saint
Pierre and Miquelon, B3 rue Boursaint BP 4244, 97500
Saini Pierre, France.
J Corresponding author; e-mail; herve.lormee@oncfs.gouv.fr
area of interest. Monitoring effort thus has to
concentrate on sample areas from which the results
arc used to draw inference about the entire area of
interest (Pollock et al. 2002). Detection probability
is important as survey methods do not detect all
individuals present in the sampled area. Monitoring
has to incorporate methods for estimating effects of
detection rate so any estimated temporal or spatial
changes in the number of individuals counted
reflect true changes and not differences in
detection. Observer identity and experience are
recognized as covariales likely to he relevant to
variation in detection probability (Sauer et al. 1994.
Kendall et al. 1996); thus, estimation of detection
probability is particularly required in long-term
monitoring where inevitable changes in observers
over time or between sample areas are likely to
impact survey accuracy.
Our objective was to estimate the population
size of a Leach's Storm-Petrel (Oceanodroma
leucorhoa ) breeding colony in the French Saint-
Pierre and Miquelon Archipelago in Ihe north¬
western Atlantic Ocean, relying on a land-based
survey conducted in 2008. We applied similar
survey methods, keeping with recent efforts to
obtain up to date estimates for major Leach’s
Storm-Petrel colonies in eastern North America
(Robertson et al. 2006). We explicitly considered
estimation of detection probability in the survey.
These surveys are expected lo be regularly
repeated in future years, and we emphasized the
double-observer method (Nichols ct al. 2000).
which appears less Jogistical/y expensive com¬
pared to other methods for estimating detection
rates (i.e., capture-recapture methods).
245
246
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 2. June 2012
METHODS
Study Site. — Field work was conducted on
Grand Colombier Island (46 49' N, 56 10' W ),
Saint-Pierre and Miquelon Archipelago, in the
northwestern Atlantic Ocean from 18 June to 18
July 2008 (Fig. I ). Grand Colombier Island has an
estimated surface area of 480,000 nr and hosts
large breeding populations of seabirds (Table 1 ),
particularly Atlantic Puffin ( Fratercula arctica)
and Leach's Storm-Petrel (Desbrosses and Etch-
eberry 1989). The island is free of all mammal
species but one, the meadow vole (Microtus
pensylvaniais). The main topographical features
of the island are a central plateau surrounded by
vegetated or rocky slopes and cliffs. Grand
Colombier has dry soils and is densely vegetated
(mainly ferns, Dryopteri, s spinulosa, and grami-
noids, Deschampsia Jlexuosa), providing diverse
and highly suitable breeding sites for burrow¬
dwelling petrels and Atlantic Puffins.
Leach’s Storm-Petrels breed almost exclusively
on Grand Colombier Island within the Saint-
Pierre ami Miquelon Archipelago where they nes
in more or less aggregated burrows, forming
relatively dense colonies (Desbrosses and Etch
eberry 1989). Petrels return to colonies in May
lay their single egg in June, and start visiting
colonies at dusk and during the first part of the
night. Young hatch in July and fledge ir
September. Males and females alternate foraging
trips at sea during breeding and feed on fish, krill,
and squid (Montevecehi et al. 1992).
Sampling Design.- We used a systematic
sampling approach to estimate Leach’s Storm-
Petrel density (Harris and Murray 1981) following
Catry et al. (2003). We conducted line transects (n
- 19) from 8 to 18 July 2008. crossing the entire
island from north to south, during the second half
ot the incubation and early brooding periods. The
irst transect location was chosen randomly and
die following transects paralleled the first' one.
The distance between successive transects was
; , m- Each dansect starting point was located
with a Global Positioning System (GPS) and
plotted on a map (Fig. 2).
We stopped at counting points every 50 m
along each transecl (measured using a 10-m rope).
e appl, cation ot these procedures resulted in all
plots („ - |62) being pseudo-randomly located in
region to habitat features and burrow deresHy
One field worker stood a. the center of the plot a,
ach location, holding the tip of a 3-m rope, while
a second observer holding the other tip walked in
circle (total surface of the plot = 28.27 nr i and
counted all burrow entrances that were within the
plot. The slope angle of each plot was estimated
using a clinometer. Petrel burrows were identified
by entrance diameter (4-5 cm). Burrows consist
of a tunnel of 23 cm (range = 1 2-39 cm I depth on
average which may be straight or with several
turns (Huntington ct al. 1996). The nest chamber
is at the end of the tunnel. We only counted
burrows used by Leach's Storm-Petrels (Hunting-
ton et al. 1996) excluding double-entrance
burrows and vole tunnel entrances. Leach's
Storm-Petrel and meadow voles, respectively,
use burrows and tunnels with similar size
entrances, hut which generally have different
tunnel shape (vole tunnels stay just below the
surface) and habitat requirements in temis of
vegetation cover and soil substrate (Cramp and
Simons 1977. Huntington et al. 1996). We
counted burrows with a clear entrance. Burrow
entrances overgrown by vegetation were consid¬
ered inactive and were not counted. Non-surveyed
areas (lakes, sleep cliffs) represented 2.2 % of
Grand Colombier Island.
Burrow density may be affected by habitat
characteristics including slope angle and/or veg¬
etation type. Fern patches on Grand Colombier
Island w'erc highly associated with steep slopes nf
the island while herbaceous vegetation was nearly
exclusively on the plateau and low slopes. We
investigated the relationship between burrow
density and slope angle using a generalized linear
model dog link, negative binomial distribution).
Estimating Harrow Occupant's Probability —
We estimated burrow occupancy probability by
acoustic playback, to minimize disturbance of
breeding birds, on a sample of 301 burrows at 19
stations spread over the island. Sample plots were
selected to be representative of the habitat
diversity and slope range; 1 1 and eight plots were
sampled, respectively, in fern and graminaceous
habitats, covering a large range in slope (from 5 *•>
38. 1%). I. each's Storm-Petrel calls are sex-specific
(Huntington et al. 1996); calls of both males and
females were played into each burrow with a digital
voice recorder during 1 min and we recorded
whether or not a bird responded tRateliffe et al.
1998, Amhagis 2004). It is known that a proportion
of Leach s Storm-Pfetrels present in burrows may
not respond to playback (Amhagis 2004), and we
systematically inspected burrows with no response
to playback using a burrow-scope. We checked nest
Lormee et al. • POPULATION SURVEY OF LEACH'S STORM-PETREL
247
FIG. 1. Location of Saint Pierre et Miquelon Archipelago and Grand Colombier Island.
TABLE I. Estimates of breeding pairs of seabirds on Grand Colombier Island in 2008 (Lormee et al. 2008).
Year
Species
Scientific name
1980s
2004
2008
Atlantic Puffin
Black Guillemot
Common Murrc
Razorbill
Great Cormorant
Great Black-backed Gull
Herring Gull
Fraiercula arctica
Cepphus grylle
Uria aalge
Alca torda
Rhalacrocorax carbo
Larus marinus
L argentatus
smithsonianus
400 (1974)
0
30 (1983)
>1,000
9,543 (7,160-11,926)
>46
>3
>50
63 (60-66)
10-20
6 0-100
Black-legged Kittiwake
Rissa Iridactyla
200(1989)
291
196 (186-204)
248
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124. No. 2. June 2012
HG. 2. Location o| transects and plots (white dots) on Grand Colombier Island.
content by hand when burrow-scoping inspectio
was not possible. Occupancy was defined as
binomial variable (1 = presence of adult, egg o
chick; 0 = empty), and occupancy probability wa
estimated as die proportion of occupied burrow
over the number of checked burrows. We tested fo
an ellect ol slope and vegetation type oi
occupancy probability using a logistic regressiot
(logit link, binomial distribution). Candidate mod
es were selected using an information theoretic
approach (Burnham and Anderson 2002) Non
breeding birds or failed breeders within burrow,
dwelling petrel species are known to visit oi
temporarily occupy unoccupied burrows, poten¬
tially resulting in overestimates of abundance
(Heaney et al. 2002). However, non-breeding birds
visit the colony mainly at night and rarely stay in
the burrow during the day (Warham 1990
Huntington et aL 1996). Ratclif fe et al. (1998^
estimated the probability of a nest being occupied
diurnal ly by a non breeder on a given day at 0 024
in the closdy related European Storm Petrel
^abates pelagians). Thus, we do not exclude
he possibility that non-breeding birds may have
occupied some burrows during our survey, but they
were unhke.y to constitute a serious bias in
estimation ol the breeding population.
Estimating Incubation Failure Preceding
probatihr'K WC eStimated incubad°n failure
uP,ed bUrr°WS at the '"Sinning of the breeding
season. Quadrats with active burrows covering all
habitat types on the island were randomly selected
(n = 13; number of burrows per quadrat = 8 ±
0.3) by 18-19 June. Burrows were individually
identified within each quadrat, using numbered
30-cm long wood sticks with red colored tips.
Contents of active burrows occupied by an
incubating adult (n — 105) were inspected at
"HO- day intervals ( 18-19 Jim. 2 Jul, 10 Jul). until
the start of the survey, allowing us to observe if
burrows were failed or successful. A nest was
considered tailed if no egg was detected during
one of the inspections. Failure was considered as a
binomial variable and failure probability was
estimated as the proportion of nests that failed
over the number of active burrows.
Burrow Detection Probability.— We used a
double-observer approach to estimate the burrow
detection probability of each observer (Nichols et al.
2000). A sample of plots (n = 13) was surveyed by
pairs of observers counting burrow entrances
independently. Plots were selected in both lent («
~ 8) and herbaceous habitats (n = 5). The ftN
observer marked all the detected burrows. Marks
were placed within the burrow's so they were
invisible for the second observer. The second
observer systematically recorded previously-marked
burrows and those missed by the first observer. The
tank of each observer alternated randomly. We ran a
set of models incorporating different sources of
variation in detection probability, i.e., observer
identity and habitat type, and selected among
candidate models using an information theoretic
approach (Burnham and Anderson 2002).
Lormee et al. • POPULATION SURVEY OF LEACH'S STORM-PETREL
249
TABLE 2. Detection probability of Leach's Storm-
Petrel burrows on Grand Colombier Island. Saint Pierre and
Miquelon Archipelago. Dev = deviance, Np = number of
parameters, Gof = goodness of fit P-valuc The selected
model is in bold.
Model
ATCr
AAlCr
Dev
Np
Col
Observer
23.85
_
19.84
2
0.99
Constant
24.37
0.52
22.36
1
0.77
Habitat
26.35
2.5
22.36
2
0.64
Observer X Habitat
27.80
3.95
19.80
4
1
Calculation of Leach's Storm-Petrel Breeding
Population Size.— The mean Leach's Storm-Petrel
breeding population size (AO was calculated as:
Ox Dx A
N=
where O is the mean burrow
px(\-B)'
occupancy probability. D is the mean burrow
density estimated from plots, A is the surface area
of the island, p is the burrow detection probability,
and B is the breeding failure probability. The
variance of N was calculated using the delta
method following Sober (1982). All values are
means ± SE, unless otherwise staled.
RESULTS
Burrow Occupancy Probability — Occupancy
probability was neither affected by slope angle
nor by vegetation type (slope: P\ = 2.13, P =
0.14; habitat: F\ - 0.50, P = 0.47) and was
considered similar for every sector (0,546 ±
0.029).
Pail lire Probability. — Breeding failure was
estimated from 73 burrows (32 of the 105 active
burrows initially chosen could not be found
during the second visit because of fern growth).
Failure probability was 0.068 ± 0.029 on 10 July,
just before we started the survey. Only 3% of the
active nests contained a recently hatched chick by
this date.
Detection Probability. — The total number of
burrows used to estimate detection probability of
all observers in = 5) was 5 13 (219 in fern and 294
in herbaceous habitats). Burrow densities within
the plots used to estimate detection probability
were comparable to those in the entire set of plots
i plots sampled on plateau: t- test = 1 .679, df = 57.
P - 0.098: plots sampled on island slope: /-test =
1.745. dt = 1 14. P = 0.084). Forty-three burrows
were detected by primary observers only. 59 by
secondary observers only, and 411 by both
observers. The detection probability of each
observer was estimated for 185 ± 3.3 burrows.
All tested models had a good fit to the data. Both
constant and observer effect models received
relatively similar support (AAICY < 2; Table 2).
Detection probabilities based on the observer
effect model, ranged from 0.787 ± 0.040 to
0.913 ± 0.018. We chose the most parsimonious
model to estimate detection probabilities, i.e.. the
constant model (detection probability of a burrow
of Leach Storm-Petrel was neither affected by
observer nor by habitat type). Detection probabil¬
ity for a single observer was obtained from the
constant model and estimated at 0.89 ± 0.01.
Relationships Among Burrow Density , Slope,
and Habitat Type.— Burrow density was positive¬
ly affected by slope (Z = 7.016, P < 0.0001). We
separated the island into four sectors depending
upon the importance of slope angle: plateau,
southern and northern sides, and steep area.
Burrow density was estimated specifically for
each sector (Table 2). This stratification w as used
to estimate the number of breeding pairs.
Leach's Storm-Petrel Breeding Population. —
We estimated the Leach's Storm-Petrel breeding
population size at 363,787 ± 19,991 (95% Cl =
295,502-432,072; Table 3) pairs on Grand Co¬
lombier Island in 2008 considering burrow
occupancy, nest failure, detection probability,
and specific burrow density for each sector.
DISCUSSION
Survey Method.— The estimates of detection
probability suggested an individual observer may
miss up to 11% of burrows. We strongly
encourage systematic estimation of detection
probability during surveys to increase their
accuracy and the power to detect subtle temporal
changes in population size. Detection probability
estimation would be particularly relevant if
observers are expected to change throughout
successive surveys.
Failure at the egg stage appears to be the main
factor affecting breeding success for Leach’s
Storm-Petrel (Bicfcnell et al. 2009). Breeding
failure preceding the survey was low at our study
site (—7%) in comparison with reported values in
the literature (hatching success = 77.9 ± 5.1%,
min = 66%, max = 86%) (Huntington et al.
1996). We may have slightly underestimated
incubation failure rate since the laying period
starts in early June and some breeding pairs may
have tailed in the 2 weeks preceding monitoring
of burrows. Additional failures also occur near
250
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 2. June 2012
TABLE 3. Estimated Leach’s Storm-Petrel breeding population on Grand Colombier Island in 2008. Parameters are
presented as mean ± SE. The 95% confidence interval is in brackets.
Sector
Parameters
Plaleau
Southern side
Northern side
Steep ana
Number of plots
54
67
36
5
Sector area (nr)
105.542
187.785
160.794
32.662
Sector slope ( )
16.3 ± 1.2
31.6 ± 0.9
36.0 ± 1.1
40.0 + 2.2
Adjusted sector area (m’)
109.962 ± 31
220.476 ± 51
198.752 + 67
42,637 + 71
Burrow density
Detection probability
Occupancy rate
Breeding success (10 Jul)
0.32 ± 0.06
0.89 ± 0.01
0.55 ± 0.03
0.93 ± 0.03
1.15 ± 0.09
1.22 ± 0.11
0.45 ± 0.13
Number of breeding pairs
Total number of breeding pairs
23,426 ± 4.063
363,787 ± 19.991
167,557 ± 12,722
[295,502-432,0721
160.267 ± 14.427
12.536 ± 3.626
hatching (mostly due to infertile eggs). Leach's
Storm-Petrel surveys should be conducted no later
than the first half of the incubation period to
minimize underestimation and if breeding failure
cannot be estimated precisely to correct survey
estimates.
Population Estimate on Grand Colombier
Island. The world Leach’s Storm-Petrels popula¬
tion is estimated to be >8 million breeding pairs
(Huntington et al. 1996). The species’ breeding
range is centered in the northwestern Atlantic
Ocean in eastern Newfoundland, Canada, where
over hall of the world's breeding population (up to
5 million pairs) occurs (Huntington et al 1996)
Most colonies are in the Newfoundland region with
the world’s largest colony reaching 3,360 000
breeding pairs at Baccalieu Island (Sklepkovych
and Montevecchi 1989). Thus, the Grand Colomb¬
ier colony contributes -6% of the North Atlantic
breeding population.
The Grand Colombier Leach’s Stonn-Petr
colony ranked second with -363.000 breedir
pairs among Leach’s Storm-Petrel colonies in tf
northwestern Atlantic (i.e., Newfoundland Lai
rad°r, Canada; and St Pierre and Miquelo,
r ranee). Previous surveys conducted during if
lend 0s and :n 2004 0ra"d C“
— 178 OOfW n 11 y e y ' estimatcd population size ;
- 43 On K amSSeS 3nd Ktehebe"y 1989) an
143.000 breeding pairs (Robertson et al 2006
Our eat, mate is twice those in previous years. Thi
Leach\ "I, “ “S kC,'y 10 e"'irel>' from
at ^ ^St°rm-Petrel population increase. A mea
S Z diM 8 0f 5 ^ (Huntington et al
). «nd overall mean annual survival of 0 7<
(Huntington et al. 1996) sUaa&Kt*
annual growth rate n \ n • maxima
max), following Niel ant
Lebreton (2005), is 1.1 (i.e., a maximal 10‘S
annual increase). Large Leach’s Storm-Petrel
colonies appeared stable in the northwestern
Atlantic from the 1970s to early 2000s. and only
small colonies showed declines (Robertson et al.
2006). The difference between the 2004 and 2008
surveys probably partly results from a sampling
artefact as sampling effort was highly variable
between surveys. The sampled area consisted of 8
X 25-nr plots in the late 1980s (200 nr). 90 *
16-trr plots in 2004 (1.440 nr), and -162 X 28.3-
nr plots in 2008 (4,585 nr). Burrow density was
30% higher in 2008 than in 2004. whereas
occupancy rate was only 11% lower in 2008.
I he 2008 survey was the first to include burrow
detection probability, which indicated that burrow
density could be underestimated bv !!%• We
showed that breeding failure from mid- June to the
start of the survey could account for a 7 % loss in
breeding pairs.
Identification of potential threats to this popu¬
lation, because of the significant size of this
colony, should be encouraged for effective
conservation. We observed Leach's Storm-Petrel
remains in regurgitation pellets at Herring Gull
(Units argentatus) nests. Predation of Leach’s
Storm-Petrels by Herring Gulls has been repotted
(Stcnhouse et al. 2000) with up to 9% of a colony
ol 269.765 breeding pairs being killed by 2.I+*
gull pairs in one breeding season. Predation was
mostly by specialized individuals or pairs (1 16%
ot the gull breeding population: Stenhouse el al.
2000). These authors considered that, despite
large losses, the Leach’s Storm-Petrel breeding
population did not appear to substantially decline,
probably because recruitment could maintain the
population. We estimated that 60-100 gull pairs
Lonnie et al. • POPULATION SURVEY OF LEACH'S STORM-PETREL
251
were breeding on Grand Colombier Island during
our survey (Lonnee et al. 2008; Table 1). The
temporal trend of the gull population on Grand
Colombier Island is not well known but no major
increase seems to have occurred recently. Thus,
the impact of the gull population on Leach's
Storm-Petrels is likely limited. Wc also found
occasional eggs inside burrows and dead chicks at
burrow entrances predated, presumably by mead¬
ow voles, during our survey.
Another potential threat to the Leach's Storm-
Petrel breeding population on Grand Colombier
Island could arise from increase of the breeding
population of Atlantic Puffins. The number of
puffin breeding pairs dramatically increased during
the last several decades, from —400 pairs in the late
! 970s ( Desbrosses and Etc he berry 1 989) to > 1 ,000
in 2004 (R. L. Bryant, unpubl. data) and reached
9,543 ± 1,2.16 in 2008 (Lormec el al. 2008). This
increase was paralleled by colonization of new
sectors on Grand Colombier Island, including slope
habitats which arc also favored hy Leach's Storm-
Petrels. Puffins dig large burrows and eject the
excavated soil around the nest, resulting in fern
disappearance and a marked reduction in vegetation
cover, making habitats unfavorable for LeacITs
Storm-Petrels. Sowls el al. ( 1980) reported similar
destruction of nesting habitat of Leach's Storm
Petrels through competition with Cassin's Anklets
(Ptychoramphus ah’ttiiats) and Double-crested
Cormorants (Phalacrocorux auritus). The spatial
colonization and population trend of Atlantic
Puffins breeding on Grand Colombier Island should
be carefully monitored in future years to detect and
quantify potential competition for breeding habitat
w ith Leach’s Storm-Petrels.
ACKNOWLEDGMENTS
We thank Philippe Casadei and Marjorie Jouglet for help
during surveys. We thank Vincent Brctagnolle for access to
song recordings and Andre Mariam for technical advice.
We sincerely thank Cyril Fraud lor help with statistical
analyses. We are grateful to the staff of the regional
delegation of Office National de la Chasse et de la Faune
Sauvage (ONCFS) overseas for logistic facilities. The work
was supported by Direction de P Agriculture et des Forets of
Saint Pierre et Miquelon and by ONCFS.
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The Wibon Journal of Ornithology 124(2):253 264, 2012
APPARENT FORCED MATING AND FEMALE CONTROL IN
SALTMARSH SPARROWS
JON S. GREENLAW1 * -4 AND WILLIAM POST3
ABSTRACT. — Saltmarsh Sparrows (Ammodramus eaudacum) arc non-territorial, lack pair-bonds, and practice
promiscuous mating behavior and obligate maternal care of young. Behavioral details of mating behavior and associated
intermale aggressive behavior are poorly understood in the species. We report the results of an observational study of
mating and agonistic behavior of individually marked breeding birds in New York. We witnessed 1,265 sexual and
agonistic interactions within and among males and females from 1977 through 1985. We found no evidence of male mating
aggregations, and male aggressive behavior was prevalent only in male-initiated sexual interactions. Females solicit
matings from males during nest-building, but the behavior is inconspicuous and not associated with male aggression. Males
spend the morning patrolling their home ranges, and chase or approach females they encounter anywhere in their breeding
habitat Males often concentrate patrol activity in the vicinity of nests under construction, but we found little evidence they
know the location of most nest sites. Some males seek to forcibly mount females on the ground at any breeding stage,
despite female resistance. Females thwart forced mountings in 579/ of cases either by fighting w ith die males, or by uttering
an aggressive call. When a more persistent male suppresses a female's resistance, she then crouches passively as he
assumes a copulatory position on her back. We discuss this behavior in terms of female control of forced mountings, female
choice of mates, and forced mating as a tactic of males that appear not to know the fertility status of females. Males have a
large cloacal protuberance, which suggests sperm competition is strongly developed in the species. We caution that
evolution of the unusual mating behavior in Saltmarsh Sparrows must he understood in relation to the different sexual
behaviors of its closest relatives. Received II April 2011. Accepted IS January 2012.
Historically, behavioral ecologists interested in
evolution of mating systems in birds often focused
their attention on species that practice unusual,
minority forms of mating behavior, Various
expressions of social monogamy represenl the
mainstream among known types of mating
systems in birds, while different forms of social
polygamy are relatively rare; overall, promiscuity
is rarest among passerines (Lack 1968). Saltmarsh
Sparrows {Ammodramus cotulacutus) arc unusual
if not unique among North American passerines in
lacking territoriality, pair-bonding, and paternal
care (Woolfenden 1956, Post and Greenlaw 19X2,
Greenlaw and Rising 1994). However, details of
sexual interactions and intermale agonistic be¬
havior in the species remain largely unexplored.
These details must he known before we can
understand the selective forces and environmental
constraints that influenced the evolution of its
mating system (Emlen and Oring 1977. Clutton-
Brock 1989).
Montagna (1940. 1942) observed aggregations
of sharp-tailed sparrows in Maine and Virginia; he
described these as “curious tangle! s|“ (1940:192)
Jon S. Greenlaw. Biology Department, Long Island
University, Greenvale. NY 1 1746. USA.
Current address: 10503 Mist Power Lane, Tampa. FL
33647, USA.
1907 I'On Avenue. Sullivan's Island, SC 29482. USA.
4 Corresponding author; e-mail: jgreenlaw@earthlink.net
or as “tangled, fighting mass res]” (1942:117).
His collecting activities and observations of males
al Popham Beach, Maine, convinced him they
were fighting over females. These meetings were
temporary and evidently involved several males
attempting to copulate with a single female.
Montagna (1940) thought the multi-male-female
aggregations in Maine involved Nelson's Spar¬
rows {A. nelsoni), bill Saltmarsh Sparrows also
occur at Popham Beach (Montagna 1942; Rising
and Avise 1993; JSG, pets. obs.). Greenlaw and
Rising (1994:10) and Shriver et al. (2007) found
no evidence that male Nelson's Sparrows aggre¬
gated around females while mating; Montagna
(1940) presumably described the behavior of
Saltmarsh Sparrows in Maine. He (1942) ob¬
served similar social groups in Saltmarsh Spar¬
rows in Virginia: he described sparrows flushing
to a perch where they “chipped softly" (a specific
call of females [Greenlaw and Rising 1994]) and
often were “immediately assailed" by one or
more other birds, resulting in u fight on the ground
(1942:116-117).
Woolfenden ( 1956) was (he first (o characterize
the divergent social system of Saltmarsh Sparrows
duiing his work in New Jersey. He reported
promiscuity by females, but his observations of
male-female interactions involved only a few
birds. He thought fighting occurred in both male-
female groups and ali-nia/e groups. Hill (1968)
witnessed males that flew to feeding females and
253
254
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 2. June 20/2
copulated without any preliminary display. Post
and Greenlaw (1982:103) characterized male
mating behavior as “scramble-competition po-
lygytiy (Alcock 1980) without elaboration, and
Greenlaw and Rising (1994) reported non-aggres¬
sive meetings of males as well as meetings of both
sexes in which the female resisted apparent sexual
coercion. Shriver et al. (2007) confirmed that
male Saltmarsh Sparrows in Maine actively
search lor and chase females, copulate, and then
continue searching. They did not mention male-
male or male-female aggression, but noted that
mate-guarding does not occur in the species. Hill
et al. (2010) greatly improved our understanding
of intersexual relations in Saltmarsh Sparrows
from a paicmity study. Other work has focused on
habitat selection, breeding biology, space use. and
conservation of Saltmarsh Sparrows (e.g {jj_
Quinzio et al. 2001, 2002; Gjerdrum et al. 2005.
2008a, b: Bayard and Elphick 2010; Shriver et al
2007.2010),
Our 9-year investigation of the social and
reproductive biology of Saltmarsh Sparrows
began tn the mid-1970s in New York (Post and
Greenlaw 1982. Greenlaw and Rising 1994). We
focused on the social behavior of Saltmarsh
Sparrows (Post and Greenlaw 1982, 2006) with
special attention to male-female and male-male
relationships. One objective in this paper is to
prov.de details from our work on these relation¬
ships, and in particular to examine the social
dynamics of male-female mating behavior in the
species. We also provide information on cloaca!
P otuberance size as it pertains to mating behavior
and sperm competition. Another objective is to
critically evaluate the previously reported and
controversia1 interpretation of apparent coerced or
orced matings (Greenlaw and Rising 1994 10
Hd let al 2010:305) and female control of these’
Wow TW ^ I"" RiSing l994) in Saltmarsh
behavior ofTh ' CValuallon Considers the sexual
coercion m ? Spa'T°WS in the “"texts of male
Sr 99^ Kin,1,Cy fl aL l983’ McKinnt-*y and
bvarts 1 997 k ma,c ^minanot access to mates
998) Hf' t T ,9?7’ B,adbury 1981 • Wagner
1998) female choice (Alcock 1984), and Cenn e
control (Stutchbury and Neudorf 1998)
females are indefensible "fn 'male^
access to mates; consequently, females visi'tTale
aggregations during the breeding season and
mostly select dominant males as sexual partners
(Bradbury 1981 ). Females that choose mates use
plumage or behavioral cues as signals of male
quality (genetic quality or genetic compatibility
to assess potential mates (Mays and Hill 20W
Generally females initiate matings in such case'
olten in situations where males aggregate (Emlen
and Oring 1977). In contrast, females that exhibit
control of a sexual situation arc able to influence
male mating success after the male initiates an
unsolicited sexual encounter.
METHODS
Study Areas. — We studied the behavior of Salt¬
marsh Sparrows in an unaltered marsh at Oak Beach
(40 38.68' N. 73 19.03' W ) and a ditched marsh at
West Gilgo Reach (40 37.010' N. 73 24.630' Wl
New York, USA. The main vegetative cover at Oak
Beach was smooth cordgrass (Spartina altemjlora )
with a narrow border of salt meadow grasses S.
patens and Distich! is spicata at higher elevations near
stands of Phragniites australis. The West Gilgo
marsh was transected hy drainage ditches and. in
areas used by sparrows, was dominated bv salt
meadow grasses growing between the ditches, and by
marsh elder {Iva frutescens) shrubs on spoil banks
along the ditches and on the drier, inner marsh edge.
Bach study area was surveyed to produce a marked
grid with comer stakes 25 nt apart. A wire prong was
al fixed to the top of each stake to prevent large,
potentially predatory birds from using the stakes as
perches.
hi eld and Analytical Methods. —The study was
conducted front May to August. 1977-1985. when
wc captured and individually marked (with color
bands (// = 604J and dyes 1 78] or wing streamers
1 1 1 1) 80-90% of observed birds each summer. We
measured or described wing chord length, size ol
cloacal protuberance or degree of brood patch
development, fat condition, molt condition, and
mass for each captured bird.
lypes of field information obtained were
behavioral frequencies during focal area sampling
al selected points at Oak Beach, and descriptions
of well -observed social interactions in the focal
areas and elsewhere in both Oak Beach and West
Gilgo marshes by ad libitum sampling (Altman*
1974). We collected frequency information on
•social interactions and other behaviors at Oak
Beach from quadrants (encompassing two 25 X
— -m grid squares/quadrant) in cardinal direction
around open-topped blinds placed on four (1977)
Greenlaw and Post • SALTMARSH SPARROW SEXUAL BEHAVIOR
255
and two (1978) 2-in platforms with the aid of
binoculars and a telescope. The platforms allowed
us to observe birds within 25-35 m of our vantage
point and witness local travel up to 100 m.
Platforms were placed 125-1,025 m apart in the
upper intertidal zone where breeding Saltmarsh
Sparrows were numerous. No platform site was
used in more than one breeding season. Each day
(0500-1000 hrs) we randomly chose one or two
platforms from which to observe sparrows; the four
quadrants around each platform were sampled in
random sequence (3-5 on each platform daily).
Observation periods were 30 min in each quadrant
sampled. A unit observation was a bird at one
location within a given quadrant. Information on
bird identity (band combination if known), location
in relation to nearest gnd marker, and type and
duration of behavior were recorded on audiotapes
and transcribed later; unidentified individuals were
numbered sequentially during each observation
period. Each revisit to a quadrant by an individual
sparrow within a 30-min period was regarded as an
independent observation. The total number of
identified males around each platform varied front
28 to 40 during the season.
We used blinds on the ground to observe
behaviors near nests during 1979-1985. We
followed several males with wool yarn wing
streamers for timed periods in 1985 to examine
patrolling behavior of males. The yarn, which
frayed and produced it visible patch of color, was
tied loosely around the inner wing next to the body
and later removed. We Were able to identify birds
directly by band combinations in -40% of out-
observations. Sex was ascertained indirectly in
other cases by the behavior of participants involved
in interactions. Males sang, performed sequences
of lookout behavior, and initiated meetings with
females, while females uttered a specific call (Tuc
call) when they left nests containing young or
during some interspecific interactions with males.
We tested the efficacy of direct and indirect
methods of sex identification to yield similar
Irequency estimates by comparing the frequency
of male-male versus male-female classifications
across the same set of observation periods by each
method. Classifications based on behavioral iden¬
tification as male or female were statistically
indistinguishable from those derived from known
band combinations (2 x 2 contingency test with
Yates' correction, two-sided: P = 0.88, n = 209).
A male morning activity budget was obtained
for the breeding season (mid-May through Jul)
from the frequencies of observed behaviors
obtained from the timed platform observations
(n = 339, 30-min periods in 2 yrs, distributed in
30-94 periods at each of 6 platforms). We
classified activities into singing, ‘lookout’, flying,
social (male-male or male-female) interaction,
and unknown activities. We did not monitor
foraging behavior during limed periods because
we often did not know whether a bird that
disappeared into the grass was foraging or
performing some other behavior. Our impression
was that males during the early morning from
sunrise to —0900 to 1000 hrs spent most of their
time roaming their home ranges and engaging in
social interactions. The roaming behavior, which
involved perched watchfulness, flying between
perches, and singing from perches or in flight
between perches, is termed ‘patrolling’. We saw
little oven foraging by males until later in the day.
Roaming males that intermittently perched silent¬
ly in an erect, watchful posture on exposed
perches are described as performing ‘lookout’
behavior. The term ‘forced mounting’ refers to
cases in which males jumped on females without
any preliminary behavior and successfully sup¬
pressed the active aggressive resistance of a
female, and assumed a copulatory position on
her back while she crouched on the ground, often
accompanied by ‘feather-pulling’ (female’s head
leathers grasped in male's beak). Male attempts
(whether successful or not) during male-initiated
meetings to mount a resisting female on the ground
and assume a mating position are categorized as
‘pounces'. These terms are descriptive of male
behavior that we observed- The term ‘forced
mating’, which implies successful or potentially
successful insemination of an uncooperative fe¬
male following forced mounts, is avoided until the
concept is evaluated later in relation to behavior of
males during pounce events. Female control in this
study involved females successfully thwarting
forced mounting attempts of some males, either
by threatening them or by fending off their efforts
to mount. Males that were repelled gave up and left
the area. We often did not know which males
successfully suppressed female aggression, or
which ones were thwarted, because we could not
see band combinations during fast-moving or
partly obscured interactions. Solicited copulations
were uncontested and initiated by females at the
beginning of her nest cycle, and invoked a pre-
copulatory visual display typical of emb erizids
(Andrew 1956).
256
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 2. June 2012
FIG. I. Representative path of a wing-flagged male
Saltmarsh Sparrow observed for I hr patrolling its home
range (male OAGIJ. 10 Jim 1985). The male spent all its
time during this period watching from perches. Hying
between perches, and occasionally singing from perches or
in flight. Large tilled circle: First observation; lines: flight
paths: small filled circles: lookout or song posts; small bar
final observation; scale bar: 10 m.
We assessed male dispersion in relation to nest
stage by a graphical method. We assumed that
males can ascertain the breeding condition of
receptive females, and predicted their distribu¬
tions would be related to the reproductive states of
females. Thus, they would be concentrated around
nests under construction or in the process of
receiving eggs. We plotted nests and locations of
b.rds on grid maps. We used the Poisson
distribution to calculate a coefficient of disper¬
sion, Dt, the ratio of observed variance to mean
Rohlfn.QQs! °SUITence in sma" P|ots (Sokal and
Rohlf 995). We tested the significance of the
observed distribution's departure from random
dispeiston with Chi-square goodness of fit
analyses (Zar 1984, Brower et al. 1990)
Saltmarsh Sparrows have a large cloaeal protu¬
berance (cp), which may be used as an index or
sperm competition (Birkhcad et al. 1993). The
fnsha^fm6 k SaUmarsh Sparrows is cylindrical
m shape from base to top. as confirmed by diameter
weesZTj" °n aSamp,e of Protuberances. Thus,
e estimated cp size (min') as the volume of •,
cinder (Briskie 1993,. We examined cp “L
year rmr'r8 "’“'p ba"dcd durin« halch-
calendTe f “ h,nc,ion °f ^ measured as
calendar year classes I to 5. Sample sizes were
versus oTderT T" !,year* and Wc spared first-year
We used ' S PS T'v' " * ' W m ClaMi fica 1 1 on ■
notation follows Sokal and Rohlf (1995) and the
rejection level was 0.05. Means are reported with
standard errors.
RESULTS
Male Mate-searching Behavior. — Males spent
about 75% of their time from 0500 to 1000 his
patrolling their home ranges (n = 5,205 unit
observations witnessed during 173 hrs of timed
periods). They roamed over circumscribed area'
(Fig. I) within their home ranges, spending
47.4% of their time on lookout. 16.8% singing.
16.3% in sexual-social interactions, 12.2% in
Rights (including flight-singing), and 7.3% in
unknown activities. Mean duration of lookout
sessions was 27.0 ± 1 .28 sec per perch (w = 417),
anil of singing bouts (on I or more consecutive
perches and song flights between them) was 16.5
1 1.15 sec (n = 203). The morning roaming
behavior was associated with male-female and
male-male meetings and appeared to be searching
behavior. Males also searched the ground, fre¬
quently emerging and peering from the top of llie
grass, then disappearing into the turf again.
Types of Social Interactions.— We recorded
1,265 inter and intrasexual encounters based on
band combinations or behavioral identifications
during 173 hrs of timed observations (Table I)-
Male-female interactions were overtly or appar¬
ently sexual in nature. Male-male interactions
mostly involved perch takeovers or meetings with
any more distant sparrow that turned out to be
other male Saltmarsh Sparrows.
Male-female Interactions.— We observed 593
male-female encounters (Table I) in which a
female solicited copulation, attacked or chased a
male, or fought with a male in male-initialed
meetings. One or more males met a female on the
ground or joined a flying female, at times striking
or grabbing her in the air and knocking her to the
ground. A male that met a female on (he ground
usually attempted to mount her immediately, or
stayed on the sidelines while the pounce effort of
another male proceeded.
typically, intersexual encounters witnessed
from platform blinds were meet-and-pounee
encounters. Sixty-five percent of these interac¬
tions (range = 56.6-79.0) involved a single male
and female. The other cases consisted of iwo lo
seven males that met one female. Usually one
( -'90% of cases) or occasionally two or three
males at the multi-male meetings attempted to
mount the female. Up to four or five males in
Greenlaw and Post • SALTMARSH SPARROW SEXUAL BEHAVIOR
257
TABLE I. Frequencies of social interactions and outcomes of intersexual encounters in Saltmarsh Sparrows in
New York.
All interactions' Inlersexual outcomes (M-F)“
Platform (Yr)
location
n
M-M
M-F
F-F
Unknown
n
Male mounts
(Fs)
Male
thwarted1'
Female
solicited'
Unknown
JO (77)
372
160
157
0
55
25
6 (6)
16
1
2
03 (77)
396
124
202
0
70
17
8(8)
5
1
3
Y-2 (77)
183
57
99
0
27
0
-
-
-
-
Y-l (77)
20
9
6
0
5
0
-
-
-
-
10(78)
145
78
67
0
0
9
5 (5)
2
0
2d
NO (78)
149
84
62
0
3
23
8 |7)
12
0
3
OBM/WGM
[1581
[21
96
36 (34)
48
5
7
Totals
1.265
512
593
0
160
170
63 (60)
83
7
17
Percent
100.0
40.5
46.9
0.0
12.6
100.0
37.1
48.8
4.1
10.0
:i Frequencies in the left panel are based only on local area (limed) samples from platform blinds in 1977 and 1978 at Oak Beach Marsh tOBMl. and observations
in the right panel describe outcomes of well-observed cases of male (Ml - female (Ft interactions on OBM and West Gilgo Marsh iWGMl. AJ libitum samples ( ) in
the left panel are shown to represent the two female-female interactions witnessed on OBM. but these data are not included in the two end rows of the panel. ‘All
interactions' refen to the total number of agonistic and social encounters detected in each social category The frequencies in the right panel are based on all
observations regardless of source (platform or ad libitum samples on the marshes). Male-lemalc interactions include single and multiple male meetings w ith a single
female. ' Inlersexual outcomes' arc results of witnessed male-female interactions in well-observed cases. Number of instances of post-copulatory flight singing (Fs)
by the male after a female was successfully subdued is in parentheses.
b Other males interfered in the mounting attempt, or female successfully fended male off.
1 Actual frequency of solicited copulations is underestimated by the observed frequency reported here.
'' Male Seaside Sparrow (A. imiritimus) interfered and disrupted the interaction in these two cases
these groups were passive ‘watchers’ of the
mounting effort. We found only males in 18
cases where we identified individuals in the
watcher group. Females in 37 of 63 well-observed
cases of successful mountings pursued the male
briefly while uttering Tuc calls as he departed. At
other times, the female disappeared silently into
the grass. Males typically grasped the female’s
head leathers during forced mountings. Attempted
mountings by males occurred without any pre¬
liminary visual display. Females resisted male
mounting attempts except in instances when they
solicited. Overall, females successfully thwarted
males in 57% of 146 pounce cases (Table 1 ).
Threat postures or Tuc calls were sufficient to
discourage the male in some instances. The female
at times evaded the male and silently disappeared
into the nearest cover and hid. The male withdrew
silently in all well-observed mountings that were
thwarted. In contrast, the male flight-sang as he
departed in 95% of encounters in which he subdued
and mounted the female. His departure behavior
proved to be a reliable marker of successful
suppression of female resistance to male mounting:
post-copulatory flight-singing was not associated
with female-solicited matings (// =7). Males at
times also uttered a muted song while interacting
with a resisting female (n - 12). Female resistance
often appeared to be quite vigorous. Frequently,
before the male was able to mount, the two tumbled
on the ground, or flew up vertically, fighting
breast-to-breast. These encounters were silent and
lasted for 5-15 sec. The male usually pursued
females that escaped, and the struggle resumed at
another site. Males that successfully suppressed
female resistance immediately assumed a copula-
lory position on the female's back. At this stage of
the interaction, the female typically crouched on
the ground with lowered tail as the male mounted
and grasped her head feathers. We have no
evidence the passive female after a fight cooper¬
ated with the male during aggressive mountings by
raising her tail and exposing her cloaca.
We observed only seven female-solicited sex¬
ual encounters with males. One female copulated
with at least two males and another female
copulated with at least three different males. The
others were observed on one occasion with one
male. This low number reflected our protocol of
making only opportunistic observations of fe¬
males building new nests as we checked nest
status or walked in the vicinity of nests. Male-
female intercepts and pounces were conspicuous,
and female soliciting behavior was inconspicuous;
thus, we believe our observations under-represent
the frequency of female sexual solicitation. We
observed pounce interactions almost daily during
our study at Oak Beach, perhaps reflecting the
258
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 2. June 2012
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pool
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1 ) in areas with no active nests, panel \ (JO 1 7 Mav ‘J'spt'rsion 111 relation to female presence: little contagion U
strong contagion (Dt»lj, panc| c (J0 Q Ju| 7 ’■ "J^crate contagion (D, > |). panel B (JO. 22 Jun 1977]). ar
!lnC.e.mt!led nearnests ^ nest-building (Nnh) or eeP-lLin,, ? ’ ‘° Ju" '977)' ln lhe ,ast two cases, male activity
separated nesLs with eggs (Nin> or young (N ) or whh f'lT in COntrasl to lit,le activity in the vicinity of wel
ma^e lookout singing, flight-singing; 'T* —* ^'bo.s: small, opened
meeting a female; large, open circle- =;5 occurrenr 1 I"a 1 meeting u female: large closed circle: two or mot
male meets another male. " Ces of Iookout singing males at a single locus: closed triangle:
high local densities of females. Estimated fe
fnl978eweere|Were 19/10 *" in 1977 and 20/
m 1978 We also wttnessed pounce interac.io
the area 8 and ,n °ther tidal marsh.
las“ JcPTher Saltmarsh SP°f
hill T ^male crouched, raisec
Wl and tail, and quivered her wings, but up
srr 1
- JJT2LT
seldom approached them; we saw males at nests
three times during 76 hrs observing 25 nests.
Twice during these three cases, the female was
present and chased the male away.
Male-male Interactions.— We witnessed 512
male-male encounters in 1,265 interactions at
Oak Beach (Table 1). No cases of inter-male
aggression were witnessed during male-female
pounce interactions. Two or three males at times
vied for access to the female during mounting
attempts, but our observations indicate these
interactions involved interference rather than
focused hostility toward one another. Males
•sc orn exhibited aggression towards other males
tvv ere in the marshes. We recorded details of
Greenlaw and Fust • SALTMARSII SPARROW SEXUAL BEHAVIOR
259
192 male-male encounters among the 512 inter¬
actions of this type that we w itnessed (Table I ).
Wc observed 143 (74.5%) non-agonistic meetings
between males, in which one or several males
approached another male and then separated. 4b
(23.9%) cases of attempted perch takeovers by
supplants, and three short chases (possible sex
mis-identification) and two brief fights (1.6%).
Seventy-nine percent of the perch -takeovers were
successful and. in most cases, no further interac¬
tion occurred. The only agonistic displays that we
saw during male-male aggressive interactions
were gaping by a male when it was approached
too closely by another, or ‘head-forward threats'
(crouch and bill pointing) that usually forestalled
a perch takeover.
Male Sexual Activity in Relation to Female
Reproductive State.— Wc observed meet-and-
pounce interactions in all stages of the nest cycle.
We were able to ascertain the incidence of forced
mountings in relation to females’ reproductive
status in 69 cases. We normalized the number of
observed mountings by the length of the nest
stages (nest-building lasted 6 days; deposition and
incubation of eggs. 15 days; care of dependent
young, 25 days). The highest rate of forced
mountings, 4.0 mountings/day (»/ 24). occurred
during nest-building, when females are assumed
to be fertile. This rate declined to 1.5/day (» : 23)
during the egg stage, and 0.9/day ( n 22) when
the female was provisioning young. The occur¬
rence of forced mountings differed between nest
stages (x2 = 23.6. df = 2. P < 0.001).
Male Dispersion in Relation to Females. — Use
of space by males was related to locations of
fertile females (Fig. 2). Male social activity was
significantly contagious in areas where at least
one female was nest-building or egg-laying (C'hi-
square tests, P < 0.01; mean coefficient of
dispersion Dt = 3.2 ± 1.62, n - 29) (Fig. 2).
Maximum observed I), values were associated
with female presence near nests under construc¬
tion (mean D, = 4.5 ± 1.38. n = II). Males
usually left Two-calling females alone at such
times after they met them and were not concen¬
trated near their nests in the same area (Fig. 2B).
The mean D, was 1.9 - 0.92 tn = 18) (e.g..
Fig. 2A) on days when no active nests were in the
focal areas.
Cloaca! Protuberance. — Breeding male Salt-
marsh Sparrows have large cloacal protuberances
(cps). Size of cps increased from a quiescent
condition at the time residents arrived in late April
until peak size was reached in mid-May. Volume
of cps averaged 562.8 ± 12.39 mm’ (n = 156)
after mid-May. Most (70%) cps were >500 mm3.
Mean protuberance height was notable as well,
averaging 7.4 ± 0.08 mm.
The range of cp sizes in young males (11-
12 months of age, or I yr) included the range of
older (>l yr) males. The variance was signifi¬
cantly greater in young males than in older males
(one-tailed) (F = 2.943, df = 18, 16; P = 0.041).
Fifty-six percent of young males in our sample
had cp volumes at least as small as the minimum
cp size (445 mm’) of older males.
DISCUSSION
Characteristics of Mating System. — This study
focused on the sexual and agonistic behaviors that
characterize the mating system of Saltmarsh
Sparrows. Our work provides an important but
only partial perspective of the mating system in
the species. Genetic information on parentage is
equally valuable, and findings from the two
perspectives should be in agreement (Johnson
and Burley 1997). Hill et al. (2010) reported an
extreme level of multiple mating in Saltmarsh
Sparrows. All broods that were fully sampled in
their study exhibited evidence of multiple pater¬
nity.
Our work is the first to describe the behavioral
dynamics of mating in detail in Saltmarsh
Sparrows. The earliest reports by Montagna
(1940, 1942) and Woolfenden (1956) were
suggestive of an unusual mating system in the
species, but their accounts were anecdotal,
incomplete, and partly contradictory. Montagna’s
(1940. 1942) important contribution was his
description of multi-male meetings with a female
that involved apparent attempts to mate with the
female against her resistance. He also reported
male-only meetings. Woolfenden (1956) docu¬
mented non-territorial behavior, and absence of
paternal care and pair bonds. He witnessed
lighting in male-female and in all-male groups,
but his views were qualified and uncertain.
Our evidence confirms that some aspects of
sexual behavior in this promiscuous species are
unusual and, perhaps, unique among passerine
birds. Fertile females also solicit copulations
silently from males in an otherwise conventional
fashion among emberizid sparrows (Andrew
1961). The most visible characteristic of male
sexual behavior is the meet-und-pounce interac¬
tion initiated by the male. Males spend morning
260
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 2. June 2012
hours patrolling their home range, stopping on
successive perches and watching the surrounding
areas, and flying out to inspect distant sparrows or
meeting females. Males apparently practice a
form °l scramble-competition polygyny, hut the
implications of this behavior need to be further
explored. Only one other promiscuous passerine,
the Aquatic Warbler ( Acrocephulus paludicola)
(Dyrcz 1989: Birkhead 1993; Schulze-Hagen
et al. 1995, 1999), is also known to perform
scramble-competition polygyny, but differs in
some details from the behavior we report for
Saltmarsh Sparrows. One difference is the ab¬
sence of meet-and-pounce behavior in Aquatic
Warblers. A key element in the Saltmarsh
Sparrow sexual system is that most males behave
as if they do not know the locations of most nests.
Two forms of evidence support this conclusion’
the rare appearance of males at active nests of
females, and the frequent practice of meet-and-
pounce interactions in all stages of nesting. The
alter behavior suggests that males often do not
know the fertility status of females in their home
ranges Females are quite stealthy around their
nests during early stages of the nest cycle and
chase males that approach the nest site. Male
patrolling and meet-and-pounce interactions in
conjunct, on with female sexual solicitation, must
be understood in the context of individual marine
tact,cs (Trivers 1972, Johnson and Burley 1997)
sexual* h N*,ta,m*cs °f Mating.- Male and female
sexual behavior ,n Saltmarsh Sparrows may
involve aspects of male coercion (forced mating?
female control, and female choice. We found no
common!?0' d°minance P^Vgyny, which
commonly occurs m other promiscuous avian
i
iwcvjss Sr and °ring i977- Bradbu^
species. Overall the U" expressed 1,1 the
ized by apparent n l"8 syste,n is character-
females^ nS ? foLTm,SCU -y by malcs
female control of coerced bch°vior’ and
oerced mounting attempts. We
found no evidence that male Saltmarsh Spanovw
followed and guarded females in New York, nor
did Shriver et al. (2007) in Maine. Consequently,
we must examine the possibility of forced mating
behavior by males and female control of this
behavior, and consider whether female choice
could have a role in the mating system exhibited
by Saltmarsh Sparrows.
It males do not know the locations of nests of
most females, or do not check them regularly, as
we believe, some males may pursue a mixed
sexual strategy of accepting solicited matings
initiated by females and practicing forced mating1
with females when they find them at other times
(McKinney et al. 1984). We do not know how
widespread this second behavior may be among
males, but we witnessed it daily during any
extended period of observations in two marshes.
Our interpretation of mounting behavior as
forced mating is provisional because we provide
no evidence that insemination actually occurs
without female cooperation. However, based on
behavior and morphology, we argue that such
matings are possible, and perhaps likely. The
aggressive tactics (pecking, wing-beating, grap¬
pling, and tumbling) that occurred between a male
and female during pounces in Saltmarsh Sparrows
were similar to actions used by males fighting
over territories (Andrew 1956, Post and Greenlaw
1975). The coercion tactics of males resemble
those ol socially monogamous species that also
practice forced mating; it occurs as well -n
extrapair matings (McKinney et al. 1984. Birk-
head ct al. 1985. Edinger 1988. Burley et al.
1994). Phis behavior is well-known among
dabbling ducks (McKinney et aJ 1983, Sorenson
1994).
Female resistance has been viewed as evidence
ol forced mating (Birkhead et al. 1989), yet recent
studies indicate that females initiate and control
extrapair matings (Wagner 1991. Stutchburv and
Neudorf 1998). The ability of female Saltmarsh
Sparrows to either discourage some males I rum
attempting to mount, or to thwart their mounting
efforts, are elements of female control, but not of
female choice. Some males, perhaps those more
vigorous and persistent, are able to overcome the
resistance of females. Some observers (e.g-
ohwer 1978) are convinced that successful
copulations in birds require the cooperation of the
female but Morris (1957) reported that in Bronze
Mannikins (Lonchura cucullata ), cloacal contact
> males when females were uncooperative
Greenlaw and Post • SALTMARSH SPARROW SEXUAL BEHAVIOR
261
apparently was fairly easy on the ground but not on
perches. All forced mountings that we observed by
Saltmarsh Sparrows were on the ground, where the
elongation of their cloacal protuberances may
secondarily facilitate cloacal contact in passive
females.
If males do not achieve cloacal contact during
forced mountings because females arc not coop¬
erating. their mounting behavior may still be a
measure of their ability to successfully suppress
female resistance. Their success may be affirmed
vocally by post-mounting flight singing. The
information gained by females about local males
during meet-and-pounce interactions may be used
when they are fertile to selectively choose mating
partners. Male ability to suppress female resis¬
tance varied from non-involvement at multi-male-
female meets (’watchers') and giving up during a
mounting effort with female resistance, to suc¬
cessful mounting despite resistance. Such behav¬
iors may represent variation in male quality of
importance to females in a promiscuous mating
system in which forms of male dominance
polygyny have not evolved.
The primary support for the hypothesis of
forced mating in Saltmarsh Sparrows is indirect
evidence provided by very large cp (this paper)
and testis sizes (Rising 1996) of males. The direct
relationships between cp size versus sperm
storage (Birkhead el al. 1993) and testis size
versus copulation frequency (Moller and Briskie
1995) in passerine birds are well established.
Greatly enlarged cps and testes in males implies
strong sperm competition (Birkhead and Mol let
1992, Moller and Briskie 1995). Extreme testes
sizes among passerines of similar body sizes are
found in polygynandrous Smith's Longspur (C«/-
carius pictus), promiscuous sharp-tailed sparrows
of both species, and obligatcly polygynous Lark
Buntings (Calamospiza melanocorys) (Rising
1996) . We suggest these morphological or
anatomical adaptations (Briskie 1993) would not
be as strikingly enlarged as they are in these
species unless rates of solicited copulations were
high (Birkhead et al. 1993). We believe we would
have noticed the behavior more often than we did
under our field protocols if solicited copulation
rates were unusually high in Saltmarsh Sparrows.
Apparently, solicited extrapair copulations from
one or a few males are widespread in socially
monogamous passerines, but none of these species
exhibit extreme development of testis or cp sizes
(Birkhead et al. 1993, Rising 1996, Stutchbury
and Neudorf 1998). Thus, forced mating seems to
be the only behavior in Saltmarsh Sparrows that
might account for extreme testis and cp sizes in
the species.
We provide evidence for female control of
forced mounting attempts by male Saltmarsh
Sparrows. Nearly two-thirds of the pounce events
reported in our study were thwarted by female
resistance or aggressive calling. Under the
hypothesis of female control, female resistance
is viewed as a manipulative tactic rather than cost-
reducing behavior ( Westneat and Stewart 2003).
Female resistance as cost- minimization implies
little advantage to males that simply suppress
female aggression and then fly off without
prospect of future benefit. However, females that
use information gained by their resistance to favor
successful males later when females solicit
copulations may be practicing a form of mate
choice based on male vigor and persistence during
forced mountings. Thus, although speculative,
female control of unsolicited mountings in Salt¬
marsh Sparrows may involve some element of
female choice later during her fertile period.
Overall, the behavior described in our study under
forced mating and female control hypotheses
imply that extreme levels of mulli-parented
broods in Saltmarsh Sparrows (Hill et al. 2010)
may best be understood by the promiscuous
behavior exhibited by both males and females.
However, we cannot exclude the view that
females selected to solicit matings from multiple
males also can explain extreme levels of multi-
parented broods in the absence of fertilizations
during coerced mountings by males (Hill et al.
2010).
Evolution of Mating System. — Saltmarsh Spar¬
rows exhibit a highly derived social system.
Several authors have offered views on the
evolution of tidal marsh sparrows (Beecher
1955. Greenlaw 1993. McDonald and Greenberg
2006, Shriver et al. 2007), and others have
identified specific social or ecological factors that
may have been important during the evolution of
sharp-tailed sparrows (Murray 1969, McDonald
and Greenberg 2006. Shriver et al. 2007. Hill et al.
2010). The marshland sparrows form a well-
corroborated monophyletic group (Klicka and
Spellman 2007). The conditions that favored the
evolution of apparent scramble competition po-
lygynv in Saltmarsh Sparrows may he elucidated
by considering the behaviors of its closest
relatives. Seaside Sparrow (A. maritimus) and
262
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 2. June 2012
Nelson's Sparrow. The former speeies is socially
monogamous (Greenlaw and Post 1985, Hill and
Post 2005). while the latter has a derived social
system that hears some similarity to that of the
Saltmarsh Sparrow, hut differs in the species’
practice of apparent male dominance access to
females and mate guarding (Greenlaw and Rising
1994, Shriver et al. 2007). The condition ancestral
to the derived systems of the sharp-tailed
sparrows almost certainly was social monogamy,
in which male mate guarding and extrapair
fertilizations were important adjunct mating
tactics. Any plausible model for the evolution of
social behavior must be able to account for a suite
of related questions that address both species of
sharp-tailed sparrows, and account for develop¬
ment ot promiscuity and sperm competition, loss
of territoriality, disappearance of pair bonding,
and absence ol paternal care. Considering the
phylogenetic history of the group (Klicka and
Spellman 2007), we suggest dial social evolution
occurred in a two-step process in the sharp-tailed
sparrows (Greenlaw 1993. model B). As yet, we
do not have a single synthetic model that meets all
these criteria and provides insights into the
evolution ol the social system of Saltmarsh
Sparrows. Much work remains to confirm and
extend our findings, and to understand social
evolution in these birds.
ACKNOWLEDGMENTS
A supplement that details well-observed examples o
social interactions in Saltmarsh Sparrows taken from ou
icld notes is available on request from the authors. W
thank C. S. Elphiek for his helpful critique durin
manuscript development. A draft of the manuscrip
benefited from the comments and suggestions by (’ p
Hraun and two anonymous referees, to whom wc an
grateful. The work reported here was supported bv Nutiona
Science Foundation Grant # HNS 77-07314 and bv fund
rom the C. W. Post Research Committee of Long Islam
University We thank the Long Island State Park Commis
s.on and the Town of Babylon for allowing access to ou
study areas.
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GJERDRUM. C, C. S. ELPHICK, AND M. A. RliBEGA. 2
siagsvold 1996. Ball 2000. Rivers and Kroodsma'
2000). Veeries will encounter more acoustic
competition at dawn than at dusk, if many of the
other species that share habitat with Vecries sine
at dawn but only some also sing at dusk. Our
objective was to test this prediction by comparing
the amount and type of interspecific vocal
masking that Veeries experience during dawn
and dusk choruses.
METHODS
We recorded samples of natural Veery singin
rom a color-banded population at the Car
Institute of Ecosystem Studies in Dutchev
County, New York, USA from mid May to lat
June in 2009 and 2010. The -325-ha Car
Institute property (41 50’ N. 73 45' W) i
dominated by a second-growth oak (Quercus spp
and maple (Acer spp.) forest with paths, trails an
ephemera1 wetlands throughout. Common bird
habiting the wooded areas include Ovenhird
;.w/uv at,roc“PMoh American Robins (Turd,,
migra,orius), and Wood Thrushes (HvlocZ
ZT (KAS. unpubl. data). Wc S fo
Zn TdPduSsk°fhVeCry *h«,n* "uri"
sunrise and sunse,. We recorded sanies ofV^
song using a Telinga parabolic reflector, a Senn-
heiser MKH 62 microphone, and a MaranlzMPD
000 digital recorder (sampling rate of 44.1 kHz. bit
rate of 705.5 kbps). This equipment allowed us i
collect high-quality directional recordings th.i:
focused on the song of the focal bird in a way that
approximates how a receiver (perhaps a potential
mate or rival) would be listening. We fixtusd on
collecting the best-quality recordings of Veery song
that were possible (at close range, which is
challenging with such visually and bebaviorally
cryptic birds) w ithout reference to die singing of
other species.
We selected 34 dawn and 34 dusk recordings to
analyze based entirely on the spectrogram quality
of Veery songs in the recording (high signal to
noise ratio), We used observations of color band-
singing locations, and spectrographic comparisons
ot song types to ensure that each sample in each
ol our dawn and dusk pools of recordings came
trom a different male. Nine males were recorded
both at dawn and at dusk, while 25 males were
recorded only once, either at dawn or dusk. Wf
discarded any recording that included songs from
more than one Veery because countersinging is
olten characterized by higher song rates, which
would shorten the time available for heterospe-
eilie masking, possibly biasing our measurements
We found conspeeific masking by Veenes was
relatively rare, possibly because Veeries have
large territories and because individual males
appear to only sing at specific intervals during the
breeding season (KLB and KAS. unpubl. data'
Spectrogram analysis was conducted vwtb
Raven Pro 1.4 (Cornell Laboratory of Ornitholo¬
gy- Ithaca. NY. USA). We selected a segment
from each recording containing the 10 consecu¬
tive songs of the highest quality for analysis. 'V
standardized the amount of Veery singing that -* e
sampled by analyzing a subset of 10 songs ft®01
our dawn and dusk recordings. We have r.oi
noticed a difference in the amount or rate of
singing by Veeries at dawn and dusk but. because
wc have not measured this explicitly, we decide
to control for the possibility that the amount of
singing might differ.
We counted the number of Veery' songs dwt
were masked by another species’ song in each 10-
s°ng segment. A song from the focal male was
considered masked if any heterospecific avian
vocalization measuring 75 db or above (measured
using Raven s average energy measurement !t"’l
overlapped it in frequency and time (Fig- D-We
Belinsky et a!. • ACOUSTIC COMPETITION IN VEF.RIES
267
FIG. I. Sound spectrograms of three Vecry songs: one
unmasked (A), one masked by a Black-capped Chickadee
(B), and one masked hy an Ovcnbird (C).
chose this amplitude threshold to mimic the
experience of a hypothetical receiver. We decided
that if a masking vocalization was below 75 db, it
was not sufficiently loud to truly disrupt commu¬
nication between the singer and hypothetical
receiver (the recordist). This threshold should be
considered arbitrary as choosing a consistent
threshold for ruling out soft/distant vocalizations
was the primary goal. We attempted to identify
the species of bird masking each masked Veery
song. We calculated the mean number of masks
occurring among the 34 dawn 10-song samples
and compared it with the mean number occurring
in the 34 dusk samples. We also compared the
mean number of different species masking in the
dawn and dusk song samples. We used JMP 5.0
software for Mac (SAS Institute Inc. 2004) lo
conduct two-tailed Student's /-tests.
RESULTS
The 68. 10-song segments were 61 ±2.8 sec
long (mean ± SE). The length of the 10-song
segments did not differ between the dawn and dusk
recordings, indicating that singing rate and/or song
TABLE I. Number of Vecry songs masked by all
unidentified and identified species at dawn and dusk.
Identified species include: Gray Catbird. Ovcnbird. Wood
Thrush. American Robin, Tufted Titmouse ( Baeolophus
hiculvr ), Red-eyed Vireo. Common Ycllowthroat ( Geothlvpis
irichcis). Red-bellied Woodpecker ( Melanerpes carolinus).
Black-capped Chickadee i Puerile citiiccipillus). Blue-headed
Vireo (Vireo solitarius). Barred Owl (S/m voria). and Rose-
breasted Grosbeak ( Pheucticns liubviciaims).
Masking species
Dawn songs
masked
Dusk songs
masked
Unidentified
10
17
Gray Calbird
20
6
Ovenbird
16
8
Wood Thrush
11
4
American Robin
3
5
Tufted Titmouse
4
2
Red-eyed Vireo
6
0
Common Yellowthroat
1
2
Red-bellied Woodpecker
2
1
Black-capped Chickadee
2
0
Blue-headed Vireo
1
0
Barred Owl
I
0
Rose-breasted Grosbeak
1
0
length did not differ between our samples (dawn =
60 ± 2.8 sec, dusk = 59 ± 2.8 sec: Student’s /: n —
34, 1 = 0.19, P = 0.86).
One hundred and twenty (17.6%) of the 680
Veery songs we recorded were masked by another
species' song. Veery songs were masked 2.4 ±
0.4 times per 10 songs at dawn and 1.2 ± 0.4
times per 10 songs at dusk (Table 1). Veeries
experienced more acoustic competition at dawn
than at dusk and. although this difference was
marginally significant (Student’s /: n = 34, / =
2.0. P = 0.05). the effect size was just below the
cut-off for medium level (Cohen’s d - 0.49.
medium effect si/e >0.5). Significantly more
species contributed lo masking at dawn than dusk
(Student’s /: // = 34, / = 3.1, P = 0.003), and this
effect size was medium (Cohen's d - 0.75. large
effect size >0.8).
At least 12 species masked the Veery songs in
our sample (Table I). All 12 species masked at
dawn, but only seven of these masked at dusk and
no species masked only at dusk (Table I). The
species that masked Veery songs most commonly
in both dawn and dusk samples were Gray Catbird
( Dumetella carolinensis), Ovenbird. and Wood
Thrush. The Gray Catbird masked many or all of
the Veery' songs in the recordings in which it
appeared (26 masks in 4 samples ). while the
268
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 2. June 2012
Dawn Dusk
FIG. 2. Average number of masked Veery songs and
average number ol masking species for Veery song samples
recorded at dawn and at dusk. Error bars represent standard
errors; P-values represent results from two-tailed
Student's /-tests.
Wood Thrush masked lewer songs per sample (15
masks in 4 samples), and the Ovenbird masked
few songs per sample, but appeared in the greatest
number of samples (28 masks in 1 1 samples).
DISCUSSION
Veeries tended to experience less acousti
competition from other birds’ songs during th
dusk chorus than during the dawn chorus. Mor
Veery songs were masked and a larger number o
species masked the Veery songs at dawn. Much o
the masking was caused by three common specie
at our site, all ol which produce songs that share
wide frequency range with Veery song. On,
species, the Wood Thrush, is closely related t«
the Veery and has songs with similar spectra
properttes (Dilger 1956, Borror 1964). The othe
two species. Gray Catbird and Ovenbird. tend h
sing loudly, at high amplitudes (KLB. JLH. an<
KAS’ Pers' obs-)- We observed Veeries will
tern tones near forest edges experienced high rate-
of masking Irom Gray Catbirds, which sing nearly
ontinuous bouts of song that varied widely in
length. I he major, ty 0f the territories that we
sampled were not edge territories. These results
represent the first empirical data documenting
natural differences in acoustic competition at
dawn and dusk.
We do not know of any other studies that have
compared hcterospecific acoustic competition dur¬
ing the dawn and dusk choruses, hut a number of
studies have found species adjust the short-term
timing of their vocalizations to avoid acoustic
competition. Knapton (1987) found Eastern Mead¬
owlarks (, Sturrwlla magna) adjust the timing of
their songs to avoid masking the songs of
con specifics, and Brumm (2006) found Common
Nightingales ( Luscinia megarhynchos) also avoid
cd overlapping playback of recorded heterospecific
songs. Ficken et al. (1974) reported Least Fly¬
catchers ( Empidonux minimus) and Red-eved
Vireos ( Vi re o olivuceu.s) adjusted the timing of
their songs to avoid overlapping each other. Popp
et al, (1985) found several passerine species it) a
Wisconsin forest community avoided overlapping
songs ol other species more often than they would
by chance. Ovenbirds regularly achieved this
overlap reduction by singing just after the end of
another bird's song. Planque and Slabbekoom
(2008) found birds in a neotropical rainforest
community that signaled in often-used frequency
ranges overlapped each other’s songs less often
than expected by chance.
Our results indicate Veeries experience more
acoustic competition at dawn than at dusk, and we
hypothesize these birds may sing at dusk to
compensate for their loss of efficiency in commu¬
nicating at dawn. Veeries and other thrushes may
have evolved a pronounced dusk chorus partly to
compensate lor the acoustical competitive disad¬
vantage caused by their complex song stmeture and
thickly vegetated habitat. If this is tme. acoustic
competition may represent one previously unstud¬
ied factor shaping the evolution of dusk singing bv
the Veery and other dusk-chorusing species.
ACKNOWLEDGMENTS
We thank B. L Kuss and J. K. Kelly for help with
spectrograph ic analysis, and E. C. Duke for help collecting
some of the recordings. Wc thank D. A. Spector and an
anonymous reviewer for help in improving the quality of
the manuscript. This research was funded by National
■Science Foundation (DEB 0746985) to KAS and a
Research Experience for Undergraduates gran, I.DBI
0552871) to Alan Berkowitz at the Cary Institute ol
Ecosystems Studies distributed to JLH. Our methods were
approved by the IACUC of Texas Tech University, protocol
# 08047-02.
Belinsky et al. • ACOUSTIC COMPETITION IN VEERIES
269
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The Wilson Journal of Ornithology 124(2):270-276. 2012
MATING AND BREEDING SUCCESS DECLINE WITH ELEVATION
FOR THE PACIFIC WREN ( TROGLODYTES PACIF1CUS) IN COASTAL
MOUNTAIN FORESTS
LESLEY J. EVANS OGDEN.1 MICH A EL A MARTIN.1 2 AND KATHY MARTIN134
ABS I RAC T. We studied the population ecology of Pacific Wrens t Troglodytes pacificus) in 2003 and 2004 breeding
across elevations from 1(H) to 1,300 in in coastal mountain forests in southwestern British Columbia. Canada to examine if
this spec.es «s adapted to upper montane and subalpine habitats. We found fewer territories at high elevation, a higher
proporimn ot unmated males, fewer nests per mated male, and no returns of banded adults or juveniles. The breeding season
was 61 ■*> shorter (31 vs. 79 days), and mass of nestlings (at 11-12 days of age) and nest survival were lower at hiah
elevation compared to lower elevation sites. Clutch size, incubation and nestling periods, parental provisioning rates of
nestlings, and adult morphology did not vary with elevation. Annual fecundity measures declined with increasing elevation
with no apparent compensatory increases in other vital rates such as survival of adults or offspring. Received 27 October
201 1. Accepted 23 December 201 1.
I lie Pacific Wren (Troglodytes pacificus), a
small migratory songbird that breeds in coastal
coniferous forests of western North America, was
recently described as a species distinct from (he
Winter Wren (T. hiemalis) in the rest of North
America and the Eurasian Wren (T. troglodytes)
in Europe (Wesolowski 1983, Toews and Irwin
2008, Chesser et al. 2010). Pacific Wrens are
common birds of northern temperate coniferous
and mixed forests of North America, but there are
few studies of their breeding ecology and nesting
success (McLachlin 1983, Van Home and Bader
1990. Waterhouse 1998, De Santo et al. 2003).
The Pacific Wren breeds across an elevation
gradient from sea level to upper montane and
subalpine habitats along the west coast of North
America (Toews and Irwin 2008).
High mountain areas are characterized by
variable weather, cold temperatures, and short
breeding seasons (Martin 2001). At least 90 bird
species breed across wide elevation gradients,
some of which range from sea level to alpine
habitats, but their ecology, behavior, and life
history at upper elevation limits arc poorly
understood. Short breeding seasons at high
elevations translated into lower annual fecundity
for the few species studied, particularly when the
'Centre lor Applied Conservation Research. Department
ot Fores. Sciences. 2424 Main Mall. University of British
Columbia. Vancouver. BC VfiT IZ4. Canada.
-Centre for Wildlife Ecology. Department of Biological
ciences, Simon Fraser University. Burnaby. BC V5A IS6
Canada.
V4KE7N^c^ulaanatl:,' ^ RohcrtSOn Road’ Delta. BC
J Corresponding author; e-mail: Kathy.Martin@ubc.ca
270
ability to initiate nesting was influenced by snow¬
melt phenology (Martin and Wiebe 2004. Martin
et al. 2009, Wilson and Martin 2010). Birds
breeding al high elevations appear to compensate
lor reduced annual fecundity by increasing their
per capita parental care, thus improving juvenile
survival (Badyaev and Ghalarnor 2001). Body
size ot adults and egg size both increase with
increasing elevation (Bears et al. 2008. Zeng and
Lit 2009, Lu et al. 2010). Several songbird species
trade reduced annual fecundity for increased
survival of both adults and young in high
elevation populations (Bears et al. 2009. Martin
et al. 2009. Camllcld et al. 2010). These studies
louml intra-specific differences with elevation as
high elevation populations shifted to a “slower
lile history with a longer life span, fewer offspring
per breeding season, but greater investment in
parental care. 7 he length of the breeding season
sharply decreases with increasing elevation due to
later snow melt and shorter vegetative growth
seasons, and birds increase their per capita
parental investment. Birds at higher elevations
are larger, heavier, and have higher survival
(Bears et al. 2009. Martin et al. 2009, Cornfield
et al. 2010).
We investigated variation in the breeding
ecology of the Pacific Wren along an altitudinal
gradient from 100 to 1.300 m. We predicted that
as elevation increased: (1) breeding season
duration, the number of broods, and/or clutch
size would decrease; (2) duration of incubation
and nestling periods would increase: (3) per capita
parental care ot nestlings and offspring mass at
fledging would increase; (4) birds would have
higher survival; and (5) mating status would not
Evans Ogden el al. • WREN
BREEDING ECOLOGY VARIES WITH ELEVATION
differ. We expected Pacific Wrens breeding at
high elevation to show a shift to a slower lifestyle
with lower annual fecundity and higher survival.
METHODS
Study Species— Pacific Wrens breed across
extensive elevation gradients in western North
America from the Alaskan Pacific Coast to central
California and inland to Alberta, western Mon¬
tana. and central Idaho (Chesser et al. 20 10). They
are typically associated with conifer forests, but
will nest in mixed forests, on cliff faces, and in
npanan habitats. Pacific Wrens use a range ol
types of nest sites and styles of nest construction.
They are often cavity nesters. excavating holes in
the root masses of upturned trees or in decaying
trees or downed logs, but will also construct non-
cavity nests in tree branches or riparian vegetation
(Waterhouse et al, 2002). Males arrive early in
breeding areas to establish territories and begin
constructing multiple nests with females arriving
shortly after to select a nest from the newly
constructed or older nests present on the territory.
Females typically lay one egg/day and complete
dutches of five to seven eggs. Only females
incubate eggs which hatch 14-16 days after onset
of incubation. Males and females provision
nestlings that usually remain in the nest 15-
19 days before fledging. Pacific Wrens may raise
two broods per season ( Hejl et al. 2002 ). No blood
parasites were found in adult or nestling Pacific
Wrens at any elevation in coastal montane coni¬
ferous forests in British Columbia (Topp ct al.
2007).
Study Area and Field Methods. — This study
was conducted over two breeding seasons, May to
August. 2003-2004 at Mount Seymour Provincial
(“ark in the coastal mountain range ol southern
British Columbia, Canada -15 km NE of
Vancouver (49 23’ N, 122 56' W). The study
area encompassed two biogeocli malic /.ones with
■ow elevation sites (100-500 m) within the
Coastal Western Hemlock (Tsuga heterophylla)
zone, and high elevation sites (750-1.300 m)
within the subalpinc Mountain Hemlock ( T .
toertensiana) zone. We also collected field data
at mid elevation (550-700 m) for several
Enables. The Coastal Western Hemlock /.one
has a mean annual temperature ol —08 C and, in
summer, temperatures arc typically >10 C
(Pojar et al. 1991). The mean annual temperature
lor the Mountain Hemlock zone is ~0 C with
temperatures >10 C only from mid-June
through August.
We searched for. captured, and color-banded
adults and juveniles during 2003-2004 and
monitored active nests (nests that contained 1 or
more eggs or nestlings) and potential nests (nests
from previous years in good condition, nests
under construction, or recently constructed nests
as indicated by the presence or addition of new
nest materials) along an elevation gradient ( 100—
1.300 m). We located Pacific Wren pairs and nests
using a combination ol behavioral cues and
intensive searching of potential nest sites. Males
wore captured and banded at or near nest sites
using mist nets and song playbacks, and most
females were captured directly off the nest during
incubation using a modified butterfly net in the
dim light just before dawn (mist-netting attached
to a round hoop on a pole). Nestlings reach near
Hedging mass at 10 days of age (McLachlin 1983)
and wc banded most al 11-12 days of age.
Search efforts for pairs and nests in 2003 were
allocated approximately evenly across elevations
with time and personnel divided between sites. We
focused our efforts in 2004 only on high (750-
1,300 m) and low (100-500 m) elevation nests to
ensure that we obtained a sufficient sample size at
these altitudes. Nests were discovered during
construction, laying, incubation, and nestling
stages. Territories were delineated based on
presence of singing males, video recordings at the
nest, and on mapped locations of active and
potential nest sites. Locations of color-banded
males were tracked throughout the breeding season
using song playbacks to assign males to territories.
Nests were visited about every 3 days to record
nest status and fate, Clutch size and nestling
number were ascertained with visual counts using
dental mirrors and flashlights. Temperature log¬
gers (HOBO Pro Series, Number H08-031-08,
Onset Computer. Pocaset. MA. USA) were placed
in nests during the incubation period with
temperatures recorded at 1-min intervals to
establish nest attendance patterns. This allowed
us to obtain precise estimates of the time of
nesting failure. Video cameras were placed 5 to
10 m from nests during the nestling period and
focused on the nest entrance to record parental
provisioning and brooding time behavior. All
parental activity near nests within 2-hr video
sessions was recorded and later transcribed by
viewing video tapes to summarize the number of
provisioning trips/adult/hr.
272
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 2. June 2012
TABLE 1. Number of territories, mating status, nesting success, and survival of Pacific Wrens in relation to elevation
on Mount Seymour, British Columbia, Canada.
Low elevation (100-390 m)
High elevation (750-1.270 m)
2003
2004
2003
2004
A. Territories and mating status
Number of territories
21
18
10
11
Number of unmated territorial males
0
0
3
9
Number of banded males
15
15
7
5
Average total nests/malc
2.4
4.0
1.3
2.6
Percent successful nests/male
25
24
0
0
B. Annual local survival
Adults
Number banded
28
19
Number returning the following year
9
0
Juveniles
Number banded
50
6
Number returning the following year
1
0
We estimated the date-of-firsi-egg-laid by
backdating (or nesls discovered after onset of
incubation and, where hatching and/or Hedging
events were observed, using average periods of 15
and 17 days for incubation and nestling periods,
respectively (Hejl et al. 2002).
Data Analysis.— We used R Version 2.4.0 (R
Development Core Team 2006) for all statistical
analyses. Clutch initiation dates were standardized
between years by subtracting the yearly median.
Clutch sizes were not normally distributed and we
used a generalized linear model with a Poisson
distribution to analyze the response of clutch size
to elevation, year, and clutch initiation date.
Linear models were used to evaluate the response
of clutch initiation (date-of-first-egg-laid). provi¬
sioning rates, and incubation and nestling periods
to elevation. Log and square-root transformations
improved model fit for clutch initiation and
nestling period models, respectively. We calcu¬
lated daily nest survival rates using the logistic
exposure method (Shaffer 2004). ANOVA was
used to test tor differences in morphology and
condition (wing chord, tarsus, body mass) of
adults and pre-fledging nestling mass among three
elevation categories (high, middle, and low
elevations) and sex (adults only). Alpha was set
at 0.05 and means are reported ± SE.
RESULTS
We located 22 and 24 active nests (containing
eggs or nestlings), 73 and 72 potential nests
TO"* COns,ructed and/or maintained and
attended by a territorial male) and one and three
recently failed nests during the 2003 and 2004
breeding seasons, respectively. Active nests were
distributed over an elevation range from 102 to
1.088 m. We did not find active nests above
UOO m, but did locate one potential nest at
1.270 m and territorial males above 1.200 m in
both years. We captured the majority of adults and
nestlings at active nests in 2003 and 2004. We
found fewer territories in both years, and fewer
males successfully obtained one or more mates at
higher elevation sites (Table 1). Our sample of
banded males at low elevation had more nests
(including both active and potential nests) and a
higher proportion of their nests were successful
compared to high elevation (Table 1).
Clutch Initiation and Clutch Size.— Clutches
were initiated over a span of 79 days (40 nests) at
low elevation, and over 31 days (6 nests) at high
elevation. There was a tendency for later clutch
initiation at high elevations, but clutch initiation
dates did not differ between elevations {F/ j: r
3.26. P = 0.08). Nests at low elevations had wo
peak clutch initiation periods, whereas nests at
high elevation had only one peak at a similar time
as the second peak period at low elevation
(Fig. I A).
Mean clutch size (including first and re-nest
attempts and second broods) was 5.5 ± 0.10 (n -
40) and did not vary with elevation (Dev Resit! , .
= 0.15, P = 0.70), clutch initiation dates (Dev
Residue = 0.411, P = 0.52), or with year (Dev
Residue = 0.01. P = 0.93: Fig IB). Fledglings
produced per eggs laid declined from an average
of 0.5 at 200-400 m to 0 above 600 m. It was not
Evans Ogden el al. • WREN BREEDING
ECOLOGY VARIES WITH ELEVATION 273
200 400 600 800 1000
B
200 400 600 800 1000
'5 200 400 600 800 1000
Elevation (m)
D
400 600 800 1000
Elevation (m)
FIG. I. Breeding parameters of Pacific Wrens nesting along an elevation gradient ( 100-1 100 m) on Mount Seymour
British Columbia, Canada. 2003-2004. A. Date-of-first egg (Julian date, day 1 - 1 Jan) lor all nesting attemp s. .
size (all nesting attempts). C. Daily nest survival probability. D. Nestling feeding rates (number ol provisioning trips
bv adults/hr).
possible to produce a good model lor these
fecundity data because of our small sample; but
Hie general relationship was non-linear and
resembled a threshold with no change up to
4(>0 m and then a decline to zero productivity.
Nest Survival. — The mean daily nest survival
across elevations was 0.960 ± 0.018 ( n = 46
nests) and ranged from 0.735 to 0.983. Daily nest
survival did not vary between years (P = 0.07,
M model: (Dev Reside - 10.06)) and gener¬
ally decreased with elevation (/’ = 0.01; Fig 1C).
All six of our active high elevation nests
foiled, one during incubation, and five during the
nestling stage. We encountered two families
with fledglings and five hatch-year individuals at
°ur high elevation site in 2003. Six hatch year
birds were observed ‘prospecting in high
elevation habitats (i.e„ singing a recognizably
juvenile male song) at different locations and
times in the autumn period. None of these hatch-
year birds was associated with our high elevation
nests, and none returned to breed the following
year.
Offspring Development Periods and Pro¬
visioning Rates. — Incubation (14.75 ± 0.33 days,
„ = |2 nests) and nestling periods (17.75 ±
0.41 days, n = 16 nests) did not vary with
elevation (F/jo = 2.88. P = 0.12; F/ = 0.17, P
= 0.69, respectively). Provisioning rates (number
of trips by adults/hr) did not differ with elevation
(F,2o — 0.009. P = 0.92; Fig. ID); however,
mass of nestlings near fledging (11-12 days after
hatching) varied with elevation (F2as = 3.36, P =
0.04. Table 2). Nestling mass was similar between
low and mid elevations (Ft = 0.12. P = 0.73),
but nestlings reared at high elevation were
significantly lighter than those at low and middle
elevations pooled (FIA6 = 6.74, P = 0.013).
274
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 2. June 2012
TABLE 2. Mass, wing chord, and tarsus of adult Pacific Wrens (breeding males and females) and nestlings (at 11-
12 days of age) across three elevations on Mount Seymour, Brilish Columbia. Canada. Means ± SE. sample sizes
in brackets.
Elevation
Male
Female Nestling
A. Mass
Low
9.35 ±0.12 (32)
8.92 ± 0.17 (21) 8.89 ± 0.20 (30)
Middle
8.96 ± 0.14 (7)
8.06 ±0.06 (4) 9.01 ± 0.14(11)
High
9.29 ± 0.12 (18)
9.03 ± 0.18 (10) 7.89 ±0.37 (7)
B. Wing chord
Low
48.30 ±0.18 (33)
45.40 ± 0.31 (21 )
Middle
48.86 ± 0.34 (7)
45.50 ± 0.91 (4)
High
47.58 ± 0.15 (17)
46.25 ± 0.22 (10)
C. Tarsus
Low
20.36 ±0.17 (33)
19.77 ± 0.15 (21)
20.09 ± 0.36 (4)
Middle
20.33 ± 0.17 (7)
High
20.41 ± 0.14 (18)
20.02 ± 0.08 ( 10)
Adult Morphology and Mass.— We observed
few morphological differences among adult wrens
breeding across elevations (Table 2). Wing chord
and tarsus were longer for males than females
(wing: F,m = 101.26, P < 0.001; tarsus (F,.S9 =
8.95, P = 0.00), bin neither trait varied with
elevation (wing: F2%HH = 0.68. P = 0.50; tarsus:
^2,89 — 0.32, P — 0.70). Adult mass varied with
both sex of adult and elevation with males being
heavier than females (F, 88 = 9.99, P = O.OOl
wrens at middle elevations were lighter than those
at high or low elevations (Fj-.S8 = 3.65, P = 0.03).
Adult mass (males and females pooled) was
similar between low and high elevation (low:
9.19 ± 0.10 g. /i = 53; high: 9.18 ± 0.10 g, n =
28), but birds at middle elevations were lighter,
especially the lour females in our sample (8 64 ±
0-16 g, n = 11; Table 2).
Load Adult and Juvenile Annual Survival.—
Nine ol 28 (33.3%) adults and one of 50 (27c)
nestlings banded at low elevation in 2003.
returned in 2004, respectively. None of the 19
adults and six juveniles banded at high elevation
in 2003 was re-observed in 2004 (Table IB).
DISCUSSION
Pacific and Winter wrens are reported breedit
from sea level to >3,700 m (Heijl et al. 2002). b
we lound Pacific Wrens on our coastal mounta
Sites in British Columbia, had lower indices ,
mating status, fecundity, nestling condition, loc
survival, and natal and breeding philopatry at hm
elevations. We found no differences with elev;
don in clutch size, offspring development time:
or per capita parental provisioning of nestlings,
riuis, we found no evidence for changes in
breeding ecology of Pacific Wrens with elevation
and no support for our hypothesis of a shift to a
'slower' life history with increasing elevation.
I his contrasts to several recent studies ol
songbirds breeding across elevation gradients in
western North America such as Dark-eyed Junco
(./unco hvenuilis). Savannah Sparrow ( Passercu -
Ins sandwichensis), and Homed Lark ( Eremophila
alpestris anicola) (Bears et al. 2009. Martin et al.
2009. Cam fie Id et al. 2010).
Hie avian breeding season at high elevation can
lx* about 60% shorter than at lower elevations.
Dark -eyed Juncos breeding at 2.000 m in Jasper
National Park, Alberta had a 59% reduction in
seasonal duration of clutch initiation compared to
juncos at 1 ,000 m in the same area (40 vs. 97 days;
Bears ct al. 2009). An alpine population of
Horned Larks initiated clutches over an average
period of 38.5 days, a 59% shorter duration than
the 94-day clutch initiation period for a low
elevation population (Cam field et al. 2010).
Juncos and alpine populations of larks and
Savannah Sparrows all had normal or high
survival of eggs, hatchlings, and fledglings
(Martin ct al. 2009). The clutch initiation period
lor Pacific Wrens breeding at high elevation was
61% shorter than for wrens breeding at lower
elevation on the same mountain: thus, there was
only sufficient time to produce one brood/season
at high elevation. The high elevation territories
still had deep snow present with some females not
yet. or only just arriving, at the same time that
Evans Ogden el al. • WREN BREEDING ECOLOGY VARIES WITH ELEVATION
275
pairs at low elevation were fledging their first
broods.
Pacific Wrens produced fewer offspring with
lower mass at high elevation compared to lower
elevation, in contrast to fecundity patterns ob¬
served for Dark-eyed Juncos (Bears el al. 2008.
2009), Savannah Sparrows (Martin et al. 2009),
and Homed Larks (Camfield et al. 2010). Pacific
Wrens did not adjust their per capita provisioning
of nestlings with increased elevation to compen¬
sate for the more rigorous conditions as observed
for high elevation finches and tits in Eurasia
Badyaev 1997. Lee et al. 201 1). Early develop¬
mental and offspring growth patterns did not vary
with elevation, and it appears that high elevation
habitats are peripheral or sub-optimal breeding
habitats for the Pacific Wren.
Species that are well adapted to high elevation
habitats exhibit increased survival to offset
reduced annual fecundity. Horned Larks breeding
at 1,500-1.850 m had about 18% higher annual
survival compared to birds breeding al a lower
elevation and latitude (Camfield et al. 2010).
Dark-eyed Juncos breeding at 2.000 m also had
18% higher survival compared to those at low
elevation on the same mountain (1.000 m: Bears
et al. 2009). Pacific Wrens had the reverse pattern
with low survival and breeding philoputry at high
elevation. Wrens breeding at low elevation
experienced an annual survival of 53%, similar
to other wren populations (Peach et al. 1995. Hcjl
etal. 2002). However, none of the birds banded at
high elevation returned the following year,
suggesting either low survival or low site fidelity
on high elevation territories.
!l was not clear which key resources limit
breeding for Pacific Wrens at high elevation. Nest
xites may be limited at high elevation as they are
predominantly associated with downed or dead
wood (Waterhouse et al. 2002), which is limited at
high elevation. Wrens are capable ol nesting on
c|itt laces and other locations, and appear adapt¬
able in their nest site selection. One male built
five nests on his high elevation territory, and still
failed to attract a mate suggesting that females
may he reluctant to settle on high elevation terri-
"fies. Food earlier in the breeding season may be
'uniting as insects and other invertebrates form
'hr mainstay of their diet (Van Horne and Bader
'WO, Hejl et al. 2002). Reduced time to breed
within a season and greater stochasticity in environ¬
mental conditions al high elevations impose strong
limits on annual fecundity, especially given the dual
disadvantage of higher failure of first clutches and
reduced opportunities for rc-nesting and second
broods compared to low-elevation populations.
We conclude Pacific Wrens lack adaptations to
high elevation, and that upper montane and sub-
alpine sites represent inferior breeding habitats.
However, we observed hatch-year individuals and
broods, indicating that a small proportion of
Pacific Wrens bred successfully at our high
elevations sites. Given that individuals and pairs
also occur at high elevation elsewhere, it is
reasonable to acknowledge that in some locations,
years or habitat types. Pacific Wrens are able to
reproduce successfully and survive at higher
altitudes.
ACKNOWLEDGMENTS
Funding was provided lo KM by the Natural Sciences
and Engineering Research Council (NSERC) ot Canada and
Environment Canada (Sciences Horizons. Georgia Basin
Ecosystem Initiative), and an NSERC Postdoctoral Fellow¬
ship to I .JF.O. Wc thank Stephanie Topp, Alana Demko.
Greg Ferguson. Tracv Sutherland, and Marty Mossop lor
field assistance. We thank B. C. Parks tor logistical support
and access.
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The Wilson Journal of Ornithology 124(2):277 285. 2012
NESTING ECOLOGY OF THE BLACK-CAPPED VIREO IN
SOUTHWEST TEXAS
KATHRYN N. SMITH.1 25 JAMES W. CAIN III.1 4
MICHAEL L. MORRISON.2 AND R. NEAL WILKINS'
ABSTRACT.— There is little information about nesting ecology of the federally endangered Black-capped Vireo ( Vireo
atricapilla) in the southern and western region of its breeding range, which is characterized by xenc thomscrub and patchy
low-growing vegetation. We mapped territories and monitored 1 19 Black-capped Vireo nests across seven study sites in
2009 and 2010 in Val Verde County. Texas in the Devil’s River region on the western edge ol the Edwards Plateau. We
• Served 69 nests with cameras to identity nest predators. Clutch si/e was significantly smaller in 2009 (3.4 ± 0.82) than m
2010(3.8 r 0.43). Both nest depredation and parasitism by Brown-headed Cowbiids (Mololhrus nn>r) were >10 r higher
hi 20<» than in 2010. There was a large diversity of nest predators identified including Brown-headed Cowbird (/i - 4).
snakes In = 4). and Greater Roadrunner (Geocoeew ctilijomianus) (» = 3). Species identified that have not been
previously observed as Black-capped Vireo nest predators were bobcat l Lynx rufus ). common raccoon IP racy on lotor).
Greater Roadrunner. and the greater arid-land katydid (Neohmrettiu spinosa\. Productivity of Black-capped Vireos in the
Devil’s River area appeared to be heavily influenced by weather, particularly precipitation during the breeding season.
Received IJ August 2011. Accepted 15 December 201 1
The Black-cappetl Vireo (Vitro utncapiltu ) is a
federally endangered migratory songbird (Raulaff
1987) with a current known breeding range
extending from central Oklahoma south through
Texas to the Mexican slates of Nuevo Leon and
southwestern Tamaulipas (Gtabcr 1961, Farquhar
and Gonzalez 2005; Fig. I). The eastern limit in
Texas follows the Balcones Escarpment (Cirabcr
*961). and small numbers Black-capped Vireos
have been observed as far west as Big Bend
National Park (Grzybovvski 1995). Breeding hab-
iiai is characterized by patchy distributions of low.
scrubby growth mostly of deciduous woody shrubs
and trees of irregular height (Graber 1961). Black-
capped Vireos establish territories in areas with
high vegetation density between 0 and 2 in in
height (Grzybowski 1995), and build the majority
°f 'heir cup nests in this zone (Graber 1961 ).
Most of the intensive studies ol the Black-
capped Vireo have occurred in a few locations in
Department of Biological and Environmental Science.
G\a% A&M University-Commerce. Commerce. I X 75429.
USA.
Current address: Department of Wildlife and Fisheries
Sciences. Texas A&M University, College Station. TX
7' *43. USA.
InMituie of Renewable Natural Resources. Texas A&M
University, College Station, TX 77843. USA.
4 Current address: U.S. Geological Survey. New Mexico
G "operative Fish and Wildlife Research Unit. Department
of Fish. Wildlife, and Conservation F.cology. New Mexico
State University, l.as Cruces. NM «8(X)3, USA.
Corresponding author: e-mail:
kathryns84@neo.tainu.edu
the Edwards Plateau region of Texas and in
Oklahoma t Wilkins et al. 2006). To date, about
75% of the known population in the breeding
range is in four well-surveyed areas (Fig. I ): Foil
Hood Military Reservation and Kerr Wildlife
Management Area (WMA) in Texas, and in two
adjacent areas in Oklahoma (Wichita Mountains
Wildlife Refuge and Fort Sill Military1 Reserva¬
tion). These areas contain most of the known
breeding population, but comprise \% of the total
area in the Texas/Oklahoma range of the Black-
capped Vireo (Wilkins et al. 2006). Kerr WMA is
the furthest location south and west that has been
intensively surveyed (Grzybowski et al. 1994.
Dufault 2004. Pope 2011).
Currently, little is known about the Black-
capped Vireo’s ecology and threats in the more
arid habitat of southwest Texas and central
Mexico, a region characterized by xeric thorn-
scrub, patchy low-growing vegetation, and 1 50—
250 mm less rainfall per year than areas (USDC
2010) where Black-capped Vireos have been well
surveyed in the past (Fig. 1 ). Black-capped Vireos
in Kinney and Edwards counties may be part of a
metapopulation or series of isolated populations
extending south and west in canyons traversing
the upper bend of the Rio Grande River including
canyons of the Devil’s River in Val Verde
County, where the status of the Black-capped
Vireo is not well known (Bryan and Stuart 1990,
USDI 1991. Grzybowski 1995). Data collected in
the Devil’s River area may also be applicable to
the ecology of Black-capped Vireos in northern
Mexico and could add to understanding the
277
278
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 2. June 2012
Legend
▲ Previous well-surveyed locations
★ Study area
| 2009 and 2010 monitored counties
Black-capped Vireo breeding range
Texas
%
in omo ,!uI?PPCd Vireo breedinS range (Wilkins et al. 2006), previous well-surveyed locations, and areas studied
in 2009 and 2010 tor comparisons (Table I).
Smith et til. • NESTING OF THE BLACK-CAPPED VIREO
279
ecology of Black-capped Vireos and its’ habitat
requirements across their entire range.
Identification of potentially critical or consis¬
tently present threats and habitat conditions can be
an essential part of effective management for the
species (Grrybowski et al. 1994). Brown-headed
Cowbird {Molothrus ater) parasitism was w idely
observed as a primary factor contributing to the
lovs reproductive success of Black-capped Vireos
at the time of listing as an endangered species
! IJSDI 1991): cowbird abundance has shown a
flight to moderate increase in southwest lexas
>ince listing of the Black-capped Virco (Wilkins
et al. 2006). Conservation and management
efforts to mitigate high nest predation require
knowledge of predators and predator-specific
management (Thompson and Burhans 2003).
Little is known about nest predators ol Black-
capped Vireos outside of Fort Hood Military
Reservation and surrounding areas in central
Texas. Monitoring of nests at Fort Hood revealed
ttim makes and imported lire ants (Solenopsis
invicta) were the primary predators from 1998 to
2001 (Stake and Cimprich 2003). Brown-headed
Cowbirds and snakes were observed to be the
primary predators of Black-capped Vireo nests in
2008 and 2009 in the same region and further
wuth at Kerr WMA (Conkling 2010).
We located and monitored vireo nests in 2009
unil 2010 to: (1) assess nest success, clutch size,
breeding season duration, and parasitism pressure:
f 2) identify nest predators; and (3) compare our
results with data from other regions ol the Black-
capped Vireo's breeding range.
METHODS
Study Area.— Our study area was in Val Verde
County, Texas in the Devil’s River region on the
western edge of the Edwards Plateau (Fig. 1).
Average rainfall from 1997 to 2008 for the
Devil's River area during the Black-capped Vireo
breeding season (Mar through Jul) was —5.0 cm,
:|nd average mean temperatures ranged Irom 17.6
C in March to 30.0 C in July (USDC 2010). Our
Mudy area encompassed Devil s River Stale
Natural Area (DRSNA) and Dolan Falls Preserve
'29 53’ N, 100 59' W). a 1.942-ha property
owned and managed by The Nature Conservancy.
The DRSNA encompasses 8.090 ha of mostly
unmanaged land. The property has a large
Population of feral sheep (Ovis spp.) and aoudad
lAmmotragus lervia), a species of sheep native to
North Africa. There is currently no management
of feral sheep on the property. Adjacent properties
were undeveloped, or used lor recreation includ¬
ing wild game hunts,
The natural plant communities at DRSNA and
Dolan Falls Preserve exhibit elements of the
mesquitc ( Prosopis spp.)-chaparral of the South
Texas Plains, the oak -juniper ( Quercus-Juniperus )
woodlands of the central Edwards Plateau to the
east, and the sotol-lechuguilla ( Dasylirion leio-
phvltum-Agave lechugnilla) of the Trans-Pecos to
the west (Hedges and Poole 1999). Topographic
features of DRSNA include a nearly level plateau
with high-domed hills and fiat-topped ridges as
well as several large drainage systems that cut
through canyons. Elevation ranges from 632 m at
the northeastern park boundary to 409 m at the
southwestern corner of the property where it
connects to Dolan Falls Preserve (Hedges and
Poole 1999). Dolan Creek, dry the majority of the
year, winds 20.1 km from the north end of
DRSNA and exits in the southwestern portion of
the park. Dolan Creek Hows through Dolan Falls
Preserve where it contains water year-round, the
result of flowing springs. Topography at Dolan
Falls Preserve is similar to DRSNA. differing only
in that Dolan Falls Preserve contains more
property adjacent to the Devil’s River,
SHe Selection.—' There was little information on
habitat use of Black-capped Vireos within the
sampling frame, and we sampled randomly across
(he study area which included DRSNA and Dolan
Falls Preserve. We used ArcGIS 9.3 to create a
grid of 1-ktrr cells lhal covered the study area and
used Hawth’s tools (Beyer 2004) to randomly
select four grid cells in 2009 and three in 2010.
We initially visited each grid cell to document
presence of Black-capped Vireos. These initial
visits occurred no earlier than local sunrise and
no later than 4 hrs after sunrise, 2-3 times
during the early part of the breeding season
(Mar and Apr): each visit was at least 4 days
apart. We systematically walked within 200 m
of all locations within each of the 1-knr grid
cells, concentrating on areas with sufficient
vegetation to support Black-capped Vireos
(i.c., cover >20%). We recorded the coordinates
of singing male Black-capped Vireos with a
Global Positioning System (GPS) unit (Garmin
Ltd., Olathe. KS. USA). We visited the cell once
a week for a month if there were no detections
of Black-capped Vireos after three visits to he
certain that no Black-capped Vireos established
territories in that cell. We randomly selected a
280
THE WILSON JOURNAL OL ORNITHOLOGY • Vol. 124. No. 2. June 2012
new grid cell to replace the cells that had no
detections after three visits.
We established seven individual contiguous
study sites that occurred in and around randomly-
selected cells with Black-capped Vireos. We
delineated study sites once we located all
territories we were logistical ly capable of moni¬
toring. The size of each study site depended upon
spacing of territories and the difficulty of
monitoring territories at that particular site, which
ranged in size from 32 to 267 ha.
Territory Mapping and Nest Searching. — We
mapped territories of adult male Black-capped
Vireos and searched for vireo nests between 15
March and 15 July. We verified that vireos were
not exhibiting nesting behavior outside these dales
in both years. We returned every 2 to 5 days to map
singing locations of males to identify locations for
subsequent nest searches. We located nests using
behavioral cues of breeding adults (i.c.. alarm calls,
carrying nest material, carrying food, males singing
on the nest). We marked nests with flagging > 1 5 m
and recorded locations using GPS units.
We monitored nests every 2 to 4 days until
nestlings fledged or the nest failed. We recorded
the dale, lime, contents of the nest, and general
activity (e.g., incubation, brooding, adult calls) at
each visit to the nest. We addled any cowbird eg«s
and removed cowbird nestlings at time of their
discovery and recorded the parasitism. Addling
cowbird eggs allowed the nest to remain active
longer and allowed us to observe as many
predation events as possible. We did not remove
cowbird eggs from nests because presence of
either real or artificial cowbird eggs deters future
parasitism (Ortega et al. 1993). We searched
territories for fledglings every 3-4 days for
2 weeks or until a fledgling was located if we
thought young had fledged. We considered a nest
successful if at least one young fledged. We
counted all parasitized nests as failures because
parasitized Black-capped Vireo nests on average
fledge only 0.2 fledglings per nest (Pease and
Grzybowski 1995).
We used nest cameras to help classify nests as:
(1) depredated, (2) successful, or (3) parasitized.
Nests were considered depredated if any contents
weie removed by a predator. We categorized nests
as parasitized if there was at least one cowbird egg
present at any stage of the nest cycle. Nests that
were parasitized were not considered successful
even if nestlings survived to fledging after the
cowbird egg was addled.
Nest Predators. — We used Rainbow Weather¬
proof IR Bullet cameras (Costa Mesa. CA. USA)
and Digital Event Recorders (DVR) (Detection
Dynamics. Austin. TX. USA) with high capacity
SD cards to monitor vireo nests 24 hrs ,i day
in 2009 and 2010. Cameras were powered by a
12-volt. 26ah battery (Batteries Plus. Hartland.
Wl. LISA) and supplemented with a 20-watt solar
panel (Suntech, San Francisco. CA. USA). We
placed cameras sufficiently close to nesLs to
observe activity but not so close as to disturb
the birds (1-2 m). Cameras were attached to a
DVR. battery, and solar panel by a 15-m cable so
the system could be maintained without disturbing
the nest. Cameras were evenly distributed among
each of the study sites monitored each year. We
placed cameras as early as possible in the nesting
cycle, but only after incubation had begun to
avoid abandonment of the nest (Stake and
Cimprich 2003). We observed the nest until adults
returned and removed the camera if the adults did
not return within 30 min. We randomly chose a
new nest location within each study site to deploy
the camera to monitor as many nests as possible
once young fledged or the nest failed.
Statistical Analyses. - We evaluated nest suc¬
cess using the Mayfield Method (1961. 1 975) and
Program MARK to calculate daily nest survival.
We only used data from nests in which eggs or
nestlings were observed in calculating daily
survival rate. We used SAS 9.2 (SAS Institute,
Cary. NC. USA) for statistical analyses. We
calculated mean and standard error by year tor
clutch size and host eggs hatched, and compared
those means using /-tests (Zar 1999:122-129). We
performed Chi-square analyses to ascertain it
parasitism, depredation, clutch size, or proportion
ol eggs that hatched were statistically different
between years.
RESULTS
We located and monitored 81 and 38 nests in
2009 and 2010, respectively. The earliest dated
incubation was 14 April 2009 and 7 April 2010.
despite early nest building in mid-March in 2004
1 lie mean (± SD) monthly rainfall was 3.6 -
2.9 cm in 2009. 1.1 cm per month below norma
and 7.0 cm above normal in 2010. averaging I
± 10. 1 cm per month from March to July. Regular
flooding ol Dolan Creek and other typically dry
drainages throughout the study area occurred in
2010. The average daily temperatures in 2009
were above normal, ranging from 18.6 C in
Smith et al • NESTING OF THE BLACK-CAPPED VIREO
281
TABLE 1. Nest observations of Black-capped Vireos in Val Verde, Kerr. 1 ravis. and Coryell counties, Texas during
2009 and 2010 (MLM, unpubl. data). ND = no data.
2009
2010
Val Verde
Kerr
Travis
Coryell
Val Verde
Kerr
Travis
Coryell
Find incubation observed
14 Apr
29 Apr
ND
9 May
7 Apr
23 Apr
15 Apr
ND
Latest date of active nest
14 Jul
19 Jul
ND
13 Jul
14 Jul
24 Jul
1 1 Jul
ND
Date of first parasitism
21 Apr
30 Apr
ND
9 May
3 May
ND
23 Apr
ND
Clutch size
3.4 ± 0.82
3.7 ± 0.45
ND
3.4 ± 0.68
3.8 ± 0.43
3.8 ± 0.44
3.8 ± 0.48
ND
March to 32.2 C in July. The mean temperature
in 2010 ranged from 16.2 C in March to 29.4 C
in June (USDC 2010).
Mean (± SE) clutch size was smaller in 2009
(3.4 ± 0.82) than in 2010 (3.8 ± 0.43; t,,7 =
-3.278. P = 0.0014). The proportion of Black-
capped Vireo eggs that hatched did not statisti¬
cally differ in 2009 (0.84 ± 0.24) from 2010
10.88 ± 0.21; l62 = -0.697. P = 0.4881).
The proportion of nests parasitized was lower in
-010 (26%) than 2009 (37%). The proportion of
nests depredated was also lower in 2010 (39.5%)
than 2009 (51,3%). These differences between
years were not statistically different for parasitism
(r' = 13324. P = 0.2484. df = I ) or depredation
(r = 1.4250. P = 0.2326, df - I). The first
record of Brown-headed Cowbird parasitism in
2009 occurred on 21 April. Nest parasitism was
not recorded in 2010 until 3 May and regular
parasitism of nests did not occur until the end of
May (Table I). We did not observe Bronzed
Cowbird (Mololhrus aeneus) parasitism in either
year.
Mayfield estimates of daily survival rate (.v *
'■'El for incubation and nestling periods combined
Were 0,947 ± 0.007 (95% Cl - 0.93 1 -0.959) and
*-*•968 ± 0.007 (95% Cl = 0.950-0.980) in 2009
and 2010. respectively. Higher nest success obser-
'cd in 2010 was primarily due to success of nests
'n the llrst half of the breeding season (Fig. 2).
(Tne monitored pair in 2009 attempted a second
brood that subsequently failed. Black-capped Vir-
e°s at six monitored territories attempted second
broods in 2010. and two Hedged young, bringing
*bc total fledged in those territories to six and
seven young. An additional second brood attempt
occurred in a nest that had not been previously
Monitored (i.e.. male observed feeding fledgling
wbile also building new nest), which was later
Parasiti/ed and abandoned.
Nest depredation was the leading cause of nest
failure in 2009 and 2010 followed by parasitism
(Fig. 3). Other causes of nest failure were
abandonment, nest tailing because of apparent
poor construction, eggs not hatching, and destruc¬
tion by flooding. No nest abandonments were
caused by cameras. Both occasions of the nest
falling and eggs not hatching occurred in 2009:
nest failure because of Hooding occurred in 2010.
We recorded video at 43 nests in 2009 and 26
nests in 2010. Cameras recorded 20 depredation
events and we were able to identify 10 predator
species (Table 2). Seven (35%) of 20 depreda¬
tions recorded were in the incubation stage of
the nest cycle and 13 (65%) were in the nestling
stage: all events resulted in nest failure. Eight
depredations occurred at night and 12 occurred
during daylight hours. Most snake depredations
occurred at night, all avian depredations occurred
during the day, and mammal depredations oc¬
curred in riparian ureas and were mainly crepus¬
cular except for ringtail {Bassariscas astutus)
depredation that occurred at night, Species
depredating Black-capped Vireo nests most often
were Brown-headed Cowbirdx (>i = 4) and snakes
(n = 4); however. Brown-headed Cowbirds were
only recorded depredating nests in 2009. We
identified three snakes to species level: two
Baird's rat snakes (Elaphe bairdi) and one
Trans-Pecos rat snake ( Bogertohis subocularis).
Avian predators accounted for 40% (n = 8) of
nest depredation events observed on video. Insects
(ants and greater arid-land katydid [Neobarrettia
spinosa ]) accounted for 15% (>/ = 3) of
depredation events recorded and all occurred
during the nestling stage. Mammals were identi¬
fied as the nest predator in 25% of the events (n =
5) and all occurred in riparian areas.
DISCUSSION
Black-capped Vireo nesting ecology in south¬
west Texas is similar in many ways to other areas
of their range. Average dutch size (3-4) is the
same as recorded in Oklahoma (Grzybovvski
282 THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 2. June 2012
Nest fate
Fia 3. Percentage of Black-capped Vireo nests that failed by cause of failure in 2009 and 2010 in the Devil’s River
area, i exas.
Smith et al. • NESTING OF THE BI.ACK-CARPED VIREO
283
TABLE 2. Nest predators identified using nest cameras
depredating randomly-selected Black-capped Vireo nests in
the Devil's River area. Texas in 2009 and 2010.
Predator
2009
2010
Totals
Brown-beaded Cowbird ( Molothrus
titer )
4
0
4
Snakes
2
2
4
Greater Roadrunner (Geococcyx
califomianiu)
2
1
3
Ants
2
0
2
Gra;> fox ( Urocyon cinereoargenteus )
2
0
2
Bohcat (Lynx mfits)
0
1
1
Greater arid-land katydid
( Neobarrettia spinosa)
0
1
1
Common raccoon ( Procyon lotor)
0
1
1
Ringtail (Bassarisais amutus )
1
0
1
Western Scrub-Jay ( Aphelocoma
lolifomica)
1
0
1
Totals
14
6
20
1995) and other studies in central Texas during
2009 and 2010 (Table 1). Nest building and
incubation began 1-2 weeks earlier in the Devil's
River area than in other areas being monitored
during the same years in Texas, but final nesting
attempts ceased at approximately the same time as
areas being monitored in central Texas (Table I).
Thus, the breeding season is longer for Black-
upped Vireos in the Devil's River region. This
vxtra time at the beginning of the breeding season
is likely giving Black-capped Vireos in south¬
western Texas and northern Mexico more oppor¬
tunity to produce young. Black-capped Vireos in
region also had an advantage over vireos
breeding in central Texas where parasitism
pressure and initial incubation began simulta¬
neously in 2009 and 2010. because parasitism
h.v cowbirds was delayed 1-2 weeks after the
commencement of incubation (Table 1 ).
Productivity of Black-capped Vireos in the
0eul\ River area appeared to be heavily influ¬
enced by weather, particularly precipitation during
'he breeding season. Other studies of avian pfoduc-
bviiy have indicated increased rainfall during the
breeding season directly affects avian populations
1 1 'emi-arid regions (Bolger et al. 2005. Djerdali et
al Several studies indicated tood supply
the main cause of increased nest success when
Precipitation increased (Nutt et al. 2002. Ulera and
Ouiz 2006). However, Coe and Rotenberry (2003)
sho\ved that supplying water i<> Black-throated
Sparrows (Amphispiza bilineata) increased clutch
s>ze independent of food availability. The increase
in mean clutch size we observed in 2010 may have
been caused by one or both of these factors, both
relating to precipitation. Long-term studies are
needed to fully understand the relationship between
climate patterns and population dynamics of
Black-capped Vireos in southwest Texas.
Nest parasitism and nest predation were >10%
higher in 2009 than 2010. although not statistically
different, but were likely biologically significant.
Weather and precipitation can affect animal move¬
ment and habitat selection (Vickcrv and Rivest
1992). The multiple occurrences of flooding of
Dolan Creek and other creeks and drainages within
our study area in 2010 may have influenced the
normal movement and activity of terrestrial nest
predators, allowing higher nest success during the
early part of the breeding season. Increased
precipitation may have increased food supply tor a
variety of other potential prey species of local
predators within the study area. Increased food
supply may have increased the survivorship and
reproduction of alternant prey, consequently increas¬
ing prey availability for predators within the study
area and decreasing predation pressure on nests of
Black-capped Vireos. The influence of cowbirds,
both as nest predators and parasites, was reduced in
2010. It is unclear how or if higher precipitation or
flooding affected Brown-headed Covvbird behavior
and abundance in 2010. The increase in nest success
due to decreased depredation and parasitism during
years with high rainfall may have a role in
maintaining vireo populations in semi-arid areas ol
their breeding range.
There is a diverse assemblage ot Black-capped
Vireo nest predators in the Devil's River region
and several had not been previously identified as
potential nest predators (Stake and Cimprich
2003, Conk ling 2010) including bobcat (Lynx
niftis), common raccoon ( Procyon lotor), Greater
Roadrunner ( Geococcyx califomianits), and the
greater arid-land katydid (Smith el al. 2012).
Avian predators (i.e.. Brown-headed Cowbird,
Greater Roadrunner. and Western Scrub-Jay
[Aphelocoma californica]) were most common,
comprising 40% of all predation events recorded.
Fire ants are a major threat to Black-capped Vireo
nests in other areas of their breeding range (Stake
and Cimprich 2003) but were not observed
depredating nests in the Devil's River area, likely
because fire ant occurrence is limited in the study
area and did not overlap with a large portion of
Black-capped Vireo breeding habitat (Campo-
mizzi et al. 2009; KNS. pers. obs.).
284
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 2. June 2012
All mammal depredations occurred in riparian
areas, which was likely because mammals used
Dolan Creek and washes as corridors between
vireo habitats to move through the study area.
Riparian corridors are an important landscape
element for predators and guide animal movement
including foraging (Small and Hunter 1988. Noss
1991, Marini et al. 1995. Barding and Nelson
2008). Most of the vegetation outside the wash
areas is thick and possibly difficult for mammals
to move through relative to the washes.
The main predator of Black-capped Vireo nests
in 2009 was the Brown-headed Cowbird. It is
possible that cowbird depredations cause hosts to
re-nest and subsequently parasitize the new host
nest attempt (Arcese et al. 1996). There were no
cattle within the study area or on the surrounding
properties during our study: however, there was a
substantial population of feral sheep and aoudad
that may have attracted Brown-headed Cowbirds.
Cowbirds may also be attracted to the food supply
created by supplemental deer (Odocoiletis spp.)
feeding occurring on many of the adjacent
properties; some deer feeders occur only a few
meters from the DRSNA fence line (KNS, pers.
obs.). Black-capped Vireo habitat at DRSNA
occurs within the typical distance to deer feeders
that cowbirds have been observed to commute
between feeding and breeding areas (7-13 km;
Thompson 1994. Curson et al. 2000), potentially
facilitating depredation and parasitism of vireo
nests within the study area.
No vegetation management or predator or
Brown-headed Cowbird control was conducted
in the Devil’s River area during 2009-2010.
Our study provides information on the impact
and diversity of nest predators, as w'ell as the
impact of parasitism and rainfall on the Black-
capped Vireo population in the area. Thus,
more concise efforts can be made to fulfill the
goal ol conserving Black-capped Vireos in
southwest Texas and all regions of their
breeding range.
ACKNOWLEDGMENTS
We thank the Texas Parks and Wildlife Department and
The Nature Conservancy for access to their properties for
field work; M. P. Sheick. C. R. Thompson. A. M. Salinas.
M. G. Hepp. and I. I . Johnson for assistance collecting
field data; 1. 1.. Conkling for help with camera logistics;
and R. T. Snelgrove, A. G. Snclgrovc, T. L. Pope II A
Mathewson. T. M. McFarland, V, L. McCallister, I.. G.
Law, and B. A. Collier for logistical and technical
support. Research funding was provided hy Texas
Department of Transportation and Texas Parks and
Wildlife Department. Additional support was provided
by the College of Arts and Sciences and Department of
Biological and Environmental Science. Texas A&M
University-Commerce.
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The Wilson Journal o f Ornithology 1 24(2):286 — 291, 2012
NEST AND EGGS OF THE MARSH ANTWREN ( STYMPHALORNIS
ACUT1ROSTRIS ): THE ONLY MARSH-DWELLING THAMNOPHILID
BIANCA L. REINERT,1 6 RICARDO BELMONTE-LOPES.1 2 MARCOS R. BORNSCHEIN."
DAIANE D. SOBOTKA,* 1-3 LEANDRO CORREA.1 ’ MARCIO R. PIE.4 AND MARCO A. PIZCf
ABSTRACT. — We describe the nest and eggs of the Marsh Antwren {Stymphalornis acutirnstris), a recently described
species which is the only member of the Thanmophilidae restricted to marsh habitats. We conducted 1,560 hrs of nes:
searching in tidal marshes ot southern Brazil and found 178 nests. All nests were of dry fibers, straw's, and silk. Nineteen
plant species were used for nest attachment. All nests had a clutch of two white eggs with several irregular brown spot'
scattered over the entire egg. concentrated at the middle or the largest pole. The strategy of nest attachment to vertical
structures used by the Marsh Antwren was previously unknown in the Thamnophilidae. Received 14 June 2011. Accepted
12 December 2011.
The vast majority of species in the Thamnophi-
litlae live in forests throughout the Neotropies
(Zimmer and Isler 2003); the Marsh Antwren
( Stymphalornis acutirnstris) is the only species
restricted to marsh habitats (Zimmer and Isler
2003). The Marsh Antwren was described as a new
species and genus by Bornschein et al. (1995). and
occurs only along the coast of the states of Paratui
and Santa Catarina in southern Brazil (Reinert et al.
2007). It is presently classified as ‘endangered’
(BirdLife International 2010). We found a large
number of nests of this species during a multiyear
study of the population ecology of the Marsh
Antwren. We describe for the first time the nest
structure and type of attachment to vegetation, as
well as the eggs of the Marsh Antwren.
METHODS
Field work was conducted from January 2006
to March 2010 in tidal marshes at Guaratuba Bay
1 Maler Natura-Instituto de Estudos Ambientais. Rua
Lamenha Lins 1080, CEP 80250-020. Curitiba. Parana.
Brazil.
Programa de P6s-Gradua?3o cm Zoologia, Departa-
mento de Zoologia. Universidade Federal do Parana, Centro
Politecnico. Jardim das Americas. Caixa Postal 19073, CEP
81531-990. Curitiba, Parana. Brazil.
Programa de Pos-Graduuyao cm Ecologia e Conserv
?ao, Universidade Federal do Parana. Centro Politdcnic
Jardim das Americas, CEP 81531-990. Curitiba. Panin
Brazil.
1 Laboratory de Dinamica Evolutiva c Sistemas Cot
plexos, Departamcnto dc Zoologia, Universidade Feder
do Pa rand, Centro Politic, lieu, Ja, dim das Americas, CE
81531-990. Curitiba, Parana, Brazil.
'UNESP-Universidade Estadual Paulista. Dcpartamem
de Zoologta. CEP 13506-900. Rio Clam. Sao Paulo, Brazi
Corresponding author; e-mail:
biancareinert@yahoo.com.br
(Folharada Island: 25 52' 00" S, 48 43' 26” W.
15.7 ha; Jundiaquara Island: 25 52’ 28" S. 48
45' 33" W, 1 1.6 ha; and the Claro River: 25 52'
26" S, 48 45' 41" W. 8.2 ha), municipality of
Guaratuba, coast of the Stale of Parana, southern
Brazil. A detailed description of the tidal marshes
in this region has been presented bv Rcinen el al.
(2007).
Nest searches were conducted daily during the
reproductive season using the focal-animal meth¬
od (Altmann 1974). We made ad libitum obser¬
vations (Allmann 1974) of birds collecting
materials for nest building during these searches.
All complete nests found were assigned to a
breeding pair (all pairs in the study area were
previously color-banded), and measured in the
field with a caliper to the nearest 0.1 cm before
onset of incubation or after predation or nesl
abandonment were confirmed. A nest was con¬
sidered abandoned after at least 3 weeks without
any modification of previous conditions, and
regarded as completed when an incubation
chamber was present. We measured the height
above ground for some nests as soon as they were
completed and when they were collected.
used only the initial measurement for calculating
mean values when nest height varied during the
breeding season.
We calculated nest and incubation chamber
volumes following Moller (1982): nest material
volume = nest volume minus nest cup volume
and volume = 4/3 X k X largest radius2 X height
X the fraction of an ellipsoid with the fraction
assigned to Zi. We recorded plant species where
nests were attached and if it was green or dry
vertical (between 71 and 90 ), horizontal (0-15 I.
or inclined. Plant species identification folio"''
Bornschein (2001) and Reinert et al. (2007), but
286
Reinert el al. • NEST AND EGGS OF THE MARSH ANTWREN
287
some species names were adapted from Forzza
ei al. 12010).
Nests were collected at the end of the breeding
season. Some nests were deposited at the Museu
«je Zoologia da Universidade de Sao Paulo
(MZUSP #s 2276. 2277, 2278. and 2279). Sao
Paulo, and some nests will be deposited at the
Museu de Historia Natural Capao da Imbuia,
iMHNCI), Curitiba. Brazil. Tw'eniy-one nests
were disassembled to analyze materials used and
nest building techniques following the categories
proposed by Hansell (2000). Well-preserved nests
were weighed after being dried using a dyna¬
mometer to the nearest 0. 1 g. Materials used for
nest building were separated, classified, and
weighed separately. Nest material categories were
libers (plant materials <2 mm in thickness), straw
(plant material >2 mm in thickness), silk (spider
webs, oothecas. and diverse kinds of cocoons),
and root or leaf fragments (independent of plant
species). Nest descriptions followed the nest type
(H.) categories of Hansell (2000) and (S&P)
Simon and Pacheco (2005) with the different sets
of categories presented in the results referring to
these two publications, respectively.
Flooded and abandoned eggs were collected,
measured (with a digital caliper to the nearest
0-1 cm), and weighed (with a dynamometer to the
nearest 0.1 g) if not damaged. Egg colors were
evaluated in comparison with ((Uppers' (1996)
color alias with acronyms referring to specific
color shades. Eggs in active nests were measured
dnth leaf fragments in about one half ot the nests
'Table I). All other materials occurred in fre¬
quencies <25%. Birds were observed collecting
fiber and straw from Panicum cf. mertensii (/? =
1 2), Schoerwplectus califomicus (n = 7). Fuirena
fobusta (n = 4). and Acrostichum danaefolium (n
= 4); leaf fragments were from S. califomicus. F.
rob ust a, and Eleocharis geniculata , while dry
TABLE I . Materials used to build nests (n = 21 ) of the
Marsh Antwren {Stymphalomis acutirostris) in Guaratuba
Bay. Parana, southern Brazil.
Total mass
Material
n
(g)
Plant
Fiber (diverse kinds of plant material
<2 mm width)
21
59.2
Straw (diverse kinds of plant material
>2 mm width)
21
24.6
Leaf fragments
11
0.1
Base of the pinae of Acrostichum
danaefolium
5
0.3
Tillandsia usneoides
4
0.1
Fragments of Acrostichum danaefolium
petiole
2
U.l
Poaceae inflorescence
2
<0.05
StigmaphvUon ciliaium and/or Vigna
luieola stems
2
j T°f llp: pensile' (E)- ToP *»Pi single horizontal top lip lini'
in .he background cmresponds 0. ! cm. Photograph” b“ BLR EaCh °f ** Sma"“t
Reinert et al. • NEST AND EGGS OF THE MARSH ANTWREN
289
TABLE 2. Nest measurements of the Marsh Antwren (Stymphalornis acutirostris) in Guaratuba Bay, Parana,
southern Brazil.
Nest characteristic
Nest height, mm
Incubation chamber depth, mm
Minimum external diameter, mm
Maximum external diameter, mm
Minimum internal diameter, mm
Maximum internal diameter, mm
Nest material volume, cm3
Incubation chamber volume, cm3
Total dry mass, g
Range
Mean ± SD
144
40.0-130.0
68.5 ± 13.7
142
20.0-80.0
44.7 ± 9.2
145
35.0-90.0
65.9 ± 9.5
145
53.1-120.0
79.7 ±11.3
145
25.0-57.5
45.3 ± 5.6
145
30.4-75.0
54.7 ± 6.9
138
26.7-527.8
156.1 ± 76.4
138
34.2-147.3
72.7 ± 22.8
39
1. 5-8.7
3.8 ± 1.2
attachment categories (H): top lip (n = 53),
bottom multiple (vertical) ( n = 22), or both
simultaneously ( n = 74). Twenty of the top lip
nests were attached to a fork. 26 to parallel
vegetation, and three were attached to the
vegetation above the nest. Four top lip nests were
attached to only one horizontal stem instead of
wo horizontal parallel stems (Fig. IE), which
does not fit any previously described category.
Some nests of the Marsh Antwren could not be
assigned to only one nest attachment category,
using the categories lateral and single horizontal
top lip (n = 22) at the same time.
The nests of the Marsh Antwren following S&P
were low cup (n = 113) or a high cup (n = 29).
The categories of support type (S&P) were fork (n
= 46), lateral (n = 22), pensile (n = 3), and
lateral and fork at the same time (n = 52) with the
latter combination being previously unreported.
The four nests that were attached to only one
horizontal stem also do not Fit any described
category (H or S&P). for which we propose the
category: single horizontal top lip.
Nests varied greatly in all measurements
including dry weight, and volume ot nest material
and incubation chamber (Table 2). The height
TABLE 3. Frequencies (percent in parentheses) of plant species used as support for nests of the Marsh Antwren
( Stymphalornis acutirostris ) in Guaratuba Bay. Parana, southern Brazil. Columns 1. 2, 3. and 4 refer to nests supporte y
°ne. two. three, or four plant species, respectively.
Number of supporting plant species
Species
Plant type
1 oial frequency -
(n = 157)
1 tn = 95)
2 (n = 50)
3 (n = 10)
4 (n = 2)
rosticlium danaefolium
herb
49 (31.2)
38 (40.0)
10 (20.0)
1 (10.0)
Oadium jamaicense
herb
35 (22.3)
19 (20.0)
14 (28.0)
2 (20.0)
2 (100)
hirew robusta
herb
29 (18.5)
10 (10.5)
1 1 (22.0)
6 (60.0)
''‘ hoenoplectus caUfbmicus
herb
26 (16.6)
18 (36.0)
6 (60.0)
2 (100)
Cnnum americanum
herb
17 (10.8)
10 (20.0)
5 (50.0)
2 (100)
1 Qlophyllum brasiliense
tree
14 (8.9)
7 (7.4)
7 (14.0)
2 (20.0)
2 (100)
hinndorus grandiflorus
herb
12 (7.6)
3 (3.2)
5 (10.0)
guncularia racemosa
tree
12 (7.6)
4 (4.2)
7(14.0)
1 (10.0)
Siruthanthus vulgaris
mistletoe
9 (5.7)
2 (2.1)
6 (12.0)
1 (10.0)
fulipariti pemamhucense
shrub
7 (4.5)
5 (5.3)
2 (4.0)
S'igmaphyllon ciliatum
Vigna luieola
liana
5 (3.2)
2 (2.1)
3 (6.0)
1 (10.0)
liana
4 (2.5)
1 (l.D
2 (4.0)
Commeltna diffusa
herb
3 (1.9)
1 (2-0)
3 (30.0)
Typha domingensis
herb
3 (1.9)
2(2.1)
Adenostemma brasilianum
herb
2(1.3)
1 (2.0)
1 (10.0)
^ Onicum cf. mertensii
herb
2(1.3)
1 (l.D
1 (1 0.0)
Rhizophora mangle
tree
2 (1.3)
1 (l.D
1 (2.0)
'\nnona glabra
tree
1 (0.6)
1 (2.0)
Knl boseboenus robust us
herb
1 (0.6)
I (2-0)
290
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 2. June 2012
above ground of the nest upper rim varied from 30
to 220 cm (110 ± 40 cm; n = 151). The height
increased 7, 11, and 15 cm front the end of nest
building to the end of the reproductive period for
three nests. Nest height for the remaining nests
decreased from I to 55 cm (15.4 ± 0.1 cm; n =
30). Increase in nest height was the result of
growth of the supporting vegetation, while the
decrease was due to the natural bending of the
vegetation.
Nests were anchored to the supporting vegeta¬
tion using from one to I I attachment points (4. 1
± 2.3; n = 150) with use of dry (50%) and green
vegetation. Most nests (;i = 151) were attached to
two supporting points oriented in different
directions (22% inclined and horizontal. 14%
vertical and horizontal, 13% vertical and in¬
clined). but some were attached to supports in all
directions (20%), or only to inclined (18%),
horizontal (8%), or vertical (7%) vegetation.
Nineteen plant species were used for nest
attachment and more than half of the nests were
supported by only one plant species, the most
common being A. danaefolium and C. jaimiicen.se
(Table 3). Up to four plant species were used as
support for some nests with use of two species
(32% ol Lhe nests) being more common than use
of three or four species (~6 and 1 %, respectively)
(Table 3). Most nests were attached to herbaceous
plants, but 11% were attached to herbaceous
plants and a tree or shrub, and 1 1 % were attached
only to trees or shrubs (Table 3). A nest attached
to the fork of an additional tree species (Tibou-
china trichopoda) was found in a marsh with
distinct physiognomy.
All nests examined had two oval-shaped white
eggs (n = 163) with several irregular spots of two
different shades of brown (N„0: A70 X M80 and
N8o: A|0 X M60; n = 12) scattered throughout the
egg, but concentrated at the middle or the largest
pole (Fig. 1). Eggs measured from 18.0 to
20.2 mm in length (18.9 ± 0.47 mm, n = 34),
and 13.2 to 15.6 mm in width (14.0 ± 0.48 mm).
Egg mass ranged from 1 .3 to 2.0 g ( 1.8 ± 0 1 7 g-
n = 33).
DISCUSSION
The reproductive season of the Marsh Antwren
occurs from the end of the winter to the beginning
of the summer in the Austral Hemisphere and,
together with egg coloration and clutch size, are
within the normal variation in Thamnophilidae
(e.g., Velho 1932, Zimmer and Isler 2003). Sick
(1985) proposed recognition of five broad nest
types used by members of the Thamnophilidae
Some nests of the Marsh Antwren do not fit in an)
of the proposed categories, and we recognize a
sixth nest type (open cup attached to vertical
structures). Thus, some nests of the Marsh
Antwren are typical open cup attached b) the
rim at horizontal structures (31%) or open cup
attached to vertical structures (15%). but most
used both building techniques (50%); the remain¬
ing nests represented unusual sanations for the
species. The great variation in height above
ground for nests of the Marsh Antwren is probably
related to the marsh habitat inhabited with tida
variation that occasionally may reach low lying
nests.
The nest placement on vertical structures used
by the Marsh Antwren is also found in other
unrelated marsh-dwelling birds of the Tyrannise.
Sylviidae, and Icteridae (Orians 1985. De la Pena
1987, Skutch 1996. Narosky and Salvador 1998,
Hansell 2000, Azpiroz 2003), as well as in
grassland birds (Emberi/idae; De la Pena 1996,
Di Giacomo 2005), The attachment of nests to
several vertical structures is a solution to prevent
the structure from slipping down in habitats with
predominant vertical structure (Hansell 2000): the
Marsh Antwren is the only thamnophilid known to
use this strategy.
ACKNOWLEDGMENTS
BLR received a grant from Coordenayao de Aperfciyoa-
mento de Pessoal de Nivel Superior (CAPESi and
Fundayao de Amparu a Pesquisa do Estado de Sao Paul"
< FAPESP: 04/13274-2). RB-t. was supported by gran's
Irom C 'onset ho Nacional de Desert vol vimento Cientificoc
Tccnoldgico (CNPq/MCT: 132893/2009-6) and CAPES,
and is currently supported by a grant from CNPqAtCT
(141823/201 1-9). DDS. MRP.’ and MAP arc supported h>
grants from CNPq/MCT (135205/2009-3, 571334 'JOtXs- ;
and 503835/2008-0. respectively). MRB and EC
supported by grants from the Programa de Reesiruiui K
das t niversidades Fedcrais (REUNI). Additional vupp'n
came from Fundayao O Boticario de Proteyao a Naiurt -
(0682/20052 and 0740/20071). Idea Wild donated equip¬
ment. Y. S. Kumvoshi, O. A. Guimaraes. and F. S. Me>cr
helped with terminology of herbaceous plants. Manv
students helped during the fieldwork. M. S. Milana
suggested and encouraged the realization of a Ph D by
BLR. C. E. Braun. K. J. Zimmer, and an anonym**5
reviewer revised the text.
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The Wilson Journal of Ornithology 124(2):292-297, 2012
FIRST RECORD OF A HARPY EAGLE (HARP 1 A HARPYJA)
NEST IN BELIZE
JAMES A. ROTENBERG,' 3 JACOB A. MARLIN,2 LI BERATO POP,2 AND WILLIAM GARCIA2
ABSTRACT.— We present the first description of a breeding record of the Harpy Eagle ( Harpia harpyja ) in Belize, and
describe the subsequent fledging of the juvenile. We discovered the nest on 27 November 2010 with a single 4-5 week-old
chick, and began focal observations. The juvenile spent 56.3% of 71 observation days feeding, and the parents delivered
food to the nest at a rate of one item every 2.04-3.33 days from late January to April. The most frequent food items were the
common opossum (Didelphis manupialis), white-nosed coatimundi ( Nasua narica), and Yucatan black howler monkn
( Alouatta pigra). We placed a satellite GPS-PPT transmitter on the juvenile Harpy Eagle on 14 April 2011 to track its
movement patterns alter Hedging. Soon alter, the parents stopped returning to the nest, the juvenile fledged, and for2Kda\s
we delivered food to the young eagle in place of its parents. The abandonment of the juvenile by the parents may have been
caused by low food abundance caused by drought conditions and/or placement of the transmitter may have had a role The
male subsequently returned to feed the juvenile. We believe these eagles represent one of the northernmost known extant
breeding pairs of Harpy Eagles in the Americas. Received 12 September 2011. Accepted 23 January 2012.
The Harpy Eagle (Harpia harpyja) once ranged
from southern Mexico to northern Argentina
(Vargas et al. 2006); however, due to deforesta¬
tion and persecution by humans the Harpy Eagle
is now extirpated across most of Central America.
The Harpy Eagle is a species of high conservation
concern over its entire range and is designated
as ‘Near Threatened’ by the IUCN (2011). The
species is considered “Critically Endangered*
(Meerman and Clabaugh 2010) in Belize and
there were only five confirmed observations
between 1980 and 2000 (Vargas et al. 2006).
Two eagles were observed in 2000. one at
Millionario near Las Cuevas in the Chiquibul
Forest Reserve, and one at Caracol Archeological
Reserve (Lewis 2000). The Harpy Eagle was
subsequently considered extirpated in Belize
(Matola 2006) and a reintroduction program
began with captive-bred birds from Panama
(Muela and Curti 2005). We made nine observa¬
tions of wild (i.e., not introduced and unhanded)
Harpy Eagles in the Bladen Nature Reserve
(BNR) in the Southern Maya Mountains since
December 2005. Two of our observations were
especially significant because they were juveniles
and young Harpy Eagles typically stay in close
proximity (< 2 km) to their nest for at least 1 year
(Rettig 1978). We began the Integrated Commu¬
nity-Based Harpy Eagle and Avian Conservation
Program tor the Maya Mountains Massif follow-
' Department of Environmental Studies, University
Norih Carolina Wilmington. Wilmington, NC 28403 US
-Belize Foundation for Research and Environment
Education (BFREE), P. G. Box 129. Puma Gorda, Beliz,
Corresponding author; e-mail; rotenbergj@uncw.edu
ing our 2005 rediscovery (Jones and Komar 2006 1
to monitor the species, find nests, and monitor
the bird community to test hypotheses on the
resources that support flagship species such as the
Harpy Eagle (Rotenberg et al. 2009).
We discovered an active Harpy Eagle nest on 2*
November 2010 in the BNR (Jones and Komar
201 1 ). We began to monitor, study, and protect the
nest, mated adult pair, and nestling. Much of what
is known about Harpy Eagle nesting behavior
comes from observations in South America (e.g..
Seymour et al. 2010) because there are few records
of Harpy Eagle nests in Central America (Vargas
et al. 2006). In addition, observations of prey
provisioned to the young al the nest are limited to
South America (Schulcnberg 2009). The distribu¬
tions of prey species differ between Central and
South America, and prey choice by Harpy Eagle*
in Belize could vary from those of birds in Soulh
America. Our objectives in this paper are to
describe: ( 1 ) our observations of Harpy Eagle nest
behaviors. (2) Hedging of the juvenile eagle and
our application of a satellite transmitter. (3) prey
species and food delivery rates, and (4) the first
breeding record of Harpy Eagles in Belize (H. L.
Jones, pers. comm.).
OBSERVATIONS
All observations were in the 40,336 ha Bladen
Nature Reserve (BNR). the core conservation area
within the Maya Mountains in the Southern May**
Mountains of Belize (Fig. 1 ), which has the highest
protection status of any protected area in Belize.
The BNR is among the last large, relatively intact
blocks of lorest in the Selva Maya region; one ot
the most pristine, biodiversity-rich areas in this
292
Rotenberg el al. • HARPY EAGLE NESTING IN BELIZE
293
HG- 1. Distribution of the Harpy Eagle (. Harpia harpyja) in Central and South America. Inset is the nest location in Belize.
Distribution data provided by NatureServe in collaboration with Robert Ridgelv. James Zook. The Nature Conservancy
Migratory Bird Program Conservation Intemational-CABS. World Wildlife Fund-US. and Environment Canada— WILD-
SPACE,
•Mesoamerican hotspot for biodiversity (Iremon-
gerand Sayre 1994). We used the Belize Found¬
ation for Research and Environmental Education
BFREE, www.bfreebz.org) field site as our oper¬
ations base.
Our first direct evidence for breeding Harpy
Eagles in Belize was the observation of copulations
°f a mated pair in April 2008, We made these
observations during 14.5 hrs of focal observations
over 2 days from a mountain lookout established to
observe a steep-sided valley for eagles; our first
observation of the juvenile was also made from this
location. The valley is mostly north-south. 2.5 km
long by 0.5 km wide, and is characterized as
primarily evergreen tropical forest (Beard 1944).
We saw an eagle repeatedly returning to the same
tree within the forest on 26 November 2010 and on
the follow ing day at 0900 hrs we located the nest in
this tree from the ground underneath it. The nest
was 35 in from the ground in the crown of a Virola
koschny tree. The nest was observed from a hill
325 m distant and it was from this location that we
294
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 2. June 2012
TABLE 1. Prey items observed at die Harpy Eagle nest, Belize, 2010-201 1.
Species
Common name
n
Percent
Didelphis marsupialis
Common opossum
4
23.5
Nasua narica
White-nosed coat i m undi
3
17.6
Alouatta pigra
Yucatan black howler monkey
3
17.6
Crax rubra
Great Curassow
2
11.8
Ateles geoffroyi
Central American spider monkey
1
5.9
Potos flavus
Kinkajou
1
5.9
Tamandua mexicana
Northern tamandua
1
5.9
Anhinga anhinga
Anhinga
1
5.9
Iguana iguana
Green iguana
1
5.9
Totals
17
100
confirmed the presence of a nestling that we
estimated to be 4-5 weeks of age.
We made 601 hrs of focal observations over
71 days between late January and May 2011.
Observation periods lasted an average of 6 days,
beginning just after sunrise and ending before
sunset. The juvenile fed on 40 of the 71
observation days (56.3%) and spent a total of
48 hrs of its time feeding (8.03%). Feeding was
coupled with the juvenile’s submissive begging
posture (wings held down) and calling. Behaviors
other than feeding observed consisted of stand¬
ing (4.6 hrs/day. 35%>) and sleeping or resting
(3.7 hrs/day, 27%). All other behaviors accounted
tor 1% or less oi the bird's behavior per day. Prey
items delivered to the nest were variable with
common opossum ( Didelphis marsupial is), just
slightly more common than white-nosed coatimun-
di ( Nasua narica) and Yucatan black howler
monkey ( Alouana pigra ) (Table I ). We observed
one prey item delivered every 2.04 days at the
juvenile's approximate age of 4 months, increasing
to one delivery every 3.33 days at 6 months
(Table 2). The adult female provided nearly all of
the food (female: n = 14. 82%; male: n = 3. 18%).
We also made periodic observations of the female
cutting, collecting, and bringing green branches to
the nest trom an adjacent Ceiba pentandra tree.
We placed an Argos System/CLS Satellite
GPS-PPT (Global positioning system-platform
transmitter terminal) transmitter and VHP trans¬
mitter on the juvenile Harpy Cagle on 14 April
2011 to track its post-fledging movements in
cooperation with experts from The Peregrine
Fund, Boise, Idaho, USA. The hope was to follow
die young eagle for up to 3 years to map Harpy
Cagle territory size and habitat. We predicted this
procedure would have little or no effect on the
feeding and care of the young, but decided not to
place any device on the adults as they currently
represent the only known breeding pair of Harpy
Cagles in Beli/,e. The juvenile was released into
the nest after deploying the satellite transmitter
The parents made only one feeding attempt after
transmitter deployment on 17 April 2011. after
which neither adult was observed at the nest
Between 2 and 14 May 2011, after finding the
juvenile perched, branching, and/or Hying 5-30 m
front the nest on low branches (< 3 m), we
decided the parents were not returning and we had
to feed the Hedged eagle or watch it die. We used
a technique similar to that used for the 'soft
release' of a captive-bred eagle (Muela et ul
2003). We followed only the feeding protocol,
which consists of (ceding the eagle at a designated
location behind a blind so the bird does not
associate food with people. Our goal was to feed
the bird until it could start to hunt by itself and
then gradually reduce the food provided to wean
the bird and encourage hunting.
We provided three dead Domestic Chicken4
(Callus gallus) to the juvenile from 15 to 25 May
2011. The young eagle fed on each chicken until all
of the body parts were consumed. We provided
TABLE 2. Mean prey delivery rates per age (by month1
of the juvenile Harpy Eagle in Belize including one
delivery after placement of the satellite transmitter at the
onset of the 7th month.
Juvenile age
Mean delivery rate
n
4 months
2.04
7
5 months
2.33
5
6 months
3.33
4
Post transmitter
4
1
Overall average
2.93
17
Rotenberg el al. • HARPY EAGLE NESTING IN BELIZE
295
a live chicken on 27 May 2011 at 0900 hrs to
encourage the young eagle to hunt and capture the
chicken on its own. The juvenile observed the live
chicken for ~ 15 min from a branch 3 m off the
ground. The eagle flew directly towards the
chicken and inserted its talons into the chicken's
breast. The kill seemed immediate upon impact,
after which the eagle Hew a short distance from the
feeding station to a log on the ground. The eagle
plucked breast feathers off the chicken for 5-10 min
before feeding and then consumed nearly the entire
chicken that morning before 1200 hrs. The Harpy
Eagle subsequently hunted, captured and fed on
four additional live chickens until we ceased our
feeding program on 1 1 June 2011. We attempted to
emulate adult delivery rates while feeding the
juvenile as reported in observations in both Panama
and South America of —2-3 days (Rettig 1978,
Seymour el al. 2010) and our own previous
observations, resulting in a rate of one chicken
every 2.15 days over a 28-day period.
Wc did not find the Harpy Eagle at the feeding
station on 14 June 201 1. The GPS satellite data
showed the juvenile eagle had flown -500 m
north of the nest, the furthest distance the juvenile
had ilown from the nest up to that date. We
located the juvenile on 27 June 201 1 using the
OPS satellite data and the VI IE signal in a large
'■~45 ni) Ceiba pentcmdni tree 300 m northwest
ot the nest. The adult male Harpy Eagle w as with
the juvenile and offered an unknown prey item to
the juvenile. The young eagle explored the entire
valley after this date, and proceeded on to a
smaller, similar valley directly adjacent in July
-dll for a total travel area of —3.2 km between
14 April and 20 July 201 1 (tracked by satellite
only between 27 Jun and 20 Jul 2011).
DISCUSSION
Our discovery of an active Harpy Eagle nest is
'he first official nest record for Belize (H. L.
Jones, pers. comm.). We believe the pair in the
BNR represents one of the northernmost known
vxtant breeding pairs of Harpy Eagles in the
Americas (Fig. 1). There has been only one
Published account of a juvenile (3rd yr bird)
HarPy Eagle north of Panama in recent years
-b02), at the Marenco Biological Station in the
Oso Peninsula, Costa Rica, which suggests the
Presence of a breeding pair ( Jones 2002), and only
one observation of a nest and pair previous to that
in 1994 from Oaxaca, Mexico (Peterson et al.
2°03). All other Harpy Eagle reports north of
Panama are of single adults, and suggest a
continued presence of Harpy Eagles in these
areas (Table 3). There was an observation of a
single adult Harpy Eagle possibly constructing a
nest in Chiapas. Mexico outside of published
accounts in the ornithological literature, as cited
in a local newspaper in February 2011 (Morales
201 I). which remains unconfirmed.
Our observations of prey delivery at the nest do
not differ significantly from data collected in
South America. On average, our rates in Belize
(2.04-3.33 days) arc similar to those reported by
Rettig ( 1978) (2.5-3.5 days) and Seymour et al.
(2010) (2. 1-2.4 days); however, both studies
reported fewer days per delivery (i.e., delivery'
with greater frequency) as the nestling grew. We
observed the opposite trend in Belize: observed
prey deliveries occurred with a greater number
of days in between (i.e., deliveries with less
frequency) (Table 2). We also note the male made
significantly fewer deliveries (3. 18%) than the
female (14. 82%) while, in the South American
studies, males had a much greater role. For
example, Rettig (1978) observed male prey
delivery at one prey item every 3.5 days until
about 20 weeks of age at which time the male
remained at the nest while the female hunted more
frequently, and Seymour el al. (2010) observed
male prey delivery at one prey item every 2.4 days
over this same period. We observed the male
make one final visit to the nest in Belize when
the juvenile was about 21 weeks ot age. The
behaviors of the Belizean Harpy Eagles weic
similar to those in Sena da Bodoquena National
Park in Brazil (Martins Pereira and Salzo 2006)
where the male also visited the nest only a few
times.
We speculate as to why these behavioral
differences occur based on two factors. First.
Belizean Harpy Eagles are breeding at the fringe
of their natural range where prey choice and
availability may be limited. Harpy Eagles in the
south of their range prey on sloths (Bradypus spp.
and Choloepus spp.). and a variety of species of
monkeys with these mammals comprising large
parts of eagle diets (Galetti and de Carvalho 2000.
Lenz and Marajd dos Reis 2011). Belize is north
of the range for sloths and only supports two
primate species. Thus, one would predict the diet
of Harpy Eagles in Belize would be quite
different, as indicated by our observations. We
observed troops of Central American spider
monkey (Ateles geoffroyi ) in close proximity to
296
THE WILSON JOURNAL OF ORNITHOLOGY • Vo/. 124. No. 2. June 2012
TABLE 3. Harpy Eagle observations north of Panama, 1990-201 1.
Years
Date
Observation type
1 an al ion. Country
Ciution
2011
Jan-Jun 201 1 Mated pair, juvenile, nest
Bladen Nature Reserve, Belize
Rotenberg et al. (this
paper)
Aug 201 1
Adult
Chiapas. Mexico
Mandujano 201 1
Feb 2011
Adult, nest (?)
Chiapas, Mexico
Morales 2011*
2001-2010
Nov 2010
Mated pair, juvenile, nest
Bladen Nature Reserve. Belize
Jones and Komar 201 1"
Oct 2010
Adult
Thousand Foot Falls. Belize
Jones and Komar 201 1
Nov 2009
Juvenile
Bladen Nature Reserve, Belize
Conference
presentation*
Apr 2008
Mated pair
Bladen Nature Reserve, Belize
Conference
presentation*
2006-2008
Adults (6 sightings)
Bladen Nature Reserve, Belize
Conference
presentation*
Dec 2005
Juvenile
Bladen Nature Reserve, Belize
Jones and Komar 2006’
1991-2000
2002
Juvenile
Oso Peninsula. Costa Rica
Jones 2002
Mar 2000
Adult
Chiquibul Forest Reserve, Belize
Lewis 2000
Feb 2000
Adult
Caracol Archeological Reserve,
Belize
Lewis 2000
2000
Adult
Peten, Guatemala
Vargas et al. 2006
1998
Adult
Chiapas, Mexico
Puebla-Oiivares et al.
2002
Apr 1994
Adult
Esperanza Camp. Toledo District.
Belize
Jones et al. 2000
1994
Adults, mated pair, nest
Oaxaca. Mexico
Peterson et al. 2003
1990
1991
Adult
Chiapas, Mexico
Morales-Perez 1998
1990
Adult
Aguacate Village, Toledo District.
Belize
Jones et al. 2000
a Unconfirmed sighting
c Observations by Rotenberg et al. (this paper).
C Xn' C°"greSS 0f The Mesoan,Bri«n Society for Biology and Conservation, j. A. Rotenberg. j. A. Marlin, and W. Garcia, 2009.
the nesl. but this was a rare prey item (n = 1).
Instead, the eagles preyed upon non-primate
species such as D. marsupialis and N. narica.
More observations are necessary, and it remains
unclear as to why A. pigra was selected in similar
numbers to the mammal species over A. geojfroxi
when spider monkeys seemed abundant. Obser¬
vations of reintroduced Harpy Eagles in northern
Belize (A. Muela. unpubl. data) also found eagles
more commonly led on N. narica rather than
primates. Second, drought conditions may have
had an adverse eftect on our Harpy Eagle parents.
Belizean climate is characterized by wet and dry
seasons with the wet season from mid-May
through November. The wet season in 2011 did
not commence until mid-June, and the dry season
was pronounced with extensive fires across the
country. Lack of food due to a drought-stressed
habitat may have caused the Harpy Eagle parents
to abandon the chick or they may have deserted
the juvenile because of human interference.
We believe there may be additional Harpy Eagle
breeding pairs within the BNR and Maya Moun¬
tains. This secretive species may not have been
observed in these areas due to the rugged terrain
and remoteness. Additional Harpy Eagle research
and monitoring in Belize similar to that conducted
in Panama (Vargas Gonzalez and Vargas 201 1 ) arc
necessary' to examine survivorship and population
size, as well as territories and home ranges in the
northernmost extent of their range.
ACKNOWLEDGMENTS
We thank the Belize Forest Department and Ya’axehc
Conservation Trust for permitting and logistical support ui
the BNR. We gratefully acknowledge the following lor
their generous support of our project: The Peregrine Fu-‘
National Geographic Society- Waiu Foundation. The Pr >■
tcctcd Areas Conservation Trust of Belize. The NaM*
Conservancy. The Belize Zoo, The Columbus Zoo
Conservation Fund. Disney Worldwide Conservation Fundi
Natural Encounters Conservation Fund. Santa Fe College
Teaching Zoo. Norcross Wildlife Foundation. Optics for the
Tropics. Biodiversity Research Institute, and the Doper:
merit of Environmental Studies. University of North
Carolina Wilmington. We thank the following individuals:
Angel Muela. Richard Foster. Sharon Matola. Steven
Rotenberg et al • HARPY EAGLE NESTING IN BELIZE
297
Brewer. Alejandro Cholum. Thomas Pop. Sipriano Canti.
j jj\ ,,nd Dan Dourson. Wilfred Mutrie, Samuel Meaehum.
JiiDiLv Abbott. Brett Gamer, and the communities of
Bladen. Golden Stream, and Trio. We also thank Lee Jones
..no Michael Patten for reviewing early versions of this
manuscript and two anonymous reviewers.
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The Wilson Journal of Ornithology 124(2):298-309. 2012
PROVISIONING OF NESTLING DICKCISSELS IN NATIVE
WARM-SEASON GRASS FIELD BUFFERS
KRISTINA L. MITCHELL,' SAMUEL K. RIFFELL.1-3
L. WES BURGER JR.,1 AND FRANCISCO J. VILELLA’
ABSTRACT. — We used video cameras in 2008-2009 to record provisioning activities at Dickcissel (Spiza americam
nests in and around Conservation Reserve Program field buffers in north-central Mississippi. USA. We simultaneously
observed foraging flight distances of parents. Provisioning rate ( P = 0.412). biomass (P = 0.161). and foraging distance
(P = 0.159) did not increase with nestling age. Parents delivered larger items to meet demand associated with older
nestlings (P = 0.010-0. 001 ). This suggests energetic costs of changes in prey selection Were less than costs of increasing
the number or distance of provisioning trips. Presence of male helpers increased provisioning rate t P < 0.001) but not
biomass (P = 0.992) because males brought smaller prey items (P = 0.001-0.021 ). Presence of observers 30 m from the
nest reduced provisioning rates (P = 0.005) and biomass delivered (P - 0.066). Lack of habitat effects for any aspect of
provisioning suggests grass field butlers provided nestling food resources similar to surrounding habitats. Use of continuous
video monitoring of nest activity allows well-concealed activities including provisioning and male helping to be directly
observed and better quantified. Received 7 September 2011. Accepted 26 January 2012.
Nestling provisioning by birds can affect
reproductive success. Short periods of decreased
provisioning (either in rate or biomass) may cause
slower growth, reduced body condition, decreased
survivorship, and reduced fledging success of
nestlings (Bryant and Westerterp 1983, Martin
1987, Saino et al. 1997). Decreased provisioning
can compromise future dominance ranks and
lower probabilities of acquiring breeding territo¬
ries (Metcalfe and Monaghan 2001). Provisioning
rates may also index available food and. conse¬
quently. habitat quality (e.g.. Brickie et al. 2000).
Adults of most passerines feed 60-100%
arthropods to nestlings to provide the proicin-rich
diet necessary for rapid development. Parents can
optimize net energetic gain per nest visit (foraging
trip) by altering provisioning rates, load size
(biomass), foraging distances, and prey taxa and
sizes (Orians and Pearson 1979. Wright et al.
1998). Provisioning nestlings is energetically
costly tor parents and impacts parent survival
(e.g., Dijkstra et al. 1990), size of future clutches,
and intervals between broods and. ultimately,
future reproductive potential (e.g., Dijkstra et al.
1990, Decrenberg and Overkamp 1999). Thus,
parents should prefer larger prey (especially for
large clutches or older nestlings with greater
Department of Wildlile. Fisheries and Aquaculture,
Mississippi Slate University. Mississippi State, MS 39762
USA.
U.S. Geological Survey, Cooperative Research Unit,
epartment ot Wildlife, Fisheries and Aquaculture. Mis¬
sissippi State University. Mississippi State, MS 39762
USA.
’Corresponding author; e-mail; sriffell@cfr.msstate.edu
demand anil wider gapes) that reduce searching
time and provide more energy per provisioning
trip (Wright et al. 1998, Britschgi et al. 20061,
Parents should minimize search time by foraging
close to the nest, and only forage at greater
distances from the nest when food near the nest
becomes difficult to find (Andersson 1981.
Brickie et al. 2000, Britschgi et al. 2006) or when
higher quality food sources are available at greater
distances.
Studying provisioning rates in grassland birds is
important because they are experiencing large
declines in the United States (1966-2009) com¬
pared to other bird guilds (Brennan and Kuvlesky
2005. Sauer et al. 201 1). Agricultural intensifica¬
tion. grassland habitat loss and fragmentation, and
increased woody growth in remaining grasslands
favoring forest-edge fauna have likely led to these
declines of many grassland birds, especially in
the Midwest and Great Plains (e.g., Samson and
Knopf 1994. Brennan and Kuvlesky 2005). The
U.S. Department of Agriculture's Conservation
Reserve Program (CRP) since initiation in 198?
has added millions of hectares of grassland habitat
to agricultural landscapes in the United States u
the form of whole field plantings and a variety ot
buffer strip practices. Ostensibly, this program has
benefited grassland bird populations (e.g., Ryan :l
al. 1998. Herkeri 2009). However, little is known
about provisioning rates, food availability (McIn¬
tyre and Thompson 2003), and habitat quality
(reviewed by Haufler 2005) of CRP grasslands,
especially in the southeastern USA (e.g.. Smi*
et al. 2005) where grassland practices are lcs-
common choices for CRP than in other regions.
298
Mitchell et al. • DICKCISSEL NESTLING PROVISIONING
299
Our objective was to quantify provisioning
activities of Dickcissels (Spiza americana ) using a
combination of continuous video recording and
direct observation. We hypothesized that: ( 1 )
provisioning rates and biomass delivered by
Dickcissels would increase with nestling age and
differ between nests in CRP buffers compared to
nesLs in non-buffer habitats (potentially primary
habitat); (2) prey size would increase with
nestling age and nestling number, and differ
between buffer and non-buffer nests; and (3)
longer foraging trips would be associated with
alder nestlings, larger clutches, and larger prey
sizes.
METHODS
Focal Species.— The Dickeissel has declined in
the United States (trend = -0.7% since 1966:
Sauer et al, 2011) and is listed by Partners in
Flight I PIF) as a species of concern in the
Southeastern Coastal Plain region because of
anthropogenic threats to breeding habitat (Rich
si al. 2004). Dickcissels are polygynous and nest
in fallow fields, unmowed hayfiekls. and old
fields with abundant forbs (Temple 2002). Nest
building to hatching lakes 15-21 days, and
nestlings Hedge after 8-10 days (Temple 2002),
Dickcissels are mostly granivorous. but feed
primarily on arthropods during the breeding
se»son (Temple 2002).
Study Area. — We conducted our research at B.
tartan Farms Inc., a 2,104-ha privately-owned farm
1:1 C'la) County. Mississippi within the Black
Fmirie physiographic region. Seventy-nine hect-
atrfk °1 mw crops had been enrolled in CP33-
Dabitat Buffers for Upland Birds in 2005. CP33 is
rot restricted to highly erodible farmland, allow ing
for wider implementation in intensive agricultural
landscapes where grassland habitat is often scarce.
Buffers are composed of 10 to 40-m strips of native
‘ arrn-season grasses planted around agricultural
re,d margins to provide habitat for Northern
Bobwhite (Col inns Virginia mis) and other conti-
nenially declining birds such as Dickeissel. Indigo
hunting ( Passerina cyanea ), and Field Sparrow
‘Wa-lln pit si l la) (Sauer et al. 2011) that may use
cp33 buffers (e,g.. Smith et al. 2005).
• P’3 buffers were planted with big bluestem
'htdropogon gerardii), little bluestem (Scliiza-
'’lynum scoparium ), indiangrass (Sorghastrum
Mans), partridge pea ( Chamaecrista fasciculate).
b>ack-eyed susan (Rudheckia hirta ), and Maximi-
l|an sunflower (Helianthus maximiliani) in May
2004. These buffers were 4 and 5 years post-
establishment at the time of our study. Producers
are required to periodically disturb buffers (e.g.,
light disking or prescribed burning), and a subset of
buffers was burned (in spring) or disked (in fall)
each year as part of a broader experiment (Adams
2011. Dollar 2011. Hale et al. 201 1 ). Dickcissels
largely avoided nesting in disturbed buffers
(Adams 2011), and we do not address disturbance
effects. We located Dickeissel nests m areas along
the periphery or near (16 km/hr) on one to four mornings
between days 4 and 7 post hatching. We did not
film before day 4 to avoid nest abandonment by
parents (Schadd and Ritchison 1998) or after day 7
to avoid premature Hedging.
We placed tripods with mounted aluminum
cans (to mimic video recorders) near nests to
familiarize birds with the recording equipment 1
to 2 days prior to filming. We positioned hand¬
held camcorders (Sony Handycam DCR-SR42®)
at nests on each recording day on tripods 0.5
to 1.0 m from nests (Dearborn et al. 1998).
Camcorders were programmed to begin recording
20 min after the technician had departed (0545 to
0730 hrs CST) to allow birds to return to normal
behavior. Each individual recording session lasted
4 hrs.
Measuring Provisioning. — Video tootage was
processed using Adobe Premiere Pro software©.
We tabulated nestling provisioning rates (adult
visits to nest/hr/nestling) and prey taxa for each
1 -hr period of video footage. We identified nestling
diet composition for taxonomical groupings of
arthropods to Order. We measured length of each
arthropod from the frons to the end of the abdomen,
not including wings, antennae, or ovipositors
(Sejberg et al. 2000). to estimate biomass (energy)
delivered per nestling/hr. We assigned each prey
item to one of three size categories (Schadd and
Ritchison 1998): small adult bird beak length,
— 16. 1 mm. Temple 2002). medium (> adult beak
length and up to 2 X*s beak length), and large (>2
X’s beak length).
300
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 2. June 2012
We collected arthropods in 2009 from 0930 to
1 130 hrs CST during mid-morning from mid-June
through early July coinciding with peak breeding
of Dickcissels. We visited three separate locations
in each habitat type where Dickcissels were
primarily foraging (burned buffers, disked buffers,
control buffers, pasture fields, hay. milo, corn,
soybean, riparian, roads). We look 50 sweep net
samples per site (38.1 cm diameter net). We dried
all arthropods at 60 C for 24 hrs (Southwood
1978). Arthropods from each size category were
weighed to the nearest ±0.0001 mg. We assigned
a mean weight to apply to arthropods of the same
taxa (Order) and size categories observed on
video (Rogers et al. 1977). Less than 1.2% of the
total items brought to nestlings were <5 mm. and
we only identified arthropods >5 mm and placed
them into one of the three size classes. Certain
species of ground-dwelling arthropods may have
been under-represented in sweep net samples
(Doxon et al. 2011), but these were more likely
to be small or fast moving insects not typically
collected by Dickcissels (e.g., orthoplerans, lepi-
dopterans). We estimated availability of arthropod
species and mass of each arthropod si/e class used
in biomass calculations.
Foraging Observations.— We recorded forag¬
ing trips of Dickcissels from a 2.5-tn ladder
positioned >30 m from the nest during 2-hr
monitoring periods concurrent with 4-hr video¬
taping sessions. We recorded straight-line dis¬
tance traveled from the nest to where food was
collected on georeferenced maps for each forag¬
ing trip. We grouped foraging distances into bands
of 10-25. 26-50. 51-75, 76-100. 100-200. and
200+ m for analysis. We recorded cloud cover as:
0 (clear), 25 (1-25% cloudy), 50 (26-50%
cloudy), 75 (50-75% or mostly cloudy), and
100% (complete overcast). We recorded wind
speed using a modification of the Beaufort wind
scale: 0-1.6 (calm). 1. 6-8.0 (light breeze, grass
and leaves slightly moving). 8.0-14.5 (grass,
leaves, and small twigs constantly moving), and
16.1+ km/hr (small tree branches moving, ground
debris blowing around).
Statistical Analysis. — We Calculated provision¬
ing rate as number of visits per nest per hour
divided by the number of nestlings (Sejberg ct al.
2000, Britschgi et al. 2006). Total biomass (g) was
the sum ot biomass brought to the nest by adults
(both males and females) per hour divided by
number oi nestlings (Sejberg el al. 2000). We
identified nestling diet composition from video
observations. Foraging distance was the distance
(m) from the nest to the location where parents
collected food for their nestlings.
We used general linear mixed models i
account for multiple nests in the same field
(random effect) and repeated observation periods
on individual nests to lest hypotheses about
continuous response variables (provisioning rate,
biomass, foraging distances) (Littell et al. 2006.
SAS Institute Inc. 2007). Predictor variable'
included nestling age, nest locations (buffer vs.
non-buffer habitat), nestling number (foraging
distance only), and male helping (male vs. no
male). We included weather variables to test for
effects of day-to-day variation in weather condi¬
tions on provisioning behavior before testing for
effects of predictor variables. We dropped any
weather variables that were not significant at t -
0.10. We calculated provisioning rates and
foraging distance in both 2008 and 2009 (biomass
was calculated for 2009 only), and included year
as a covariate in all analyses. We included
observer presence (observers making foraging
observations) as a covariate in nestling provision¬
ing and biomass analyses to account for the
possibility that technicians observing foraging
trips could have affected provisioning activities.
We used selection ratios (Manly et al. 2002)
for eight Orders delivered to nests to measure
selection of prey types. Orthoptera. Lepidoptera.
and Araneuc comprised 99% of prey items and we
restricted subsequent analyses of prey taxa tc
those three groups. We tested hypotheses about
factors influencing prey type and prey size using
multinomial generalized linear mixed models
(PROC GLIMMIX; SAS Institute Inc. 2007) to
account for multiple observations li.e.. each prey
item provisioned) from the same nest. We used
prey tava and prey size (small, medium, and large
as response variables and buffer, observer pres¬
ence, nestling age, and nestling number as
predictor variables. We used a separate multino¬
mial model to test if foraging distance was related
to prey size, because foraging distance data only
existed lor a subset of the video observations
u hen an observer was present. We used general¬
ized linear mixed models to test effects of nestling
age and nestling number on probability of male
helping. We used ot = 0.10 for all tests.
RESULTS
We filmed 18 nests in 2008 and 25 nests in
2009 for 282, 1 -hr observation periods (125 in
Mitchell et al. • DICKCISSEL NESTLING PROVISIONING
301
TABLE 1- Variables examined with general linear
models for Dickcisse! foraging in native grass field buffers
in north-central Mississippi (USA). May to August 2008-
2009.
Variable
F
df
P
Provisioning rate (visits/nestling/hr)
Nestling age
0.98
3. 40.4
0.412
Buffer
0.01
1. 63.0
0.925
Observer present
7.97
1. 237
0.005
Male helping
15.60
1. 97.9
<0.001
Year
2.45
1. 38.9
0.126
Biomass (g/nestling/hr), 2009 only
Nestling age
1.89
3, 21.9
0.161
Buffer
0.54
1, 15.3
0.475
Observer present
3.43
1, 130
0.066
Male helping
0.00
I. 82.4
0.922
Foraging distance from nest (m/nest/hr)
Cloud cover
3.67
4, 87.8
0.008
Wind speed
3.09
3, 92.8
0.031
Nestling age
1.78
3, 68.4
0.159
Buffer
2.52
1 . 34.8
0.121
Nestling number
0.32
4, 33.4
0.861
Male helping
1.05
1. 68.6
0.310
Year
0.56
1, 51.8
0.456
-008; 157 in 2009). We observed 2.384 indiv idu.il
provisioning events and recorded 2.417 prey items
delivered to nestlings. Total filming hours for
provisioning rales were 264.02 (124.35 in 2008;
139.67 in 2009). We observed 822 foraging trips
uVer 1 18.30 observer hours (56.93 in 2008; 61.37
m 2009).
Nestling Provisioning Rate. — Cloud cover.
uind speed, and temperature were not related to
provisioning rates and were not included in
subsequent analyses. Provisioning rates (mean ±
^E.i were higher when a male helped (3.63 it 0.28
with male; 2.64 ±0.18 without; F,.g7» = 15.60.
V < 0.001; Table 1. Fig. 1) and lower when
observer* were present (2.97 ± 0.21 with
observer; 3.30 ± 0.20 without; F\z*n - 7.97.
^ = 0.005). Provisioning rate of nestlings did not
"itrease from 4 to 7 days (/•%.- «>.4 = 0.98. P =
did not differ between buffer and non¬
buffer habitats (F,.M0 = 0.01, P = 0.925). and
d,d not differ between 2008 (2.88 ± 0.28) and
-009 (3.39 ± 0.23; F,.3*.y = 1-89, P = 0.126).
Biomass Delivered.— Cloud cover, wind speed.
:ind temperature were not related to biomass and
Wcre dropped from subsequent analyses. Biomass
provided to nestlings in 2009 was 0.124 ±
0.005 g/nestling/hr. Biomass provided to nestlings
Was less when an observer was present (0.120 ±
0.012 g/nestling/hr) compared to periods with no
observer present (0.138 ± 0.012; F u-u, = 3.43,
P = 0.066; Table 1. Fig. 2). Nestlings received
>50% more biomass on day 7 compared to day 4.
but this difference was not significant (F3.21.9 =
I n9. P = 0.161 ). Biomass delivered did not differ
between nests in buffer versus non-buffer habitats
- 0.54. P = 0.475) and did not differ
when males helped (F\.»2A = 0.00, P — 0.992).
Prey Taxa.—1 Orthoptera comprised nearly all of
nestling diets in 2008 (91% of items) and 2009
(86%). Less common prey (both years combined)
included Lepidoptera (7%) and spiders (Araneae,
4%). Prey (Orthoptera. Lepidoptera. Araneae)
provisioned by Dickcissels were not the most
available taxa in surrounding habitats in 2009
(Fig. 3). Dickcissels preferentially selected Or-
thoptera (w = 3.71. P < 0.001) and avoided
Araneae (w = 0.22, P < 0.001), Coleoptera (w =
0.02. P < 0.001), Diptera (>r = 0.06. P < 0.001),
Hemiptera (»• = 0.00. P < 0.001). and Hyme-
noptcra {w = 0.02, P < 0.001) based on selection
ratios. Selection of Lepidoptera (w = 1.33. P =
0.436) and Mantidae (tv = 4.37, P = 0.491)
was not different from availability. We restricted
subsequent analyses of prey taxa to Orthoptera.
Lepidoptera. and Araneae because they comprised
>99% of the prey items.
Dickcissels in 2008 were more likely to bring
Orthoptera as nestling age increased (94% of total
items on day 7 vs. 91% on day 4; F 4.000 =
P = 0.028; Table 2). when nests were positioned
in buffers versus adjacent habitats (94 vs, 91%;
F,ft (H) = 4.91. P = 0.008), when observers were
absent (95 vs. 90%; F2,m = 7.65. P < 0.001).
and when nests contained <5 nestlings (94-100%
when > 4 nestlings vs. 88% with 5; = 2.41,
P = 0.026); the size of these actual differences
was small. Males were substantially more likely to
bring Lepidoptera (21% for males vs, 4% for
females) and less likely to bring Orthoptera (77
vs. 94%; F2.600 = 7.59. P < 0.001 ). None of these
factors influenced prey taxa brought to nestlings
in 2009 (F = 0.04-1.53, P = 0.166-0.992).
Prey Size. — Adults were more likely to bring
medium versus small prey items as nestling age
increased in 2008 (med. items = 73% of prey items
on day 4 vs. 80 and 79% on days 5 and 6; F4.640 =
3.36. P = 0.010; Table 2). Adults were more likely
to bring large items as nestling age increased in
2009 (e.g.. 30% on day 7 vs. 1 1 % on day 4; F6./026
= 6.26. P < 0.001 ; Table 2, Fig. 4). Males in 2008
were more likely to bring medium prey compared
302
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 2. June 2012
36
34
3.2
36
3.4
32
O)
c
(/)
(U
c
o
3.0
2 8
2 6
36
34
3.2
3.0
2.8
26
4 5 6 7
Nestling age (days)
Observer No
present observer
3.0
2.8
26 -
Buffer Non-buffer
FIG. I. Mean provisioning (least-squared means ± SE) rates at Dickcissei nests with young of various ages, buffer
locations, and with/without observers present in north-central Mississippi (USA). May to August 2008-2009.
to both small and large items (16% small, 60%
medium, and 23% large vs. 12, 79, and 9% 1'or
females; F2.M0 = 3.89, P = 0.021 ; Table 2); males
in 2009 were more likely to bring small items (27
vs. 20% for females; F2J02h = 7.28, P < 0.001).
Adults were slightly more likely to bring medium
items versus small items when observers were pre¬
sent in 2008 (81% medium with observers vs. 76%'
without; F2m o = 2.35. P = 0.096). but this effect
was small and did not appear in 2009 (F2 l02o =
0.1 1, P = 0.898). Neither placement of nest in a
buffer nor number of nestlings affected prey size
delivered (F = 0.01-1.92. P = 0.148-0.994).
Foraging Distances. — Foraging distance de¬
creased with increased cloud cover (F4t87S = 3.67,
P = 0.(X)8) and increased wind speeds (F, x =
3.09, P = 0.03 1 ; Table I . Fig. 5). Foraging distance
increased as nestlings became older, but this
increase was not significant (F3.68.4 = 1.78,
P = 0.159). Foraging distance was not different
between nests in buffers ;uid nests peripheral to
buffers (F,.34.« = 2.52, P - 0.121), was not related
to nestling number (F4,33.4 = 0.32, P = 0.861), was
not different when males helped (F|.6s.6 =
P — 0.310), and did not differ between years
(/'1.51.x = 0.56, P = 0.456). Size of prey items did
not differ across foraging distances (F|W,49i =
P = 0.500).
Probability of Male Helping. — We observed
male helpers at four nests (22%) in 2008. We
filmed 46 visits by males (13%) and 309 by females
(87%) at these nests. We observed male helpers, at
five nests (20%) in 2009 when we filmed 83 not
visits by males (23%) and 278 by females (77% ■
We filmed a single case of a male brooding ice
92 sec in 2008. Probability of male helping was n»t
related to nestling age (F3^39 = 1.96. P = 0.121 ) or
nestling number (F4 239 = 0.06. P = 0.993).
DISCUSSION
Nestling Provisioning. — Neither provisioning
rate nor biomass delivered per nestling significant
ly increased with nestling age. However, patfm-
chose larger items for older nestlings. This suggC'1’
energetic costs of changes in prey selection wen:
less than costs of increasing number of trips
Mitchell et al • DICKCISSEL NESTLING PROVISIONING
303
Nestling age (days)
020
0 18
016
0.14
012
0.10
0.08
*
i
Observer No
present observer
0 20
0 18
0 16
0 14
0 12
0 10
0.08
i i
Male No Male
FIG. 2. Mean biomass (least-squared means ± SE) delivered to Dickcissel nestlings of various ages, buffer locations,
and with/without observers in north-central Mississippi (USA). May to August 2008-2009.
FIG. 3. Proportion of total number of arthropods
observed on videos (dark bar) and collected in sweep nets
(oPen bar) from different habitats available to nesting
bickcissels in north-central Mississippi (USA), May to
August 2009.
However, adults may have made some other, more
subtle changes to meet increased demand. Biomass
delivered and foraging distance may have in¬
creased with increasing nestling age (P = 0.161
and 0. 1 59. respectively), hut these differences were
not significant. Possibly, these were small, but
biologically important responses that may have
been significant with a larger sample. A likely
explanation is that parents attempted to meet
increased demand by searching farther for larger
prey items. Increasing prey size may have allowed
adult Dickcissels to avoid energetic costs that more
frequent trips would have entailed. Wc did not
observe feeding behaviors past nestling age of
7 days, and it is possible that biomass delivered
continued to increase via changes in prey size and
taxa.
Dickcissel prey selection favored Orlhoptera,
similar to other diet studies of grassland birds
(e.g.. Kaspari and Joem 1993, Kobal et al. 1998).
However, selection of Lepidoptera and Coleoptera
prey was comparatively less in our study.
Orthoptera may have greater protein (e.g.. Robel
304
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124, No. 2, June 2012
TABLE 2. Variables examined with multinomial regression models for prey type and prey sizes
nests in native grass field buffers in north-central Mississippi (USA). May to August 2008-2009.
brought to Dickcissel
2008
2009
Variable
F
df
P
F
df
p
Prey type
Nestling age
2.73
4. 600
0.028
1.53
6. 901
0.166
Buffer
4.91
2. 600
0.008
1.15
2. 901
0.318
Observer present
7.65
2, 600
<0.001
0.04
2. 901
0.965
Nestling number
2.41
6. 600
0.026
0.14
6. 901
0.992
Male helping
7.59
2. 600
<0.001
1.39
2. 901
0.250
Prey size
Nestling age
3.36
4. 640
0.010
6.26
6. 1026
<0.001
Buffer
1.92
2. 640
0.148
0.01
2. 1026
0.994
Observer present
2.35
2. 640
0.096
0.11
2. 1026
0.898
Nestling number
0.51
8, 640
0.847
0.22
6. 1026
0.971
Male helping
3.89
2. 640
0.021
7.28
2, 1026
<0.001
et al. 1995) compared to other available arthro¬
pods (e.g., Lepidoptera and Araneae), and provide
proportionally more biomass per prey item, while
Lepidoptera are high in calcium and arachnids are
high in phosphorus (Rebel et al. 1995). Hemipleru
were more abundant than Orthoptera at our study
site, and they have greater energy content and fat
than Orthoptera (Robel et al. 1995). Dickcissels
may have avoided Hemiptera because they are
small and fast-moving compared to Orthoptera,
which could increase searching and handling time.
We excluded prey items <5 mm from analysis
because observing adults provisioning nestlings
I I Small prey clems
I I Medium prey items
U Large prey items
S'
c
75%) often occurred simulta¬
neously and preceded rain at our site. Thus, female*
may have spent more time brooding and watching
Mitchell el til • DICKCISSEL NESTLING PROVISIONING
305
0-1.6 1. 6-8.0 8.0-14.5 14.5 +
Wind speed (km/hr)
Cloud cover (%)
FIG. 5. Mca. foraging distances (least-squared means ± SE) of adult Dickcissels from nests in north-central
Mississippi (USA), May to August 2008-2009.
"ver nestlings, or foraged closer to the nest (sensti
^hnson and Best 19X2. Wittenberger 1982. Rosa
;in971; Temple 2002) because they may contain
higher amounts of food, more forbs, and a more
heterogeneous structure than prairies (Finck
1984). Adjacent non-buffer habitats in our study
closely resembled old field vegetation and
structure, and could potentially be considered
primary habitat over planted buffers. Females that
nested in non-buffer habitat (potentially primary
habitat) should have provisioned in predictable
ways (higher rates, more biomass, prey items of
different size and taxa) compared to nests in
306
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 2. June 2012
buffers. The only difference we observed was that
birds nesting in buffer habitat brought slightly
more Orthoptera (2008) than those nesting in non¬
buffer habitats. Foraging distances did not differ
between buffer and non-buffer sites, suggesting
birds had relatively equivalent foraging resources
and opportunities around the nest. Thus, in terms
of nestling provisioning, any difference in habitat
quality was not large, and native grass conserva¬
tion buffers in the CRP may represent additional
primary habitat.
Observer Effects on Provisioning. — Dickcissels
made — 10% fewer feeding visits, brought pro¬
portionately fewer orlhopterans (2008), and nest¬
lings received -14% less biomass when observ¬
ers were present. Our results are of concern
because human presence was low ( I observer) and
was not near the nest (~30 m distant). Observers
were careful to minimize disturbance (i.e., no loud
noises or sudden behaviors), and human presence
was not novel because technicians conducting
nest searching and monitoring were present prior
to filming. In contrast, using a ladder for
observations may have potentially increased
threats perceived by Dickcissels because it
mimicked vertical perches used by visual preda¬
tors (Andersson et al. 2009). Our observer
presence would be qualitatively similar to or less
intrusive than many farming activities occurring
in agricultural landscapes (e.g.. herbicide appli¬
cation. mowing, harvesting, checking fields) that
would pul humans and/or machinery in or near
bulfer habitats. Our levels of presence are
qualitatively similar to many recreational activi¬
ties (e.g.. wildlife-watching, hiking, etc.) that
occur in both crop and non-crop habitats (e.g.,
more natural areas) in agricultural landscapes.
Human disturbance has become more frequent
in recent years as the exurban footprint expands
into agricultural landscapes and more natural
areas such as parks and refuges allow access to
increasing numbers of recreationists and ecotour-
ists (Cordell et al. 2008).
Birds modify choices in foraging behavior and
limit activity around the nest if threatened by
predators, and humans may be perceived as
predators (Dunn el al. 2010). Birds may thus
choose to forage in habitats that are suboptimal
(e.g., Fernandez-.! uricic and Tcllcria 2000) or
reduce provisioning rates. Reduced nestling
growth rate can be a direct result of chronic
predator presence (Clinchy et al. 2004, Dunn et al.
2010), which indirectly may increase time to
fledging and prolong nestling exposure to preda¬
tion (Bize et al. 2003). Birds may also have
chronic stress (elevated glucocorticostcroid lev¬
els) when food availability and predation ask act
together (Clinchy et al. 2004. Eggers et al. 200X,
Dunn et al. 2010) which may impact reproductive
capacities (Zanette et al. 2003). Stressed females
may pass elevated hormone levels to eggs with
subsequent effects on offspring phenotype (Saino
et al. 2005). Nestlings with poor body condition
and slow growth rate may have lower social
rankings as adults and continue to experience
reduced body size and lifespan (Metcalfe and
Monaghan 2001 ).
Human presence may reduce foraging rates of
adults (e.g.. Fernandez-Juricic and Telleria 2000).
influence seasonal timing of song (Gut/.willer et
al. 1997), and decrease survival rates of nestlings
and fledglings (e.g., Safina and Burger 1983), We
know of no documentation of decreased provi¬
sioning as a direct result of human presence for
grassland birds other than our study. Seemingly
benign human activities may have more substan¬
tial effects on breeding success than currently
assumed if reduced provisioning is a common
response to low levels of human intrusion.
Remote monitoring of birds with video technol¬
ogy also may decrease potential for research-
related effects on nesting birds compared to direct
observation.
Male Helping. — Male helping increased provi¬
sioning rates but biomass delivered was not
different because males brought fewer Orthoptera
(2008) and smaller prey items (2009) than
females. The major benefit of mule helping
appears to be decreased effort by the female
rather than increased provisioning of the young
(and hence greater survivorship).
Several hypotheses may explain male helping
First, males may be more likely to help when food
abundance is low (e.g., Wittenberger I9S2)
Rainfall during the breeding season increased
almost two-fold in 2009 versus 2008 (May-Aug
2008 rainfall - 222 mm: May-Aug 2009 rain¬
fall = 420 mm: Mississippi State Department i'i
GeoScicnces). Vegetation density and subsequent
invertebrate abundance are typically greater in
wetter years, but males helped in both years-
Sccond, males may have more incentive to help
al late -season nests ( Igl and Best 2001 ) as predation
risk increases (daily survival rate of nests decreased
as the breeding season progressed in our study:
Adams 201 1 ). However, we observ ed male helping
Mitchell et al. • DICKCISSEL NESTLING PROVISIONING
307
in the early (2009) and middle (2008 and 2009)
pans of the nesting season. Third, helping may be
more advantageous to the male al later nest ages
because the nest's reproductive value increases
dose to fledging (Igl and Best 2001 and references
(herein). We observed male helping on days
4 through 7 but. because we only filmed during
those days, we cannot say whether male helping
increased at >7 days of the nestling period or was
absent prior to day 4. Fourth, male provisioning
could be favored in lower quality habitats (lgl and
Best 2001), but there is no evidence that old field
habitats and field buffers in which male helping has
been observed (Igl and Best 2001. this study) are
low quality for Dickcissels. Fifth, male helping
may be unique to specific individual Dickcissels or
local populations (Maddox and Bollinger 2(MX). Igl
and Best 2001 ). However, 14 of 2 1 locations where
this behavior has been observed (including our
study) are in the core breeding range of Dickcissels
(Igl and Best 2001). Males may be more likely to
help w'hen there are few females (Sejberg et al.
7000. Igl and Best 2001) because, in polygynous
systems, monogamous males (or those w ith fewer
females) have more time available to help
compared to males with multiple females (Sejberg
et al. 2000). We did not mark birds and cannot
address this hypothesis.
CONSERVATION IMPLICATIONS
Accessible and nutritional arthropod prey lot-
grassland birds is a key factor for conservation of
grassland species that use conservation set-aside
lands (Whittingham and Evans 2004). Native
grass held buffers in our study provided nestling
t(»d resources similar to or better in quality (e.g.,
I'iotnass and prey taxa) compared to surrounding
habitats. Native grass habitats (like CP33 buffers)
may typically provide habitat for more farmland
h,rds compared to clean-farming practices (e.g.,
Hellenes et al. 2003); greater structural com¬
ity on a landscape level may attract more
birds overall (Rodenhouse and Best 1994. Jones
ela|, 2005). Agri-environmental practices which
support arthropod populations and decrease per-
eeived and actual predation risk may improve
foraging rates and survival (Whittingham and
Evans 2004). More research on nestling provi¬
sioning by grassland birds should be conducted in
intensively managed agricultural landscapes and
native prairies, particularly prey selection and
foraging success of adults away from the nest.
Continuous video documentation of nest activity
allows well-concealed activities to be directly
observed and better quantified. More intensive
video documentation of Dickeissel nesting behav¬
ior should be conducted with other populations to
understand the true frequency of male helping and
identify its causes.
ACKNOWLEDGMENTS
We thank the USDA-NRCS Agricultural Wildlife
Conservation Center, College of Forest Resources. Mis¬
sissippi Agricultural and forestry Experiment Station, and
the Forest anti Wildlife Research Center for funding. We
thank B. Bryan Farms Inc. for allowing us to work on
private property. II. L. Adams. K K. Armstrong. J. R.
Bradford. A. S. Brown. J Ci. Dollar. A. B. DiNuovo, S. L.
Male, R. A. Hicks, W. H. Mitchell II. and A. A. Workman
helped collect data. W. If Mitchell II and N. A. Stukey
helped process videosand enter data, h D. Doxon reviewed
an earlier version of our manuscript. I he use of trade names
or products does not constitute endorsement by the U.S.
Government.
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The Wilson Journal of Ornithology 1 24(2):3 1 0- 3 15, 2012
THE EFFECT OF HABITAT EDGES ON NEST SURVIVAL OF
SPRAGUE’S PIPITS
STEPHANIE L. JONES'-3 AND GARY C. WHITE1 2
ABSTRACT. — We explored the relationship between Sprague’s Pipit (Anthus sprugueii) nest (n = 125) survival and the
distance from their nests to grassland edge and other linear features on Bowdoin National Wildlife Refuge in north-central
Montana from 1997 to 2007. Specifically, we studied the effect of distance to roads (secondary paved road and tertian
improved and unimproved dirt roads), an agriculture field, an active railroad right-of-way, and lacustrine shoreline on nest
daily survival rate (DSR). The overall DSR was 0.95 ± 0.0057 (SE) with a 95% confidence interval of 0.94-0.%. We
considered how models with distance thresholds (within 50. MX). 200, or 300 m) affected DSR while controlling for
important eovariates. None of the distance models improved the model over the minimum A1C, model containing only non¬
distance covariates. There was no support for distance to any of the edges, including roads, having an effect on DSR relative
to the minimum AIC,. model that contained three non-distance eovariates. Received 7 September 201 1. Accepted 2i
December 2011.
Sprague’s Pipits (Anthus sprcigueii) are grass¬
land songbirds endemic to the northern Great
Plains, breeding in south-central Canada anil
north-central United Slates. Concern about threats
to native mixed-grass prairie, coupled with
observed population declines and range contrac¬
tions, has led to listing of the species as threatened
in Canada (COSEWIC 2002) and proposed for
listing in the United States (USDI 2010).
Primary threats to Sprague's Pipit breeding
populations include degradation, fragmentation,
and loss of native mixed-grass prairies (COSEWIC
2002, Environment Canada 2008, Jones 2010,
USDI 2010). The level of threat that habitat
fragmentation poses relative to the effects of
habitat loss and degradation has been challenging
to identify (Environment Canada 2008) with some
studies suggesting Sprague's Pipits are area-
sensitive (e.g.. Davis et al. 2006). Habitat frag¬
mentation may contribute to the decline of
Sprague s Pipit populations through reduction in
average patch size, increased isolation of habitat
patches, and breaking the prairie into a mosaic of
small native grasslands interspersed with non¬
grassland habitat patches (Environment Canada
2008, Jones 2010).
There are several mechanisms or factors that
may influence how roads affect nest survivorship
of grassland bird populations. These factors could
1 U.S. Fish and Wildlife Service, P. O. Box 25486 DFC
Denver, CO 80225, USA.
Depaiimeni of Fish, Wildlife, and Conservation Biol-
CO 80523WUSA' Cl>l°rad° S,a,C Umvcrsit>'- Fon Collins,
’Corresponding author; e-mail;
Stephanie_Jones@fws.gov
include changes in food abundance and availabil¬
ity, attraction or repulsion of predators, increased
noise and dust from traffic, spread of non-native
vegetation in rights-of-way. enhanced develop¬
ment. and other disturbances radiating from these
features (Fahrig and Rytwinski 2009). Similar
effects may be associated with other linear
anthropogenic and natural features including
railroad rights-of-way, agriculture fields, fences,
and natural edges including lakes and streams.
The effects of the proximity to habitat edges and
roads on the rate of nest depredation are not
obvious with grassland studies showing both
positive and negative effects (Lahti 2001).
Fragmentation from linear features is considered
to be a threat to Sprague’s Pipit abundance and
demography (Environment Canada 2008); how¬
ever, the number of studies on this topic is limited
and the results are mixed. For example, Koperand
Schmiegelow (2006) found abundance of Spra¬
gue's Pipits was inversely correlated with distance
to cropland and to water, and Sutter et al. (2000
found Sprague's Pipits were significantly more
abundant along two-track trails than along roads
with adjacent ditches, fences, and non-name
vegetation. However, Koper et al. (2009) reported
abundance of Sprague’s Pipits in Alberta vvas
not influenced by distance to roads. We analysed
the effect of the distance to the nearest road
(secondary paved road and tertiary dirt roads or
trails), agriculture field, an active railroad rig.hr-
of-way, and a lake shoreline on nest survivorship
ot Sprague’s Pipits. We hypothesized there should
be an inverse relationship between distance Iron'
linear anthropogenic and natural features, and
daily nest survival rates (DSR); however, we only
310
Jones and White * NEST SURVIVAL OF SPRAGUE'S PIPIT
311
TABLE 1. Mean distance (m) from Sprague Pipits nests to linear anthropogenic and natural features at Bowdoin
National Wildlife Refuge, Montana, USA.
Fealure
Mean
Range
Primary road
Secondary’ roads
Agriculture field
Railroad rights-of-way
Shoreline
313.6
62.1-654.1
201.7
14.5-503.5
251.3
69.1-401.8
357.4
242.9-569.8
387.5
28.6-805.2
158.64
40
124.43
125
94.91
32
102.70
17
175.10
125
addressed the effect on DSR of the distance from
the nest to the habitat edges created by the linear
features.
METHODS
Study Area.— This study was conducted during
1997-2007 at Bowdoin National Wildlife Refuge
iNWR) in Phillips County, near the town of Malta
in north-central Montana. USA (48 24’ N. 107
39’ W; - 750 m asl). The study area consisted of
five permanent sites (26-59 ha) totaling 218 ha
largely consisting of native mixed-grass prairie
with flat to gently rolling terrain. The climate was
continental and semiarid, and characterized by
strong winds and high evaporation rates. The plant
community was dominated by western wheatgrass
( Puscopyruin smithii). needle-and-thread (Hesper-
usttpa comma), blue grama ( Boutehua gracilis),
and spikemoss (Selaginella densa). Low shrubs
(Sarcohalus vermiculatus, Artemisia catui, Cer-
atoides lanaia) were widespread but sparse and
trees were largely absent (Jones et al. 2010).
Nest Searching. — Sites were searched for nests
^-5 times per week from 10 May through - 15
August in all years in an attempt to locate all
active nests. Search techniques were primarily
rope dragging (Davis 2003. Jones et al. 2010), but
also included behavioral observations (Martin
and Geupel 1993) and opportunistic fool flushes;
details of the nest-searching techniques are
reported in Jones et al. (2010). Nesting outcomes
were: (I) successfully fledged at least one young
°i the parental species, (2) depredated or aban¬
doned (j.e., eggs or nestlings left permanently
unattended), or (3) unknown. Observations of
fledglings in the natal territory within 3 days ot
expected fledging, presence ol leces and leather
scales in the nest, fledglings near the nest, and
adults uttering alarm calls nearby or feeding new
fledglings within 50 m of the nest were evidence
of reproductive success. Predation was assumed
when eggs or nestlings too young to fledge
disappeared from the nest or the nest was
destroyed.
The locations of all Sprague's Pipit nests ( n =
125) were mapped. We used Arclnfo/GIS (ESRI
2007) to map the non-grassland features of
interest in and around Bowdoin NWR: (1)
secondary road. (2) tertiary roads and trails, (3)
agriculture field. (4) active railroad rights-of-way.
and (5) the shoreline of Lake Bowdoin. We used
Arclnfo/GIS (ESRI 2007) to measure the shortest
distance from each nest to each ot these attributes.
The secondary paved toad was a small, raised-bed
two-lane farm road with low to moderate traliic
volume. The vegetation along the side ot this road
included u higher density of trees and shrubs than
present in the surrounding grasslands. Also, along
this road were ditches with moving water, fences,
and rural farm development. The tertiary dirt
roads or trails were administrative maintenance
roads with dikes and low ditches on each side, and
u public birding trail with a low volume of
seasonal traffic. Ditches associated with roads and
the railroad rights-of-way held water for an
extended period, resulting in taller and denser
vegetation than the adjacent native prairie. Exotic
vegetation was more prevalent immediately
adjacent to the secondary toad, mainly brome
(li minus spp. ) and thistle ( Cirsium spp.). The
railroad rights-of-way included a built-up rocky
bed and exotic vegetation moving out from the
tracks. The agriculture field was fenced and
irrigated. The shoreline of Lake Bowdoin was
an alkaline salt flat of crusted mud with little or no
vegetation. The secondary road, agriculture field,
and railroad rights-of-way were adjacent to one
site; the tertiary roads and trails and shoreline of
Lake Bowdoin were adjacent to all five sites
(Table 1).
Data Analysis. — We estimated the relationship
of roads and other edges on Sprague's Pipits DSR
using the nest survival program in Program
MARK (White and Burnham 1999, Dinsmore
312
THE WILSON JOURNAL OF ORNITHOLOGY • Vo/. 124. No. 2. June 2012
TABLE 2. Models exploring the relationship between daily survival rate (DSR) of Sprague's Pipil and distance to hahitat
edges at Bowdoin National Wildlife Refuge. Montana using Akaike's Information Criterion, corrected for small sample sizes
(A 1C, .). AAIC, l A1C, model / - AIC, minimum), Akaike weight (w,|. and the number of parameters (k) are included for each
model (*S = DSR; 7 = date of nest on initiation; Age = age of nest; ORIENT = direction of nest opening). Minimum
distances to roads and edges are the potential thresholds beyond which there is no effect of the road or edge
Model
AICr
AAIC,
H’,
Model likelihood
k
Dcvuttt
{5(7 + Age + Clutch Size)}
496.97
0
0.119
1
4
488.95
1 S(T+ Age)}
497.47
0,50
0.093
0.78
3
491.45
fS "°”s °
ORIF.NT - the direction the nest opening was
facing. We used the minimum of the distances to
roads and edges as the predictive variable, and
included a threshold lo examine if there was an
effect within 50, 100. 200, or 300 in. We ran the
model separately for each distance threshold and
compared all possible models including or
excluding all variables. There may be an effect ot
distance on nest survival within some threshold-
hut we assumed there would be no effect on the in¬
dividual nest beyond this threshold. Thus, the
distance variable was used in the model up to the
threshold with all distances > threshold replaced
with the threshold value. These models exfttninci-
di Herein thresholds to assess effects immediate o
edges. We did not include any models with vi>
effects, because the sample size was smaJI wheo
partitioned into years. We also did not examine
models with interactions because of small sanipk
sizes. The likelihood of detecting spurious ellec v
increases with the number of models evaluated
f Burnham and Anderson 2002). particularly "i'll
small sample sizes as in this study.
RESULTS
The overall DSR (n = 125) was 0.95 ± W®5'
(SE) with a 95% confidence interval of 0.94-t' 9b
Jones and White • NEST SURVIVAL OF SPRAGUE'S PIPIT
313
FIG. I . Effect of nest age on nest daily survival rale of Sprague’s Pipit plotted tor early (days 1-25), mid (days 45-69),
and late (days 89-113) season nests with estimates taken from the top-ranked model [S(T + Age + C lutch Size)). The trend
(T) variable models the season effect, while clutch si/e was held at the mean of 4.6 eggs per nest. Data were collected at
Bowdoin National Wildlife Refuge, Montana. USA, 1997-2007.
The mean distances to Ihe linear anthropogenic
and natural features (Table I ) varied throughout
the study area. The minimum AIC(. model
(Table 2) included three non-distance variables
that were good predictors of DSR prior to
including the road and edge variables: T, age
(Fig. I), and clutch size (Fig. 2). The CONCEAL
and ORIENT covariates were considered, but did
FIG. 2. Effect of nest age on nest daily surv ival rate of Sprague’s Pipit plotted for clutches of 1 (minimum in this
study ), 4.6 (mean clutch size in this study), and 6 (maximum in this study) eggs with estimates from the top-ranked model
(A'(r + Age + Clutch Size)}. Season (trend 73 was taken at mid-season, days 45-69. Data were collected at Bowdoin
National Wildlife Refuge, Montana. USA, 1997-2007.
314
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 2. June 2012
TABLE 3. Regression coefficients on a logit scale for the minimum model exploring the relationship between daily
survival rate and distance to habitat edges for Sprague's Pipit at Bowdoin National Wildlife Refuge, Montana using
Akaike’s Information Criterion, corrected for small sample sizes. T = date of nest initiation. Age = age of nest.
MIN(Edges) = minimum distance to linear features.
(V-estimale
SB
Lower Cl
Upper a
{S[T + Age + Clutch Size + MINI Edges)])
Intercept 1 .62
0.95
-0.25
3.49
T
0.01
0.01
0.00
0.02
Age
-0.05
0.02
-0.09
-0.0 1
Clutch Size
0.32
0.18
-0.04
0.68
MINI Edges)
0.00
0.00
0.00
0.00
not improve the base model containing T. age. and
clutch size (Table 2). We considered different
distance variables to evaluate the effects of roads
and other edges, given our minimum AIC,. model
with T. age, and clutch size. A model with five
additional covariates lor the five distance catego¬
ries was considered, but was poorly supported
(Table 2). likely because of the excessive number
ol parameters allocated to the distance portion of
the model. We used the minimum ol' the distances
to roads (MINI Roads]) and the minimum of the
distances to any edge as predictive variables. We
also considered models with thresholds (within
50. 100, 200. or 300 m) on these minimum dis¬
tance variables; we would not expect the effect of
distance to edge to be important beyond these
threshold values. None of the distance models
improved the minimum AICc model with T, age
of nest, and clutch size (Table 2). There was no
support for variables with distance to any of the
edges, including to roads, having an effect on
DSR relative to the minimum AIC,. model that
contained three non-distance covariates (Table 3).
DISCUSSION
We observed no relationship between nest
survival and distance to roads, or to habitat
changes and edges at Bowdoin NWR. We
controlled (or time-specific factors including age
and date of clutch initiation (season) and found
these to be more important in explaining DSR
than distance to edges, similar to results in
Saskatchewan (Davis ct al. 2006), However, the
difference (AAIC,.; Table I ) between the best and
the worst models was small, suggesting that no
model explained a large portion of the variation
in nesting success. Nest depredation typically is
the primary cause of nest failure in grasslands
(Johnson and Temple 1990, Vickery et al. 1992.
Martin 1993, Davis 2003. Jones and Dieni 2007).
Some predators may use roads for hunting and
travel; however, the predator community in the
area studied is diverse and opportunistic (Jones
et al. 2010), and predation could occur indepen
dent of proximity of the nest to edges.
Differences among studies that have evaluated
an effect of distance to roads on nest survivorship
could reflect several confounding factors. Many
studies that have evaluated road effects have
focused on primary roads (Fahrig and Rytwinski
2009), which are characterized by greater vehic-
ular traffic, greater landscape alterations (e.g.,
buildings, suburban development), and othei
disturbances (e.g., oil, gas. wind energy develop¬
ment; Dale et al. 2009) that are not associated
with secondary and tertiary roads and trails
Higher disturbance levels on primary roads may
not he comparable to those in rural northern
mixed-grass prairies. Bowdoin NWR is crossed
by many diked vehicle roads and trails; however,
these roads generally have low and seasonal
traffic levels. Bowdoin NWR occurs within •'
landscape expanse of native mixed-grass praine
Grasslands in this region are characterized bv e
low proportion of edges and a high interior a/ea-
to-edge ratio, which may be the reason for the
lack of effects on nest survivorship in our stud;
Our work at Bowdoin NWR represents only
one point in both geography and time; however
there arc few studies on the effects of roads and
edges on Sprague's Pipits (Sutter el al. 30<"
Davis 2004. Koper and Schmiegelow 2006. Koper
et al. 2009). The response of Sprague's Pipits
may vary geographically, similar to area sensitivity
in other grassland birds (Johnson and Igl -200 1 1
Conservation of Sprague's Pipits may require
information on relative levels of the threats to thei'
populations throughout their range. Combining data
Jones and While • NEST SURVIVAL OF SPRAGUE'S PIPIT
315
from diverse locations should present a more
complete picture of the natural history and habitat
requirements of this unique grassland species.
ACKNOWLEDGMENTS
This project was funded by the U.S. Fish and Wildlife
Service. Nongame Migratory Bird Program. Region 6. M. J.
Aitmann measured and mapped the nest data using GIS. J.
S. [>ieni. V D. Niemuth, S. K. Davis. L. D. Igl, and two
anonymous reviewers provided helpful comments on earlier
versions of this manuscript. Mention of trade or product
names does not indicate endorsement; the findings and
conclusions in this article are those of the authorls) and do
not necessarily represent the views of the U.S. Fish and
Wildlife Service.
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The Wilson Journal of Ornithology 124(2):3 16-320, 2012
POPULATION DENSITY OF THE HELMETED CURASSOW
0 PAUXI PAUXI) IN TAMA NATIONAL PARK, COLOMBIA
VICTOR SETINA,14 DIEGO J. LIZCANO.1 DANIEL M. BROOKS.2 AND
LUIS fAbio SILVEIRA'
ABSTRACT. — We estimated the population density of the Helmeted Curassow ( Pauxi panxi ) in Tama National Park
(TNP) Colombia, using visual counts between December 2006 and December 2008. We used six line transects (1 km each)
equitably distributed in a natural forest between 800 and 1 .200 m asl in the southern part of the park. The sampling effort was
588 hrs with a total distance of 490 km. a detection rate of 0.06 record s/hr, and an encounter rate of 0.08 indivtduals/km.
Only solitary individuals were recorded (n = 40); the estimated density was 4,8 individuals/km*. Most detections occuned in
the lower strata of the forest (floor and sub-canopy) where hunters take advantage of curassows in the lower strata for
successful harvest. The southern sector of TNP becomes important in the dry season. Our study suggests a large population is
in TNP . but harvesting activities including removal of eggs, chicks, and juveniles, and hunting adults are affecting the
reproductive rate and population of the species. Received 6 June 2011. Accepted 2 February 2012.
The Helmeted Curassow (Pauxi pauxi) occurs
in Venezuela and Colombia. Its distribution in
Colombia is discontinuous in the Perija Mountain
Range and the Cordillera Oriental. It inhabits
dense rainforest and montane cloud forest at
altitudes from 500 to 2,800 m asl (Naveda-
Rodriguez and Strahl 2006), but is most com¬
monly seen within the cloud forest between 1.000
and 1,500 m asl (Hilty and Brown 1986). It has
been subjected to loss of habitat and hunting
pressure (Silva and Strahl 1997a. b). The latter
has a negative effect on populations due to low
density and slow intrinsic rate of reproduction
(Silva and Strahl 1 991, Renjifo et al. 2002. Brooks
and Fuller 2006). The Helmeted Curassow usually
avoids human presence in hunted areas (Silva
1999), making visual counts complicated and
requiring intense sampling effort to obtain reliable
data. The density of this species may also depend
on social behavior, along with availability and
quality of habitat (Buckland el al. 1993). The
population has been estimated at 1,000-2,499
individuals and globally is classified as Endan¬
gered (Naveda-Rodriguez and Strahl 2006. Bird-
Life International 201 lb). The objectives of our
research were to estimate: (1) the density of
Helmeted Curassows in the southern sector of
1 Laboratorio de Eculogfa y Biugeografia. Univcrsidad de
Pamplona, Facultad de Ciencias Basicas. Universidad de
Pamplona. Pamplona, None de Santander, Colombia.
2 Housion Museum of Natural Science. Department of
Vertebrate Zoology. 5555 Hermann Park Drive, Houston
TX 77030, USA.
Sefao de Aves, Musen de Zonlogia da Univcrsidade de
Sao Paulo. Caixa Postal 1 1461 . CEP 05422-970, Sao Paulo
Brazil.
Corresponding author; e-mail: vsetina@gmail.com
Tama National Park, and (2) the population size iri
a forest between 800 and 1 ,200 m asl.
METHODS
Study Area. — This study was conducted in
Tatna National Park (TNP) (07 27' N, 72 28'
W) al the northern lip of the Cordillera Oriental in
the jurisdiction of Herran and Toledo municipal¬
ities. Norte de Santander, Colombia (Fig. I). The
Park contains 48.000 ha of protected area and
is connected to a park of the same name in
Venezuela, which together comprise the Tama
massif in the Tama Binational Park (UAESPNN
2008). I NP has different climates due to altitu¬
dinal variation, ranging between 350 and 3.500 m
asl. This area is considered an Important Bird
Area (IB A# CO 189) by Bird Life International
(2011a).
Surveys were conducted in an area of 1.000 ha.
covering ~12% of the 8.640 ha of the Helmeted
Curassow distribution within TNP (UAESPNN
2008). This area is characterized by mature forest
with altitudes ranging from 800 to 1.400 m asl
with annual rainfall of 863 mm and a rainy season
from April to September.
Field Work. — We used a line-transect method
(Buckland et al. 1993) with two visual obseners
and repeated surveys along six line transects of
I km each, evenly distributed in the study area
Transects were sampled between 0400 and 08CX
hrs EST in one direction, and in the reverse
direction between 1400 and 1800 hrs at an
average speed of I ktn/1.2 hrs (70 min) surveyed
at the rate of one transect/day. Survey population
censuses were conducted during 2007-2008.
except for May, June, and September 2007 and
316
Selina el al. • HELMETED CURASSOW DENSITY
317
FIG. 1. Geographic distribution of Helmeted Curassows.
May, September, and October 2008 for total of
245 days in the 17 months sampled.
Data were collected upon each visual contact
with a curassow. The perpendicular distance from
the bird to the nearest point of the transect was
measured with a standard metal tape; the meeting
point with the bird was estimated when the
observation was not directly perpendicular and
walked to measure the perpendicular distance to
the nearest point of the transect. Other data
recorded included time of the encounter, number
of individuals observed, and the forest stratum in
which the bird was observed (floor, understory
6-20 m, or canopy > 20 m).
Data were analyzed using Distance 5.0 (Thom¬
as et al. 2006). Density estimates and resulting
population estimates were obtained by selecting
the best detection curve model based on Akaike
Information Criterion (A1C). which is based on
the Kullback-Lcibcr model (Akaike 1981).
Line transects
FIG. 2. Number of individual Hcmeted Curassows
detected in each transect in Tama National Park. Colombia.
FIG. 3. Pattern of detections of Helmeted Curassows in
morning and afternoon in Tama National Park, Colombia.
318
THE WILSON JOURNAL OF ORNITHOLOGY • Vul 124. No. 2. June 2012
35
FIG. 4. Number of individual Hclmeted Curassows
detected in different strata of the forest in Tamd National
Park, Colombia.
RESULTS
Forty visual records of Helmeted Curassow
were obtained during 2 years along 490 km of
line transect surveys with a sampling effort of
588 hrs, a detection rate of 0.06 records/hr, and
an encounter rate of 0.08 individuals/km. Only
single birds were observed. Birds were seen in
all transects except L 6. at perpendicular
distances ranging from 1.2 to 30 m. More
contacts were made on transects L I and L. 3
(Fig. 2). No individuals were recorded by
sound: 52.5% of the detections were obtained
in the morning, and 47.5% during the afternoon
(Fig. 3). Thirty-two individuals were observed
on the ground during the census, seven were in
the subcanopy, and one was observed in the
canopy (Fig. 4).
We obtained a density of 4.8 individuals/km2;
the model Half-normal cosine adjustments order ~>
was the lowest Akaike Information Criterion
(Table 1) with an effective band width (ESW) of
7.988 m (Table 2). We truncated detections
>14 m perpendicular to the transects to obtain
an adequate detection curve (Fig. 5)
DISCUSSION
This study is the first to documenl the
distribution of Helmeted Curassows in Colom¬
bia. Reports on the population density ol
Helmeted Curassow in Venezuela range from ]
to 8 individuals/km2 (Silva and Strahl 1191
Our study reports a density of 4.8 individual
knr, the first for TNP. and is in the range m
densities estimated for the species. However
there were differences within the methodologies
used, scale of sampling, and type of analyses,
which can affect density estimates (Strati' and
Silva 1997)
Franco-Maya and Alvarez (2002) estimated a
population of Helmeted Curassows between .-,850
and 15,400 individuals in Colombia, based on a
potential area of 1,925 km2 and an estimated
population of 2-8 individuals/km2 reported by
Silva and Strahl (1991). If the potential habitat
of the species is occupied and has the density
reported in our study, the population would be
9,240 individuals in Colombia, indicating here
may be an important population in TNP Tie
number of individuals may be lower considering
30% of the habitat is estimated to have been lost
due to agricultural expansion in the Andes 3nd
hunting pressure in TNP (Franco-Maya and
Alvarez 2002). Additional work is needed to
assess the current potential distribution in Colom¬
bia. as well as information about the subspecies
Pauxi p. gilliardi in the Serrania del Perija n
identify the current status of populations in
Colombia.
There is no clear information on habitat use and
behavior of the Helmeted Curassow. Visual
detections obtained in our study indicate roc**
individuals were in the lower strata of the loro1
(floor and sub-canopy); hunters take advantage1 1
curassows using the lower strata to harve-
individuals (Setina et al. 2010). Poaching
common in the dry season as well as haru--: -
TABLE 1 Detection models for Helmeted Curassows in Tama Na
Model I
National Park. Colombia.
Model 2 Model 3
Value likelihood (Ln)
Akaike Information Criterion
(AIC)
-91.379085
-90.889244
187.07147
186.75816
187.77849
Selina el al • HELMETED CURASSOW DENSITY
319
TABLE 2. Effective band widths of transects used to
detect Helmeted Curassows in Tama National
Park. Colombia.
Model Estimate %CV 95% Confidence interval
Half-normal cosine Adjustments order 2
AIC 186.75816
ESW(m) 7.988 30.07 4.398-14.508
Density 4.8 41.40 2.11-1 1.56 ind/knr
eggs, chicks, and juveniles from TNP (Franco-
Mava and Alvarez 2002, Selina et al. 2008).
The Helmeted Curassow is considered rare and
locating individuals requires a large sampling
effort in sub-Andean forest. The sub-Andean
topography varies and is challenging to traverse:
it can be difficult to encounter curassows along
established transects. One of the six transects ( 1. 6)
had no visual records. Curassows likely avoided
this transect because it was along the forest edge
near human settlements. Observations on other
transects occurred during the dry season and were
inside the forest. The study area borders a stretch
of the Margua River, which is an important
resource for humans and wildlife during the low-
water season. Studies of phenology, food avail¬
ability, and additional surveys are needed in other
areas to identify important areas for Helmeted
Curassows.
The TNP administration should consider
strengthening their educational programs and
initiating a process of learning about conservation
biology with residents of the buffer zones of the
park. Our study suggests there may be an
important population of Helmeted Curassows in
TNP. but activities such as egg extraction and
poaching may he affecting the reproductive rate
and consequent population stability of Ihe species.
It is also necessary to strengthen inter-institutional
agreements between the administration of TNP
and academic institutions to generate knowledge
of the species to improve conservation efforts.
ACKNOWLEDGMENTS
We thank the Cleveland Zoo, Conservation International.
Omacha Foundation. University of Pamplona, Tama
National Park, and the administrative unit of the Natural
Parks for financial support. Bird Exchange and IdeaWild
donated equipment for field work. We are grateful to the
staff of TNP. especially Cesar Leal and Henry Meneses.
Dan Brooks and Victor Setina are research associates of the
1UCN/SSC Cracid Specialist Group (CSG). and acknowl¬
edge the scientific and technical support of this group. L. F.
Silveira was supported by FAPESP and CNPq, and is an
Associate Researcher of ihe World Pheasant Association
(UK). We thank Saul Hernandez for being our field guide
and Erika Guerrero for his support during manuscript
preparation. We appreciate the comments of Ross MacLeod
and Clait Braun, which helped improve the quality of this
manuscript.
LITERATURE CITED
Akaike. H. 1981. Likelihood of a model and information
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BirdLife International. 2011a. Important bird areas
factsheet: Parque Nacional Natural Tama. Cambridge,
United Kingdom, http://www.birdlife.org
2 4 6 8 10 12 14
Perpendicular distance (m)
FIG. 5. Detection probability curve of Helmeted Curassows in Tama National Park, Colombia using DISTANCE 5.0.
320
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 2. June 2012
BirdLife International. 2011b. Species factsheet: Pauxi
pauxi. Cambridge. United Kingdom. http://www.
birdlilc.org
BR(«iks. D. M. and R. A. Fullfr. 2006. Biology and
conservation of cracids. Pages 9-2! in Conserving
cracids: the most threatened family of birds in the
Americas (D. M. Brooks, Editor). Number 6. Miscel¬
laneous Publications of the Houston Museum of
Natural Science. Houston. Texas. USA.
Buckland, S. T.. D. R. Anderson. K. P. Blrnham. and
J. L. Laake. 1993. Distance sampling. Estimating
abundance of biological populations. Chapman and
Hall. London. United Kingdom.
Franco. A. M. and M. Alvarez. 2002. Pauxi pauxi. Pages
131-134 in Libra rojo de aves de Colombia (L. M.
Renjifo, A. M. Franco-Maya. .1. D. Atnaya-Espinel.
C. II. Kattan. and B. Lopez-Lamis, Editors). Serie
Libros Rojos de Especies Amenazadas de Colombia.
Institute dc InvesLigaeidn de Recursos Bioldgicos
Alexander von Humboldt y Ministerio del Medio
Ambiente. Bogota. Colombia.
Hilty. S. L. AND W. L. brown. 1986. A guide to the birds
ot Colombia. Princeton University Press, Princeton.
New Jersey, USA.
Na veda- Rodriguez, A. and S, D. Straw.. 2006. Helmet
ed Curassow ( Pauxi pauxi). Pages 56-58 In Conserv¬
ing cracids: the most threatened family of birds in the
Americas (D. M. Brooks. Editor), Number 6. Miscel¬
laneous Publications of the Houston Museum of
Natural Science, Houston, Texas, USA.
Renjifo. l. M . A. M. Franco-Maya. .1. D. Amaya-
Espinfl. G. H. Kattan. and B. Lopez- Lancs, 2002,
Libro rojo de las aves de Colombia, Instituto de
Invcstigacion de Recursos Bioldgicos Alexander von
Humboldt y Ministerio del Medio Ambiente. Bogota
Colombia.
SEI"^-D- ' v «®c. a. suakk.
-008. Percepctones y attitudes hacia el Paujil Copcte
de Ptedra (Pauxi pauxi) y la Pava negra (Aburria
ahum) en el Parquc National Natural Tamil. Colom¬
bia. Bolen n de la UICN/Birdlife/WPA Grupo de
Especialistas en Cracidos 25:23-32.
Setina. V.. M. Morales. D. J. Lizcano. and D. M. Brooks
2010. Registros de caceria del Paujil Copcte de Piah
( Pauxi pauxi) en el extremo None de la Cumilln
Oriental de los Andes. Colombia. Boletin de la Il l'V
Birdlife/WPA Grupo de Especialistas en Cnkidt-
Silva. J. L. 1999. Notes about the distribution of Asm
pauxi and Aburria aburri in Venezuela. 'Si
Bulletin 111:564-569.
Silva, J. L. AND S. D. SlKAHL. 1991. Human irupac
populations of chachalacas. guans and cui>
(Gallifomics: Cracidae) in Venezuela, Pages
in Neotropical wildlife use and conservation iJ. G
Robinson and K. H. Redford, Editors). L'niversu;-
Chicago Press. Chicago, Illinois, USA.
Silva, J. I. and S. D. Stkahl. 1997a. Condict6n actual jeh
poblaciones de Cracidos en ocha localtdaJcs en Ye
zuela. Pages 396-397 in The Cracidae: their biof .
conservation (S. D. Strahl, $. Beaujon. D. M. Brwk '
J. Bcgazo. G. Sedaghatkish. and F, Oltnos. Ediav
Hancock House Publishing, Blaine, Washington, ISA
Sil va. J. L. and S. D. Strahl. 1997b. Presion de eat;'
sobre poblaciones de cracidos en los parquc- nxio-
nales al norte de Venezuela- Pages 437—448 c T N
Cracidae: their biology and conservation (S. 0. Snahl.
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Sedaghatkish. and F. Olmos. Editors). Hancock Hou r
Publishing, Blaine. Washington. USA.
Straw.. S. D. and J. L. SILVA. 1997. Census methods lor
eracid populations. Pages 26-33 in The Cracidae, did
biology and conservation (S. D. Strahl, S Beat;®,
D. M. Brooks. A. J. Begazo. G. Sedaghatkish. uno f
Olmos. Editors). Hancock House Publishing, Blaine
Washington. USA.
Thomas, L.. j. l. Laake, S. Strindberg. F. L
M arques, S. T. Buckland, D. L. Burghers. D. R
Anderson, K. P. Burnham. S. L. Heoley. J. H
Pollard. J. R. B. Bishop, and T. A. Marqies. 2006
DISTANCE 5.1. Research Unit for Wildlife Popula¬
tion Assessment, St. Andrews. United Kingdom
UAESPNN. 2008. Plan de Manejo Parque Naciooal Naiura-
Tama. Ministerio de Ambiente. Vivienda y Desam)
Territorial. Bogota. Colombia.
The Wilson Journal of Ornithology 1 24(2):32 1 — 327, 2012
THE RED-BILLED CURASSOW (CRAX BLUMENBA CHIP) : SOCIAL
ORGANIZATION, AND DAILY ACTIVITY PATTERNS
ANA CAROLINA SRBEK- ARAUJO,1" LUIS FABIO SILVEIRA.15 AND A. G. CHIARELLO4
ABSTRACT— We studied the Red-billed Currasow ( Crux blumenbachii) in Vale Natural Reserve, Linhares, Espirito
Santo State. Brazil, using camera traps. We found the Red-billed Curassow present in the entire area of the reserve
- 22.000 ha) during 40 months of camera trapping (2005-2008). Most records were of single individuals, especially
males, but pairs and even groups of individuals were also recorded. Males were paired with one and two females,
suggesting polygyny in the species. The species was recorded throughout the day with one peak from 0500 to 0600 hrs and
another after 1600 hrs. The daily activity pattern was similar for males and females. The number and w idespread nature of
the records suggests the local population of this species may be higher than previously thought. Received 10 March 201 1.
Accepted 5 December 2011.
The Red-billed Curassow (Cm. x blumenbachii)
is endemic to the Brazilian Atlantic Forest and
originally occurred in lowland forests from
southern Bahia (Iiubera) to Rio de Janeiro and
eastern Minas Gerais states (Hellmayr and Con¬
over 1942, Delacour and Amadou 1973. Sick
1997. IB AM A and Ministerio do Meio Ambiente
2004). This curassow has disappeared from much
ot its original range and is now considered extinct
in Minas Gerais and Rio de Janeiro, where indi¬
viduals were Iasi seen in 1963 near Sao Fidclis:
there are no recent records for native populations
in Minas Gerais (Sick 1969. IBAMA and
Ministerio do Meio Ambiente 2004). However,
reintroduction programs are ongoing in both those
states (Bernardo et al. 201 1).
Recent reports of this curassow are only from
southern Bahia (Una Biological Reserve, Desco-
brimento National Park, ltubera) and northern
Espirito Santo (Vale Nature Reserve. Sooretama
Biological Reserve) (IBAMA and Ministerio do
Meio Ambiente 2004). Current estimates place the
total numbers at 250 individuals, which makes
this species one of the most threatened in the
Neotropics (IBAMA and Ministerio do Meio
Programa de Pos-gntduufao cm Ecologiu. Couscrvayao
v Manejode Vida Silvcslre, Universidadc Federal dc Minas
Gemis-Avenida Antonio Carlos, n 6627. Pumpulha, CEP
9270-yoi, Belo Horizonte. Minas Gerais, Brazil.
Vale S.A./Rcservy Natural Valc-Caixa Postal n 91.
Centro. CEP 29900-970. Linhares. Espirito Santo, Brazil.
Museu de Zoologia, Universidadc de Sao Paulo-Caixa
Postal 11461. CEP 05422-970. Sao Paulo, Brazil.
J Departamento de Biologia. Fuculdade de Eilosofta,
Ciencias e Letras de Rikdrao Preto. Cniversidade de Sao
Paulo- Avenida dos Batidcirantcs. n 3900. CEP 14040-901,
Ribcirao Preto, Sao Paulo. Brazil.
'Corresponding author, e-mail: lfsilvei@usp.br
Ambiente 2004. IUCN 2009). The Red-billed
Curassow is considered endangered both nationally
and internationally (Silveira 2005, IUCN 2009); it
is critically endangered in the states of Espirito
Santo (Sitnon et al. 2007) and Minas Gerais
(Funda^ao Biodiversitas 2007), and is probably
extinct in Rio dc Janeiro (Alves et al. 2000).
Habitat loss in the Atlantic Forest and hunting
are considered ihe most important factors con¬
tributing to the decline of the Red-billed Curas¬
sow (IBAMA and Ministerio do Meio Ambiente
2004. IUCN 2009). Habitat loss occurs in a
variety of ways, all of which contribute to the
declines, including the increasing incidence of
forest fire (IBAMA and Ministerio do Meio
Ambiente 2004, IUCN 2009). Hunting was first
noted many years ago (Wied 1821. 1940) and
later when the bird was in imminent danger of
extinction (Hellmayr and Conover 1942).
The lack of information about the general
biology of the Red-billed Curassow is alarming
considering the gravity of the situation. The few
reports of its natural history are anecdotal (and
often conflicting), rather than based on scientific
observations (Wied 1821; H. Sick. pers. comm, in
Delacour and Aniadon 1973).
The objective of our paper is to report natural
history data for this species obtained during a 3-year
study using camera traps m Vale Nature Reserve
(Linhares City). This reserve, together with the
adjacent Reserva Bioldgica de Sooretama (Soor¬
etama City), represents the largest area for survival
of Red-billed Curassows in Espirito Santo State.
METHODS
Study Area. — We studied the Red-billed Curas¬
sow' in the Vale Nature Reserve (VNR-Reserva
Natural Vale). 30 km north of Doce River in the
321
322
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 2. June 2012
Legend:
Status of Sample Points
© Year 1 , Absence
• Year 1, Presence
A Year 2, Absence
A Year 2, Presence
0 Year 3, Absence
■ Year 3. Presence
L _ Atlantic Forest Biorrm
Road Network
. Internal Road s and Trails
——Main Roads
Hydrographic Network
— Streams
^HWater Bodies
FIG. I. Vale Natural Reserve showing trapping locations sampled for Red-billed Curassows during the first year
(circles), second year (triangles), and third year (squares). Filled symbols indicate where curassows were photographed
empty symbols = where they were not,
State of Espi'rito Santo ( I 9 06'- 19 18'S,39 45’-
40 19' W) (Fig. 1), This reserve (— 22.000 ha)
includes about 5 % of the remaining forest in the
state (Funda?ao SOS Mata Atlantica and IN PE
2005) and is adjacent to the Sooretama Biological
Reserve, which includes another 24,250 ha. The
combined reserves comprise one relatively large
block ot native vegetation and. together, are one of
the most important forest fragments in the state and
one of the largest protected areas of Atlantic Forest
north ol Rio de Janeiro State. The reserves are
within the central corridor of the Atlantic Forest,
which is considered one of the most important
areas lor Atlantic Forest conservation in Brazil
(Ministerio do Meio Ambiente et al. 2000) and a
part of the Discovery Coast World Heritage Site,
defined by UNESCO in 1999.
Vale Nature Reserve is relatively flat wi
elevation ranging from 28 to 65 m above sea lev
and is notable for its Tabulciro forests (lowlar
forest on Hat terrain) (Jesus and Rolim 2005). T1
chmate is tropical, hot and humid with a rail
season from October to March and a dry seasc
2005)eThAPnl anJ September (Jesus and Rolii
e average annual temperature is 23.3
with an average annual range of 14.8-34.2 <
Average annual rainfall is 1.202 mm with high
variation (Jesus and Rolim 2005).
The reserve is in technically dense rainionS
( 1BGE 1 993) or perennial seasonal forest accordi -
to other authors (Jesus and Rolim 2005). The
is an intermediate stage between the former aid
semi-deciduous seasonal forest. In addition
Tabuleiro forests and occasional open he-’-
(Native), a local vegetation type (Mussununsu
forest in sandy soils) is also present. Surrounds
the reserve are mostly pastures and crops. ■
daily for cultivation of fruit (Jesus and R-
2005) and Eucalyptus.
Data Collection. — Camera traps were in 7 -
from June 2005 to October 2008. Cam Ti*^
(Forestry Suppliers Inc., Jackson. MS. OS A l *
used during the first year and was
association with Tigrinus Cameras (Tignnus R-
search Equipment, Timbo. Santa Catarina. Bn
in the second year: only Tigrinus Camera’'1''1 '
used in the third year. Both brands used
cameras loaded with 36 exposures of 400
01m. Camera traps were operational 24 hrs/da}
were adjusted to trigger at minimum intern '
Srbek-Araujo et al. • RED-BILLED CURASSOW BEHAVIOR
323
20 sec to take multiple photos of the same animal or
groups of animals. Cameras were checked and
maintained even- 30 days. Camera traps were
attached to trees >15 cm DBH. 45 cm above the
ground No bait w as used.
Camera traps w'erc placed along unpaved roads
in the reserve during the first year. These roads
were 4 m wide and used solely by internal stall
and researchers. Three areas were sampled with
10 trapping stations each: north, south, and west
totaling 30 trap stations. Every trapping station
included a pair of cameras, placed facing each
other, one on each side of the road. The minimum
distance between trapping stations was 2 km.
Ten trapping stations with pairs of camera traps
were placed during the second year inside the
forest 100-200 m from the nearest road to deter
theft. The camera pair was relocated to another
position within 200 m of the original location
if few photographs were taken after 30 days,
keeping the same original distance from the
nearest road. The minimum distance between
trapping stations was 4 km. The spatial design of
camera traps during the third year was similar to
that of the second year; however cameras were
placed at distances even farther from roads (500 m
from i he nearest road).
Data Analysis. — Photographs from camera
traps were considered records ( = captures). Only
die first photograph was considered as a record
when more than one photograph of the same
species was taken at the same trapping station
within a 1 -hr interval. The number of trapping
stations and sampling effort varied from year to
year, and we balanced comparisons using capture
success. Sampling effort (camera-days) was calcu¬
lated by multiplying the number of cameras (or pair
of cameras) by the number of sampling days
(24 hrs). Capture success was calculated by
dividing the number of records by the sampling
effort and expressing the result as a percentage
(Srbek-Araujo and Chiarello 2005).
We used Chi-square tests ty; ) lor comparisons,
corrected for bias when necessary (Yale's correc¬
tion: Zar 1996). Expected frequencies were
calculated respective to sampling effort in each
case when comparing the record frequency among
habitats (roads, edges, and forest interior). We
used only data from the first year to compare
number of captures among regions (north, south,
and west), when these regions were subjected to
similar sampling effort. Wet and dry- seasons were
contrasted using data from all 3 years and
TABLE 1. Number of records, sampling effort, and
capture success of Red-billed Curassows in the Vale
Natural Reserve. Brazil using camera traps from June
2005 to October 2008.
Season
Variables
Totals
Dry Wet
First Year
Number of records
83
62 21
Sampling effon (camera-days)
3.032
1.563 1.469
Capture success (%)
2.74
3.97 1.43
Second Year
Number of records
64
19 45
Sampling effort (camera-days)
3.468
1.998 1.470
Capture success (%)
1.85
0.95 3.06
Third Year
Number of records
50
31 19
Sampling effort (camera-days)
3.034
1.688 1.346
Capture success (%)
1.65
1.84 1.41
Totals
Number of records
197
112 85
Sampling effort (camera-days)
9.534
5.249 4.285
Capture success (%)
2.07
2.13 1.98
separately for each year. Captures were classified
into individual (either male or female), pair (male
and female) or group (2 or more individuals apart
from pairs). Males and females were distinguished
given the dimorphism in plumage. The capture
frequency of males, females, and associations
(pairs and groups) was compared for the entire
period and also yearly (3 X 3 contingency table).
We examined the time of the photographs to
define when captures were most frequent using
2 -hr intervals. The daily activity pattern was
contrasted between males and females using Chi-
square analysis with a 2 X 8 contingency table,
considering data from all 3 years. We used
Program BioEstat (Version 5.0) (http://www.
mamiraua.org.br/downloads/) for analyses.
RESULTS
We logged 9,534 camera trap-days and 197
records of Red-billed Curassows (Table 1 ). The
species was recorded throughout the reserve at 1 5
trap stations during the first year, nine during the
second year, and eight during the last year
(Fig. 1 ); 18 (36%) of the 50 trap stations did not
capture this species. Most records during the first
year were from the north region (n = 51 ),
followed by the south (n = 21). and w-est (n =
1 1) (x2 = 33.0. df = 2. P < 0.005).
324
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 2. June 2012
80 -
70
Third year Total
■ Pair ■ Group
first secon/r:!^ °' ^ shnw‘ng males’ ,ema*es- pairs, and groups of Red-billed Curassows obtained during the
first, second, and third year of the study in Vale Natural Reserve, Brazil.
The overall capture frequency was si milt
between wet and dry seasons (y2 = ().25, df = |
P > 0.5) (Table 1). However, analyzing each yea
separately, records were more frequent during th
dry season in the first year (y: ~ \ 7.8, df = 1 p <
0.005). and during the wet season of the secom
year (y- = 20.4. df = 1. P < 0.005); the captun
frequency was similar between seasons in the thin
year (r = 0.82, df= 1, P > 0.1; Table I ).
Smgle individuals were captured more ofter
(85%. n = 167) than either pairs or groups (15%
" ~ 30)- Males were commonly capturec
(57 7c, n - 112), followed by females (28%, n =
55), pairs (8%. n = 16), and groups (7%. n — 14
Fig- 2). The proportions of males, females, and
associations (pairs and groups) differed (y- =
53.8. df = 2, P < 0.005) and varied from year to
year (*- - 10.9, dl = 4. P < 0.05), Individual
males were captured more often than expected in
the first and third years while individual females
were captured more than expected in the second
year. Croups were captured more than expected in
tne tirst and second years.
Six of the 14 recorded groups were of two
females, four were Iwo males, two were a male and
two females otte was three females, and one was
four females (two adults and two young). Captures
ot a male and two remales were obtained in
ovem ei (tirst year) and in June (third year). The
HrZ , TT SeX individuals ««« captured
Red-billed Curassows were captured over a lb-
hr interval with the first record at 0523 hrs and the
last at 1812 hrs (Fig. 3). Captures had a binuxiai
distribution; the first peak occurred soon after
0600 hrs and the second after 1600 hrs (Fig. 3).
This bimodal distribution was similar amorrst
years. Males and females had similar daily
activity patterns (y2 = 5.5. df = 7, P > 0.5),
DISCUSSION
The cameras were useful to gather information
on aspects of the natural history of Red-billed
Curassows. The relatively large bode size (total
length ~ 90 cm. 3.5 kg) and mostly terrestnal
habit o! these birds were adequate to trigger the
infrared sensors of the camera traps.
Information about the natural history of the Re 1
billed C urassovv is often anecdotal. It is generally
considered monogamous (Sick 1997) although
polygyny has been observed in captive birds or
hunted populations, due to the female-biased v*
ratio resulting from instances where males are
more heavily hunted (Sick 1970). Single-^'
groups have also been seen during the
breeding period (Collar and Gonzaga 1988. Sick
1 997). However, this species has also been report
to be polygamous (Augusto Ruschi in Ddaco-
and Amadon 1973) while others (Sick 1970. 0-'U
and Gonzaga 1988) suggest they live in pairs or
family groups of up to four individuals.
Our data demonstrated the occurrence of a i 1
with two females in two independent record
suggesting polygyny. These findings air aho
supported by observations in Cupido and R<-’,uf 1
Sr bek- Araujo et al. • RED-BILLED CURASSQW BEHAVIOR
325
FIG 3. Overall record of frequency of Red-billed Curas sows by I -hr intervals obtained during 3 years of study in Vale
Natural Reserve. Brazil.
Farm (adjacent to Vale Natural Reserve and
Soorctama Biological Reserve) where single
males have been recorded with up to four females
i Gustavo Magnago, pers. comm.). However, use
of camera traps may underestimate polygyny in
this species. For example, if individuals are not
close to each other, it is possible for a group to
pass by the camera, but only the individuals
nearest to the one that triggers the camera are
captured. Thus, if camera recycling is in process,
the first individual is photographed and the
remaining members of the group are not necessary
captured on film.
We captured pairs from May to January. Pairs
may be seen together even when not breeding
• Wied 1821). and capturing pairs with cameras
does not imply that reproduction is occurring. The
breeding season is unknown at the Vale Natural
Reserve but capture of females with two young
females in July 2005 suggests the pattern is
similar to that elsewhere. The reproductive period
of Red-billed Curassows is poorly known and the
first nest was not discovered until 1979 near Vale
Natural Reserve (Teixeira and Snow 1982). An
egg was found fallen from a nest near Itubera,
Bahia, in December 2007 (Lima et al. 2008) and
young were seen in August and September
I Teixeira and Snow 1982). October (H. Sick,
pers. comm, in Delacour and Arnadon 1973). and
January (Scott and Brooke 1985).
Red Curassows were most active in the early
morning and less so during mid day. The late
afternoon activity peak suggests movement to
night roosts. Other mostly terrestrial cracids,
such as Crcix fasciolata, C. alector. Mini tomen-
tosa, and M. tuberosa (L. F. Silveira, pers. obs.),
follow a similar pattern. Our data also suggest
seasonal changes in Red-billed Curassow habitat use
in the Vale Natural Reserve. Red-billed Curassows
were recorded more during the dry season when
cameras were placed along roads (first year), and the
number of captures was higher in the wet season in
the forest interior (second and third years). These
movement patterns may indicate changes in habi¬
tat use as a reflection of the variation in resource
abundance throughout the year. The diet of Red¬
billed Curassows includes lleshy and sweet fruits or
hard seeds, leaves, invertebrates, and even small
vertebrates (Sick 1997, IB AM A and Ministerio do
Meio Ambiente 2004), most of which they find on
the forest floor; thus, it is likely that availability of
food resources varies seasonally. Foraging in the dry
season may be more profitable along roads due to
food resources (flowers, faiits. seeds) provided by
secondary vegetation along roads and the ease in
finding them in open areas.
The higher number of captures of Red-billed
Curassows in the northern area of the reserve may
be due to: larger concentration of streams, larger
area of Tabuleiro forest, and the proximity of
this region to the Sooretama Biological Reserve.
Another potential factor that cannot be discarded
is differential hunting pressure, as the south and
west regions apparently are more visited by
326
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 2. June 2012
poachers (proximity to municipal unpaved roads
and farms).
The population density of the Red-billed
Curassow is unknown and inferences about its
conservation status are difficult at best. Population
densities for other species of the genus have been
reported and recently reviewed by Setina (2009).
Density of forest species such as C. rubra
griscomi in Mexico varied between 0.91 and
1.02 birds/km2, while 4 birds/km2 were reported
for C rubra rubra in Guatemala. Species of
similar size as the Red-billed Curassow such as
Crax globulasa had densities of 3-4 birds/km2 in
Peru, while C. fascial ata was recorded as 4.66
birds/km- in Brazil (Desbiez and Bernardo 201 1 ).
Higher densities were recorded for C. alector ,
which had 8-14 birds/km2 in Venezuela (Silva
and Strahl 1991) and 7.2-9.5 birds/km2 in French
Guiana (Thioilay 1989). while C. daubentoni
varied from 8 to 161 birds/km2 in Venezuela
(Bertsch and Barreto 2008). If population den¬
sity is similar to that of C. globu/asa. one of the
Red-billed Curassow's closest relatives (Frank-
Hoeflich et al. 2007), the Vale Natural Reserve
(—185 km* of available habitat, considering forest
only) could support a population between 555 and
740 curassows. The number and widespread
records we documented suggests the local popu¬
lation of this species may be higher than
previously thought (Collar et al, 1992, IB AM A
and Ministerio do Meio Ambiente 2004). Addi¬
tional studies are required to properly estimate
population density, but Vale Natural Reserve
together with the neighboring Sooretama Biolog¬
ical Reserve is clearly important for conservation
of the Red-billed Curassow.
ACKNOWLEDGMENTS
We (hank Vale S.A./Instiluto Ambiental Vale for
financial support. A. G. Chiarello received financial support
from CNPq (301100/2005-5 and 303273/2008-9). L. F.
Silveira was supported by FAPESP and CNPq. and is an
Associate Researcher of the World Pheasant Association
(UK). We thank C. S. S. Bernardo. J. J. Roper, and two
anonymous reviewers for providing constructive criticism
ot the manuscript, and Gustavo Magnago for sharing
observations at Cupido and Refugio Farm. We thank H. .1.
Del-Duque Junior. E. R Coelho. B. A. Guerin, and J. C.
Simplicio for help with field activities. Andrd Hirsch kindly
provided the map.
LITERATURE CITED
Alves. M. A. S.. J. F. Pacheco, L. A. P. Gonzaga. R. B.
Cavalcanti. M. A. Raposo. C. Yamashita, N. C.
Maciel. and M. Castanheira. 2000. Aves. Page*
1 1 3- 1 24 in A Fauna Amea?ada de Extinyuo do Hstado
do Rio de Janeiro W N°rm“‘
Northwest Center for Medical Education Indiana
University School of Medicine, Gary. IN 46408. USA
Key Laboratory of Animal Ecology and Conservation
s? ^ a""=“ ■=
“U'"'TC ■zhang@tom.com.
considered here, and this study provides only j
first detailed description of the musculature of the
pelvic limb of the Chinese Grouse, as a basis tw
studies on its arboreal mode of life.
METHODS
Four adult individuals that died from predatioi
or during capture while attaching radio transmit¬
ters in Lianhuashan Natural Reserve of Gansu
Province, China, were collected and fixed in v
ethanol for dissections, which were perform^
under a stereomicroscope at 6X and 1-'
magnifications. The descriptions here include thv
location and nature (fleshy, tendinous) of the
origin and insertion, muscle shape, fiber archils
ture (e.g,. bipennate, unipennale), position, ai;
size relative to adjacent structures, and .m
additional details. Muscles were described
proximal to distal, from superficial to deep
layers, starting from a lateral view. Draw ing'
were made freehand. Nomenclature for '•
musculature and the various bony structures w
which Lhe muscles are attached follows thu'
Nomina Anatomica Avium (Baumel et al. F1-1
DESCRIPTION
M. iliotibialis cranialis (Fig. 1; IC) is the m1'
cranial superficial muscle in the thigh. Its one 11
mainly fleshy from the cranial half of the cri-
iliaca dorsalis. The Hat. strap-like belly Pa>'
downward, and merges into the ligaments
patellae which inserts on the crista patella^
the tibiotarsus.
M. iliotibialis lateralis (Fig. 1: IL) is the im'
extensive superficial muscle on the lateral flirty
°1 the thigh. The origin, arising from die doN
iliac crest and crista dorsolateralis ilii, is aP°K’
328
Zhang et al. • CHINESE GROUSE MYOLOGY
329
FIG. 1. Lateral view of the superficial muscles of the
thigh and shank of the Chinese Grouse. Abbreviations: AIF,
Ansa m. iliofibularis; FB. M. fibularis brevis: FCLP. M.
Ilexor cruris lateralis; FCM, M. Ilexor cruris medialis; FDL,
M flexor digitorum longus: FL, M fihulans longus;
I IW2. M. flexor perforans ct perforatus digiti II: FPPD3,
M flexor perforans et perforatus digiti III; GAL, Pars
hiteralis of M. gastrocnemius; GAM, Pars medialis of M.
gastrocnemius; 1C, M. iliotibialis cranialis; IF, M. iliofibu-
.ms IL. M. iliotibialis lateralis.
r°lic in the cranial two-thirds, and fleshy in the
caudal third. The thin, expansive, sheet-like belly
is closely attached to M. iliotibialis cranialis
cranially and to M. flexor cruris lateralis caudally,
concealing M. iliotrochantcriei, Mm. femorotibia-
lis externus and medius, M. iliofemoralis ex-
ternus, and the proximal two-thirds of M.
iliofibularis. There arc two distinct, large aponeu¬
rotic portions at the proximal and distal ends of
the belly. The insertion contributes, together with
M. iliotibialis cranialis and Mm. femorotibialis. to
Ihe formation of the patellar ligament.
M. iliofibularis (Figs. 1. 2, 4, 5: IF) is a large,
triangular muscle that arises mainly by fleshy
libers from nearly the entire dorsolateral crest of
the ilium, ventral to the overlying M. iliotibialis
lateralis. The belly passes down the back of the
thigh deep and caudal to M. iliotibialis lateralis.
FIG. 2. Lateral view of a second layer of muscles of the
thigh and shank of the Chinese Grouse. Abbreviations: AIF,
Ansa m. iliofibularis; CFC, M. caudofemoralis pars
caudalis; CFP. M. caudofemoralis pars pelvica: FB, M.
fibularis brevis; FCLA. Pars accessoria of M. flexor cruris
lateralis; FCLP. M. flexor cruris lateralis; FCM. M. flexor
cruris medialis: FDL. M. flexor digitorum longus; FPD4.
M. flexor perforans digiti IV; FPPD2. M. flexor perforans et
perforatus digiti II; FPPD3. M. flexor perforans et
perforatus digiti III; f-TE, M. femorotibialis externus; IF.
M. iliofibularis; IFF, M. iliofemoralis externus: ISF, M.
ischinfemoralis; ITCD, M. iliotrochantericus caudalis;
ITCR. M. iliotrochantericus cranialis; PTF. M. pubo-
ischio-femoralis; TC, M. tibialis cranialis.
and superficial to M. caudofemoralis, M. ischiofc-
moralis. and pars accessoria of M. flexor cruris
lateralis, finally tapering to a strong tendon behind
the knee. The tendon, together with the blood
vessels and nerves, passes through the ligamentous
ansa m. iliofibularis (Figs. 1.2,4: AIF) and inserts
on tuberculum m. iliofibularis on the fibula.
M. ambiens (Fig. 4: AM) is one of the most
medial muscles of the thigh and arises by a short
tendon front the tuberculum preacctabulare. The
narrow, spindle-shaped belly extends between M.
femorotibialis ntedius and M. iliotibialis cranialis,
and gives rise to a thin tendon above the knee. The
tendon passes diagonally through the patellar
ligament to the lateral side of the knee, and continues
downw ard deep to the tendon of M. iliofibularis. The
tendon gives origin to M. flexores perforati digiti 11,
III. and IV in the upper part of the crus.
M. iliotrochantericus caudalis (Fig. 2: ITCD)
lies deep to M. iliotibialis cranialis and M.
330
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 2. June 2012
FIG. 3. Lateral view of a third layer of muscles of the
ihigh of the Chinese Grouse. Abbreviations: CPC, M.
caudofemoralis pars caudalis: CFP. VI. caudofemorulis pars
pelvica; FCLA. Pars accessoria of M. flexor cruris lateralis:
FCLP, M. flexor cruris lateralis; FCM, M. flexor cruris
medialis; FTM, M. femorotibialis medius: ISF, M.
ischiofemondis; ITCR. M. iliotrochantericus cranialis;
ITM, M. iliotrochantericus medius; PIF, M. pubo-ischio-
femoralis.
iliotibialis lateralis, and originates by fleshy fibers
from the fossa iliaca dorsalis. The bulky belly
converges on a short, flat and wide tendon, which
inserts on the lateral surface of trochanter femoris.
M. iliotrochantericus cranialis (Figs. 2. 3;
ITCR) originates by tendinous and fleshy fibers
from the cranial two-thirds of the lateral crest of
the ilium. The insertion is by a wide, flat tendon
on the lateral surface of the proximal femur, distal
to the insertion of M. iliotrochantericus medius.
M. iliotrochantericus medius (Fig. 3; ITM) is
the weakest of die iliotrochanteric muscles. It
arises fleshy from the caudal third of the lateral
crest of the ilium and inserts by a thinner tendon
on the lateral side of the femur between the
insertions of M. iliotrochantericus caudalis and M.
iliotrochantericus cranialis.
M. iliofemoral is exlcrnus (Fig. 2: IFE) is a
small, flattened, triangular muscle, which arises
directly from (lie dorsal ridge of the ilium, cranial
and dorsal to the acetabulum. The belly is closely
attached to that ot M, iliotrochantericus caudalis
and terminates on a small tendon which attaches
on the caudoluteral aspect, between the tendons of
M. iliotrochantericus cranialis and M. iliotrochan-
tericus medius.
FIG. 4. Lateral (left) and medial (right) views of the
third layer of muscles of the shank of the Chinese Grouse.
Abbreviations: AIF. Ansa m. iliofibularis: AM. M.
ambiens; F,DL, M. extensor Jigitorutn longus: FB. M.
lihularis brevis; FDL, M. flexor digitorum longus; FPD3.
VI. flexor perloruns digiti III: FPD4. VI. flexor perforans
digiti IV; IF. M. iliofibularis; PLA. M. planlans; TC. M.
tibialis cranialis.
M. iliofemoralis internus is the smallest of ail
the thigh muscles and arises by fleshy fibers from
the lateral crest of the ilium, just medial to the
origin of M. iliotrochantericus medius. The thin,
band-like belly passes diagonally caudolaterally
to insert on the caudomedial side of the shaft of
the femur, proximal to M. femorotibialis internus.
M. femorotibialis externus (Fig. 2; FTE) lies
deep to M. iliotibialis cranialis and M. iliotibialis
lateralis, and is the largest of the three parts of this
complex and arises primarily by fleshy fibers
from the cranial and lateral surfaces of the
femoral shaft throughout nearly its entire length.
The belly is notched to accommodate the tendon
of insertion of M. iliotrochantericus cranialis at
the proximal end. and gives rise to a dense
aponeurosis distally for the formation of the
patellar ligament.
M. femorotibialis medius (Fie. 3: FTM) an>es
hv fleshy fibers from the distal half of the lateral
surface of the femoral shall. The belly is closely
attached to the overlying M. femorotibialis
externus on the caudal edge.
M. femorotibialis internus is the weakest of the
three parts of the M. femorotibialis complex and
originates by fleshy fibers from slightly more than
half of the distal part of the medial surface of the
femoral shaft The belly increases in size as it
passes distally and inserts by a flat tendon on the
craniomedial surface of the head of the tibiotarsus.
Zhang el al. • CHINESE GROUSE MYOLOGY
331
FIG. 5. Anterior (right) and posterior views of the
fourth layer of muscles of the shank of the Chinese Grouse.
Abbreviations: EDL, M. extensor digitonim longus; EB, M.
tibularis brevis: FDL. M. flexor digitoruni longus; FHI M.
Hexor hallucis longus; IF. M. iliofihularis; PLA. M.
plantaris; POP, M. popliteus.
M. flexor cruris lateralis (Figs. 1, 2. 3; FCLP)
and M. flexor cruris medialis form the caudal
border of the thigh. M. flexor cruris lateralis arises
mainly by fleshy fibers from the caudal end of the
dorsolateral crest of the ilium, by aponeurosis
bom the processus transversus of the first free
caudal vertebra. The belly, passing downward and
forward, joins in a tendinous raphe with a clearly
developed pars aecessoria (Figs. 2. 3: FCL.A) at
•be distal half of the thigh. Pars aecessoria extends
forward from the raphe and inserts by fleshy
fibers on the eaudolaieral surface of about the
distal third of the femoral shaft. The main belly ol
M. flexor cruris lateralis extends distally. and
gives rise to a wide tendinous sheet in common
with M. flexor cruris medialis. attaching to the
medial surface of the proximal tibia.
M. flexor cruris medialis (Figs. 1. 2. 3: FCM) is
•he most medial muscle in the caudal part of the
•high and arises partly aponeurotic from the ventral
edge of the distal third of the ischium, caudal to the
origin of M. pubo-ischio-femoralis. The flattened,
band-shaped belly gives rise to a flat and wide
aponeurosis passing between the internal and
medial heads of M. gastrocnemius to its insertion
on the medial surface of the proximal tibial shaft.
M. caudofemoralis pars caudalis (Figs. 2, 3:
CFC): M. caudofemoralis is composed of pars
caudalis and pars pelvica. These two parts have
separate origins and bellies, but share a common
insertion on the eaudolaieral surface ol the
proximal femoral shaft, just distal to that of M.
ischiofemoralis. Pars caudalis arises b> a narrow
tendon from a heavy tendinous sheet on the ventro¬
lateral surface of the pygostyle. The spindle-shaped
belly extends forward between the superficial M.
flexor cruris lateralis and the deep M. flexor cruris
medialis.
M. caudofemoralis pars pelvica (Figs. 2. 3:
CFP) arises by fleshy fibers from the ventral edge
of the distal fourth of the dorsolateral crest of the
ilium. The belly is thin, strap-shaped, and nearly
the same width as that of pais caudalis, presenting
a small, dorsal, triangular tendinous area at the
midway.
M. ischiofemoralis (Figs. 2. 3: 1SF) is a deeply
situated, roughly triangular shaped muscle. It
arises fleshy from nearly the entire lateral surface
of the ischium, beginning at the caudal margin of
the foramen obturatum and extending to the
caudal end of the bone. The bulky, fleshy belly
converges on a strong, flat tendon, which attaches
to the lateral surface ol the proximal femoral
shaft. The area of insertion lies caudal to, and
between the insertions ol Mm. iliotrochantericus
cranialis and medius.
M. obturatorius lateralis is a very small muscle
that arises from the lateral surface of the pubis,
just caudoventral to the acetabulum, cranial to the
obturator foramen. The belly fuses w'ith the
tendon of M. obturatorius medialis near its
insertion on the trochanter of the femur.
M. obturatorius medialis is a long, roughly
oval-shaped muscle which originates fleshy from
the medial surface of the postacetabular pelvis,
including most of the ischium and the pubis, and
the caudal part of the ilium. The fleshy belly
converges on a stout tendon, which passes through
the obturator foramen and inserts on the caudo-
lateral side of the trochanter of the femur, caudal
to the insertion of M. iliotrochantericus caudalis.
M. pubo-ischio-femoralis (Figs. 2. 3: PIF) is
composed of two separate bellies. Pars medialis is
deeply situated and arises by aponeurosis from the
332
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124, No. 2, June 2012
ventral margin of the proximal two-thirds of the
ischium, and the adjacent pubis. There is a large,
triangular, tendinous sheet in the caudoproximal
part of the belly. The tendinous insertion occupies
a long line on the caudal surface of more than the
distal two-thirds of the femur. The origin of the
superficial pars lateralis is partly fleshy, dorsal to
the origin of pars medialis, and constricted to the
ventral margin of the middle half of the ischium.
The insertion is mainly Heshy on the caudal
surface of the femoral shaft, lateral to that of pars
medialis.
M. tibialis cranialis (Figs. 2, 4: TC) has two
heads of origin, one by a short tendon from the
distal end of the condylus lateralis of the femur,
the other mainly by fleshy fibers from cristae
cnemialis cranialis and lateralis, and crista
patellaris of the tibiotarsus. The well-developed
belly occupies the cranial portion of the proximal
two-thirds of the tibiotarsus, immediately beneath
the M. fibularis longus. The stout tendon of
insertion is ossified before passing beneath the
fibrous loop near the distal end of the tibiotarsus.
The tendon inserts on tuberositas m. tibialis
cranialis on the proximal tarsometatarsus after
traversing the intertarsal joint.
M. extensor digitorutn longus (Figs. 4. 5: EDL)
lies deep to M. tibialis cranialis. This bipennatc
muscle arises fleshy from cristae cnemialis
cranialis and lateralis, and sulcus interenemialis
of the tibiotarsus. The belly extends downward
from its origin and becomes gradually narrowed
before merging with the tendon at about the
proximal end of the distal third of the bone. The
distal part of the tendon is ossified and passes
through the fibrous loop shortly above the
condyles in company with that of M. tibialis
cranialis. Just below this fibrous loop, it passes
alone beneath pons supratendineus before travers¬
ing the cranial side of the intertarsal joint. The
tendon continues its course along the craniolateral
surface of the tarsometatarsus. first passing
beneath a fibrous loop near the proximal end of
this bone, then bifurcating near the proximal end
of the distal three-fifths of the tarsometatarsus.
The medial branch supplies Dig. II and sends a
tendon to the medial side of Dig. Ill: the lateral
branch bifurcates to the lateral side of Dig. HI and
to Dig. IV. The individual branch inserts on the
dorsal surface of each phalanx of the correspond¬
ing toe. More than the proximal half of the tendon
is ossilicd along the cranial surface of the
tarsometatarsus.
M. fibularis longus (Fig. 1: FL) is the superfi¬
cial musculature on the craniolateral surface of ilk-
lower leg. and arises mainly by aponeurosis from
the cranial and lateral cnemial crests, and the
craniomcdial surface of the proximal tibiotarsus,
The flat, fusiform belly is confined to the
proximal two-thirds of the lower leg and close!;,
attached to M. tibialis cranialis and the pars
medialis of M. gastrocnemius and M. flexor
perforans et perforatus digiti III. which lie deep,
medial and dorsal to it. respectively. The ossified
tendon is formed at about the middle of the lower
leg. It is wider proximally and narrows as it passes
caudolaterally. The tendon is unossified jusi
above the condylus lateralis and sends a short
caudal branch to the proximal end of the lateral
side of the cartilage tibialis. The cranial mam
branch passes a bony canal at the distal end of the
shaft, then continues distally over the lateral side
of the intertarsal joint, and finally inserts on the
cranial edge of the ossified tendon of M. flexor
perforans digiti 111, a short distance inferior to the
hypotarsus.
M. fibularis brevis (Figs. 1, 2. 4, 5: FB) is a
relatively weak, bipennate muscle. It originates
mainly bv fleshy fibers from the craniolateral
surface of the tibiotarsus and the adjacent surface
of the fibula, beginning just distal to the insertion
ol M. iliofibularis to the distal sixth of the lower
leg. The tendon of insertion is held in place by
passing through a small fibrous canal just above
the lateral condyle. It then crosses the intertarsal
joint, and inserts on the lateroproximal end of the
tarsometatarsus. The distal end of the belly and
the proximal end of the tendon enclose a
sesamoid.
M. gastrocnemius is the largest and most
superficial muscle on the medial and caudal
surface of the lower leg. It is composed of three
separate origins and bellies that join to form one
combined tendon. The tendon covers the posterior
surface of the tibial cartilage and inserts on the
caudal surface of the hypotarsus and tarsometa-
tarsus. Pars lateralis (Fig. 1: GAL) arises hv a
short tendon from the lateral surface of the lateral
condyle of the femur. The origin tendon i>
partially fused with the proximal end of the lateral
arm of the ansa m. iliofibularis. The belly extends
a little less than two-thirds the way down the
lower leg and ends on an ossified tendon.
Pars intermedia is the smallest of the three parts
of M. gastrocnemius and arises by fleshy fibers
from caudomedial surface of condylus medialis of
Zhang et at. • CHINESE GROUSE MYOLOGY
333
the femur. The caudal surface of the belly is
strongly attached to the pars accessoria of M.
lienor cruris lateralis. The belly is rounded
proxiraally. and separated by the insertion tendon
ofM. flexor cruris medialis from the belly of pars
mediate: it becomes flat, finally ending on an
aponeurosis. The aponeurosis extends distal ly
between the bellies of pars lateralis and medialis,
and fuses with them.
Par^ medialis (Fig. 1: GAM) is the largest ol
the three parts of M. gastrocnemius and arises by
fleshy fibers from the patellar ligament, crista
cnemialis cranialis, and the facies gastrocnemialis
of the tibiotarsus. The large flat belly covers most
of the medial surface of the lower leg and embeds
a large sesamoid in its distal half.
M. plantaris (Figs. 4, 5: PLA) arises fleshy
from the proximal seventh of the caudomedial
surface of the tibia. Its roughly triangular belly
extends along the proximal third of the shank and
gives rise to a slender ossified tendon, which
inserts on the proximal end of the medial side of
die tibial cartilage.
M popliteus (Fig. 5: POP) is the deepest
muscle on the caudal surface of the lower leg
near the proximal end. It is small and roughly
triangular in shape, arising directly from the
caudomedial surface of the fibular head. The
belly broadens mediodistally and inserts on
tuberositas poplitea of the tibia.
M. flexor perforans et perforatus digit i II
'figs. I, 2: FPPD2) is composed of two parts.
Hie dorsal head is large and originates fleshy
from the patellar ligament and ansa m. iliotibu-
Inns, The ventral head is partly fleshy from the M.
ribulans longus and the crista cnemialis lateralis
°f Ihe tibia. The belly of the dorsal head tapers
Jnd embeds a sesamoid at its distal third, before
foxing with the belly of the ventral head about
two-thirds of the way down (he shaft of the lower
leg. The insertion tendon passes through the tibial
cartilage and hypotarsus, and is ossified again for
most of its length along the tarsometatarsus, and
hnally attaches to the vcntroproximal surface ot
foe second phalanx of digit II.
M. flexor perforans et perforatus digiti 111
(Figs. 1. 2: FPPD3) is a bipennate muscle that is
visible superficially on the lateral surface of
Proximal end of the lower leg. It arises by fleshy
libers from the patellar ligament. The belly is
strongly attached to M. flexor perforans et
Perforatus digiti 11 and M. I'ibularis longus. ending
near the middle of the tibiotarsus in a tendon
which is ossified for most of the length before
reaching the tibial cartilage. The tendon of M.
flexor perforans el perforatus digiti III and M.
flexor perforans digiti IV is enclosed in the
sheath-like tendon of the M. flexor perforans
digiti 111 when passing through the tihial cartilage
and hypotarsus. The tendon is again ossified for a
considerable distance along the caudal side of the
tarsometatarsus before receiving a small branch
from the tendon of M. flexor perforans digiti 111.
Opposite phalanx I of digit III, it perforates the
tendon of the M. flexor perforans digiti III. and is
in turn perforated by M. flexor digitorum longus.
The insertion is on the ventral surface near the
middle part of the second phalanx.
M. flexor perforans digiti IV (Figs. 2.4: FPD4)
is visible in the caudolateral side of the lower leg
after removing M. gastrocnemius, and has three
heads of origin. The largo medial head originates
by fleshy fibers from the intercondylar area of the
femur. The intermediate middle head arises by
aponeurosis from the lateral surface of the lateral
condyle of the femur, and ansa m. iliofibularis.
The smallest lateral head, in common with those
of Mm. flexores perforate digitii II and HI,
attaches to a heavy combined tendon, which
arises from the fibular head and receives the
tendon of insertion of M. ambient. The belly
terminates about three-fourths the way down the
lower leg. The tendon of insertion is ossified for a
considerable distance from the distal part oi the
belly to the distal end of the tibiotarsus. It is
enclosed in the sheath-like tendon of the M. flexor
perforans digiti Ill. in common w ith the tendon ol
M. flexor perforans et perforatus digiti III when
passing through the tibial cartilage and hypotar¬
sus, and is ossified again in the middle portion of
the tarsometatarsus.
M. flexor perforans digiti III (Fig. 4: FPD3) lies
medially to M. flexor perforans digiti IV and
arises by two heads. The larger medial head
originates by aponeurosis from the intercondylar
region of the femur, and the belly gives rise to a
definite ossified tendon above the point ol union
with the lateral head. The lateral head arises from
the distal part of the combined tendon, deep to the
lateral head of M. flexor perforans digiti IV. The
slender, fusiform belly of the lateral head forms
an unossified tendon before fusing with the
ossified tendon of the medial head at the distal
end of the tibiotarsus. The insertion tendon
broadens at the caudal-most part or the tibial
cartilage and encloses the tendon of M. flexor
334
THE WILSON JOURNAL OF ORNITHOLOGY • Vo/. 124. No. 2. June 2012
pertorans digiti IV and M. flexor perforans et
perforatus digiti III. It is ossified for most of the
length of the tarsometatarsus. uniting with the
tendon of M. fibularis longus just below the
hypotarsus. and sending a small branch to the
tendon of M. flexor perforans et perforatus digiti
III. Insertion is on the ventral surface of the distal
end of the proximal phalanx and the proximal end
of the second phalanx of the third toe.
M. flexor perforans digiti II is a bipennate
muscle and lies deep to M. flexor perforans digiti
III and IV. It arises by two heads. One arises by
aponeurosis from the intercondylar region of the
femur, medial to the head of M. flexor perforans
digiti IV; the other lateral head arises by fleshy
fibers from the ansa m. iliofibularis. the lateral
surface of the lateral condyle of the lemur, and the
proximal part of the combined tendon. The belly
of the medial head is strongly attached to that of
the medial head of M. flexor perforans digiti III at
the proximal half. The tendon is ossified for a
considerable distance in the lower leg above the
tibial cartilage, and for most of the length of the
tarsometatarsus. It is perforated by the tendon of
M. flexor perforans et perforatus digiti II and M.
flexor digitorum longus at the base of the second
toe, and inserts mainly on the ventrolateral side of
the proximal end of phalanx I. digit II,
M. flexor hallucis longus (Fig. 5: FHL) origi¬
nates by fleshy fibers from the intercondylar area
of the femur. Its relatively weak belly lies lateral
to, but is shorter than that of M. planiaris, and is
confined to the proximal fourth of the tibiotarsus.
With the exception of the distal-most part, nearly
the entire slender tendon, including the part
enclosed within the distal belly, is ossified in Lhe
region of the tibiotarsus. The tendon passes
through the tibial cartilage on the deep lateral
side and then through a groove immediately
lateral to the crista lateralis hypolarsi. The tendon
is ossified again after emerging from the groove
and passes diagonally toward the medial side over
the caudal surface of the M. flexor digitorum
longus near the base of the metatarsus I. The
tendon of insertion splits into two unossified
branches: the short, weak branch joins the lateral
side ol the distal tendon of M. flexor digitorum
longus; the other main branch perforates the M.
flexor hallucis brevis near the base of digit I, and
inserts on the ungual phalanx of the hallux.
M. flexor digitorum longus (Figs. I, 2, 4 5*
pDL) is a unipennato muscle and the most deeply
situated muscle on the caudal surface of the lower
I IG. 6. Anterior (left) and posterior views of the
intrinsic foot muscles of the Chinese Grouse. Abbrevia¬
tions: ABD2, M. abductor digiti II: ABD4, M. abductor
digiti IV: LBD4, M. extensor brevis digiti IV: EIIL. M.
extensor hallucis longus: KPD3. M. extensor pruprius digiti
HI: FHB. M. flexor hallucis brevis.
leg. I he distal part of the belly is visible
superficially on the lateral surface of the lower
leg. It arises by two fleshy heads, one from the
lateral surface of the fibula, just proximal to the
insertion of M. iliofibularis, the other from lhe
caudal surface of the tibiotarsus and the adjacent
tibular. The bellies arc separated by the insertion
tendon of M. iliofibularis at the proximal end. and
then merge extending about four-fifths the way
down the lower leg. There is an ossified tendon
embedded in the caudomedial surface along die
distal hall of the belly. The tendon passes through
a fibrous canal in the deepest medial side ot the
tibial cartilage and then through the hypotarsus
to the tarsometatarsus. After receiving a branch
of M. flexor hallucis longus. it broadens and
trifurcates, sending branches to insert on die
ventroproximal surface of the ungual phalanges of
the second, third, and fourth digits.
M. extensor hallucis longus (Fig. 6; EHL) is
unipennate muscle that arises bv fleshy libers
from the craniomedial surface of the proximal
halt of the tarsometatarsus. The tendon extends
dislally along the medial side of the bone and then
along the dorsal surface of the proximal phalanx
of the hallux, inserting on the base of the ungual
phalanx.
M. flexor hallucis brevis (Fig. 6: FHB) arises
by fleshy fibers from the caudomedial surface ol
the proximal tarsometatarsus and the adjacent
Zhang el al. • CHINESE GROUSE MYOLOGY
335
medial surface of the hypotarsus. The belly is
narrow distally and extends one-third the way
down die bone. The tendon of insertion en-
sheathes that of M. flexor hallucis longus at the
base of the hallux, and inserts on the ventral
surface of the proximal end of phalanx I.
M. abductor digili 11 (Fig. 6: ABD2) is the
weakest of the intrinsic foot muscles. It arises
by fleshy fibers from the medial surface of the
tarsometaiarsus. The weak belly extends slightly
less than the distal third of the bone and inserts by
a short tendon on the ventromedial surface of the
base of phalanx I of digit 11.
M. extensor proprius digiti 111 (Fig. 6; EFD3)
lies between M. extensor brevis digiti IV and M.
abductor digiti 11. It originates by lleshy fibers
from the cranial surface of the distal third of the
larsometatarsus. The short, flat tendon inserts on
the dorsal surface of the base of the proximal
phalanx of digit III.
M. extensor brevis digiti IV (Fig. 6: EBD4) is a
stout muscle that arises directly from the cranio-
lateral surface of a little more than the proximal
half of the tarsometaiarsus. The belly is nearly
bipennate and narrows distally. The slender
tendon passes through the foramen vasculare
distale between the troehleae for digits III and
IV. and inserts on the medial surface of the base
°t phalanx I, digit IV. Most of the tendon,
including the part enclosed by the distal belly, is
ossified.
M. abductor digiti IV (Fig. 6: ABD4) is
unipennate and the strongest among the intrinsic
loot muscles. It originates directly from the
caudolateral surface of the larsometatarsus with
the belly extending almost to the base of trochlea
IV. The short tendon inserts on the ventrolateral
comer of the base of phalanx I, digit IV.
DISCUSSION
The following muscles are absent in Chinese
Grouse: M. adductor digili II. M. adductor digiti
IV. M. extensor brevis digiti 111 and M. lumhri-
calis. Data for the Chinese Grouse agrees with
t'lher tetraonids in the absence of M. adductor
digiti II. the same number of sesamoids, and the
relatively weak development of the intrinsic foot
muscles which originate from the larsometatarsus
and insert on the digits (Hudson et al. 1959). Four
intrinsic foot muscles are absent in Chinese
Grouse. The loss of intrinsic fool muscles is
commonly found in species of small size, such as
hummingbirds (only M. extensor hallucis longus.
M. flexor hallucis brevis, and M. adductor digiti II
are present) (Zusi and Bentz 1984) and more
highly derived taxa. c.g., Passeriformes, in which
the intrinsic foot muscles It) the forward toes are
almost entirely lost (Raikow 1982. 1985). The
bellies of M. extensor proprius digiti 111 and M.
abductor digiti II in Chinese Grouse are limited to
the distal third of the tarsometatarsus. M. extensor
hallucis longus and M. flexor hallucis brevis are
confined to the proximal half and proximal third
of the larsometatarsus. respectively. Similar to
other tetraonids, the tendency for the short toot
muscles to be weak and attenuated may be an
adaptation to the extreme cold climate occurring
in northern high latitude regions (Hudson et al.
1959).
Forest tetraonids, including genera Bonasa and
Tetrastes, habitually forage in trees and shrubs
during winter and early spring, and are more
arboreal than tundra and grassland species. The
branch to relatively shorter limbs and the broad,
low sacrum ensures better equilibrium while
hopping from or moving along branches (Kuz'¬
mina 1992).
The pelvic myology of Chinese Grouse exhibits
four features related to an arboreal mode of life.
One feature is the modification of the vinculum
between the two superficial flexors supplying
digit III. The third toe has three sets of flexor
tendons in birds. The deepest, M. tlexor digitorum
longus inserts mainly on the angular phalanx and
is important in flexing distal phalanges. The other
two superficial flexors. M. flexor perforans digiti
111 and M. flexor perforans et perforates digiti III,
function as the flexors of subdistul phalanges.
During perching, when the weight of the bird
does not necessarily rest uniformly upon all of the
toes or toe surfaces, independent flexion of
various subdistal phalanges must be of impor¬
tance (Owre 1967). The tendons of M. flexor
perforans digiti III and M. flexor perforans ct
perforatus digili III. in their course down the
posterior side of the larsometatarsus, are connect¬
ed by a strong tendinous band (vinculum) which
suggests simultaneous action of the two toe
flexors in some birds, such as Anatidae. Catli-
artidae. Grits. Lams, most Galliformes and ratites
(Hudson 1937, 1948; Fisher 1946; Berger 1956;
Hudson el al. 1959; George and Berger 1966;
Patak and Baldwin 1998). The vinculum is
typically broad and short, and divided into a
group of parallel, more or less separate strands.
This vinculum is absent in Accipitridae, Pandion ,
336
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 2, June 2012
Falco, Ardeidae. Cochleariidae, Cuculidae, Up-
upa. Derulrocopos, Coracias , and all passerine
birds ilius far studied (Hudson 1948, George and
Berger 1966. Vanden Berge 1970, Raikow 1987).
Unlike the typical structure in galliform birds, the
vinculum of Chinese Grouse is present as a small,
single tendon sent from the tendon of M. flexor
perforans digiti 111 to that of M. flexor perforans
et perforatus digiti Ill. This kind of weak
vinculum is probably of little functional signifi¬
cance and. suggests greater independent action of
these muscles, permitting more efficient and
subtle bending of the segments of the third toe
while perching and moving in trees.
A second feature is the modification of the deep
plantar vinculum between M. flexor digitorum
longus and M. flexor hallus longus. Birds show a
bewildering variety of different structural rela¬
tionships between these two deep plantar tendons
from complete separation to virtual separation
except for a simple vinculum, through a variety of
degrees and patterns o I fusion and interconnection
in association with different functional and
adaptive specializations of the feet (Raikow
1987). A vinculum is present between the
insertion tendons of M. flexor digitorum longus
and M flexor hallus longus in Chinese Grouse,
but is a small tendon sent from M. flexor hallus
longus, structurally different from the typical
vinculum in other galliform birds. This kind of
connecting structure, like that of the M. flexor
perforans digiti III and M. flexor perforans et
perforatus digiti III. is of little functional signif¬
icance and might be correlated with greater digital
dexterity and independence needed in arboreal
locomotion (Owre 1967).
A third feature involves the function of M.
flexor perforans digiti II. The typical insertion
of this muscle is on the plantar surface of the
proximal phalanx of digit II and Ilexes the entire
digit at its articulation (George and Berger 1966.
Raikow 1985). However, this muscle in Chinese
Grouse functions as both the flexor and adductor
of the second toe by inserting mainly on the
proximolateral corner of phalanx I. The absence
of M. adductor digiti II in Chinese Grouse is
lunctionally compensated by M. flexor perforans
digiti II. The adduction of the second toe is
important tor Chinese Grouse to move in trees,
especially on thin branches. It has been reported
the middle toe is held on top of the curved surface
°. ,he hriinch antl '*10 second and fourth toes fall
slightly below and lightly support the foot from
both sides when moving on a thin branch
(Kuz’mina 1992).
A fourth feature is the augmentation of the
flexion and adduction of digit IV. M. flexor
perforans digiti IV arises by three heads in
galliform birds, the middle head being mainly
tendinous in most forms (Hudson et al. 1959). The
relatively better development of this muscle in
Chinese Grouse, indicated by a more fleshy middle
head, suggests a greater bending force of this toe
than other gallifomts. The bipennatc M. extensor
brevis digiti IV acts more as an adductor than as an
extensor by inserting on the medial surface of the
proximal phalanx. Furthermore, it is the only
intrinsic foot muscle possessing an ossified tendon.
Ossified tendons are denser and stiffer than
unossified tendons, and experience less deforma¬
tion under a given load (Bennett and Stafford 1988,
Bledsoe et al. 1993, Landis and Silver 2002). The
functional role of ossified tendons in birds is
obscure: possibly they serve in some way to
reinforce the action of the muscle, as well as to
accurately control the positions of the digits (Bock
and von Wahlert 1965, Vanden Beige 1970.
Bennett and Stafford 1988, Bledsoe et al. 1993).
In this ease, it facilitates the adduction of the toe
related to grasping thin branches tightly from the
lateral side when moving in trees.
ACKNOWLEDGMENTS
We are exiremely grateful to R. L. Zusi for reading the
manuscript and providing useful suggestions and comments:
M. D. Spit/cr. H. F. James, and C. M. Milensky assisted with
many aspects. We also thank C. E. Braun and an anonymous
reviewer for their constructive comments and useful edits
This work was supported by the National Science Foundation
of China (30870263, 31071931), and Funding Project for
Academic Human Resources Development in Institutions nl
Higher Learning Under the Jurisdiction of Beijing Munic¬
ipality (Grant No. PHR201 107120).
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The Wilson Journal of Ornithology 1 24(2):338-344, 2012
PREDATION ON SEEDS OF INVASIVE LA NT AN A CAMARA BY
DARWIN’S FINCHES IN THE GALAPAGOS ISLANDS
JORGE CARRI6N-TACURI,14 REGINA BERJANO,1 GIOVANNY GUERRERO,2
ENRIQUE FIGUEROA.1 ALAN TYE,' AND JESUS M. CASTILLO1
ABSTRACT. Observations on birds feeding on fruits of the invasive shrub Lantana camera (Supirrosal were
conducted on Santa Cruz Island. Galapagos (Ecuador) in the Dry Zone during the 2009 dry season. The endemic ground
finches Geospizt i magnirostris (Large Ground Finch) and G. forth (Medium Ground Finch) were recorded eating Loam
seeds w ith G. fortis the main consumer (>90% of records). Both finch species crushed the seeds and ate the embryos,
discarding the exocarp and empty seed coats. They also dropped entire fruits to the ground, which could contribute to >hon-
distance dispersal, but both finches also consumed fruits of L. camera on the ground. Density of L camera seedlings under
aduli plants was higher in rockier areas than in bare soil since seeds were less accessible to predators and/or found more
suitable irucrosites lor germination and establishment. Both species of finches serve as short-distance dispersers, hut rnainlv
as seed predators of L, camera fruits. Received S July 2011. Accepted 15 November 2011
The introduction, spread, and subsequent inva¬
sion ot alien species has become a problem
worldwide, but is of particular concern on oceanic
islands (Vitousek el al. 1997, Dulloo et al. 2002,
Kueffer et al. 2010). The geographic isolation of
islands limits immigration of new species while
those that arrive subsequently evolve with fewer
competitors and predators. The accelerated intro¬
duction of new species by people alters the natural
ecological equilibrium of islands and can exert
severe pressure on native species biodiversity
(MacArthur and Wilson 1967).
Frugivorous animals, by acting as seed vectors,
have an essential role in the reproductive cycle of
their food plants (Herrera 1995). Disperser avail¬
ability may be an important factor affecting
invasion success, and alien plants arriving in new
habitats have no guarantee of finding suitable
dispersal agents ( Parker 2001 ). However. Richard¬
son et al. (2000) noted that invasive plants rarely
sufter from a lack ol mutualistic services such as
pollination and Jruit dispersal. Birds are recognized
as the main dispersal agent of many invasive plant
species around the world (e.g.. Dean and Milton
2000. Renne et al. 2002. Gosper et al. 2005), and
may directly affect conservation efforts.
Entire seeds passed through the gut of frugivore
birds often have increased germination "rates,
although they may also lose viability and reduce
Depart uinento de Biotogfa Vegetal y Ecologt'a. Uni
verst dad de Sevilla. Apartado 1095. 41080 Sevilla. Spain.
- Untvers.dad Central de Ecuador. Ciudad Universitaria
Quito, Ecuador.
’Secretariat of the Pacific Regional Environment Pro
gramme. P. O. Box 240. Apia, Samoa.
Corresponding author; e-mail: jorgccarrion@us.es
germination (T raveset 1 998. Orrock 2005. D’ Avila
el al. 2010). Seed predators may also contribute to
dispersal if pulp is consumed and seeds are
discarded in suitable microsites (Shiels 2011).
However, when seeds are crushed before ingestion,
their viability is reduced as recently demonstrated
tor frugivores and seed predators in the Galapagos
Islands (Buddenhagen and Jewell 2006, Guerrero
and Tyc 2009, Guerrero and Tye 2011 ).
Lantana camara (Verbenaceae) (Supirrosa) is
one of the most invasive plants in the Tropics,
now occupying a wide variety of habitats in
countries worldwide (Parsons and Cuthbertson
2001). It was introduced to the Galapagos Islands
us an ornamental species in 1938 (Tye 2001 > and.
in 1987. covered >2,000 ha (Lawesson andOrti/
1990). L. camara produces a great number ol
fruits (Sharma et al. 2005) that are usually
dispersed by frugivorous birds (Day et al. 2003'
However, no specialist frugivores occur in the
Galapagos Islands and most landbird species cl
the archipelago were traditionally considered to
be granivores (seed predators) or insec tivores
(Guerrero and Tye 2009). However, some birds,
including Darwin’s finches, may act as dispersers
for short and long distances of endemic, natn
and introduced plants (Buddenhagen and Jewel
2006; Guerrero and Tye 2009, 2011: Heleno et 0
2011). Guerrero and Tye (2009. 2011). report
Darwin’s finches and other Galapagos birds
demonstrate three main types of fruit-seed han¬
dling techniques: (I) swallow die entire fmrt lir
pieces of it, (2) discard the seeds, eating only the
pulp, and (3) crushing the fruit and seed Our
objectives were to: (1) analyze the interaction o'
Galapagos bird species with L. camara fruit'’
338
Carrion-Tacuri et al. • PREDATION OF LANTANA CAMARA SEEDS
339
during the dry season in the dry lowlands ot Santa
Cruz Island, and (2) investigate seed dispersal.
Seed predation, and seedling colonization pattern.
METHODS
Study Site.— The Galapagos Islands are
-960 km west of Ecuador in the Pacific Ocean.
The vegetation of Galapagos is strongly zoned by
altitude and aspect with the Dry Zone being most
extensive, occupying the majority of the lowlands
•if the archipelago (McMullen 1999. Trueman and
d’Ozouville 2010). Tw'o distinct seasons can be
distinguished during the year in the Galapagos
Trueman and d’Ozouville 2010). The warm
season (Jan to Jun) is caused by warm ocean
currents sweeping southward from Central Amer¬
ica. Mean daily maximum temperature is 29 C
and mean daily temperature is between 25 and
26 C (Ziegler 1995). During this season, the skies
are normally clear, hut heavy showers are frequent;
this season is the wettest in the Dry Zone of the
islands. The cool season (Jul to Dec) is caused by
(he Humboldt Current, resulting in cooler air
temperatures (18-26 C) with skies usually over¬
cast. A mist layer, known locally as 'gartia',
frequently occurs at higher elevations, but little
precipitation occurs in lowlands (Ziegler 1995);
this season is the driest in the lowlands (Trueman
and d'Ozouville 2010).
Our study was conducted in the dry' lowlands
at 26 m above sea level on Santa Cruz Island
tOO 1 9' \\ . 00 44' S) near Puerto Ayora. The vege¬
tation at the study site was dominated by the native
tree Bursera graven lens (Burseraceae) (51% rela¬
tive cover) and the endemic Galapagos lanlana
Montana peduncularis) (46% relative cover). The
relative cover of L. camara was 37% ( relative cover
^as measured by contact every 50 cm along live
linear transects, each of 30 m).
Study Species. — L. eanuira is a pantropical
'pecies inhabiting a wide variety of habitats
around the world (Sharma et al. 2005). It usually
colonizes open sunny areas such as degraded
lands, grasslands, crop edges, abandoned crop
Helds, and coastal areas or forest edges. It also
colonizes forests alter disturbances including fire
Dr logging (Parsons and Cuthbertson 2001). Fruits
01 L camara are two-secded drupes, 4-8 mm in
diameter, green and hard when immature, turning
to shiny purple/black when ripe < Auld and Medd
1^87, Parsons and Cuthbertson 2001 ).
Sampling.— Our study was conducted during
August and September 2009, when L. camara was
finishing fruiting and fruit pulp was dry. Bird
activity was observed from sunrise to midday, as
preliminary sampling confirmed that most forag¬
ing activity was concentrated in this period. We
conducted 24 hrs of observations on five different
mornings recording bird species and foraging
behavior at five individual shrubs of L camara.
Information on foraging behavior tor each bird
included: number of infructescences visited, fruits
consumed per foraging bout, and bird behavior
after feeding. Birds were identified following
Swash and Still (2000).
Fruit productivity ol L. camara in our study site
was measured for 10 tagged adult plants. The total
number of infructescences per plant and the total
number of fruits per infructescence (10 infructes-
cenccs/plant) were recorded. The area occupied
by each plant was recorded to calculate fruit
production/nr.
Ten other adult plants of the same population
were lagged to record fruit removal. Twenty
infructescences of these plants were carefully
bagged with fine mesh nylon for I month to
measure fruit fall without external intervention.
Fruit traps consisting of plastic containers 28 cm
in diameter and 8 cm deep covered with 1-cm
metallic wire mesh were placed under the marked
plants to collect fallen fruits. The mesh prevented
further predation once the fruit entered the
container. Ten additional plots (10 X 10 cm)
were marked on the ground surface near the
tagged L. camara plants and 25 L. camara fruits
were placed in each. These were followed during
I month to measure predation ot fruits on the
ground.
Colonization patterns ot L. camara seedlings
were studied by recording their presence under 10
adult plants. The percentage of soil covered by
rocks was also recorded under each adult Lanlana
plant to investigate the ellect ot substrate at
colonized sites, especially the effect of rocky
habitats in seedling establishment.
Statistical Analysis. — Analyses were conducted
using SPSS Release 18.0 (SPSS Inc.. Chicago, IL,
USA). Deviations were calculated as the standard
error of the mean (SEM). Outlier values were
identified and discarded following the formula
(mean ± 2 SD’s). Pearson correlation coefficient
was used to assess correlation between the
behavior of birds after feeding on L camara and
the number of eaten fruits, and between the
number of seedlings and the percentage of soil
covered by rock.
340
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 2. June 2012
TABLE 1 . Number of recorded visits per bird species, visited infructescences (mean ± SE). consumed fruits per boui,
and per infructescence in the Dry Zone of Santa Cruz (Galapagos Islands) during the 2009 cool-dry season.
Species
No. visits (%)
Visited infructescences
per bout
Consumed fruits per
infructescence
Consumed frails per fens
Geospiza fortis
G. magnirostris
83(92)
7(8)
6 ± 1
22 ± 9
5 ± 0
3 ± I
26 ±4
60 ±22
RESULTS
/-. comma plants produced an average (± SE)
of 1,075 ± 158 infructescences, each containing
12 ± I fruits per infructescence. Adult L. camara
plants had an urea of • 6.0 i 0.8 m*, and were
2.5 ± 0.2 m in height on average; thus, each
plant produced a mean of 2,820 ± 229 fruits/nr.
Only four (2%) of a total of 252 fruits in the
bagged infructescences fell into the bags alter
1 month.
Ninety records of birds feeding on L. camara
fruits were obtained during 24 hrs of observation:
8% corresponded to the Large Ground Finch
( Gcospiza magnirostris) and 92% to the Medium
Ground Finch (G. fortis) (Table I). Neither finch
species swallowed entire fruits of /.. camara. but
crushed them, eating the embryo and the endo¬
sperm and discarding the empty fruit coal. G
fortis removed 2.138 fruits and G. magnirostris
149 fruits. G. magnirostris ate fruits front an
average of 22 ± 9 infructescences on each visit to
a L. camara plant, consuming 3 ± I fruits per
infructescence. G. fortis visited 6 ± 1 infructes-
cences. consuming 5 ± 0 fruits per infructescence
(Table 1). The number of fruits removed per
foraging bout was variable: 1-157 fruits for G
magnirostris and 1-207 fruits for G. fortis. On
average. G. magnirostris ate 60 ± 22 fruits pet-
bout and G. fortis 26 ± 4 fruits per bout (Table I ).
Some fruits were observed falling intact to the
ground as a consequence of infructescence
manipulation by both species of finches.
Most G. fortis (59%), after feeding on L
camara , flew from the area (out of sight), while
25% flew to a nearby tree. 12% continued feeding
on another L. camara plant, and 4% flew to the
ground and continued foraging. Twenty-nine
percent ol the G. magnirostris flew from the area
after feeding on L. camara. 29% flew to a nearby
tree. 29% continued eating on another L. camara
plant, and 13% Hew to the ground (Fig. |) The
“ ar™Lfinchcsf after ,cedins l ~
™ independent of ,lle number of fruits eaten
caison correlation coefficient. P > 0.05).
Fruit traps under L. camara plants collected an
average of 684 ± 105 fruits/nr during a month,
which represented 24% of the fruit production ot a
plant (Fig. 2). Of the trapped fruit. 311 r 59 were
entire fruits and 373 ± 67 were empty fruit coats,
indicating seed predation on the plant. Thus. 13T
of the fruit production was consumed on the plant,
w hile I I % was dislodged, mostly as a consequence
ol infructescence manipulation (Fig. 2).
After I month, 66% of the fruits placed in plots
on the ground had been removed by unknown
agents, 15% were crushed and eaten in situ (fruit
remains were found, similar to those dropped by
finches), and 19% remained intact on the soil
surface (Fig. 2).
The number of seedlings under adult L. camara
plants varied from 0 to 12, resulting in an average
°f I 1 0 seedlings/m2. A significant positive
correlation was found between seedling density
and percentage of soil covered by rock ( r - 0,67.
P < 0.05, n = 9), discarding as outlier an adult
plant under which was a high density of seedlings
(3 seedlings/m2) and 50% rock cover.
DISCUSSION
Our results demonstrate that seeds of invasive L
camara are part of the diet of endemic ground
finches (G. magnirostris and G. fortis ) during die
cool-dry season in the Dry Zone of Santa Cmz
Island (Galapagos). Guerrero and Tve (2009 1 and
Buddenhagen and Jewell (2006), reported ground
finches most commonly crush dry seeds. We ab
found that both finch species behaved mostly *
seed predators of L. camara rather than disperers.
crushing the dry fruits and feeding on seed enibO' '
Ground finches, despite their predominant
predatory role in this study, may also act as shori-
distance dispersers as their foraging activity
caused fruit drop, which may be important given
the low percentage of fruit drop from baggeJ
infructescences. G. magnirostris visited n,n
infructescences and ate many fruits per bout- b|‘
this species was only occasionally observed- 6
fortis visited more plants, ate at fewer intrude-
cences per plant and ate less fruits per bout, hm
Carrion-Tacuri et al • PREDATION OF LANTANA CAMARA SEEDS
341
100
80
^ 60
>
'■g
to
sz 40
o
c
Ll
20
0
HO. I. Activity of Ceospiza fortis <92% of records) and G. tmgnirostris (8% of records) when feeding on Lantcma
tamara fruits during the 2009 cool-dry season in the Dry Zone of Santa Cruz. Galapagos Islands.
zzzzz
m
i i Flyaway
i 1 Nearby tree
i 1 Nearby L. camara
r / a Ground
G. fortis G. magnirostris
(92%) (8%)
ate more fruits per infructescence. G. fortis thus
moved less on each I.. canurni shrub and would
probably stimulate less fruit fall. Thus, G. fortis
may be a more effective seed predator and
perhaps a less effective short-distance disperser
of L. camara, as it ate a larger proportion and
dislodged a smaller proportion of the fruit than
were removed from the bush by its activity at each
visit.
Both species of finches also foraged on the
ground, which reduces their role as short distance
dispersers. Fifteen percent of the fallen fruits
appeared to have been removed by the two finch
species from the ground during just 1 month.
A great number of fruits on the ground were
removed, many of them probably by introduced
rodents. This may be effectively equivalent to
predation since rodents either eat seeds or store
them in deep larder hoards from which successful
seedling establishment is unlikely (Montgomery
and Gurnell 1985. Hulme 1998). Reducing
dispersal distances acts to concentrate seeds
FIG. 2. Fate of fruit on shrubs due to foraging activity by ground finches (A), and fate of fallen fruits during 1 month
(B) of the cool-dry season in the Dry Zone of Santa Cruz Island (Galapagos). Percentage for each fruit class is in
parentheses (n = 10 shrubs).
342
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 2. June 2012
around parent plants, making them especially
vulnerable to seed predators (McConkey and
Drake 2002, Chimera and Drake 2011), in this
case, ground finches or rodents. However, intro¬
duced rodents act as both seed predators and seed
dispersers, which may also contribute to the
spread of L. camara as occurred in the Hawaiian
Islands (Shiels 2011. Shiels and Drake 2011).
Most seedlings recorded under L. camara adult
plants were rooted in fissures between rocks
where they were less accessible to predators.
Seeds of L camara would have a higher
probability to survive post-dispersal predation in
fissures between rocks, and/or they would find
more appropriate environment for germination
and establishment as soil moisture is higher than
on non rocky surfaces.
Introduction of invasive species can alter
ecosystem function, resulting in direct species
ieplaccment and changes in ecosystem processes
that control plant and animal activities (Mack and
D' Antonio 1996). Food during the cool dry season
in the Dry Zone of Galapagos is scarcer than
during the wetter season, and availability of /..
camara fruits represents an important food source
for the finches. Availability of the invasive
Imm ana could be altering the feeding behavior
of endemic finches, and changing their interac¬
tions with endemic or native plant species such as
L. pedimcularis, which also grows in the Dry
Zone invaded by L camara. It is not known
whether the availability of the more abundant L
camara fruits might benefit the endemic congener
by reducing predation pressure by finches, or
whether it might disadvantage it, by reducing
dispersal of its fruit. Little predation was observed
on L. peduncularis fruits (just 6% of the total fruit
production, unpubl. data).
Transport of seeds by frugivores from the
parent plant could improve the overall chances
of seedling dispersal to suitable establishment
sites (Schupp 1993, 1995; Schupp and Fuentes
1995) but no birds were observed carrying L.
camara fruits. Our observations were concen¬
trated in the dry season, when fruits are
completely dry and perhaps relatively unappe¬
tizing for frugivores, although at higher altitudes
it was observed that both finch species also
crushed fresh fruits of L. camara (J. Carridn-
Intact seeds of L. camara have been found in
the stomach of the invasive Smooth- billed Am
{Crotophaga uni) (Guerrero and Tye 2011). Buis,
an introduced bird species could be a long distance
disperser of L. camara fruits in Galapagos, as in the
Hawaiian Islands, where no native bird has been
observed eating L camara fruits but six introduced
bird species have been implicated in its spread
(Perkins and Swezey 1 924, Day et al. 2003. Chimera
and Drake 2010). Experiments with captive Gafa-
pagos Mockingbirds (Mimas pamilus ) revealed
they eat L camara seeds, and seed viability wjs
not significantly different after passing through ;is
gut ( Buddenhagen and Jewell 2006).
Effective vertebrate seed dispersal is an impor¬
tant attribute of successful woody plant invaders
(Rejmanek 1996, Westcott and Fletcher 201 1 ) L
camara already occupied 2,000 ha in the Galapa¬
gos Islands by 1 987, and the absence of specialist
frugivores in the islands may reduce the dispersal
and invasion velocity of L. camara. Seed
predation by the endemic ground finches and
other animals may reduce L camara' a rate of
spread and therefore its impact on the Galapagos
ecosystem (finches removed —15% of L camara
Iruits in just 1 month). This effect could be
reduced by birds such as the Smooth-billed Ani.
which was introduced to Galapagos in l%0v
(Rosenberg et al. 1990), or other generalist
frugivores that could facilitate seed dissemination
and invasion of L. camara or other fleshy-fruitcd
non-native species.
ACKNOWLEDGMENTS
This research was supported by ‘Agenda EspanoU &
Cooperacidn Internacional para el Desarrollo' (AD- -
through a grant to the first author and ‘El Plan Pn-TID L
Investigacidin de la Universidad de Sevilla’ We thank the*’’
of Galapagos National Park for providing the research pemi.:
and Mabel Gonzalez and Tania Quisingo for field
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biapicata)
TABLE 1. Continued.
348
THE WILSON JOURNAL OF ORNITHOLOGY • Vo/. 124. No. 2. June 2012
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350
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 2. June 2012
were orb weavers except for a single case, an
African black widow (Latrodectus sp.) that killed
a Red-billed Firefineh ( Lagonosticta senega la).
One-half ot all reported cases ( n = 23) that
identified the spiders entrapping birds in webs
were in the genus Nephila. including N. inaurata
0), -V. maculara (2), and N. clavipes (14). Other
forms of orb weavers included six cases for the
genus Argiope including 4. auruntia (I) and A
caphinarium (3). two cases for Eriophora biapi -
cata and Nepliilengys crueniata. and single cases
for Aranens trifolium. Mastophora sp., and
Neoscona hentzii.
I he only species of spider with sufficient
tor analysis of patterns of bird entrapment
• clavipes. This species entrapped nine spi
representing 14 cases (31% of all spider reco
lapped birds ranged in si/e from Ver
Hummingbird (,m,ss = 2 g> wing t,hord
-7 ram) to Swain. son's Thrush (mass - r
themselves, and wrapped birds dying in the web;
the remaining seven were released with human
intervention.
DISCUSSION
Patients of Birds Trapped in Spider Webs.—
Most entrapped birds had a mass of ^15 g and
wing chord <90 mm. Larger species of birds am
especially vulnerable to entrapment when the w<
was approached at an indirect angle with dc"
flight speed (Cox and Nesmith 2007). Larger binfc
with longer, more powerful wings appear t< he
able to break through webs easier than snul-*r
birds, which would explain the higher rate'
entanglement for smaller species (Fig. D-
longer a bird is entrapped, the more likely it i> 1
succumb due to stress and fatigue. It is po>sibll
that large species (>)5 g mass, s90 mm win;
chord) were entangled more frequently, hut in**1
themselves before the event could be documented
It is not surprising that hummingbirds (range
2-5 g mass, 37-56 mm wing chord) represent not
only the most diverse family (9 species), but aU
the family with the most cases of being trapped
Brooks • BIRDS CAPTURED IN SPIDER WEBS
351
in a spider web (20 cases). The small size ol
members of this family makes them more
vulnerable to web entrapment, especially the
smaller species: six (67%) of the nine species
and 14 (70%) of the 20 cases have a mass 2=4 g
and wing chord ^50 mm. The next smallest birds
trapped in comparison include only three cases in
two families: Aegithalidae (Bushtit. Psaltri parus
minimus: 5 g mass. 40 mm wing chord) and
Regulidae (Goldcrest. Regains regains: 5 g mass.
55 mm wing chord and Golden-crowned Kinglet,
R. satrapa: 5 g mass. 57 mm wing chord).
More than one-half {n = 36) of the cases ol
birds entrapped in spider webs were released
unharmed by the humans reporting the incident.
When these cases were excluded, 73% (» = 22)
died due to web entrapment, and the only cases ol
birds naturally freeing themselves in = 8) were
not wrapped in silk. Consequently, the chance for
a bird to survive web entrapment is affected by its
ability to free itself prior to being immobilized by
the spider. The sheer size of a bird alone could
deter a spider from immobilizing it, as spiders
are often reluctant to wrap prey too large to
successfully consume (Sakai 2007).
\re Spiders and their Webs a Threat to Birds? —
Orb weavers will cut their web to rid it of
undesirable debris (Robinson and Mirick 1971).
However, it is not desirable for a web to be
destroyed by a bird Hying through it, and one of the
many functions of a web is to visually deter birds
from flying into them (Bruce et al. 2005). This was
illustrated by Robinson and Robinson ( 1976) who
described how a tame, experimental Hooded
Butcherbird (Cracticns cassieus) accidentally flew
through a Nephila macula! a web with devastating
results to both the spider with a destroyed web. and
the bird which took several minutes to preen the
web threading from its feathers and was cautious
lor the subsequent 3 weeks. This case details the
consequences to both bird and spider of a web
collision but. more importantly, indicates that webs
do not always serve as visible deterrents to flying
birds. This synthesis presents 69 cases of birds
entangled in spider webs, suggesting that spider
webs can fail as visual deterrents for many species
of birds, concordant with Robinson and Robinson
(1976).
The primary purpose ol venom in most species
of spiders is to subdue insect prey rather than
harm larger species ol vertebrates (Shear 1986).
Certain tarantulas (e.g., Theraphosa, Avirularid)
are sufficiently large to depredate eggs and
nestlings of birds but do not specialize on them
(Shear 1986). Orb weaver size, web radius, and
web height are the most important factors
affecting abundance and size of prey captured;
these same parameters arc important for interspe¬
cific niche separation (Brown 1981). These
spiders catch winged prey in higher webs whereas
larger, jumping insect prey are caught more
frequently at lower strata (Brown 1981). Orb
weavers use a variety of tactics to immobilize
prey. More primitive forms such as Nephila often
bile to subdue their prey whereas Argiope and
Eriophora wrap their prey in silk (Weems and
Edwards 1978). Most research on orb weaver
foraging has shown specialization on insects
(Rypstra 1985. Higgins 1987). Orb weaver
mouthparts are too small to specialize on birds
(Sakai 2007) or lo suggest coevolution for bird
specialization, but orb weavers will opportunisti¬
cally depredate a small bird that gets caught in the
web. This review documents 18 cases of birds
wrapped in silk for consumption, and each case
resulted in death unless freed by a human
observer. A more limited number of cases showed
actual consumption by a spider without the bird
being wrapped in silk (Levy 1987. Peloso and de
Sousa 2007). These cases are contrary' to Gra¬
ham’s ( 1997) speculation that orb weavers do not
prey on birds.
Spider Webs and Natural Environmental Threats
to Birds.— A variety of avian species feed on
spiders and use spider web for nesting material
(Waidc and Hailman 1977); birds in these
situations are likely to be aware ol the web and
do not become entangled (McKenzie 1991). Birds
traveling along direct flight paths, the same open
understory areas favored by orb weavers to build
webs (Graham 1997). are more likely to become
caught, just as a bird can collide with a mist-net.
Trapped birds may have been moving within a lek
site (Sakai 2007). chasing prey, fleeing danger, or
traveling to a new site. Orb weavers are perhaps the
largest arboreal spiders with a web that can attain
>1 in in radius with strong and sticky fresh silk
strands (Lubin 1978. Griffiths and Salanitri 1980).
Over 50 different species of birds (Table 1) have
been trapped in these large webs spanning open
flight paths. Being trapped in a web also makes a
bird vulnerable to predation by a larger vertebrate
predator (Graham 1997), if the bird is not
immobilized by the spiders themselves.
Natural environmental hazards are rare in
nature. Another example besides spider webs is
352
THE WILSON JOURNAL OF ORNITHOLOGY • Vo/. 124. No. 2. June 2012
bird entanglement in plants, which was reviewed
by Hager et al. (2009). They similarly reviewed
the anecdotal literature and found 32 cases of
plant entanglements affecting 25 species of birds,
compared to a much higher 69 cases of spider web
entanglement of 54 species in my study. The
overall size of birds trapped in plants was much
greater with seabirds (e.g.. pelicans, gulls, and
murrelets) and hawks representing one-third of
the cases. Moreover, all but one of those cases
involving larger species resulted in mortality. The
overall mortality rate between the two studies was
similar with 78% (/? = 25) of avian mortalities
due to plant entanglement versus 73% (// = 22) of
30 cases of birds trapped in spider webs that were
not assisted by human observers. More than one-
hall of the cases involved the plant burdock
{Arctium minus ), whereas all birds but one case in
my study were trapped in orb weaver webs.
The number of orb weaver webs increases with
environmental disturbances, such as following a
hurricane (Brooks et al. 2008) or local extinction
of predators which consume spiders (e.g.. Guam;
Haldre Rogers, pers. comm.). The number of webs
could ostensibly increase following environmental
disturbance with environmental instability. This
may increase the number of birds trapped in webs
(Brooks et al. 2008) as spider webs become
concentrated at higher densities.
ACKNOWLEDGMENTS
This research provides an example of the importance c
reporting interesting natural history notes and keeping got:
field records. The data synthesized to examine the reiwrtc
patterns would not have been possible without the caret!
records ot others, including amateur naturalists wh
pubhshed their field notes. | kindly thank the man
^ Wh° rCplietJ to series on NEQORN-l
OKN1TH-L. AfncanBirdtng-L. and BirdingAus-L I ar
grateful to the following individuals for providing unpul
hshed accounts: Fred Beaudry. Gustavo Caban'ne. Pep
Clavajo. Andres Cuervo. Jodie Finley. Dick Foreman. Kcvi
Fraser. Brush Freeman. Kimball Garrett. Don Hadden R„
Hargreaves. Bill Howe, Nicole Michel. Jenny Normar
SiT " S'™ deDMd° Thomi,s R,ecke- Rojas. Bori
r,T Jr;?mart- PaU‘ Srni,h' Peo Ushcr. Philip Vecrmar
Usher. Dirk Van Tucr- ih ^ ^*Ul1 Smi11’' J°hn ,Uckcr. Pc,
gratitude it tended mm ’ ^"cr. M>
permitting access to collections "ldiVidl'a,S fo1
etions or assisting with data
collection: Mary Hart and Christina Riehl (AMNH). Peter
Lowther (FMNH), and Donna Meadows and Marth.. My-
( HMNS). Dave Willard kindly commented on taxonomy
and helpful edits and comments were provided by (Tail
Braun, Monica Brooks. Boh and Maggie Honig P;:;.
Lowther. Christina Riehl. Junclle Mikulas. and Erin Mills
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The Wilson Journal of Ornithology 1 24(2):354— 36 1 , 2012
ENVIRONMENTAL FACTORS AFFECTING NEST-SITE SELECTION
AND BREEDING SUCCESS OF THE WHITE STORK {CICONIA
C/CONIA) IN WESTERN TURKEY
ORTAC ONMU§,' 3 YILDIRIM AGAOGLU,' AND OR HAN GUL1
ABSTRACT. We investigated nest site selection and breeding success of White Storks (Ciconia ciconia) in relation lo
geographical features, weather, and land use in western I'urkey. Locutions of nests in relation to altitude, distance to the
nearest river and stream, slope, and aspect were examined between 2008 and 2010 in Sindirgi District. Population dynamic-
of breeding White Storks were surveyed in the central town in 10X4. 1087. and between 1992 and 21110. WJuteStoib
nested in only 17 of 74 settlements. Twenty-six of 46 nests were occupied in 2010 with a mean density of 1.72 heed®
pairs/knr. Settlements with nests were significantly lower ix ± SD) in elevation (283.3 r 77 t vs 622.5 ± 230.7 m -an!
closer to the nearest river (1.646.2 ± 1.004.5 vs. 4.101.7 ± 3.231.5 m) than settlements without nests. No signified
difference was found between the mean aspects of the settlements and the distances to the nearest stream between iw.*w
groups ol settlements. The number of breeding pairs and fledglings had a significantly decreasing trend througtiou; tk
study period. The number of breeding pairs was positively correlated vs ith the annual total area of crop fields and itef/jv*
com ated with the total at ea ol Iruit production. The number of breeding pairs was positively correlated with to;al and
maximum precipitation in April, but breeding success was negatively correlated with mean total precipitation and m a
maximum precipitation during the breeding season. Received 12 September 201 1. Accepted 26 December 2011.
The White Stork (Ciconia ciconia) is a polytypic-
species that breeds extensively in the Western
Palearctic Region. This species breeds near open
natural or extensively cultivated lowland, wet
grassland or farmland, and high breeding densities
occur along rivers with regularly flooded grass¬
lands (Cramp and Simmons 1977).
The breeding success and productivity of White
Storks have been studied for many years.
Tsachalidis and Goutner (2002) found the growth
rate ol White Stork fledglings depended on food
provisioning rates, parental care, and diet. Tryja-
nowski and Kuzniak (2002) reported population
size and productivity of White Storks were
strongly correlated with the density of common
voles (Microtus arvcilis). Tryjanowski el al.
(2005a) found that water level and livestock were
correlated with productivity and numbers of
breeding pairs. Similarly. Tortosa et al. (1995,
2002) found that rubbish dumps positively
influenced breeding, as well as wintering numbers
of White Storks. There is little quantitative
information on nest site selection of White Storks
Carrascal et al. (1993) found that density of
breeding pairs was negatively correlated with area
ol woodland and scrub habitat, and positively
f B'ol0gy’ Fuculfy of Science, Na
History Museum Research and Application Center
University, 35 1 00 Izmir, Turkey '
BaliI“ri^rSk",ar"’aCy- °f Rcr-Nic. Sindi
1 Corresponding author; e.mail: o,,ac.„„mus@ege.ed
correlated with area of dry and wet grasslands.
Similarly, Nowakowski (2003) found that While
Storks commonly breed close to rivers, and there
was a positive correlation between number of
nestlings raised and the proportion of wel mea¬
dows. peat bogs, and water bodies. Few studies
have examined the importance of other geograph¬
ical parameters in nest site selection by While
Storks and information on nest site preferences
has rarely been quantified.
There is little standardized monitoring and few
studies relating to the conservation of White
Storks despite its high popularity in Turkey Mom
studies are unpublished project reports or theses,
which arc not available to the wider scieuriit-
community. The wide range in estimates of
breeding population size for White Storks in
Turkey ( 1 5. 000-3 5, 000 pairs) also indicates j
deficiency of appropriate data (BirdLife Inten¬
tional 2004). Local population surveys have been
conducted over the Iasi two decades in TurlO
but most are short term focusing on number
breeding pairs and few collect data on nunrn-'f 1
fledglings.
We report on the population of White Sic -
breeding in Sindirgi. western Turkey studied' '
19 consecutive breeding seasons between
and 2010. This is the longest monitoring sl1'
within the country. Our objectives were m.
investigate the effects of altitude, slope, asp6'
and distance to nearest river and stream on ,R‘
site selection of White Storks: and (2) invest^
the influence of environmental factors 11
354
Onntuf el al. • WHITE STORK NEST-SITE SELECTION AND BREEDING SUCCESS 355
weather, land use, drainage, and changes in
electricity transmission) on breeding parameters
(specifically number of breeding pairs, juveniles,
and breeding success).
METHODS
Study Area.— The study was conducted in
Sindirgi, a District of Balikesir Province in
western Turkey (39 14' N, 28 10’ E) (Fig. 1).
The site has a typical Mediterranean climate. The
long-term mean annual temperature is 14.3 C
'mean rwulter = 3 C. mean f,unirncf = 36.3 C).
The annual precipitation is between 600 and
700 mm with highest rainfall in January and
lowest in June and August (Turkish State
Meteorological Service, www.dmi.gov.tr). The
study area covered ~ 1,5 10 knr of which 47%
were forests, mainly Red Pine (Pinus brutia),
European Black Pine (P. nigra), and oak (Quo reus
spp.); 22% arable land (mainly wheat and
tobacco); 20% arid and mountainous zones; 3%
grassland, pastures for grazing, and irrigated
agriculture; and 7% inhabited areas, roads, and
reservoirs (based on data from the Local Admin¬
istration Office in Sindirgi). The mean altitude of
the study area is 830 m (range = 157-1,706 m).
The main rivers in the study area are Simav,
Cuneyt, and Ilicali which How throughout the
year, and Caygoren Lake (700 ha). There are also
numerous small and temporary streams.
Nest-Site Selection.— Nest-site selection was
examined in all inhabited areas (central town
and 73 villages; settlements hereafter) and
throughout the countryside between 2008 and
2010. The locations and boundaries of all
inhabited areas, rivers, and streams were delin¬
eated from a LandSAT image (taken in 2000) of
15 m pixel resolution. A Digital Elevation Model
(DEM) of 30 m pixel resolution was used to
measure mean altitudes and to calculate aspects
and slopes of all the settlements with ArcGIS 9.3.
Aspects were reclassified into four different
categories: North (315 -45 ); East (45 -135°);
South (135 -225 ); West (225 -315°). Slopes
were classified inlo four different categories: flat
(0-5 ). slightly inclined (5.1 -10 ). moderately
inclined (IO.f-30 ). and severely inclined
(30.1 -90 ). The dominant (> 50%) aspect and
slope of each settlement was calculated from these
data. The study am a was visited during mid May
and all active and inactive White Stork nests were
documented. Large obvious nests of the White
Stork are associated with human settlements and it
is highly unlikely that any nests were missed. The
locations of White Stork nests within the study
area were recorded with a Global Positioning
System (GPS) and settlements having at least one
active/inactive White Stork nest were considered
as settlements with nests for analyses. The exact
location of each nest (active or inactive) was used
28°20’E
I
28°40'E
I
Settlements with Stork Nest
— Elevation (m)
. Other settlements
_ _ _ 157 - 250 H 751 - 1000
Streams 251 ’ 500 ■ 1001 - 1250
£3> caygoren Dam ■ 501 - 750 wm 1251 - 1706
fig. 1. Location of the study area in northwestern Turkey and its settlements, rivers, streams, and main altitudinal
features. Settlements with White Stork nests are numbered and indicated differently from the other settlements.
(M = Mountains).
356
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 2. June 2012
in calculating the distance to the nearest river and May. June, and July between 1992 and 2010. Data
to the nearest stream lor villages with nests, while on land use of the study area between 1995 and
the center of the settlement was used for 2009 were obtained from the Turkish Statistical
measurements of those without nests for the Institute (www.tuik.gov.tr) in four categories:
distance to the nearest river or stream. The mean crop fields, vegetable production, fruit production,
altitude of settlements with and without nests was and fallow land. The primary agricultural products
compared with Student’s t- tests and their domi- were crops for human food, animal feed, and
nant aspects, and distances to the nearest river and livestock production. Crop fields were mainly
stream were compared with Mann-Whitney U- grain crops including wheat, cereals, and maize,
tests. Altitude was positively correlated with both Vegetable production consisted of beans, cluck-
d' stance to the nearest river and slope, and pea, lentil, peas, and spinach. Fruit production
separate univariate logistic regression models was mainly tomatoes, peppers, and eggplant,
were used to explore the magnitude of their The annual number of breeding 'pairs. total
e sets on the presence of nests and their Akaike s number of tledglings, and breeding success (mean
Information Criteria (AIC) were calculated. The number of flcdglings/pair) were 'compared with
ogistic distribution and the logit link function both maximum, minimum, mean temperatures, and
were used to obtain the odds ratio. Principal total and maximum precipitation data for each
components analysis was not performed as the month separately (Apr, May, Jun. and Jul) and tor
Kaiser-Meyer-Olkm measure of sampling ade- the entire breeding season (averaging the values of
quacy was . 6. t|lese 4 montflsy ancj wj[h tf,e area 0f each
l he mean standard density of active White agricultural category using correlation analysis.
01 , n^sf-s (StD"pa) m the study area was ealeu- Information on flood control, drainage works, and
ated (Schuz 1952, Nowakowski 2003, Now- changes in electricity distribution schemes in the
akowski and Wasilewska 2006). The structure study area was obtained from the regional office of
on which the nest was placed (nest types) was the General Directorate of State Hydraulic Works
recorded and grouped into three categories: build- (DSI, www.dsi.gov.tr), National Electricity Au-
ing. electricity pylon, and tree. Chi-square tests thority (TEK). and the Regional Electricity Com-
were used to investigate differences between the puny (UEDAS. www.uedas.com.tr), respectively,
nest types ot towns with the villages. Analyses
were conducted using PASW statistical software
(Version 18.0, www.spss.com). The significance
level was set at P < 0.05.
Nest-Site Selection. — White Storks were breed¬
ing in only 17 (23.0%) of 74 settlements. Those
with White Stork nests were significantly lower in
elevation and closer to the nearest river than
settlements without nests (Table 1). The mean
± SD elevation of nests was 283.3 r 77.3 m
(range - 185—436 m). No significant difference
was found between the mean aspects of settle¬
ments and distances to the nearest stream between
settlements with and without nesting White Storks
(P " 0.284 and 0.529, respectively). The number
of settlements with nests increased with decreas¬
ing slope (Table I ). Altitudes and distances to the
nearest river of settlements with and without
White Stork nests varied significantly (Fig. 2).
RESULTS
Breeding Success and Number of Breeding
Pairs.— The total number of nests, number of
breeding pairs (occupied nests), and total number
of fledglings of White Storks were recorded in the
central town in 1984, 1987. and between 1992 and
2010. The study area was visited several times
during each breeding season. We confirmed the
presence ol a breeding pair when we observed at
least one individual constructing, defending,
incubating, feeding chicks, or perching on the
nest (Aguirre and Vergara 2009). We counted the
total number of fledglings when they were about
6 weeks of age. A graph was prepared to docu¬
ment changes in number of pairs and fledglings
throughout the years, and polynomial cubic
regression lines were added based on highest R~
and lowest AIC values.
al . WHITE STORK NEST-SITE SELECTION AND BREEDING SUCCESS 357
Onmu$ et
TABLE 1. Comparison of villages
respect to geographical variables.
with and without active or inactive nests of White Storks in western T urkey with
Factor
With nest*
Without nest* Test stutistics
Univariate OR (95% Cl)
R'
AIC
Altitude (m)
283.3 ± 77.3
622.5 ± 230.7 t = 9.461. P < 0.001
0.988 (0.982-0.994)
0.568
49.04
Distance to nearest
river (m)
1.646.2 ± 1,004.5
4,101.7 ± 3,231.5 U = 222.0. P = 0.001
0.999 (0.999-1.000)
0.269
69.31
Slope (degree)
0-5
10 (52.6)
9(47.4) x2 = 12.976. P < 0.001
12.22 (2.77-54.01)
0.249
70.56
5.1-10
4(21.1)
15 (78.9)
2.93 (0.58-14.77)
10.1-90
3 (8.3)
33 (91.7)
1
Totals
17 (23.0)
57 (77.0)
•= mean and SD far altitude and distance; n. row** for slope. OR = Odds Ratio; Cl = Confidence intervals: R' = percentage of variance explained by the
model; A1C = Akaike's Information Criterion.
The total number of White Stork nests within
the 17 different settlements was 46 and the total
number of occupied nests was 26 between 2008
and 2010 with a standard mean density (StDn,,a) of
1 .72 breeding pairs/km2 (Table 2). The distribution
anti nest types of occupied and empty nests varied
(Table 2). Nests on electricity pylons were signif¬
icantly more frequent in villages, while nests on
buildings were significantly more frequent in the
town. Fifteen (75%) of the nests on buildings were
on chimneys and five (25%) were on roofs.
White Storks at 18 of 19 nests on electricity
pylons were considered to be al high risk of
electrocution, collision or nest fire. Thus, 10
(56%) were relocated and eight (44%) were
replaced. Fifteen (83.3%) of these conservation
actions were accepted by White Storks, one
(5.6%) was not accepted, one (5.6%) was visited
by a pair which was displaced due to a territorial
conflict with the neighboring pair, and no pair was
observed to return from migration at one nest.
Breeding Success and Number of Breeding
Pairs— The total number of nests, breeding pairs
(occupied nests), and fledged White Storks in the
central town decreased over time (Fig. 3). The
total number of breeding White Storks was
relatively stable between 1984 and 1996. How¬
ever, the total number of breeding pairs decreased
from 13 pairs in 1996 to eight pairs in 1997,
and six pairs in 1998. There was a significant
decreasing trend throughout the study period (P <
0.001 ) and only one pair remained in the town in
2010.
Breeding success was negatively correlated
with mean total precipitation (r = -0.557, P =
0.013, n = 19) and mean maximum precipitation
(r = -0.483, P = 0.036) throughout the entire
breeding season, but was not correlated with
mean, minimum, and maximum temperatures
during the entire breeding season. The number
of breeding pairs and number of fledglings were
not conelated with any of the mean meteorolog-
points represent maximum values exceeding outliers.
358
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124, No. 2, June 2012
TABLE 2. Nest locality preferences of White Storks in western Turkey.
Nesl location
Building
Tree
Electricity pylons
Totals
Town n (column %) _ Village n (column <5-) Total n (column %)
13(68.4) 7 (25.9) 20(43.5)
4 (2 Li) 3(11.1) 7(15.2)
2(10.5) 17(63.0) 19(413)
19<4l-3> 27 (58.7) 46 (100.0)
Each nest location category (building, tree. E. pylon, is compared to the total of others due to small sample sizes.
Chi-square /"
0.0042
0.4244
0.0004
ical variables of the breeding season. The number
of breeding pairs was positively correlated with
total (rs = 0.470, P = 0.042) and maximum
precipitation (r, = 0.550, P = 0.015) only in
April. Breeding success and number of fledglings
were not correlated with any of ihe monthly
meteorological variables.
The number of breeding pairs was positively
correlated with the total area of crop fields (r. =
0.619, P = 0.014, n = 15) and negatively
correlated with fruit production (rv = —0.870,
P < 0.001). Breeding success was negatively
correlated with the total area of crop fields (r =
-0.657. P = 0.008).
DISCUSSION
Altitude and distance to the nearest river
strongly influenced nest site selection of White
Storks and had an important role in affecting the
pattern of abundance in our study area similar to
research in Poland (Nowakowski 2003,2006- The
distance covered during foraging trips is important
in affecting provisioning of nestlings (Jolist eral.
2001). Flight behavior studies for some bin!' of
prey during the breeding season strongly indicate
that parents balance energy consumption and
demands of nestlings (Hedenstrom et al. 1999,
Rosen and Hedenstrom 2002). Energy demands of
nestlings and parents are high and parents have lo
commute several times per day between the nesting
site and foraging areas to feed their chicks (Damp
and Simmons 1977). Foraging trips of White
Storks are known to not exceed a radius of 5 km
around the nest (Johst et al. 2001). Balancing
energy demands among parents and nestlings under
unfavorable conditions is important: White Storks
may control intra-brood food distribution which
enables them to invest more in larger siblings or to
control the number of young (Djerdali et al. 2010),
There was no relationship with distance to the
his nega¬
tive trend continues. Management of nest sites
providing support. We also acknowledge Oiner Diimijren
for helping during nesl replacements, and Raika Durusov
and llayal Boyacioglu for assisting with statistical analyse
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Short Communications
The Wilson Journal of Ornithology 1 24(2):362-366. 2012
Prolonged Incubation and Early Clutch Reduction of White Storks
( Ciconia ciconia )
Andrzej Wuczynski1
ABSTRACT.-— Two cases of prolonged incubation
by White Storks I, Ciconia ciconia) were observed in the
same nest m 2009 and 2010 in southwest Poland.
Incubation lasted at least 59 and 65 days, respectively;
i-e- lS4 and 103% longer Lhan the average incubation
period. Extended incubation was accompanied by other
abnormal breeding behavior. The luck of observed
copulation in either breeding season, an extremely short
arrival-breeding interval, and early clutch reduction
suggest the eggs were infertile. This is the first record of
prolonged incubation in the Ciconiidae. and probably
the first record of repeated prolonged incubation by
wild birds. Received 12 September 20/1. Accepted 21
December 201 1 .
extended incubation is preceded or accompanied
by other abnormal behavior which could induct
prolonged incubation. Moreover, there is no
information about an individual bird's tendency
to incubate longer than average. To my best
knowledge, repeated cases of prolonged incuba¬
tion in the same nest or by the same individuals
have not been previously documented in wild
birds.
Prolonged incubation has been recorded for a
number ol bird species (Holcomb 1970. Sutcliffe
1982. Margalida et al. 2006), but is extremely
The incubation period is primarily affected by
the initial egg mass and speed of embryonic
development (Deeming 2002). This period varies
little within the particular species in the case of
fertile eggs (but see Drent 1975). Occasionally,
anomalies in the incubation period occur and the
duration may be extended. Prolonged incubation
is an instinctive behavior, thought to provide a
safety margin for eggs that take longer than
normal to hatch (Skuteh 1962). However, exces¬
sively Iona incubation periods relate to infertile
eggs and the adaptive significance of this behavior
is questionable (Afik and Ward 1989. Kloskowski
1999). The duration of incubation should be as
short as possible due to energy constraints for the
incubating bird (Reid et al. 2002) and increased
mortality risk from predators at the nest (e.e..
Visserand Lessels 2001, Martin 2002, Weidinger
2002, Miller et al. 2007). It remains unclear why
incubating birds fail to recognize infertile eggs.
It is also unknown what causes termination of
incubation. The secretive behavior of parental
birds usually prevents continuous observations,
and available accounts on prolonged incubation
are based on intermittent visits to the nest by
researchers. Thus, it is not known whether
Institute of Nature Conservation. Polish Academy .
Sciences. Lower-S.lesian field Station, Podwale 75. SO-4,
Wroclaw. Poland; e-mail; a.wuczynski@pwr.wroc.pl
rare. This phenomenon occurs regularly only in
the Proeellariiformes (Boersma and Wheelwright
1979. Hu in 1997) and occasionally in the
Podicipedi formes (Kloskowski 1999). An exten¬
sive literature search did not locate reliable
records ol prolonged incubation by White Storks
(f iconiu ciconia) and other Ciconiidae. One case
ol this behavior was observed in western Poland
in 201 1 but exact length of incubation is unknown
(Marcin Tobolka. unpubl. data). Possible cases of
extended incubation should be much easier 10
document for White Storks than for other wild
birds because it is one of the most popular and
charismatic bird species in Europe. The White
Stork is exceptionally well studied (reviews in
Schulz 1998. Tryjanowski et al. 2006). it nest- on
easily observed structures (buildings, chimneys,
poles), and is subject to restoration projects which
include captive breeding (Biber et al. 70<).\
Olsson 2007). Several dozen stork nests in Europe
are monitored on-line with a camera providing
continuous data during the course of the breeding
season (Dolata 2006). However, in-depth infor¬
mation on incubation behavior of this species is
surprisingly scarce. For example, factors affecting
the onset of incubation and quantitative contribu¬
tions of male and female to incubation period are
poorly recognized. Little is known on the length
ol incubation recesses, egg sensitivity to cooling,
or egg reduction by parental birds.
The White Stork has biological attributes
thought to favor prolonged incubation (but not
362
SHORT COMMUNICATIONS
363
supported by empirical data). These features
include: (1) one breeding attempt per year, i.e..
birds which cannot renest are under strong
reproductive pressure: (2) hatching asynchrony,
i.e.. naturally wide variation in incubation dura¬
tion for viable eggs; and (3) low predation risk,
i.e.. low potential costs of incubation (Marks
1983. Margalida et al. 2006). The absence of
reports on prolonged incubation by White Storks
and related species, despite the above character¬
istics. indicate this phenomenon is extremely rare
in the Ciconiidae.
I describe two cases, 1 year apart, of prolonged
incubation, observed in the same nest of the While
Stork. I also describe abnormal behavior of the
breeding pair which may help explain the
prolonged incubation.
METHODS
Study Species.— The While Stork has one brood
per year and the full breeding cycle lasts 1 6 weeks.
The average incubation period is 32 (29-34) days
and usually starts with the second egg. Both mates
incubate, but the female contributes more than the
male. Incubation begins —2 weeks after arrival of
the second partner at the nest. The second partner,
usually the female, arrives on average 4.3 days
later than the first partner (all data after Schulz
1998. Profits 2006).
Field Procedures. — The extended incubation
whs observed in 2009 and 2010 in the village
of Sieniawka (SW Poland. 50 46' N, 16 46' E).
The location is inside a study plot used for long¬
term (since 1989) monitoring of the White Stork
population. The local population is characterized
bv one of the lowest stork densities in Poland
tl.76 pairs/100 knr in 2010) with a continuous
decrease in numbers (x = 1.4 breeding pairs/yr.
1996-2010). and low reproductive success (Wuc-
zyriski 2006a. h). The nest in which the prolonged
incubation was observed was on a pole not con¬
nected to an electric power line. The first breeding
attempt at this site was noted in 1994. The nest
location allowed for consistent and repeated obser¬
vations throughout the breeding season. The
conspicuous breeding habit of the White Stork
provided a unique opportunity to monitor the
behavior accompanying prolonged incubation. The
presence of the birds in the nest and their behavior
was viewed from the ground several times each
day. The area under the nest was inspected for
discarded engs or nestlings. The incubation
duration was established based on the behavior of
the breeding pair: intermittent attentive periods,
turning of the eggs, and parents taking turns
incubating the eggs. Initiation of incubation was
difficult to ascertain due to long but intermittent
periods of sitting on the nest preceding actual
incubation. An additional sign of approaching incu¬
bation was when the birds began to line the nest.
The end of incubation was unambiguously pro¬
nounced when the eggs were thrown out. followed
by the sudden leaving and long absence of the birds.
OBSERVATIONS
The first partner permanently occupied the nest
starting on 18 April 2009. and both partners were
at the nest on 19 April (Table 1). One egg was
discarded (direct observation) immediately after
the second bird appeared at the nest. The
minimum clutch size in the 2009 breeding season
was four eggs, based on the number of discarded
eggs. The latest accepted date for beginning of
incubation was 24 April (possibly 1-2 days
earlier), as this was the date that a tightly sitting
bird was observed. Continuous incubation lasted
59 days until 22 June.
The first arrival date in 2010 was on 29 March
and coincided with consistent nest occupation
by the first partner. The second bird appeared
14 days later. The start of the incubation period
was assumed to be 15 April. Continuous incuba¬
tion lasted 65 days and finished on 19 June. Two
eggs were found under the nest during the course
of the breeding season, which was the minimum
clutch size.
The contents of the eggs which had been
discarded after the end of the incubation period
indicated embryo development did not occur in
either year. The lack of observed copulations was
prominent in both years during the pre-incubation
period. Start of incubation was abrupt, soon after
the arrival of the second partner.
The length of incubation in 2009 and 2010 was
27 and 33 days beyond the normal incubation
period (84 and 103%, respectively). These values
could be slightly higher as the precise starting
point of incubation was not known. The incuba¬
tion period was average in the 2001-2008
breeding seasons, when hatching occurred in this
nest. The nest was not occupied in 201 1.
DISCUSSION
The length of the prolonged incubations
observed is within the range reported for other
species of birds. Margalida et al. (2006) reviewed
364
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124. No. 2. June 2012
I ABLE I. Reproductive timing of the White Stork in breeding seasons when early clutch reduction was noted, and in
two breeding seasons when prolonged incubation occurred (2009-2010).
Breeding variables
First arrival date
Arrival of the first
partner ( =
permanent nest
occupation)
Arrival of the
second partner
Incubation period
Eggs or eggshells
discarded
Last visit at nest
2003
5 Apr (2 birds,
short visit)
14 Apr
17 Apr
—22 Apr-25 May
19 Apr
23 Aug
2005
26 Mar (2 birds,
short visit)
15 Apr
7 May
~16 May-19 Jun
7-8 May (2 eggs).
II Jun
29 Aug
2006
4 Apr
4 Apr
17 Apr
? — -4 Jun
20 Apr. -26
Apr (2 eggs)
25 Aug
2009
13 Apr (I bird.
short visit)
18 Apr
19 Apr (18 Apr in
vicinity)
~24 Apr-22 Jun
19 Apr. 21 Apr, 15-
22 Jun. -28 Jul
17 Aug
2010
29 Mar
29 Mar
12 Apr
— 15 Apr-19 Jun
21 Apr. 19 Jun
18 Aug
the records of prolonged incubation for 18 species
of diurnal and nocturnal raptors. The range of
prolonged incubation found was 33-161% in
excess of the normal period (the average was
94% j. The length of extended incubation in seven
nests of the Red-necked Grebe ( Podiceps gri.se-
gena) was 42-50%’ beyond the average incubation
period (Kloskowski 1999). Cases of extremely
long incubations were also recorded for the Eur¬
asian Wren ( Troglodytes troglodytes), 219% in
excess of the normal period: European Robin
( Erithacus rubeeula )t 243% (Skutch 1962); and
Northern Bobwhile {Colinus virginiunus): 326%
(Hernandez et al. 2006).
There were behavioral indications suggesting
the prolonged incubation in 2009 and 2010 was
caused by laying infertile eggs, rather than
embryo death. First, there was a distinct lack of
copulation by the breeding pairs in both breeding
seasons. 1 did not notice one case of copulating
storks at the site throughout the entire breeding
seasons in 2009 and 2010. despite intensive
observations. The White Stork is a species with
a high copulation rate. The average number of
copulations reaches -200 during the breeding
season with a frequency up to two times/hr
(Tortosa and Redondo 1992, Bochenski and
Jerzak 2006). Copulations at this particular nest
were regularly observed in previous years,
especially in the pre-incubation period.
Second, the period between arrival of the
second partner and beginning of incubation was
distinctly short in both years. The period amount¬
ed to 6 days in 2009, and 3 days in 2010. A
reduced arrival-breeding interval is believed to
enhance breeding success (Fulin et al. 2009)-
however, the recorded values were several times
shorter than average. It takes 12-13 days on
average, before the first egg is laid after the arrival
ol the second partner to the nest in western Poland
(Tryjanowski el al. 2004. Kosicki 2010). The
short period between arrival of the second partner
and beginning of incubation by the observed
slorks, may indicate that some eggs were formed
before being fertilized, even if both birds were
able to breed. However, the lack of copulations in
2009 and 2010 and rapid initiation of breeding
imply that at least one bird was immature or
inlertile. or the pairs were of the same sex.
Production of eggs could also be influenced by
food stress (Deeming 2002). Insufficient food and
low digestive efficiency by the female (Kwie-
einski and Tryjanowski 2009) may cause breeding
stress that leads to production of infertile eggs
Egg losses for White Storks are usually caused
by fights with intruders trying to take over a nest
already occupied by a pair (Profus 2006. Tobdlka
et al. 2011). However. White Stork females may
occasionally lay infertile eggs before the male's
arrival and then throw them out (Schulz 1998).
This happened in 2009; one egg was discarded
after the second partner arrived at the nest. Similar
clutch reduction occurred soon after arrival ot the
Second partner at this nest in previous years. In
2003. one egg was discarded 2 days after the
arrival of the second partner. In 2005. two eggs
were discarded up to I day after the arrival of the
second partner. In 2006, one egg was discarded
3 days after the arrival of the second partner
(Table 1). Regular occurrence of early clutch
reduction has not been reported for the White
Stork. This suggests the nest was repeatedly first
SHORT COMMUNICATIONS
365
occupied by females, which is also unusual in this
species (Bocheriski and Jerzak 2006). These obser¬
vations indicate that early laying of infertile eggs
by the White Stork may occur more regularly than
believed It is possible that in some years laying
infertile eggs may initiate extended incubation.
It is of interest, that prolonged incubation in the
same nest occurred in two consecutive years. It is
probable that in both cases, one or both of the
birds were the same as the previous pair, in view
of the high return rale of While Storks to previous
nest-sites (Chernetsov el al. 2006, Vergara et al.
2006). This could not be confirmed as the
observed storks were unmarked.
Several phenomenon believed to be rare in
birds were documented. To my knowledge, this is
the first record of prolonged incubation in the
Ciconiidae, and probably the first record of
repeated prolonged incubation for wild birds in
the same nest. Prolonged incubation was accom¬
panied by other behavioral abnormalities, based
on continuous nest observations. The breeding
behavior of the parental birds was atypical and
finished with nest failures. This suggests pro¬
longed incubation in the observed White Storks
resulted from a set of factors, related to individual
attributes of the parents which reduced reproduc¬
tive possibilities. Thus, cases of incubation well
beyond the expected hatch date for many species
of birds may be associated with abnormality in
breeding. Behavior accompanying prolonged in¬
cubation is difficult to detect in other bird species,
unlike in the White Stork, and may be unnoticed,
further investigation is necessary to understand
the regulation of incubation behavior of birds,
especially prolonged incubation.
ACKNOWLEDGMENTS
I am grateful to Piotr Profus for help in searching the
stork literature, and for contributing to our discussions on
the issue. I thank C. E. Braun and two anonymous reviewers
for valuable comments on the initial version ol the
manuscript.
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Hun, N. 1997. Prolonged incubation in the Black-browed
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KI-OSKdwski. J. 1999. Prolonged incubation of unhatchable
eggs in Red-necked Grebes ( Poiliceps grisegena).
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Kosicki, J. 2010. Reproductive success of the White Stork
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KwiECINSKl, Z. AND P TRYJANOWSKI. 2009. Differences
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67:559-567 (in Polish, English summary).
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DAvila. 2006. Nesl-sitc fidelity and breeding success
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The Wilson Journal of Ornithology 124(2):366-370. 2012
Stopover Site Fidelity by Tennessee Warblers at a Southern Appalachian
High-elevation Site
David F. Vogt,1 Mark E. Hopey,2 G. Rad Mayfield III,3 Eric C. Soehren,4 Laura M. Lewis,5
John A. Trent,4 and Scott A. Rush6-7
1 84 Cherry Street, Pikevillc, TN 37367, USA.
2 Southern Appalachian Raptor Research, Big Bald Band¬
ing Station. P. O. Box 305. Mars Hill. NC 28754. USA.
4 8 19 Forest Avenue. Orono, ME 04473, USA.
4Elhew Field Station, Wehlc Land Conservation Center,
State Lands Division, Alabama Department of Conservation
and Natural Resources. 4819 Pleasant Hill Road. Midway Al
36053. USA.
U.S. Department of Agriculture, Forest Service. Chero¬
kee National Forest. 2800 Ocoee Street. North. Cleveland
TN 37312, USA.
Great I akes Institute lor Environmental Research, Uni
•sity ol Windsor. Windsor. ON N9B 3P4. Canada
Corresponding author; e-mail: srush@uwindsor.ca
ABSTRACT. — We examined stopover site fidelity
by Tennessee Warblers ( Oreothlypis peregrina) at two
Tennessee handing stations (Whigg Meadow and Big
Bald) operated during fall migration. —1.000 km trom
the nearest breeding areas. We captured and bandd
4.324 Tennessee Warblers at Whigg Meadow from
1999 to 2008 with 14 individuals (0.3%) recaptured in
subsequent years. We banded 5.514 Tennessee War¬
blers at Big Bald from 2003 to 2008 where, despite
relatively close geographical proximity to Whig?
Meadow (< 150 km between sites), no individuals were
recaptured outside of the initial capture year. The*
inter-annual recaptures, to our knowledge, reflect the
highest reoccurrence of a Nearctic-neotropical migraion
SHORT COMMUNICATIONS
367
passerine at a single stopover site. Our results provide
evidence that passerine stopover site hdelity may occur
at considerable distances from both breeding and
wintering areas, and differ between geographically
similar stopover sites. Received 19 May 201 1. Accepted
12 November 201 1.
Stopover site fidelity, or return of an individual
to a location >160 kin from breeding or wintering
areas isensu Nisbet 1969). has been well docu¬
mented among several groups of migratory birds,
including waterfowl (Fox et al. 2002) and
shorcbirds (Gudmundsson and Lindstrdm 1992.
Mimas et al. 2010). However, low return rates to
stopover sites within several groups also suggest
this behavior varies among species. For example,
the fidelity of shorebirds to stopover sites has
been reported to be as high as 54% (Sanderling,
Catidris alba ) (Gudmundsson and Lindstrom
1992), hut remains minimally documented among
other species (Gavrilov et al. 1998, Taylor and
Bishop 2008). Stopover site fidelity by passerines
has been reported, but accounts are largely from
Palearctic-Ethiopian migrants (Nisbet 1969. Calry
etal. 2004) w ith few reports of site fidelity among
Nearctic-neotropical migrants (Nisbet 1969.
Winker 1991. Somershoe and Chandler 2000,
Somershoe et al. 2009).
fidelity to specific stopover sites may provide
advantages similar to those gained from breeding
or overwintering sites, including increased famil¬
iarity with the physical and biological attributes ot
local resources, and predator avoidance (Evans
andTownshend 1988, Catty ct al. 2004. Minias
el al. 2010). However, migrating passerines arc
often flexible in habitat selection, obtaining
critical resources in a variety of habitats (Cantos
and Telleria 1994. Schaub and Jcnni 2001, Catry
et al. 2004). Additionally, songbird movements
during migration can be influenced by wind con¬
ditions. making the need to reorient to a specific
stopover area energetically expensive (Calry et al.
2004).
Flexibility in habitat selection and movements
among stopover sites has been posited as explana¬
tions for the low incidence of stopover site fidelity
By passerines (Catry et al. 2004, Bachler and
Schaub 2007). For example. Nisbet (1969) reported
eight cases where birds had been recaptured at
various stopover sites in subsequent years, and
Winker et al. ( 199 1 ) cited records of 2 1 individuals
exhibiting stopover site lidelity. More recently.
Somershoe et al. (2009) reviewed the literature and
documented stopover site fidelity by 25 individuals
representing nine species. These examples gener¬
ally reflect only a few individuals captured over
periods typically spanning a single year.
Our objective is to report the highest incidence
of stopover site fidelity by a Nearctic-neotropical
migratory passerine', the return of 14 Tennessee
Warblers ( Oreothlypis peregtina) to a migratory
stopover site in the southern Appalachian Moun¬
tains. We also compare inter-year recaptures of
Tennessee Warblers at this study site with another
geographically similar site, drawing comparisons
between the two locations.
METHODS
Study Area. — Tennessee Warblers were studied
at two fall migration banding stations in eastern
Tennessee: (1) Whigg Meadow Banding Station
(35 18’ N, 84 02' W; elevation: 1 ,490 m: Monroe
County), and (2) Big Bald Banding Station (36 01 '
N. 82 42' W; elevation: 1,640 m: Unicoi County;
Fig. I ). Both stations are on high-elevation grass¬
lands or ‘balds’ (Whigg Meadow: 3 ha; Big Bald:
22 ha), and are -140 km apart (Fig. I). The
dominant habitat type at both sites was torest-edge
ecotone transitioning between open grassland and
northern hardwood forest. The forest community
consisted primarily of young (<50 yrs of age),
second growth or stunted American beech (bogus
grundi folia). yellow birch (Retula ulleghuniensis),
sugar maple ( Acer saccluinon), northern red oak
(Quercus rubra), and hawthorn (Crataegus spp.).
The margins of meadows were surrounded by a
dense thicket of smooth blackberry (Ruhus cana¬
densis) with scattered highbush blueberry (Vaccin-
iunt corymbosum).
Field Procedures. — Tennessee Warblers mi¬
grate through our study sites from late August
through early October and represent the most
numerous captured species at both banding
stations (Table 1). We evaluated capture data
collected from 1 to 30 September 1999-2008 at
Whigg Meadow and from 1 to 30 September
2003-2008 at Big Bald. Mist-netting and banding
were conducted following Ralph et al. (1993).
Mist nets used at both Whigg Meadow (n = 9)
and Big Bald (n = 16) were primarily 12-m long
with 30-mm mesh and spaced —15 to 20 m apart.
Mist nets were usually opened tor at least 6 hrs
per day. typically from sunrise until early
afternoon. All captured birds were banded with
368
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 2. June 2012
known breeding an»e T T w u ' h,Sh-eIevation Ending stations in eastern Tennessee, relative tot!
abu ndance ^ num be^coi n t IT™ ^ forests' M*p coloration reflects patterns of region,
abundance (number counted) obtatned from counts conducted along Breeding Bird Survey routes (Sauer et al. 2004).
USGS aluminum bands, and classified to age and
gender following Pyle (1997).
RESULTS
We captured and banded 4,324 Tennessee
Warblers at Whigg Meadow from 1999 to 2008;
14 were recaptured in subsequent years at this site
(0.3%), including one individual recaptured in
two different years. The median value among all
recapture intervals was 1 year with the maximum
interval of 5 years (3 individuals). All but two
recaptures were hatch-year birds when first
captured. We banded 5,514 Tennessee Warblers
at Big Bald from 2003 to 2008 and none was
subsequently recaptured.
DISCUSSION
Our finding of 14 returns is unprecedented for
migrant Parulidae. However, despite the relatively
large number of inter-year returns, only a small
percentage of Tennessee Warblers used the same
stopover site during successive autumn migra¬
tions. This finding supports previous studies
which, although reporting higher incidence or
stopover site fidelity (i.e., 3.6%. Tennessee
Warbler; 3.2%, Yellow Warbler [Seiophagd
petechial; 3.5% Blackpoli Warbler (5. srruita]
(Nisbet 1969]). are limited to evidence drawn
from a smaller number of individuals (all cases ^
4). Some studies have reported intervals of up to
5 years (our study) between inter-annual recap¬
tures at some stopover sites (3 years; Magnolia
Warbler | .S'. magnolici\: Goodpasture 1979;
3 years: Northern Waterthrush [Parkesia now-
boracensis]: Somershoe et al. 2009). but most an.’
limited to periods spanning 1 year.
The limited suite of passerines thaf have been
I mind to be site faithful suggests this behavior
may be relatively unique among this group of
birds. If migratory species such as Tennessee
Warblers follow relatively narrow migratory
SHORT COMMUNICATIONS
369
TABLE 1. Five most common species banded by site
and total recaptures for each species at two high elevation
migration banding stations in Tennessee. USA,
Tola) species captured = 7-1
Whigg Meadow (1999-2008)
Tola) captured
Number of intomnnual
recaptures
Tennessee Warbler
Oreothlypis peregrina
4,324
14
Swainson's Thrush
Catliarus ustulaius
855
0
Black-throated Blue Warbler
Selophaga caerulescens
795
0
Dark-eyed Junco
Junco hxemalis
780
0
Ovenbird
Seiurws aurocapilla
437
0
Total species captured = 80
Big Bald (200.V2008)
Total captured
Number of inter-annual
recaptures
Tennessee Warbler
5,541
0
Swainson's Thrush
2,484
0
Black-throated Blue Warbler
1,631
0
Cape May Warbler
Selophaga tigrina
674
1
Ovenbird
587
0
routes it could be expected that some individuals
would show up repeatedly between years at some
stopover locations. The low incidence of stopover
site fidelity bv most passerines may reflect their
flexibility in selecting migratory routes (Catty et
al. 2004). For instance, wind conditions during
migration may cause migrating passerines to drift
from their intended path. Adjusting for this drift
might require additional energy, which may
exceed the benefits of returning to a familiar
stopover location during some years. Despite
potential limitations to passerine stopover site
fidelity, the high incidence of inter-annual recap¬
tures of Tennessee Warblers at Whigg Meadow
could provide evidence of a specific migratory
route over the southern Appalachian Mountains
lor this species.
Most migration banding stations along coastal
and inland migration pathways in North America
report fewer captures of Tennessee Warblers than
reported here (J. Woodcock, R. Keith, and E.
Soehren; pers. comm.). Our data highlight the
southern Appalachian Mountains as an important
migratory route for this species (Rimmer and
McFarland 1998). Research addressing the role of
-southern Appalachian habitats, such as high
elevation balds and adjacent scrub forest, in
supporting songbird migration is needed. The
placement of additional migratory monitoring
stations, coupled with passive monitoring tech¬
niques such as acoustic monitoring arrays (Blum-
stein et al. 2011) could provide more information
on the importance of these stopover locations.
The between-year recaptures of 14 Tennessee
Warblers at Whigg Meadow provides additional
evidence that some individuals of this species
exhibit stopover site fidelity. These findings
require interpretation of the suite of factors that
shape this behavior in this and other migratory
passerine species.
ACKNOWLEDGMENTS
This research was made possible through the assistance
of numerous volunteers. Funding anti logistical support was
provided by the USDA Forest Service. Cherokee National
Forest and a Katherine A. Goodpasture Award from the
Tennessee Ornithological Society. We are indebted to Scott
Somershoe and two anonymous reviewers for comments
provided on earlier drafts of this manuscript.
LITERATURE CITED
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permanent local emigration and encounter technique
on stopover duration estimates as revealed by
telemetry and mark- recapture. Condor 109:142-154.
BLUMSTEIN, D. T.. L>. .!. MENNILL, P. Clemins, L. Girod.
K. Yao. G. PATR1CEI 1.1, J. L Deppe. A. H. Krakauer.
C. Clark, K. A. CoktopaSSI, S. F. Hanser. B.
McGowan. A. M. An. and N. G. Kirschel. 2011.
Acoustic monitoring in terrestrial environments using
microphone arrays: applications, technological con¬
siderations and prospectus. Journal ot Applied Ecol¬
ogy 48:758-767.
CANTOS. F. J. AND J. L. TELLERI'a. 1994. Stopover site
fidelity of four migrant warblers in the Iberian
Peninsula. Journal of Avian Biology 25:131-134.
Catry, P.. V. Encarncao, A. Araujo, P. Fearon. A.
Fearon, M. Arm run, and P. Delaloye. 2004. Are
long-distance migrant passerines faithful to their
stopover sites? Journal of Avian Biology 35:170-181.
Evans. P. R. and D. J. Townshend. 1988. Site faithfulness
of waders away from the breeding grounds: how
individual migration patterns are established. Proceed¬
ings of the International Ornithological Congress
19:594-603.
Fox. A. D„ J. O. Hilmarsson. O. Einarsson, A. J.
Walsh, H. Boyd, and J. N. Kristiansen. 2002.
Staging site fidelity of Greenland White-fronted
Geese Anser albifrolts flavirostris in Iceland. Bird
Study 49:42-49.
Gavrilov, E. I„ S. N. Erokhov. and A. E. Gavrilov.
1998. Between-year recapture rates of waders ringed
on migration in south-eastern Kazakhstan: constancy
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in timing and location of fly way routes. International
Wader Studies 10:414-416.
GooDPAsri’RF, K. A. 1979. A transient Magnolia Warbler
returns. Bird-Banding 50:265.
GUDMUNDSSON, G, a. and A. LindstrOm. 1992. Spring
migration of Sanderlings Calidris alba through SW
Iceland: wherefrom and whereto? Ardea 80:315-326.
Mimas. P„ K. Kaczmarek, R. Wiodarczyk. T. Janis-
7i avski. and R. Bargif.l. 2010. Feeding conditions
determine return rates to stopover sites of inland
waders on autumn migration. Ibis 152:840-844.
Nismrr, I. C T. 1969. Returns of transients: results of an inquiry.
Fasten 1 Bird Banding Association News 32:269-274.
Pylk. P. 1997 Identification guide to North American birds.
Part I, Slate Creek Press. Botinas, California, USA
RAt.m, C. J„ G. R. Guera., P. Pvi e, T. E. Martin, and
D. F DeSaNTE. 1993. Handbook of field methods for
monitoring landbirds. USDA, Forest Service, General
Technical Report PSW-GTR-144. Pacific Southwest
Research Station, Albany. California, USA.
RtMMliR, c. C. and K. P. McFarland. 1998. Tennessee
Warbler (Vermivora peregrina). The birds of North
America. Number 350.
Sal er. J. r.. j. h. Hines, and J. Fallon. 2004. The North
American Breeding Bird Survey, results and analysis
1 966-2003. Version 2004.1. USGS. Patuxent Wildlife
Research Center. Laurel. Maryland, USA.
SctiAL'b. M, and L. Jenni. 2001. Variation of fuelling rates
among sites, days and individuals in migrating
passerine birds. Functional Ecology 15:584-594
SOMERSHOE, S, G. AND C. R. CHANDLER. 2000. SlOpOVcr-
site fidelity of migrant songbirds along the Georgi„
coast. Oriole 65:7-9.
SOMERSHOE, S. G„ D. G. COHRS. AND D. A. Cohrs. 2009.
Stopover-site fidelity at a near-coastal banding site in
Georgia. Southeastern Naturalist 8:537-546.
TaYI.or. A. R. and M. A. Bishop. 2008. Stopover site
fidelity of a Western Sandpiper on the Copper River
Delta, Alaska. Waterbirds 31:294-297.
Winker. K.. D. W. Warner, and A. R. Weisbrod, 1991.
Unprecedented stopover site fidelity in a Tennessee
Warbler. Wilson Bulletin 103:512-514.
The Wilson Journal of Ornithology 1 24(2):370— 374. 2012
Female Song in the Common Yellowthroat
Conor C. Taff," Katherine A. Littrell,1 2 and Corey R. Freeman-Gallant2
ABSTRACT. — A mated female was observed sing¬
ing in a color-banded population of Common Yellow-
throats ( Geothlypis trichas) in New York State in 201 1.
This female continued to sing, often concurrently with
her mate, for 1 week, at which time she completed
nest construction and was not observed singing for the
remainder of the season. Her song did not resemble anv
normal Common Yellowthroat song or vocalization. No
previous publications have described female song in this
species; common explanations for female song in other
species include abnormally high testosterone levels,
development ol male-like characteristics with age, and
increased territory defense demands at high densities.
We found little support for any of these hypotheses, as
our singing female was within the normal range for
breeding density, testosterone, morphology, ornamen¬
tation. and several physiological parameters. Wc did not
know the age of our female and could not discount old
age as a cause of singing: however, other known-age,
old females in the population were not observed
1 Animal Behavior Graduate Group and Department of f
luti on and Ecology. University of Califomia-Davis, f
Shields Avenue. Storer Hall. Davis. CA 95616. USA
Department of Biology. Skidmore College, Sarai.
Springs. NY 12866, USA.
Corresponding author; e-mail: cctaff@ucdavis.edu
singing. The potential explanations for singing serm
inadequate in this case and the female may have been
anomalous in some dimension that we did not measure,
or a combination of factors may have contributed to the
behavior. Alternatively, female song may be functional
but only used in rarely observ ed social situations in this
species. Received 24 October 2011. Accepted N
January 2012.
Female song is either rare or unreported in most
species of temperate breeding birds despite the
frequency of female song and male-female duets
in tropical birds. Temperate wood-warblers gen¬
erally follow this pattern, as males of most species
sing repeatedly throughout the breeding season m
defend a territory and attract mates, while females
usually do not sing (Spector 1992). However,
atypical female singing has been observed on rare
occasions in at least 1 1 temperate breeding wood-
warbler species from six different genera (re¬
viewed in Spector 1992, Gilbert and Carroll 1999,
Ogden et al. 2003). Several explanations for
atypical female singing have been proposed, and
it is possible that more than one process could act
SHORT COMMUNICATIONS
371
in concert. First, female singers may have
anomalously high androgen levels, resulting in
the development of male-like characteristics (e.g.,
Baldwin et al. 1940, Byers and King 2000).
Similarly, song may develop in older females that
have begun to acquire more androgen-mediated,
male-like characteristics (Nolan 1978). Alterna¬
tively. atypical female singing may be functional,
but only used by a limited number of individ¬
uals in specific situations, for example, at high
breeding densities (Hobson and Sealy 1990) or
during pair-bond formation (Gilbert and Carroll
1999).
The most frequent vocalizations of the Com¬
mon Yellowthroat, ( Geothlypis trichas), have
been well studied; males produce two main non¬
singing calls, chips and rattles, along with two
songs, a commonly repeated perch song and a less
frequently used flight song (Wunderlc 1978,
1979; Kowalski 1983; Ritchison 1991, 1995;
Guzy and Ritchison 1999). Females also chip
and produce infrequent rattles (CCT. pers. obs.).
Female Common Yellowthroats also have been
observed singing on rare occasions (pers. comm,
from B. E. Byers to D. A. Spector; Spector 1992)
but. to the best of our knowledge, no previous
publications have described their song or provided
recorded evidence of their singing. We observed
one potentially singing female in 2010 (KAL,
pets, obs.), and a confirmed singer in 2011 in
observations of 141 individual females over
7 years. We compare measurements of morpho¬
logical. physiological, and plumage characteris¬
tics of the 201 1 singing female with those of
typical males and females at our study site, and
discuss the implications these measurements may
have on understanding reasons for atypical female
singing.
METHODS
We monitored a breeding population of Com¬
mon Yellowthroats in Saratoga Springs, New
York. USA (43° 10' 24.6" N. 73 53' 19.7" W)
from early May to late July 2011. Yellowthroats at
our study site had been closely observed for seven
breeding seasons (2005-2011). All adults were
captured and banded each year with a U S.
Geological Survey aluminum band and a unique
combination of colored plastic leg bands. We
collected information at time of capture on bib size
and coloration, and morphology. We also collected
blood samples to measure hematocrit and paternity
following Freeman-Gallant et al. (2010. 201 1) and
Taff et al. (201 1 ). We used plasma from our blood
samples to measure total antioxidant capacity and
testosterone levels with commercially available
microplate kits (total antioxidant capacity: Cayman
Chemical, Ann Arbor. MI. USA; testosterone:
Enzo Life Sciences. Furmingdale. NY. USA). We
mapped the boundaries of each breeding territory
and measured the distance from the centroid of
each territory to the centroid of nearby territories.
We calculated breeding density as the number of
territories with centroids <300 m from the centroid
of each focal territory.
We recorded the singing female with a
Sennheiser ME 66 shotgun microphone and a
Sony MZ-M200 Hi-MD recorder. The archived
recording is available through the Macaulay
Library at Cornell University (www.macaulay
library.org. catalog number: ML Audio 166385).
We monitored only one singing female and were
unable to perform statistical tests to evaluate
possible associations between female singing and
correlated parameters. We compared the traits ot
the singing female with the average trait values
for all males and females breeding at our site in
2011. Specifically, we compared measures for
trails relevant to three hypotheses for female
singing: (1) acquisition oi male-like traits (wing
and tarsus length, bib size and coloration), (2)
high androgen levels (plasma testosterone), and
(3) functional singing at high breeding density
(neighborhood density). We also compared
several other traits as potential indicators the
singing female was anomalous in some way that
was not accounted for by the three hypotheses
considered imass, total antioxidant capacity, and
hematocrit).
RESULTS
Wc monitored 141 individual females in the
7 years that we studied our field population. Many
of these females returned to the study site over
multiple years and wc observed 193 female
breeding attempts. One female may have sung in
2010 (KAL, pers. obs.), but this observation was
not confirmed and we were unable to obtain a
recording. Only the female observed in 201 1 sang
conclusively. Thus, female song appears to be rare
in this species.
We first observed this female singing on 27
May 2011. The female continued to sing each day
until 2 June 2011, at which time she had
completed nest building. We did not observe the
female singing again after that date for the
372
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 2. June 2012
remainder of the breeding season, includin
during construction of a replacement nest alk
her first nest had been depredated. The femal
sang a total of 29 songs in a I -hr observation fror
0715 to 0815 hrs on 31 May 2011, mostly Iron
the top of a bush. The female's mate also sanj
from a nearby perch in the top of another bus!
during the same period. We did not see the femal,
singing and carrying nest material on the saint
day and it is unclear if these behaviors over
lapped. The female successfully built and laic
eggs in two nests during the breeding season anc
was apparently physiologically capable of repro¬
ducing. We were unable, however, to collect data
on her nestlings: the first nest was depredated
during the egg laying stage, and the second was
depredated after the eggs had hatched, but before
the nestlings had fledged or been sampled.
The female s song did not resemble a typical
Common Yellowthroat male song. Male songs
consist of a series of clear repeated phrases with
rapid frequency modulation across a wide band¬
width (Fig. 1A). The female’s song also had
repeated phrases and limited frequency modula-
lon, but had a raspier quality and noisier syllables
I'g a! , Ti,IS song was dwsimilar froni |he
broadband chips and rattles typically given by
males and females (Fig. IC, D) ^
We do not know the age of the singing female,
but she was a first time breeder at our site.
Females usually move <400 m between years at
our study site (CCT, unpubl. data) and, because
much of the study site is surrounded by
unsuitable woodland habitat, unhanded birds
generally are assumed to be first time breeders.
However, the singing female's territory was near
one end of the site where unmonitored territories
are accessible across a road. We estimate 2-3
additional territories were within 400 m across
the road and we cannot discount between-season
dispersal by an older female from the unmoni-
tored area.
The singing female was within ±1 SD of the
mean for wing and tarsus length, and bib size and
coloration ( Table 1 ). She had somewhat less mass
than the average females in the population (1.9
SD below the mean: Table 1 ). This difference was
most likely caused by an earlier than average
capture date, rather than smaller body size; the
lemale was captured just after arriving from
migration whereas many other females were
captured after they had been in breeding areas
lor 2 weeks or more and some may have been
gravid. Her territory was in an area with a typical
breeding density for our site. The female's
physiological measures (hematocrit, testosterone.
SHORT COMMUNICATIONS
373
TABLE 1. Trails of male and female Common Yellowthroats breeding at Saratoga Springs, New York, USA in 201 1 in
comparison to ihe singing female. The measure for each trait is shown for the singing female and the number of standard
deviations from the mean of other breeding females and males.
Rdtiant hypmheses
Trail
Breeding males
Breeding females
Singing female
n
X = SD
n
X ± SD
Obs.
SD from F
SD from M
Mass (g)
37
10.1 ± 0.35
23
10.8 ± 0.78
9.3
-1.9
-2.3
Male-like
Tarsus (mm)
37
19.9 ± 0.48
24
19.5 ± 0.61
19.2
-0.5
-1.5
Male-like
Wing (mm)
37
54.9 ± 1.26
24
51.8 ± 1.40
51.0
-0.6
-3.1
Male-like
Bib (mm1)
37
671 ± 161
24
397 ± 142
283
-0.8
-2.4
Male-like
UV B.a
37
10.0 ± 2.24
24
3.5 ± 2.96
3.8
0.1
-2.8
Male-like
Yellow B.“
37
31.2 ± 3.42
24
24.9 ± 4.30
24.7
-0.1
-1.9
Male-likc
Bih Cc„c
37
0.91 ± 0.04
24
0.84 ±0.10
0.89
0.5
-0.5
Hematocrit11
34
0.53 ± 0.04
22
0.45 ± 0.04
0.47
0.7
-1.5
TAC
34
1 .6 ± 0.55
22
1.9 ± 0.69
1.0
-1.3
-1.1
Androgens
T
23
3.3 ± 1.45
9
1.7 ± 0.82
2.6
1.2
-0.5
Functional
Density*
23
4.0 ± 1.90
23
4.0 ± 1.90
2
-1.1
— 1.1
" l:V brightness of bib feathers: average refleclanee from 320 to 400 nm.
h Yellow brightness of bib feathers: average reflectance from 550 to 625 nm.
r Carotenoid chroma of bib feathers: ( Reflectance,,,! Reflectance^i/ReflectanceToo-
“ Ratio of blood cells to plasma: (blood cell volume + plasma Vwhole sample volume.
Total antioxidant capacity: measured in antioxidants iniM).
Testodcrone: measured in pg/ml.
8 Number of neighboring pairs holding a territory with centroid to centroid distance <300 in.
and total antioxidant capacity) were normal for
females in our population (Table I ).
DISCUSSION
Rare but regular observations of singing females
occur in many species where only males normally
sing, The persistence of these observations has led
to speculation about the causes of atypical female
singing. However, the scarcity of observations does
not allow hypotheses to be evaluated because the
relevant correlates have not been measured. We
had observations of only a single singing female
hut measured covariates that were relevant to most
of the proposed explanations for atypical female
singing. We found no compelling evidence that any
proposed hypothesis was adequate to explain
singing by the female yellowthroat wc observed,
and the basis for atypical female singing remains
unclear.
The most commonly accepted explanations tor
atypical female singing arc an over-expression ol
androgens or the acquisition of male-like traits by
older females (Baldwin et al. 1940. Nolan 1078,
Byers and King 2000). Our singing female’s
testosterone levels were no higher than those in
other females at our study site that did not sing.
She may, however, have had high levels ot
androgens during critical developmental stages
before our observations. Alternatively, she may
have had abnormally high sensitivity to the effects
of androgens; in this case, even normal levels of
testosterone may have been sufficient to produce
song. Finally, although our singing female’s
measured testosterone was not abnormal, it was
relatively high, and this may have predisposed her
to sing based on factors that were not measured 01-
in combination with other traits. Thus, we cannot
rule out the possibility that testosterone had a role
in her singing. Both the unconfirmed singer in
2010 and the singing female in 2011 were first-
lime breeders at our site, and may have been
young. We observed eight breeding females 4 or
more years of age (extremely old lot females in
this species) in previous years and we did not
observe singing in these older individuals. None
of the morphological traits we measured lor this
female (i.e.. wing and tarsus length and parame¬
ters associated with bib size and color) was 'male-
like*. further suggesting that age- and androgen-
related hypotheses are not adequate explanations
for singing in this case.
Common Yellowthroats have been well stud¬
ied and female song is unlikely to have been
routinely missed. However, if females use song
only during short windows each breeding season,
female song may not be as rare as previously
suspected. The female that we observed in 201 1
sang repeatedly for only 5-6 days and the
suspected singing female in 2010 sang much
less frequently and for only 2-3 days. Females in
both cases sang a highly abnormal song that
would not be easily recognized as a Common
374
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 2. June 2012
Yellowthroat by a casual observer. The singing
female yellowthroat mentioned by Spector
(1992) also sang a raspy, non-species typical
song (B. E. Byers, pers. comm.). Additionally,
all three sang during the pair formation stage of
the breeding season and were not heard after
nesting. Gilbert and Carroll (1999) suggest the
atypical song they observed by a female Wilson’s
Warbler ( Cardellina pusilla) may have functioned
during an extended period of pair bond formation
and maintenance. Our female sang for only a few
days, but the timing of singing suggests the
behavior could have a similar function in pair
bond formation in yellowthroats.
The female that we observed appeared to be
typical in all measured parameters except for
singing. Our study provides no evidence that
androgens, age, or breeding density had a role in
inducing song. It is possible that song is functional
in pair bond formation but it is apparently rarely
used, as previous researchers have not reported it.
Even if functional, it is unclear why this particular
female sang when most females did not. Ulti¬
mately, die explanations available seem inade¬
quate and this female may have been anomalous
in some dimension that we did not measure.
ACKNOWLEDGMENTS
We thank L. M. Duval and F,. A. Krasner for help with
field observations and recordings, and W. M. Gilbert and an
anonymous reviewer for comments that improved the
manuscript. A National Science Foundation Graduate
Research Fellowship to CCT supported this work. Research
was conducted under Skidmore College Animal Care and
Use Committee protocol #69 and the University of
Califomia-Davis 1ACUC protocol #16362.
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Effects of testosterone propionate on female roller
canaries under complete song isolation. Experimental
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Dunn. L. A. Whittingham. and S. M, Tsang, 2010.
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and condition-dependent signaling in the Common
Yellowthroat. Evolution 64:1007-1017.
Freeman-Gallant, C. R.. J. Amidon, B. Berdv, S. Was.
C. C. Taff. and M. F. HaussmaNN. 2011 Oxidative
damage to DNA related to survivorship and carwen-
oid-based sexual ornamentation in the Common
Yellowthroat. Biology Letters 7:429-432.
Gilbert. W, M. and A. F. Carroll 1999. Singing in a
mated female Wilson's Warbler. Wilson Bulletin III:
134-137.
GU7.Y, M. J. and G. Ritciuson. 1999. Common Yellow-
throat ( Geoihlypis trie has). The birds of North
America. Number 448.
HOBSON, K. A. and S. G. Sealy. 1990. Female song in the
Yellow Warbler. Condor 92:259-261.
Kowalski, M. 1983. Factors affecting (he performance
of flight songs and perch songs in the Common
Yellowthroat. Wilson Bulletin 95:140-142.
Nolan Jk., V. 1978. The ecology and hehavinr of the
Prairie Warbler, Dendroiea discolor. Ornithological
Monographs 26.
Ogden, L. J. E.. D. L. H. Neudorf. T. E. Prchfr. and
B. J. M. Stutchbury. 2003. Female song in me
Hooded Warbler. Northeastern Naturalist 10:457-464.
RlTCHJSON, G. 1991. The flight songs of Common
Yellowthroats: description and causation. Condor
93:12-18.
Ri rr 1 1 ison, G. 1995. Characteristics, use and possible
functions of the perch songs and chatter calls of male
Common Yellowthroats. Condor 97:27-38.
Spector, D. 1992. Wood- warbler song systems: a review
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9:199-238.
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L. A. Whittingham. 2011. Relationship between
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Wunderle Jr., J. m. 1978. Differential response of
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SHORT COMMUNICATIONS
375
The Wilson Journal of Ornithology 1 24(2):375— 379, 2012
Nesting Density of Hermit Thrushes in a Remnant Invasive Earthworm-free
Portion of a Wisconsin Hardwood Forest
Scott R. Loss1-2
ABSTRACT— I observed an exceptionally high
density of Hermit Thrush (CiUharits guttatus) nests
3.1 nests/ha) over two breeding seasons in an isolated
1.3-ha portion of an earthworm-free study site in the
Chequamegon-Nicolet National Forest. Wisconsin. This
density was much greater than the 0.1 to 0.6 ncsts/ha
observed over the rest of the study area and exceeds hv
an order of magnitude most previously reported
estimates for this species. The mean distance among
Hermit Thrush nests in earthworm-free sites (215 m:
95% Cl = 180-250 m) was lower than in invaded sites
(250 m; 95% Cl = 236-264 ml: this difference was
not statistically significant. Nest density did not differ
significantly between categories. An abundance ol
suitable nest sites in a favored nesting substrate
(clubmoss: Lycopodium spp.) could have contributed
to the exceptionally high density of Hermit Thrush nests
observed. High Hermit Thrush nest densities may occur
in association with forest Hour conditions that are
characteristic of earthworm- free areas. Received 3
August 2011. Accepted 1 6 January 2012.
Invasive European earthworms (Lumbricus
spp.) are spreading through north temperate
hardwood forests of North America that were
previously glaciated and historically earthworm-
free (James 2004). Lumbricus earthworms alter
soil structure and the seed bed. and consume the
leaf litter layer (Hale et al. 2005). These changes
result in reduced cover and diversity of herba¬
ceous plants and tree seedlings, and a preponder¬
ance of disturbance-adapted sedges and grasses
(Hale et al. 2006. Holdsworth et al. 2007a).
Ground-nesting passerines are also affected by
earthworm-caused habitat changes. Density ot
singing male Hermit Thrushes (Cat hurus gallants)
and Ovenbirds ( Seiums aurocapilla ) is reduced by
Lumbricus invasions at the scale of 10 to 20-ha
forest stands, and Ovenbird nest success is
reduced in relation to decreased litter depth and
increased sedge cover caused by Lumbricus in
'Conservation Biology Graduate Program, University ot
Minnesota, 1980 Folwcll Avenue, St. Paul, MN 55108, USA.
'Current address. Smithsonian Migratory Bird Center.
National Zoological Park. P. O. Box 37012 MRC 5503,
Washington, D.C. 20013, USA: e-mail: LossS@si.edu
hardwood forests ot Wisconsin (Loss and Blair
2011). Relationships between invasive earth¬
worms and nest success and nest density of other
ground-nesting species, including Hermit Thrush¬
es, are unknown.
Density of Hermit Thrush breeding territories is
highly variable across the species' range (Jones
and Donovan 1996; Table I). Density estimates
front most Hermit Thrush studies are based on
indirect observation of breeding activity (e.g., spot
mapping surveys), and few studies report density
based on direct nest observations. Habitat factors
influencing variation in Hermit Thrush density are
poorly understood, but nest locations are likely
selected based on concealment from predators
(Flaspohler et al. 2000), abundance of suitable
nest sites in potential nest patches (Martin and
Roper 1988), and habitat in the surrounding
landscape (Flaspohler et al. 2001). The above
factors are thought to interact with predator
communities to influence nest predation rates
(Martin 1993).
Lumbricus invasions substantially alter forest
floor habitats, and it is possible they influence
Hermit Thrush nesting locations and territory
densities. My objectives were to: (1) report
observations of exceptionally high nesting density
of Hermit Thrushes in an isolated earthworm-free
forest stand in the Chequamegon-Nicolet National
Forest in northern Wisconsin, and (2) compare
Hermit Thrush nest density and nest success
between Lum^r/cus-invaded and Lumbricus-ixte
forest stands.
METHODS
I conducted Held research at six study sites in
2009 and 2010 in the Chequamegon-Nicolet
National Forest in northern Wisconsin (46 N,
91 W) that were a subset of 10 sites used for an
analysis of Ovenbird nesting success relative to
earthworm invasions (Loss and Blair 2011). The
sites were selected based on status of earth¬
worm invasion ascertained during previous work
(Holdsworth et al. 2007a); three sites were
376
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124, No. 2, June 2012
TABLE I. Estimates of Hermit Thrush territory densities (some estimates were converted to density/ha to facilitate
comparison with current study).
Geographic location
Density (per ha)
Source
Wisconsin
0. 1-3.1
Direct observation of nests
Arizona
1.9
Spot mapping
Wisconsin
0.8
Direct observation of nests
Nova Scotia
0.6
Spot mapping
Colorado
0.2-0.3
Spot mapping
Wyoming
<0.1
Strip transect counts
California
<0.1
Spot mapping
Michigan
<0.1
Direct observation of nests
Study
Current
Franzreh and Ohmart 1978
Flaspohler et al. 2001
Morgan and Freedman 1986
Snyder 1950
Salt 1957
Bock and Lynch 1970
Pettingill 1930
invaded by Lumbricus earthworms (average
biomass = 5.74 g/m), and three were effectively
earthworm-free (i.e., either containing no earth¬
worms or only Dendrobaena octaedra , a small
species with comparatively minor effects on the
forest floor) (average biomass = 0.05 g/m').
Follow-up sampling at all sites in 2008 indicated
they had not changed invasion status (Loss and
Blair 201 1 ). Four of the original 10 sites were not
used; two had variable invasion status within the
site and two had only one Hermit Thrush nest
found in each year. Sites were 10-20 ha in size, at
least 2 km from each other, and all were in sugar
maple ( Acer sacchartmi)/ basswood (Tilia ameri-
cana) forest stands >60 years of age that had
experienced no timber management in the last
40 years and were on sandy-loam or loamy-sand
soils (Holdswonh et al. 2007a). Remnant patches
of eanhworm-free forest in the study region are
far from roads, fishing locations (e.g., boat
launches and lakeshores). and human settlements
(Holdsworth et al. 2007b). The earthworm-free
sites in the current study had likely escaped
invasion because of their remote locations in
designated wilderness areas that were >1.6 km
from the nearest road.
I searched for and monitored Hermit Thrush
nests between 20 May and 14 July 2009 and 17
May and 9 July 2010, taking care to expend
equivalent search effort at all sites and to evenly
distribute search effort within each site. I used a
geographical positioning system (C.PS) to record
all nest locations and monitored nests every 3-
4 days until they had successfully Hedged at least
one nestling, or were depredated or abandoned.
Nests were classified as successful if empty after
the expected Hedging date. (I M2 days: Jones and
onovan 1996), and I observed fledglings
agitated adults, or droppings near the nest. Nests
were classified as depredated if eggs were
destroyed or if nestlings were absent from ihe
nest before the expected Hedging date with no
evidence of Hedging. Nests were classified as
abandoned if eggs remained in the nest with no
adult activity during four consecutive visits.
1 used Arc Map Version 9.3 (ESRI 2008) lo
calculate a matrix of distances among (I) all nests
in a 1 .3-ha valley that was part of one earthworm-
Irec study site (but spatially separated from the rest
of the site by a 15—25 m high ridge system), and
had a high density of Hermit Thrushes and nests
(hereafter Porcupine Lake) (Fig. i); and (2) all
nests (excluding Porcupine Lake) within each of
the six study sites. All distance values within each
site were averaged to calculate mean distance
among nests. Nest density was calculated t nests
divided by area searched) for Porcupine Lake and
lor each site (excluding Porcupine Lake). .Areas
used corresponded to the perimeter within which I
searched for nests at each site and the 1 .3-ha area of
Porcupine Lake. All calculations were conducted
separately for 2009 and 2010; however, data were
averaged across years for both calculations. All
density estimates are reported as nests per hectare
Independent samples /-tests were used to
compare nest density and mean distance among
nests between Lumbricus-f ree and invaded sites.
Program MARK'S nest survival package (Dins-
more and Dinsmore 2007). w hich accounts for the
exposure (i.e.. number of days observed active) ol
each nest, was used to separately estimate nest
success probability for nests at Porcupine Lake
(« = 8) and for all other nests (n = 64). The
sample size of nests at Porcupine Lake was small
and 1 also report observations on whether
individual nests were successful.
SHORT COMMUNICATIONS
377
200 m
50 m
FIG. 1. Study area location (black circle) in Wisconsin. USA (A), and Hermit Thrush nest locations in 2009 and 2010 at
Porcupine Lake (dashed box in B. C). Shading in (B) indicates land cover (light gray = hardwood forest: medium gray =
mixed hardwood/coniferous forest; dark gray = water). Nests (C) sharing letters indicate overlapping period of activity,
subscript indicates nest fate (0 = depredated; I = successful), and X indicates point-count survey location.
RESULTS
Seventy-two Hermit Thrush nests (2009: n —
33; 2010: n = 39) were found with 28 in the three
invaded sites and 44 in the three Lumbricus- free
sites (8 of the nests were at Porcupine Lake). I
found three nests in 2009 at Porcupine Lake. Two
nests were 12.0 m apart and a third nest was 48. 1
and 53.0 m from these nests (Fig. I). The three
nests were simultaneously active on 8 July 2009
and each was incubated by a different female (I
checked all nests within 3 min and observed a bird
incubating on each nest). I found five nests at
Porcupine Lake in 2010; however, nests were
more evenly spaced than in 2009 (minimum
distance = 46.0 m). Two nests were found on
17 May: the activity period of these nests did not
overlap with the three other simultaneously active
nests found between 17 June and I July.
One nest of the closely spaced pair at Porcupine
Lake was depredated in 2009. and the other two
nests were successful. Three of five nests were
successful in 2010. and the other two nests were
378
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 2. June 2012
depredated. Probability of nest success for nests at
Porcupine Lake was 51% (95% Cl = 13-80%).
Probability of nest success for all nests except those
at Porcupine Lake was 26% (95% Cl = 16-37%).
Nest density ranged from 0.1 to 0.6 nests/ha
across the six study sites. Nest density at
Porcupine Lake was exceptionally high (3.1
nests/ha). Mean distance among nests was smaller
in Lumbricus-f ree sites (215 m. 95% C'l = 1 80—
250 m) compared to invaded sites (250 m, 95% Cl
= 236-264 m); however, the difference was not
significant (t =2.21, df =5 . P = 0.092). Nest
density did not ditter between Lumbricus-free and
invaded sites (t = 1.08, df = 5, P = 0.37).
DISCUSSION
I observed exceptionally high nesting density
of Hermit Thrushes in a remnant earth worm- free
area of northern hardwood forest in northern
Wisconsin. The 2-year mean Hermit Thrush
density in the highest density area (3.1 nests/ha)
was greater than the previous maximum density
of 74 territories/40 ha (1.9 nests/ha) in Arizona
(Franzreb and Ohmart 1978) and more than an
order of magnitude greater than many other
published estimates (Table 1).
Evidence from this study for a causal link
between Lumbricus invasions and Hermit Thrush
nest density is limited. 1 found no difference in
nest density between Lumbricus- free and invaded
sites; however, nests in Lumbricus- free sites
averaged slightly closer to each other compared
to nests in invaded sites. A previous study in the
same study area found significantly reduced
density of singing Hermit Thrushes in relation to
Lumbricus invasions (Loss and Blair 201 1). It is
unclear why density of singing Hermit Thrushes is
not consistently proportional to nesting density
across invasion categories in my study area, but
differences in rales ot pairing success and nesting
attempts between invasion categories may have
influenced these patterns.
Other factors could have contributed to the high
densities observed at Porcupine Lake. The forest
floor in this area was characterized by cover of
clubmoss {Lycopodium spp.) that was more
extensive (17.4% on average) than in other
Lwnbricus-Wce (12.1% on average) and invaded
areas (4.3% on average) (SRL, unpubl. data).
Clubmoss at Hermit Thrush nest sites provides
more concealment than other nesting substrates
(Flaspohler et al. 2000); extensive cover of
clubmoss at Porcupine Lake may have provided
an abundance of suitable nest sites. A similar
conclusion was reached in a study in Arizona about
the importance of small firs (Abies spp.) for
providing concealment and potential nest sites for
Hermit Thrushes (Martin and Roper 1988). Further
study ot relationships between earthworm invasion
and the presence and abundance of clubmoss is
needed to clarify whether invasions have a negative
effect on this plant group. Proximity to forest edges
may also influence Hermit Thrush density (Flas¬
pohler et al. 200 1 ); however, it is unlikely that edge
effects were present in my study because the sites
were >0.5 km from forest openings.
It is possible that individual male Hermit
Thrushes were paired to more than one female
and nest, given the proximity of Hennit Thrush
nests to each other at Porcupine Lake, and that
two nests in 2009 were only 12.0 m apart. I
confirmed that each nest was incubated by a
different (ostensibly female) Hermit Thmsh but
the secretive nature of males made it difficult to
know whether each nest was attended by an
independent pair. Three Hermit Thrushes were
simultaneously recorded singing on several occa¬
sions during point counts conducted at Porcupine
Lake (Fig. 1) in a previous study (Loss and Blair
2011). This observation suggests there were
sufficient males present for each nest to have
been attended by a separate pair.
Nest density estimates were based on all nests
with no differentiation between first nesting
attempts and re-nesting following abandonment
or predation. It is possible that nest density
estimates in Lumbricus- tree sites were inflated by
higher predation rates resulting in more re-nesting
attempts. Two lines of evidence from previous
work in the same sites (Loss and Blair in 201 H
suggest that nest density differences between
Lumbricus-free and invaded areas are real: (1) nest
density of another ground-nesting species, tlte
Oven bird, was higher in Lumbricus-free sites
compared to invaded sites, and (2) singing male
density of Ovenbirds and Hennit Thrushes was
greater in Lumbricus-free sites. The probability of
Hermit Thrush nest success was higher at Porcu¬
pine Lake compared to outside areas, suggesting
the possibility that re-nesting attempts at Porcupine
Lake may have actually been less common than in
other areas. The sample size of nests at Porcupine
Lake was small [n = 8); therefore, the nest success
results should be interpreted cautiously.
Earthworm- free forests have become exceeding¬
ly rare throughout northern Wisconsin (Holdsworth
SHORT COMMUNICATIONS
379
et al. 2007b). and invasive earthworms continue to
spread ihroughout most of north temperate North
America (Hendrix et al. 2008). It is not econom¬
ically or logistically feasible to remove earth¬
worms, and it is important to prevent invasions into
the remaining undisturbed areas. My study pro¬
vides evidence that some Lumhricus- free forest
patches may provide optimal habitat conditions for
supporting exceptionally high breeding densities of
Hermit Thrushes. Additional research is required to
clarify the relative influence of Lumhricus inva¬
sions, habitat characteristics of nest sites and
patches, and abundance of important nesting
substrates (e.g., clubmosses), on patterns of Hermit
Thrush abundance. Research is also needed to leant
if invasive earthworms provide a food benefit to
Hemiit Thrushes, and whether a benefit could
outweigh any adverse effects of earthworms to
forest floor habitat. Finally, investigation of Hermit
Thrush density in relation to invasion patterns
across regional spatial scales will clarify whether
earthworms are a significant concern for conser¬
vation of this species.
ACKNOW LEDG M ENTS
Field research was funded by the American Museum of
Natural History, Bell Museum of Natural History, Dayton
W'ilkie Foundation, Explorer's Club. Minnesota Ornithol¬
ogists’ Union, and Wisconsin Society for Ornithology.
SRL was supported by a University of Minnesota
Graduate School Fellowship and a National Science
Foundation IGERT grant: Risk Analysis for Introduced
Species and Genotypes (NSP DGF.-0653827). I thank
C. C. Hakseth. L. E. Lambert. J. C. Mulligan, M. W.
Shairow, Tammy Johns. H. M. Sireby. S. M. Peterson. B.
M. Breen, C.-M. Hung, and S. S. Loss for Held assistance.
• also thank R. B. Blair, L. E. Frelich. D, E. Andersen, and
P. V. Bolstad. for guidance. B. M. Breen. H. M. Streby.
and K. S G. Sundar for comments that improved the
manuscript, and the Cable Natural History Museum for
housing and office support. Fieldwork was conducted with
appropriate permits and approval by the University of
Minnesota Institutional Animal Care and Use Committee
(protocol 0904A63062 ).
LITERATURE CITED
Bock. C. E. and J. F. LYNCH. 1970. Breeding bird
populations of burned and unburned conifer forest in
die Sierra Nevada. Condor 72:182-189.
Dinsmore, S. J. and J. J Dinsmore, 2007. Modeling avian
nest survival in Program MARK. Studies in Avian
Biology 34:73-83.
Environmental Systems Research Institute (ESRI).
2008. Arc Map Version 9.3. Environmental Systems
Research Institute, Redlands, California, USA.
Flaspohler, D. J.. S. A. Temple, and R. N. Rosenfield.
2000. Relationship between nest success and conceal¬
ment in two ground-nesting passerines. Journal of
Field Ornithology 71:736-747.
Flaspohler, D. J.. S. A. Temple, and R. N. Rosenfield.
2001. Species-specific edge effects on nest success and
breeding bird density in a forested landscape. Ecolog¬
ical Applications 1 1:32-46.
FRANZRF.B, K. E. AND R. D. OHMART. 1978. The effects of
timber harvesting on breeding birds in a mixed-
coniferous forest. Condor 80:431-441
Hale, C. M„ L. E. Frelich. and P. B. Reich. 2006.
Changes in hardwood forest understory plant commu¬
nities in response to European earthworm invasions.
Ecology 87:1637-1649.
Hale. C. M„ L. E. Frelich, P. B. Reich, .and J. Pastor.
2005. Effects of European earthworm invasion on soil
characteristics in northern hardwood forests of Min¬
nesota, USA. Ecosystems 8:91 1-927.
Hendrix, P. F., M. A. Callaham Jr., J. M. Drake. C.-Y.
Huang, S. W. James. B. a. Snyder, and W. Zhang.
2008. Pandora's Box contained bait: the global
problem of introduced earthworms. Annual Review
of Ecology and Systemalics 39:593—613.
Holdsworth, A. R.. L. E. Fkei.ich. and P. B. Reich.
2007a. Effects of earthworm invasion on plant species
richness in northern hardwood forests. Conservation
Biology 21:997-1008.
Holdsworth, A. R.. L. E. Frelich. and P. B. Reich.
2007b. Regional extent of an ecosystem engineer:
earthworm invasion in northern hardwood forests.
Ecological Applications 17:1666-1677.
James- S. W. 2004. Planetary processes and their
interactions with earthworm distributions and ecology.
Pages 53-62 in Earthworm ecology (C. A. Edwards,
Editor). Second Edition. CRC Press, Columbus, Ohio,
USA.
Jones, P. W. and T. M. Donovan. 1996. Hermit Thrush
(i Catharus guttaius). The birds of North America.
Number 261.
Loss, S. R. and R. B. Blair. 2011, Reduced density and
nest survival of ground-nesting songbirds relative to
earthworm invasions in northern hardwood forests.
Conservation Biology 25:983-992.
Martin, T. E. 1993. Nest predation and nest sites.
Bioscience 43:523-532.
Martin, T. E. and J J. Roper. 1988. Nest predation and
nest-site selection of a western population of the
Hermit Thrush. Condor 90:51-57.
Morgan, K. and B. Freedman. 1986. Breeding bird
communities in a hardwood forest succession in Nova
Scotia. Canadian Field-Naturalist 100:506-519.
Pettingill Jr., O. S. 1930. Observations of the nesting
activities of the Hermit Thrush. Bird Banding 1:72-77.
Salt, G. W. 1957. An analysis of avifaunas in the Teton
Mountains and Jackson Hole. Wyoming. Condor
59:373-393.
Snyder. D. P. 1950. Bird communities in the Coniferous
Forest Biome. Condor 52:17-27.
380 THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 2. June 2012
The Wilson Journal of Ornithology 124(2):380-384. 2012
First Nesting Information for the Orange-eared Tanager
( Chloroch rysa cci / 1 i pa re a )
Manuel A. Sanchez Martinez1,4 and Gustavo A. Londofio2,3
ABSTRACT. — The Orange-eared Tanager ( Chloro -
chrysa caUiparea) occurs from southern Colombia to
northern Bolivia between 900 and 2,000 m elevation.
We describe for the first time the nest of the genus
Chlorochrysa, based on live nests of C. caUiparea, and
provide information on incubation and nestling growth
from August through December 2009 and 2010 in IVtanu
National Park, Cusco, Peru, the Orange-cared Tanager
has a distinct and unique nest location in clumps of
moss hanging from horizontal branches, previously
unknown among tanagers. The nest structure, however,
was similar to that ol most tanagers. We observed use
of a nest-like structure as a dormitory, not previously
reported lor the Thraupidae. Clutch si/e was one egg
and the nestling period was 2 1 days. The female made
an average ol 8,8 foraging trips/day from the nest which
lasted on average 33.1 min with nest attentiveness of
58.9%. The small clutch suggests close affinity with
mountain tanagers. Received 24 February 2011. Ac¬
cepted 31 October 201 1.
The tanager genus Chlorochrysa (Thraupidae)
is considered to be sister to the clade comprising
Stephanophorus, Diuca, Neothraupis. Lophospin-
gus, Cissopis, Schistoclamys, and Paroaria. The
Chlorochrysa and Stephanophorus — Paroaria
clade is in turn sister to the group of colorful
mountain tanagers (Sedano and Bums 2010).
There are three species in the genus Chlorochrysa
(C. calliparaea, C. nitidissima, and C. phoenico-
tis) with exclusively South American distributions
in the Andean foothills from Venezuela to Bolivia
with an elevational distribution from 1,000 to
1,800 m in low/wel outlying ridges within the
Andes region, where mossy cloud forest is
generally found. The genus is characterized by
their long and slender bills, strong tarsi, and a
small patch of distinctive club-shape feathers on
' Departamcnto de Biologfa, Universidad del Valle, A. A.
25360, Cali-Colombia.
-Florida Museum of Natural History. Dickinson Hall. Univer¬
sity of Florida, Gainesville, FL 3261 1. USA.
3 Department of Biology, 227 Bartram Hall. University of
dorida. P. O. Box 1 18525. Gainesville, FL 3261 1, USA
Corresponding author:
e-mail: manusama79@gmail.com
the ear-coverts (Hilty and Brown 1986, Isler and
Isler 1999. Ridgely and Tudor 2009).
flic breeding biology of the Orange-cared
Tanager ( Chlorochrysa caUiparea ) is almost
unknown. There is only one brief description of
a cup nest of the Glistening-green Tanager (C.
phoenicotis) hollowed in moss on the side of a
limb in the middle strata (Hilty and Brown 19861,
We describe for the first time the nest for the
genus Chlorochrysa based on five nesls of C.
caUiparea. and detailed information on incubation
and nestling growth.
METHODS
Study Area. — This study occurred at the Cock-
of-the-Rock Lodge (13 03' 1 9.4" S, 7 1 ' 32' 48.5"
W) managed by the Peruvian non-governmenlal
organization (NGO) Peru Verde. It is in the buffer
area of Munu National Park. Cusco. Peru, on the
eastern slope of the Andes at the confluence of the
Sun Pedro and Kcosnipata rivers. The Reserve
covers an elevation gradient from 1 .000 to 2,000 m.
and protects a cloud forest with abundant mosses
and epiphytes, a canopy height of 25 m, and
average temperature of 16.15 C (min-max =
13.6 to 19.8 C) with a rainy season between
November and April and a dry season from May
to August.
Nest, Egg. Incubation, and Nestling Measure¬
ments. — Daily nest searches were conducted by
six researchers each year betw'een August and
December 2009 and 2010 (10 hrs/day, 6 days/
week). Each researcher had a unique plot of 10-
15 ha throughout the field season. We found five
active nests of C. caUiparea. Most nests had an
egg or a nestling, but one was found during die
building stage. W'e measured length and width ol
eggs when found with a caliper to the nearest
0.1 mm and mass with a digital pocket scale
(FlipScale F2, Phoenix. AZ. USA) to the nearest
0.05 g. We placed two small thermal sensors (2
I mm), one inside the nest under the egg and the
other next to the external surface of the nest wall
The thermal sensors were attached to a U12 four-
SHORT COMMUNICATIONS
381
FIG. 1 . Nest and egg of the Orange-eared Tanager (C calliparea). ( A) Mossy clump on a horizontal branch where nests
were located. (13) Cup^nest inside the mossy dump. (C) Inner view of the cup nest showing nest layers and materials. (D)
White egg with brown spots.
channel hobo data logger (Onset Computer
Corporation, http://www.onsetcomp.com, Cape
Cod, MA, USA), which stored thermal data every
minute for 15 days. We visited the nest 3 days
after the sensors were placed to check if they were
producing accurate data, and again after 12 days
to download data. We then made daily visits to
record the exact hatching day. Wc collected daily
measurements on wing, tarsus, and mass ot the
nestling. We described nestlings every Other day.
We took nest measurements to the nearest 0. 1 mm
with a caliper and. when the egg or nestling was
depredated (or Hedged), collected the nest and
described the materials of each nest layer.
Incubation Rhythm Analysis. — Incubation be¬
havior was obtained by analyzing the thermal
changes recorded by the thermal sensor under the
egg. Cooper and Miles (2005) developed an
algorithm to detect all intervals when tempera¬
tures decrease monotonically. This algorithm
retrieved three quantities for each interval:
duration, total decrease in temperature, and initial
rate of temperature decrease. For example, the
start of a foraging trip (incubation recess) was
when the nest temperature decreased monotoni¬
cally for at least 1 min and decreased at least 2 C
at an initial rate of at least 0.5 C/min.
We calculated the nestling growth rate to
compare it with other passerine species using a
logistic equation, W (t) = AH 1 + e1 l'"
proposed by Ricklefs (1967). W ( t ) is the mass at
age t. A is the asymptote of the growth curve, K is a
constant scaling rate of growth. /, is the inflection
point on the time axis where growth becomes
asymptotic, and ? is the base natural logarithm.
RESULTS
The Five nests of the Orange-eared Tanager
were between 1,299 and 1,376 m elevation: all
were found when an adult flushed from the nest
(except 1 that was found during construction), and
all contained one egg or one nestling. Each nest
was built within thick mossy clumps hanging
from horizontal branches.
We found three nests during the 2009 field
season. The first, found on 5 October containing a
382
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124, No. 2. June 2012
FIG. 2. Incubation rhythm and nestling growth of C.
calliparea : (A) 24 hrs of incubation of one individual C.
calliparea in 2010, and (B) nestling growth during the
entire nestling period for one nest during 2009.
fresh egg, was 2.25 m above ground in a small
tree. The second, tound on 1 1 October, contained
a developed egg and was 3.5 m above ground in a
small tree. The last nest was on 13 October on a
small tree next to a trail 3.5 m above ground. It
contained a fully feathered nestling that flushed
from the nest the following day. We found two
active nests during the 2010 Held season. The first
contained a fresh egg on 21 October and was in
secondary forest next to a large gap 3 m above
ground. The second was on 8 November when
we observed a male carrying nest material to a
middle-sized tree 4 m above ground; on 20
November the nest contained a fresh egg.
In addition, an individual was Hushed at
dusk from a hanging moss structure (resembling
a globular nest) above a frequently used trail
between September and December. Wc did not
observe an egg, nestling, or activity during the day
and believe this structure served as a dormitory.
We know this structure was used frequently as we
p aced a leaf on the entrance at least two times a
week and it was removed. The globular structure
was 2 m above ground on a small tree and the
inner measurements were 65.6 X 4S.4 mm with
a wall thickness oi 17.6 mm. The horizontal
entrance was 94.8 mm in length and the external
dimensions were 108.8 X 81.6 X 355.5 mm
(length, width, and height).
Descriptions of Nests and Eggs. — The cup nev
was built W'ithin a natural clump of moss hanein;
from horizontal branches of small or middle-sized
trees (Fig. I A). Nests were placed within clumps
ol moss and had one or two side entrances. Hie
location of the nest on mossy clumps made it
difficult to locate by sight (Fig. 1A. B). Nests were
composed of two distinctive layers; the external
layer weighed (x ± SD) 3.96 rt 1.4 g (« = 5) and
was composed mainly of mosses (60%), and fem
rachises and dry roots (40%). The internal layer
weighed 2.30 ± 2.1 g (// - 5) and was composed of
line monocot liber (60%) and soft seed fluff of
bromeliads (40%) (Fig. 1C). The five nests were in
the forest interior at an average height from the
ground of 2.58 m (min-max = 2 to 4 m; n = 5).
The average internal dimensions were 55.2 x
48.9 mm with a wall thickness of 19.6 mm and
depth ol 32.6 mm; the external dimensions were
93.3 x 76.4 mm with a height of 48.9 ram.
Four ol the five nests had single eggs. The egg*
were white with small light-brown speckles,
located principally at the large end of the egg-
1 lie density ol the speckles was high and the large
end ol the egg appears brown (Fig. ID). The
brown speckles decrease rapidly in density toward
the smallest end of the egg. Eggs (x - SD)
measured 22. 1 ±0.91 X 15.5 mm ± 0.38 (n = 4)
and Iresh weight (embryo development had not
started) was 2.9 ± 0.3 g (n - 3).
Incubation Rhythm. — We documented incuba¬
tion behavior for two nests during 120 hrs (5
complete days), where the adults left the nest io
forage on average 8.8 times/day that lasted on
average 33.1 min (min-max = 3 to 88: Fig. 2A).
The nest tound in 2009 was monitored only lor
24 hrs as the egg hatched the day after the sensor
was placed in the nest. The adult made 1 3
foraging trips during this 24 hrs that lasted on
average 21.1 min (min-max = 3 to 55). The
temperature during incubation was 31.5 C (rain-
max = 27.8 to 34.7) and decreased to 26.1 C
(min-max = 22.9 to 30.4) when the adult was
absent. We monitored one nest during 5 complete
days in 2010; this individual left the nest at dawn
between 0516 and 0529 hrs, and the first eight
foraging trips lasted on average 54.5 ± 25.5 mm.
SHORT COMMUNICATIONS
383
The last trip before continuous incubation during
night occurred in early afternoon between 1301
and 1501 brs and lasted on average 31.75 ±
19.4 min. The adult spent on average 58.9 ±8.1%
of the time incubating the egg during these 5 days.
The bird made an average of 7.8 foraging trips/
day (min-max = 6 to 9) that lasted on average
36.1 min (min-max = 11.3 to 66). Nest temper¬
ature fluctuated between 30. 1 and 15. 1 1 C. and the
average nest temperature during incubation was
26 2 C (min-max = 22.3 to 31.4) decreasing to
23.5 C (min-max = 20.7 to 26.7) when the adult
was absent. We could not confirm directly how
many individuals incubated, but we only saw the
female entering or leaving the nest. The low nest
attentiveness (58.9%; Deeming 2002) and data
from other tanager species (Isler and lsler 1999)
suggest that only the females incubate.
Nestling Description.— Two of five nests had
nestlings. One nest was found with an egg on 1 1
October 2009 which hatched in the afternoon on
12 October. We monitored the nest until 2
November when the nestling successfully left
(he nest; thus, the nestling period was 21 days.
The first day the nestling had black down on the
head, back, rump, shoulder, and Hanks, the skin
color was a pale yellow, the eyes were closed, the
commissures were yellow, and the tip of the bill
was black. The eyes began to open on day 7 and
by day 9, the eyes were completely open. The
leather sheath breaking through the skin was a
green color on the head, wings, back, flanks,
rump, and abdomen, but the nestling still had
down, and the bill was totally black. The bill was
completely black on day 14; the nestling had a
yellow eve ring, green feathers all over the body,
and blue feathers on the abdomen. The nestling
was fully feathered on day 20 and the tail feathers
were almost completely emerged from the
sheaths. The next day the nestling left the nest.
It weighed 4.15 g on hatching, and gained mass at
a rate of 0.8 g/day during the first 14 days,
reaching a mass of 15.35 g. The mass ranged
between 14.60 and 15.15 g on following days,
finally reaching 16.95 g on day 21 . The calculated
'Pecific rate of growth (A'l was 0.26. Recently
hatched nestlings (day 2) had a tarsus length of
8 mm and a wing length of 8 mm. and grew at a
rate of 1 . 1 mm/day and 2.6 inm/day, respectively,
reaching a length of 23 and 54 mm on day 20
(Fig. 2B). The second nest with a fully feathered
nestling was empty (he following day. The
nestling weight was 16.3 g when found on 13
October and the tarsus and wing measured 22 and
53 mm. respectively.
DISCUSSION
Hilly and Brown (1986) published the only nest
information known for the genus Chlorochrysa-, a
brief description of the nest of the Glistening-green
Tanager. Our study provides the first detailed
description of the nests, eggs, and nesting biology
of a member of the genus Chlorochrysa. The cup
nest of the Orange-cared Tanager is similar to that
of most tanagers (lsler and Isler 1999). but the nest
location in hanging mossy clumps from horizontal
branches seems to be unique to this genus (Hilty
and Brown 1986) and different from other tanagers
(Isler and lsler 1999). The dutch size is one egg
(Stiles and Skuteh 1989, Isler and Isler 1999,
Martin et al. 2006, our study). One-egg clutches are
not common among neotropical passerines but
members of the mountain tanager clade. which is
sister to the Chlorochrysa and Stephanophorus—
l’ a maria clade (Sedano and Bums 2010). also have
a clutch size of one egg (G. A. Londono, unpubl.
data). Thus, it is possible this trail is present in
other neotropical passerines. The concentration of
brown spots at the large end of the egg in C.
calliparea differs from other members of the
subfamily Thaupinae that commonly have white
eggs covered with dense spots or lines all over the
egg surfaces (Greeney et al. 1998. Isler and Isler
1999). We are not aware of any other tanager using
a nest-like structure as a dormitory. The growth
rate of C. calliparea nestling when contrasted with
other passerine species was slower than temperate
passerine birds (Remes and Martin 2002). and was
also slow compared with tropical passerines
(Greeney 2008).
We believe the unique location of a cup nest
inside dense clumps of moss on horizontal
branches has made it difficult to locate Chlor¬
ochrysa nests. We hope this paper will encourage
researchers to look for these nests and investigate
if the unusual nesting habits described for C.
calliparea apply to other species of this genus.
ACKNOWLEDGMENTS
We thank Adam Carter and Jamie Miller for finding and
monitoring some of ihe nests. We thank David Ocampo
Rincon. Rachel Hanauer. and Julio Cesar Bermudez, for
help during the 2009 field season. Comments by two
anonymous reviewers, S. K. Robinson, D. W. Steadman,
and C. E. Braun improved the manuscript. Our study was
possible thanks to the logistical support of tiie NGO Peru
Verde that allowed use of the Cock-of-the-Rock Reserve
384
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 2. June 2012
during 4 years. Financial support was provided by the
Katherine Ordway Foundation and the Dexter Fellowships
in Tropical Conservation Biology. Alexander Skutch
Award (Association of Field Ornithologists). Louis Agassiz
Fuertes Award (Wilson Ornithological Society), and
Alexander Wetrnore Award (American Ornithologists’
Union). Wc thank SERNAP for allowing us to work in
the buffer area of Manu National Park.
LITERATURE CITED
COOPER. C. B. AND II. Mtt.ES. 2005. New software for
quantifying incubation behavior from time-series
recordings. Journal of Field Ornithology 76:352-356.
Deeming. D. C 2002. Behaviour patterns during incuba¬
tion. Pages 63-86 in Avian incubation behavior,
environment, and evolution (D. C. Deeming. Editor).
Oxford University Press. New York. USA.
Grff.NHV, II. F. 2008. Nestling growth and plumage
development of the Spotted Barbtail {Pmnnoplex
brunnescens), Kempffiana 4:21-29.
Greene v, H. F„ M. Lysinger, T. Walla, and J. Clark.
1998. First description of the nest and egg of the
I'anager Finch (Oreothniupis ctrremonops Sclater
1855.) with additional notes on behavior. Ornithologica
Neotropical 9:205-207.
Hii.ty, S. L. and W. L. Brown. 1986. A guide to the birds
of Colombia. Princeton University Press, Princeton.
New Jersey, USA.
Jsij-K, M. L. AND P. R. Isler. 1999. The tanagers
Smithsonian Institution Press. Washington. D C . USA.
Marlin. T. E.. R. D. Bassar, S. K. Bassar. J. J. Fommm
P. Lloyd. H. Mathewson, A. Niklbon. aso a.
CHALFOUN. 2006. Life history and ecological cent-
lates of geographic variation in egg and clutch maw
among passerine species. Evolution 60:390-398.
KEMt5, V. and T. E. Martin. 2002. Environmental
influences on the evolution of growth and develop¬
mental rates in passerines. Evolution 56:2505-25 IS.
Ricklees. R, E. 1967. A graphical method of fitting
equations to growth curves. Ecology 48:978-980
RlDGELY. R S. and G. Tl'DOR. 2009. Field guide 10 the
songbirds of South America. University of Tevav
Press. Austin. USA.
Sedano, R. E. and K. .1. Burns. 2010. Are the NoiiiKrn
Andes a species pump for neotropical birds1 Phyloge¬
netics and biogeography of a clade of neotropical tanagers
(Aves: Thraupini). Journal of Biogeographv 37:325-343.
Stiles, F. G. and A. F. Sketch. 1 989. A guide to the birds
of Costa Rica. Cornell University Press. Ithaca. New
York, USA.
The Wilson Journal of Ornithology !24(2):384-389, 2012
Does Nest-box Size Impact Clutch Size of House Sparrows?
Peter E. Lowther1
ABSTRACT. — I monitored the breeding biology of
House Sparrows ( Passer domesticus) in a suburban
colony in Cook County, Illinois, USA. I found a
significant statistical correlation between dutch size
and the base area of the nest box (r 0.592, P <
0.0029) with mean clutch size varying from 4.49 eges
(in a 'small' nest box, 1 12 cm* basal area) to 4.77 eggs
(in a ’large’ nest box, 221 cm* basal area). Other
measures ol breeding success (hatching and Hedging
success, mean egg mass, and nestling condition) had no
statistically significant relationship with nest-box size.
Measures ol nest site preferences, as suggested by
earlier date of first egg of season or by greater number
of broods per season, also show no statistically
significant correlation with nest-box size. Received 28
September 2011. Accepted 12 December 201 1 .
The ‘natural’ non-cavity nest of House Sparrows
(Passer domesticus) is u globular structure placed in
IL USeUm ■ |,40° SUU"’ Lake Shore D"ve. Chic
il 60605. L.SA; e-mail: plowther@fieldmuseum.org
trees, —20-25 cm diameter and 15-20 cm height:
however. House Sparrows have a close association
with human-impacted habitats and will make use of
nooks, crannies, and other cavity-like sites within
which to build nests, and readily use nest boxes
(Anderson 2t)06). Nest boxes are convenieni for
investigators to monitor the breeding biology of
birds. They also provide a nest site environment tlial
can be easily quantified or that can allow
experimentation (Lambrechts et al. 2010).
Experiments and field studies of several cavity-
nesting species have found that clutch size varies
with size of the cavity or nest box (e.g.. Lhhrl
1973, Gustafsson and' Nilsson 1985), but this
relationship has not been found to be true for all
species lor which this has been investigated (e.g .
Karlsson and Nilsson 1977, Purcell et al. 1997).
There is no clear understanding of actual causes
that can explain this relationship.
I monitored the breeding biology of a small,
suburban nest-box colony of House Sparrow'
SHORT COMMUNICATIONS
385
since 1988 (Lowther 1996) and found differences
in clutch size in comparing average measures of
breeding activity between 'normal' and ‘small'
nest boxes in use at this site. My objective in this
study is to examine and describe relationships
which may exist of nest-box size with several
measures of nesting activity and breeding success.
METHODS
I placed seven nest boxes on the garage at my
residence in Homewood. Cook County. Illinois.
USA, in October and November 1987. I added to
this number in successive years to have 10 nest
boxes in 1989. 15 in 1990, 17 in 1992 and. since
1993. between 20 and 25 nest boxes available.
Nest boxes were built with scrap lumber follow¬
ing the general design for ‘bluebird* boxes and
most have outside measurements of - 10 X 15 cm
basal area. 20 cm height, and a 3.8 cm diameter
entrance hole. Entrance holes were on the ‘front*
or 'side' of the nest box and most were south-
facing. These nest boxes were placed between
1.7 and 2.4 m above ground and. once placed,
generally maintained their position and specific
identity from year to year. Removals and minor
position adjustments (i.e., changing height above
ground <20 cm) were made generally in response
to predation by common raccoons ( Procyon Intor)
or cats (Feiis catus ): repairs were made as needed.
General nest box maintenance, cleaning, and nest
removal was conducted in September or October.
I use the term 'nest box' primarily to refer to an
actual nest box placed at a unique position or
coordinate on or near the garage. (In field notes, a
single, physical nest box used in 2 positions would
receive 2 different ‘nesi box' designations; 2 nest
boxes used in single position [e.g., replacement
tor a damaged nest box| would still have the
designation of a single ‘nest box’). Nest boxes
have been placed at 34 unique locations since
the 19X8 breeding season: nest boxes at these
locations have been available for one to 24
seasons through 201 I. Internal dimensions of the
70 nest boxes present during the 201 1 season were
measured in September 2011. Internal dimensions
of nest boxes at the remaining locations were
obtained from field notes regarding nest box
movements or nest measurements. Base urea for
nest boxes with known internal measurements
ranged from 112.1 cm2 (9.5 X 11.8 cm) to
221.2 cm2 (11.4 X 19.4 cm).
Nest boxes were chocked every 2 or 3 days
during the breeding season to allow documenta¬
tion of dates of egg laying, hatching, nest losses,
and young birds leaving the nest. Eggs were
measured on their first appearance. Young were
measured during each nest check until — 10 days
of age and banded when reaching 15-20 g with
IJ.S. Geological Survey bands. Mass of surviving
young at age 7 days, from the measurement made
at 7 days or estimated from measurements on days
bracketing 7 days, was used as an index of nestling
quality. 1 calculated overall mean clutch size,
hatching success, surviving brood size, mean egg
mass, and mean mass ol young at age 7 days for all
nesting attempts within each nest box (with >1
season of data). Nest attempts with completed
clutches ranged from 17 (over S yrs) to 64 (over
22 yrs) for the 23 nest box locations with known
internal measurements and which were used in
analysis; nest attempts for the 1 1 nest box locations
not used ranged from 0 (over 1 yr) to 23 (over
9 yrs). Pearson product-moment correlation coef¬
ficients were calculated to provide a measure of
association between nest- box basal area and
measures descriptive of breeding activity.
Almost all surviving nestlings were banded and
some efforts were made to band and color mark
other young and adults. Efforts to identity
individual parents for each nesting attempt have
been considered loo disruptive and have not been
done. Incidental observations allow association ol
some adults with specific nest boxes and unique
characteristics of some eggs or clutches suggest
that particular females retain nest boxes within
and between seasons (see also Anderson 2006).
RESULTS
There was a significant, positive relationship ol
clutch size w-ith basal area of the nest box (r =
0.592. df = 21, P < 0.0029; Fig. I). This same
positive and statistically significant relationship
holds if. instead, clutch size of individual nesting
attempts was used rather than each nest box’s
overall mean clutch size: r — 0.118, df = 893,
p < 0.00 1. The difference in mean clutch size
between smallest and largest nest boxes was
almost 0.3 eggs: mean clutch size in nest box G23
(basal area 1 12.1 cm2) was 4.49 eggs (based on 36
clutches over 13 years), mean clutch size in nest
box GI0 (basal area 221.2 cm2) was 4.77 eggs
(based on 52 clutches over 22 years). The greatest
mean clutch size (Fig. 1) was associated with nest
box G19 (with base area of 144.0 cm2). This nest
box accounted for almost all (6 of 7) of the 7-egg
clutches recorded in this study; apparently, from
386
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 2. June 2012
2000 lo 2004, a single female laid five 5-egg. fou
6-egg, and five 7-egg clutches in G 1 9 plus one eacl
6-egg and 7-egg clutch during 2000 in th<
neighboring nest box G20 (base area o
215.3 cm2). Excluding clutches of this female
reduced the mean value for GI9 from 5.05 eggs,
nest (n = 44) to 4.60 eggs/nest (n = 30) and result.'
in a significant correlation, r = 0.728 df = "> ] p <
0.0001 (Fig. 1).
Other summaries of individual nesting success
do not exhibit statistically significant relationships
with nest-box base area. The relationships be¬
tween base area of nest box with hatching success
(r - 0.353, df = 21, P = 0.099) and with
surviving brood size (r = 0.357. df = 21, P =
0.100) have near statistical significance (Fig. 2),
but these variables themselves are correlated with
clutch size. No statistically significant relationship
exists between basal area of nest box and mean
egg mass (r = 0.094. df = 21. P = 0.45), nor
between basal area of nest box and mean mass
ol surviving young at 7 days ot age (r = -0 1 36
df = 21. P = 0.753).
There is no indication of any preference for
particular nest boxes based on nest-box base area.
There is only a slight positive, but non-significant,
correlation between base area and date of the nest
box’s first egg of the season (/• = 0. 188, df = 21.
P - 0.396) and a slight negative, but non¬
significant. correlation between base area and
number ol clutches/ycar (/• = -0.210, df = 2 |
DISCUSSION
Clutch size of House Sparrows varies season¬
ally with a mid-season high (Murphy 1978.
Anderson 2006, pers. obs.). The use of multi¬
year, whole-season, multi-female data for the
mean clutch size for each nest box masks several
factors known to have affects on clutch size. All
nest boxes at this site were within a circle with a
6-m radius and pairs, potentially, could select any
ol the available nest boxes except for constraints
imposed by behavioral interactions within the
colony, by which, for example, older, successful
pairs would likely retain nest sites within and
between seasons (Anderson 2006).
I his present study suggests two questions lor
consideration. ( I ) Do House Sparrows show any
preference for size of cavity for a nest site:
specifically, do they show any preferences for nest
boxes with regard to base area? (2) Do the physical
characteristics of a nest box have any impact on the
breeding success of House Sparrows?
1 he first question can be addressed best in an
experimental setting. Mv observations seem to
show no overt preference for nest boxes with
regard to size of the base area, but slight trends
allow speculation of possible biological signifi¬
cance. House Sparrows may prefer smaller nest
boxes since first nesting attempts begin earlier in
the season for smaller nest boxes and. as one
consequence, these nest boxes tend also to have
more nesting attempts. My own subjective
impressions are that preferred nest boxes at this
SHORT COMMUNICATIONS
387
FIG. 2. Relationship between base area of nest box and number of young House Sparrows surviving nest box life.
site are based more on location within the overall
configuration of nest box placement on the
garage; preferred nest boxes are those on the
back of the garage which are less disturbed by the
usual human activities about the house and yard -
but only one of the five smallest nest boxes was
on the back side.
The second question has been investigated for a
number of hole-nesting species. Observations and
experiments have shown a positive correlation
between the bottom area of a nesting cavity or
nest box and clutch size (e.g.. Boreal Owl,
Aegotius June reus |Korpimaki 1985); Tree Swal¬
low. Tachycineta bicolor (Rendell and Robertson
1989); Willow Tit. Poecile montcmus [Ludescher
1973); Marsh Tit. P. palustris | Ludescher 1973,
Wesolowskt 20031; Great Til, Punts major
IGraczvk 1967; Johansson 1974; Lohri 1973,
1980; Karlsson and Nilsson 1977; van Balen
1984; Gustafsson and Nilsson 1985); Eurasian
Blue Tit. Cyanistes cae rule its (Hnemar 1981. van
Balen 1984); European Pied Flycatcher. Ficedula
hypoteuca [Johansson 1974. Karlsson and Nilsson
1977, Gustafsson and Nilsson I985|: Collared
Flycatcher, F. aibicollis | Gustafsson and Nilsson
1985); and European Starling. Sturmis vulgaris
1C lobe rt and Berthet 1983, Trillmich and Hudde
1984]). This is not a universal finding among
cavity-nesting species (e.g., Ash-throatcd Fly¬
catcher, Myiarchus cinerascens [Purcell et al.
1997); Oak Titmouse, Baeolophus inornatus
| Purcell et al. 1997); Eurasian Nuthatch, Sitta
europaea [Pravosudov 1995); House Wren. Trog¬
lodytes action [Purcell et al. 1997); European Pied
Flycatcher (van Balen 1984, Alatalo ct al. 1988,
Czes/.czewik and Walankiewiez 2003 1 ; Eastern
Bluebird, Sialia sialis [Pitts 1998); Western
Bluebird, S. mexicana [Purcell et al. 1997);
European Starling | Karlsson and Nilsson 1977,
Moeed and Dawson 1979)). The distinction
between these groups is not understood but there
seems to be taxonomic and size differences.
Experiments undertaken by Lohri (1973) com¬
pared Great Tits using nest boxes with diameters
20 cm (or 3 14 enr basal area) and 9 cm (or 64 cm2
basal area) and reported dutch size in smaller nest
boxes to be statistically smaller than clutch size in
larger nest boxes. Other measures of breeding
success (hatching success, nestling mortality or
Hedging mass) did not differ between small and
large nest boxes (Lohri 1973). This difference in
final clutch size in later experiments was evident
even when the size of the nest box was changed
during laying of the first four eggs (Lohri 1980).
Gustafsson and Nilsson (1985: 384) suggested
clutch size differences were just "an adjustment
of the clutch to the size of the nesting cavity”.
House Sparrows have been identified as indeter¬
minant layers (Haywood 1993; Anderson 1995,
2006) and it might be supposed that any tactile
388
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 2. June 20/2
sensation from ‘eggs in the nest' may influence the
completion of egg laying - in smaller nest boxes
with potentially a smaller nest cup. any sense of a
‘full nest' may he achieved with fewer eggs (i.e.. a
smaller clutch size) than would be achieved in
larger nest boxes. The impact of the smaller nest
boxes is just a slight reduction in clutch size and
little other effect on breeding biology. This effect is
magnified when considering the entire season or
life time production if individuals maintain the
same nest box from year to year as is true for House
Sparrows (Anderson 2006).
There may be a nest-box size (or cavity size)
too big to have any restrictive impact on size or
bulk of any nest that may be built; below this size
the nest box imposes physical limits on the size of
the nest itself. It can be imagined the relationship
between increasing cavity size with clutch size
holds until cavity (or nest-box) size reaches (he
point at which nest building has no constraints.
Further investigation of House Sparrow nest box
preferences would suggest looking at nest boxes
encompassing a larger range in basal area or using
nest boxes with a single entrance to two cavities
of diflerent sizes. House Sparrows, being some¬
what colonial in their nesting biology, can be
presented a situation offering a variety of nest-box
types and sizes. Most nest boxes used by my
Homewood colony were within I m of their
nearest neighbor; individual pairs potentially have
the full range of choice in selecting nest sites. This
present examination has only looked at variation
in basal area from 112 enr to 221 cm2 and
included no experimentation.
Understanding preferences and nest box micro¬
climate is difficult to examine outside the labora¬
tory. Nest site selection involves more than just
nest-box size; nest site preferences for House
Sparrows in this colony setting would be influ¬
enced by interactions among all individuals in the
colony, past breeding histories, and future available
choices. The differences noted in clutch size
among different nest-box sizes in experiments with
European Starlings were explained by differences
in the age composition of females using the
different box sizes: young females were over¬
represented in the smaller boxes (Trillmich and
Hudde 1984). First time breeders among House
Sparrows have a smaller average clutch size and
select nest sites later than older birds; however,
once situated. House Sparrows show some site
fidelity (Anderson 2006); all of these factors add
complications for understanding.
ACKNOWLEDGMENTS
Over the years, a number of people have assisted in
monitoring I louse Sparrows at this colony: Carvn. Gretchen.
Gail, and Gloria Lowthcr; Monica and Judy Wilks: and Brian
Wayne. I appreciated the generosity of neighbor Donald
Callender (t) in allowing placement of four nest boxes on his
garage just 1.9 m to the north of the main stud) sire. Editor
Gait L. Braun, reviewer Douglas \\ . Mock, and an anonymous
reviewer were helpful in their criticism and guidance.
LITERATURE CITED
Alatalo. r. v.. A Carlson, and A. Lindberg 1988.
Nest cavity size and clutch size of Pied Flycatchers
Ficedula hypo/euca breeding in natural tree-holev
CJrnis Scandinavica 19:317-319.
ANDERSON, T. R. 1993. Removal indeterminacy and the
proximate determination of clutch size in the House
Sparrow. Condor 97:197-207.
Anderson. T. R. 2006. Biology of the ubiquitous House
Sparrow. Oxford University Press, New York, USA.
Clobert, J. and P. Berthet. 1983. Les jeunes habitent
peiiton impact de la rSdeuction du volume intercut du
nichoir sur le comportement d’une population ni-
chcusc d'etourneax sunsonnets (SjUmus vulgaris I-).
Annales de la Societe royale zoologique de Belgie
1 13:183-192.
C7.ESZCZEWIK. D. AND W. Wai ankilwic/. 2003. Natural
nest sites of the Pied Flycatcher Ficedula lixpoleuca in
a primeval forest. Ardea 91:22.1-230.
I-Ni-MAR. A. 1981. Fiirsok nied holkar lor triidkrypure
Certhia fanri/iaris. |A trial with nest-boxes for the
Treccrecper Cerrhia familiaris. | Var Fagclvarld
40:233-238..
GraCZYK, R. 1967. The fecundity of tits (Pandaei in
dependence upon size of nesting box. Omithologia
Stosowana 2:41-47.
Gt STAFSSON, L. AND S. G. NILSSON. 1985. Clutch size and
breeding success of Pied and Collared flycatchers
Ficedula spp. in nest-boxes of different sizes Ibis
127:380-385.
Haywood, S. 1993, Sensory and hormonal control of clutch
size in birds. Quarterly Review of Biology 68:33-59.
JOHANSSON. H. 1974. Kullstorlek och hackningsframgdng
hos vissa holkhackande smSfaular i centrala Sverige
1972-1974 11952-1963). Faunaoch Flora 69:212-218.
Karls son. J. vnd S. G. Nilsson. 1977. The influence of
nest-box area on clutch size in some hole-nesting
passerines. Ibis 1 19:207-21 1.
Korpimaki. F3. 1985. Clutch size and breeding suux»
relation to nest-box size in Tengmaim’s Owl Aeg 'U.cs
June reus. Holarctic Ecology 8:175-180.
Lamhrlchts. M. M.. F. Adriaensen, D. R. ARDF. A. T
Artemyev. F. Atienzak, j. Banblra. E. Barba l -C
BOUVtER, J. CAMPRODON. C. B. COOPER. R &
Dawson. M. Eens, T. Eeva, B. Faivke. L L.
Garamszlg), A. E. Goodenough. A. G. GOSlfcR. A-
GrEgoirh. S. C. Griffith. L. Glstafsson. L S.
Johnson. W. Kama. O. KeiSs. P. E. Lumbias. M X
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The Wilson Journal of Ornithology 1 24(2): 3X9— 392. 2012
An Unusually Synchronous Double Brooding Attempt by a Northern
Flicker Pair
Elizabeth A. Gow12
ABSTRACT. — Wc report an unusual case of a
monogamous pair of Northern Flickers ( Colaptes
auratus) initiating a second clutch while there were
still nestlings in ihe first nest. The male and female
incubated at both nests but only the male fed nestlings at
the first nest. The second nest attempt was abandoned
alter the first nestlings Hedged, possibly because the
two broods were too synchronous in timing lor the male
to contribute sufficiently to both. Double- brooding has
nut been previously documented for Northern Flickers.
Received 13 September 2011. Accepted 20 January
2012.
There are two types of breeding strategies
which allow monogamous birds to Hedge two
’Department of Biology, University of Saskatchewan.
112 Science Place, Saskatoon, SK S7N 5E2. Canada.
’Corresponding author: e-mail: eliz.gow@usask.ca
and Karen L. Wiebe
broods within a breeding season. Double brood¬
ing. or having two successive broods, is not
uncommon among altricial birds, and it increases
reproductive success (Nagy and Holmes 2005.
Mulvihill et al. 2009). The second clutch in
double brooding is typically laid several days to
weeks after nestlings from the first brood Hedge,
when demands for parental care Irom the first
brood decline (e.g., Ingold 1987. Mulvihill et al.
2009). Double brooding differs from the phenom¬
enon of double clutching which occurs when a
female lays a clutch for her mate and a separate
clutch for herself, which they care for separately,
and more or less simultaneously (Blomqvist et al.
2001 ). Double-clutching requires that offspring can
survive with uni-parental care and occurs in species
where males incubate and can rear offspring alone,
e.g.. Mountain Quail ( Oreortyx pictus ) (Gutierrez
390
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 2. June 2012
and Delehanty 1999) and Mountain Plovers
0 Charadrius montanus) (Blomqvist et al. 2001 ).
Male woodpeckers are responsible for most of
the incubation (Ligon 1999. Wiebe 2008). and this
facilitates alternate reproductive strategies of
females, such as polyandry (Wiebe and Kempe-
naers 2009). There are rare reports of male
woodpeckers rearing nestlings alone from time
of early incubation (Wiebe 2005). but the number
of fledglings from single-parent broods is low
suggesting that bi-parental care is generally
required for Hedging a complete brood (Ligon
1999). Double-brooding also seems to be rare in
North American picids. It has been documented
only in Red-headed Woodpeckers (Melanerpes
erythroceplialus ), (Smith and Layne 1986, Ingold
1987). Gila Woodpeckers (M. uropygialis ), (lid-
wards and Schnell 2000), and Red-cockaded
Woodpeckers (Picoides borealis) (Connor et al.
2001). We present evidence of an unusually
compressed double-brooding attempt by a pair
°f Northern Flickers (Colaptes an ranis) where
a second brood was initiated before the first
nestlings fledged.
METHODS
This observation occurred near Riske Creek.
British Columbia. Canada (51 52' N. 122 21' W).
the site of a long-term study on flickers where
1.818 nest attempts have been monitored since
1998 (Wiebe 2008). Each year, >95% of adults in
the study area were trapped and color-banded for
individual identification and a subset of these were
fitted w ith radio transmitters. The unusual breeding
behavior we observed was for a radio-marked pair
in 2011. The parents were tracked simultaneously
for 3-hr sessions when nestlings in the brood
were 5. 10, 13. and 20 days of age. The nest was
videotaped during these tracking sessions to record
parental provisioning. Parents were tracked 1.5 hrs
every-other day during the fledgling period.
OBSERVATIONS
We observed a Northern Flicker pair initiate a
second clutch while still raising nestlings at a first
nest. The first egg of the first nest was laid on 20
May and the complete clutch contained eight
eggs, which is a typical clutch size for birds at our
study site (Wiebe and Moore 2008). We assume
incubation began with the last egg and the pair
would have begun incubation on 27 May. The
male was (rapped and banded at the nest while
meubatmg on 2 June and the female was trapped
while incubating on 4 June. The male was
brooding newly-hatched nestlings on 8 June but
it was raining and they were not counted until 12
June when there were five. It is possible that up to
eight of the eggs hatched but several nestlings
would have died in the first few days. We banded
four nestlings on 28 June and they left the nest
cavity on 3-4 July.
We found the second nest in an existing tree
cavity, -50 m from the first nest on 21 June
(13 days after hatching of the first nest) when it
contained tour eggs. We flushed the male from
the second cavity on this day, and a few1 minutes
later saw him copulate with the radio-marked
female from the first nest. The first egg of the
second nest presumably was laid on Is June
(fig. 1 ) and the second clutch consisted of eight
eggs on June 26.
file male and female flickers spent —50% of
their time within 50 m of either nest, but the
female did not provision nestlings at the first nest
based on 967 min of video on days 5, 10, 13, and
20. We do not know if she provided care in the
first few days after hatching. We observed the
male incubating eggs at night on day 20 in the
second cavity while the female was roosting
within the nest clump -100 m from the second
nest with eggs, and —50 m from the first nest. The
second nest was observed for 396 min on its third
day of incubation when the nestlings at the first
nest were 20 days of age. The male incubated for
33 min and the female for 255 min. but the eggs
were left unattended tor 27% of the time.
T he male but not the female continued to care
for the nestlings from the first brood after they left
the nest. Four nestlings fledged from the first nest
which is lower than the average for the popula¬
tion. The male no longer returned to the second
nest to incubate during the post-fledging period.
The female still took incubation shifts leaving the
cavity unattended for up to 30 min at a time. On h
July. 10 days after incubation began at the second
nest, we found it abandoned with cold eggs
covered in wood chips.
DISCUSSION
Our observation does not fit into the definition
°f double-clutching because both the male and
female contributed to parental care (incubation) at
both nests. Neither does it fit into typical double-
brooding because the second nest was initiated
before the first brood fledged, i.e., when the
nestlings were only 9 days of age. Compressed
SHORT COMMUNICATIONS
391
First egg
’
r
' 1
Cavity
#1
Nestling
Fledgling
Hatch
Fledge
Male stops feeding
fledglings
Ma!e stops Femak
!
^ *
Cavity
Laying
Incubating
#2
— — P* ^
HG. 1. Timeline illustrating important events during nesting at the two cavities of a Northern Flicker pair.
breeding attempts have been documented only
rarely across all species of birds. It has been found
in Rock Pigeons ( Columba livid) which may lay a
second clutch I week after the first brood hatches,
but bi-parental care (incubation and feeding)
occurs at both nests (Hurley 1980). Similarly,
some Common Terns (Sterna hirundo) laid a
second clutch while still caring for the first clutch
(Moore and Morris 2005) and a population of
Whiic-rumped Swiltlets ( Ae rod ramus spodiopy-
gius) regularly laid a second clutch in the same
nest as the first, while the first nestling was still
there {Jamieson et al 1987).
The male Northern Flicker, in the case we
observed, successfully raised four nestlings to
fledging without the female providing any food
from day 5 to fledging. The male was also able to
incubate at night at the second nest and to take
daytime incubation shifts because nestlings at the
first nest were sufficiently old to thcrmoregulate
without brooding. The male seemed to be able to
successfully divide his care between two nests
early but. apparently it became difficult after the
first brood fledged. Perhaps once fledglings were
mobile, it was too time-consuming to keep track
of their locations on the landscape, and to fly to
the second nest for incubation shifts.
During incubation at typical flicker nests, the
eggs are covered 99 % of the time with daytime
bouts alternating between partners (Wiebe 2008).
No female continued with the breeding attempt
after mate loss during incubation; whereas, some
males continued but had low (50%) hatching
success of the eggs (Wiebe 2005). Thus, it was not
surprising the female we observed abandoned the
second nest once the male stopped incubation,
although whether females are unable, or only
unwilling to incubate alone because of life-history
trade-offs is not known.
There are a few explanations for why this pair
attempted two broods. We do not know whether the
female abandoned the first nest after being trapped
and banded while incubating. Abandonment occurs
only in 2% of cases, and we have not observed
birds start a new nest nearby while the previous
nest was still active. Alternatively, the female may
have stopped caring for the nestlings alter hatching
because she chose not to invest further in a brood
w ith low reproductive value (i.e., containing only 4
nestlings from the original 8 eggs, flickers typically
fledge -90% of nestlings that hatch, Wiebe 2005).
Female desertion of young nestlings may lead to
reproductive gains if females can secure a second
mate (Wiebe 2005, Wiebe and Kempenaers 2009).
However, polyandry in this population seems
constrained by available males and the female
may have been limited to attempting a second
brood with the current male. Polyandmus flickers
are significantly older than monogamous females
(Wiebe and Kempanaers 2009) and the female in
our observations was fairly old. at 4 years. Thus,
she was within the age class most likely to
392
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 2. June 2012
participate in alternate reproductive strategies.
Extra-pair paternity has not been documented in
socially monogamous flicker pairs (Wiehe and
Kempenaers 2009) and it is unlikely that any of the
eggs were sired by other males.
Double brooding may increase fecundity in
several species (Nagy and Holmes 2005. Mulvi-
hill et al. 2009) but it was not the case for this
flicker pair. The timing of the nests may have
been too close and the male was unable to
contribute sufficiently to two broods. Connor et
al. f 200 1 ) documented a similar unusual case of a
monogamous pair of Red-cockaded Woodpeckers
successfully reining two nestlings: one nestling
from each ot two simultaneous tree cavities.
Apparently the male and female incubated the
clutches alone, but each provisioned at both
cavities. The flexible roles of woodpeckers
suggest they may be in a transitory evolutionary
stage where true double-clutching and uniparental
care could evolve. However, the poor success
from such attempts suggests bi-parental care is
still needed to raise large or multiple broods.
ACKNOWLEDGMENTS
We thank Midori Mitsutam and Marika Van der Pol for
help finding nests and radio-tracking. This research was
funded by the Matson Foundation. NSERC Discovery
Cram (KLW), NSERC CGS (EAG). and Isabel Maria
Lopez Martinez Memorial Scholarship (EAG). This study
was conducted with permits from the University of
Saskatchewan Animal Care Committee.
LITERATURE CITED
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Successive clutches and parental roles in waders: the
importance of timing in multiple clutch systems.
Biological Journal of the Linnean Soceity 74:549-555.
Burley, N. 1980. Clutch overlap and clutch size:
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American Naturalist 115:223-246.
Connor. R. N„ J. R. McCormick. R. R. Schaefer, D.
Saenz, and D. C. Rudolph. 2001. A Red-cockaded
Woodpecker group with two simultaneous nesl trees
Wilson Bulletin 1 13:101-104.
Edwards, H, H. and G. D. Schnell. 2000. Gila
Woodpecker ( Melanerpes uropygialis). The birds of
North America. Number 532.
Gutierrez. R. J. and D. J. Delehanty. 1999. Mountain
Quail (Oreoryx pictus). The birds of North Ameri.'i
Number 457.
iNtiOLO. D. J. 1987. Documented double-broodedness in
Red-hcaded Woodpeckers. Journal of Field Ornithol¬
ogy 58:234-235.
Jamieson. 1. G.. J. L. Craig, and E. O. Minot 1987
Incubation by young, nonbreeding birds: pulenlial
versus realization of behaviour. Canadian Journal of
Zoology 65:2567-2570.
Eicon, .1. D 1999. The evolution of avian breeding systems.
Oxford University Press. New York. USA.
Moore.. D. J. and R. D, Morris. 2005. The production of
second clutches in the Common Tem: proximate effects
of timing and food supply. Waterhirds 28:458-467.
Mm vihii.l. R. S.. s. C. Latta. and F. L. Newell. 2009.
Temporal constraints on the incidence of double
brooding in the Louisiana Waterthrush Condor
111:341-348.
Nagy, L. R. AND R. T. Hoi mbs. 2005. Food limits annual
fecundity of a migratory songbird: an experimental
study. Ecology 86:675-681.
SMITH, I). R. AND j. N. Layne. 1986. Occurrence of a
double brood in Red-headed Woodpeckers in south
central Florida. Florida Field-Naturalist 14:98-99.
WlEBE, K. L. 2005. Asymmetric costs favor female
desertion in the facultatively polyandrous Northern
Flicker ( Colaptes auratus): a removal experiment.
Behav ioral Ecology and Sociobiology 57:429-U~.
WlHti . K. L. 2008. Division of labor during incubation in a
woodpecker Colaptes auratus w ith reversed sex roles
and facultative polyandry. Ibis 150:115-124.
Wiebe. K. L. and W. S. Moore. 2008. Northern Flicker
I Colaptes auratus). The birds of North America.
Number 166.
Wiebe. K. L. and B. Kempenaers. 2009. The social and
genetic mating system in flickers linked to partially
reversed sex roles. Behavioral Ecology 20:453-458
SHORT COMMUNICATIONS
393
The Wilson Journal of Ornithology 124(2): 393-396, 2012
Brood Sex Ratio of the Lilac-crowned Parrot {Amazona finschi)
Shannon M. Pease.1 Alejandro Salinas-Melgoza,' Katherine Renton,2
Patricia Escalante,3 4 and Timothy F. Wright14
ABSTRACT. — Evolutionary theory predicts birds
should adjust the sex ratio of their broods in response
to external factors that differentially affect the repro¬
ductive value of each sex. We examined the brood sex
ratio in the Lilac-crowned Parrot (Amazona finschi) in
relation to climate, hatching date, and hatching order.
We used polymerase chain reaction amplifications to
identify the gender of 66 nestlings from 32 clutches
-panning 7 years. There was a tendency to produce
more female offspring in years of high nestling survival
following high rainfall with a slight female-bias in
third-hatched nestlings. We found no significant
associations between brood sex ratio and rainfall,
hatching date, or hatching order within clutches. Our
results suggest the examined factors provide insufficient
differential costs or benefits of offspring gender to
promote sex ratio bias in this monomorphic species.
Received 17 August 2011, Accepted 29 November 201 1.
Animals that have the ability to alter the .sex
ratio of their offspring are predicted to do so as an
adaptive response to external factors (Trivers and
Willard 1973). Parents are expected to bias
offspring sex ratio toward the gender that will
yield the greatest fitness benefits (Trivers and
Willard 1973, Addison et al. 2008; but see
Fawcett et al. 2011). Factors shown to affect
brood sex ratio in birds include resource avail¬
ability' (Budden and Beissinger 2004, Addison
ei al. 2008). date of hatching (Dijkstra et al. 1990,
Radford and Blakey 2000). and sequence of
hatching (Genovart et al. 2003).
Strong dimorphism and non-monogamous mat¬
ing systems are usually an indication of strong
sexual selection, which may promote a bias in
hrood sex ratio at hatching (Hcinsohn et al. 1997.
Trewick 1997. Genovart et al. 2003), or second¬
1 Department of Biology. Mail Stop Code 3AF. New
Mexico State University. Las Cruces, NM 88003. USA.
Estacidn dc Biologta Chamela. Instituto de Biologfa.
Uiversidad Nacional Autonoma dc Mexico. Apartndo Postal
21. San Patricio. Jalisco, Codigo Postal 48980. Mexico.
Departamenio dc Zoologia. Institute dc Biologta. Uni-
versidad Nacional Autonoma dc Mexico, Mexico D.F.
4 Corresponding author; e-mail: wright@nmsu.edu
arily through differential mortality of young of a
specific gender (Pike and Petrie 2003. Addison
et al. 2008. Hcinsohn et al. 201 1 ). It remains less
clear whether monogamous or monomorphic
species should exhibit similar control over hrood
sex ratios.
Among parrots, the Eclectus Parrot ( Eclectus
roratus) and the Kakapo ( Stngops Itabroptila)
have shown extreme bias in brood sex ratio
(Hcinsohn et al. 1997, Trewick 1997. Hcinsohn et
al. 2011); both species are sexually dimorphic
with non-monogamous mating systems. In con¬
trast. no sex ratio bias was found in the sexually
monomorphic Yellow-napcd Amazon (Amazona
auropaUiata) (South and Wright 2002).
We studied the Lilac-crow ned Parrot (Amazona
finschi). a socially monogamous and sexually
monomorphic species endemic to the tropical dry
forest of western Mexico. Clutches are usually
small (mean = 2.6. range = 1-4 eggs), and eggs
hatch asynchronously (Renton and Salinas-
Melgoza 1999, 2004). There is no difference in
nestling growth rate between first- and second-
hatched chicks; third-hatched chicks demonstrate
significantly slower growth and lower probabili¬
ties of survival, while fourth-hatched chicks
occurred only in 1 year and all chicks died within
a few days of hatching (Renton 2002. Renton and
Salinas-Melgoza 2004). Previous work has shown
marked inter-annual variation in reproductive
success with fluctuations in rainfall resulting from
the El Nino-La Nina cycle of the Southern
Oscillation (Renton and Salinas-Melgoza 2004).
Thus, there is potential for inter-annual fluctua¬
tions in rainfall and resulting differential parental
investment to affect brood sex ratio in this
species.
We measured nestling sex ratio to test three
hypotheses that predict an association between
external factors and sex ratio. ( 1 ) We used annual
rainfall to test the local resource hypothesis, which
predicts a brood sex ratio bias in years of relative
resource abundance (Trewick 1997. Sasvari and
Nishiumi 2005), (2) We examined distribution of
males and females across the breeding season for
394
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 2. June 2012
TABLE 1. Lilac-crowned Parrot productivity and sex ratios from 2001 to 2009.
Breeding season Number of clutches Nestlings examined
Nestling survival
( lledglings/hatchlings l Proportion of males
2001
2002
2003
2004
2006
2007
2009
Overall
11
0.583
0.55
17
0.778
0.59
9
0.313
0.56
10
0.909
0.40
4
0.50
0.50
8
0.50
0.50
7
0.813
0.29
66
0.619
0.50
all years combined to test the date of hatching
hypothesis (Dijkstra et al. 1990. Genovart et al.
2003), which predicts manipulation of brood sex
ratio early in the season to allow more parental
investment and ensure survival of the most fit
young. (3) We examined the distribution of males
and females with hatching order within a clutch to
test the sequence of hatching hypothesis (Dijkstra
et al. 1990, Genovart et al. 2003). which predicts a
sex bias with order of hatching within clutches.
METHODS
The study population inhabits the tropical dry
forest o! the Chamela-Cuixmala Biosphere Re¬
serve along the Pacific Slope of Jalisco. Mexico.
Rainfall is highly seasonal with 80% occurring in
the rainy season from June to October (Bullock
1986). Lilac-crowned Parrots nest during the
dry season from February to May (Renton and
Salinas-Melgoza 1999). and fluctuations in rain¬
fall influence subsequent availability of food
resources (Renton 2001. 2002). We used the
amount of rainfall from June to February, the
period prior to egg laying, as a proxy for
environmental quality. We monitored 32 nesting
attempts between 2001 and 2009, and collected
f °-6
E °«
I “
a 02
e
0.1
200 400 600 800 1000
Rainfall Jun-Feb (mm)
FIG. 1. Linear regression of ihe proportion of m
L lac-crowned Parrot offspring produced in the populat
,ainfa" ” «
blood samples from 66 nestlings; no samples were
collected in 2005 or 2008. About 20 pL of blood
was collected when nestlings were >1 month of
age. Blood was stored in lysis buffer at -20 C
until analysis. Purified DNA was extracted using a
Qiagen DNEasy kit. The primer multiplex of Han
et al. (2009) (PO-P2-P8) was used for polymerase
chain reaction (PCR) amplification (conditions
available upon request). PCR products were
examined on a 2% agarose gel to score sex by
product size.
We calculated sex ratios for the entire data set and
by year. A Chi-square goodness of fit test was
applied to identify any deviation from a 0.5
proportion of males in the entire population of
nestlings. We used linear regression on the yearly
proportion of males with the amount of rainfall poor
to egg-laying to evaluate whether sex ratio wa-
related to environmental quality. The breeding
season was divided, for analysis of hatch date, into
three hatch periods of equal length between the
earliest (26 Feb) and latest (1 Apr) recorded hatch
date over the 7 years, and young were assigned to a
period by hatch date. We used Chi-square contin¬
gency table analysis to examine whether offspring
gender was associated with (I ) hatching period, and
(2 ) hatching order within a clutch (first, second or
third-hatched). We used nominal logistic regression
to examine the effects of rainfall prior to egg-laying
hatch date, and hatch order on gender of nestlings
1 ABLE 2. Frequency of male and female Lilac-crowned
Parrot offspring by hatching order.
Hatching order
Males
Females
First hatched
15
14
Second hatched
15
13
Third hatched
3
6
SHORT COMMUNICATIONS
395
Sex ratios are presented as mean ± SD and
significance was set at P < 0.05.
RESULTS
The overall sex ratio was 50 % male with 33
males and 33 females of 66 nestlings (Table 1).
The annual sex ratio was 48.3 ± 1 0.6% males, and
ranged from 28.6% males in 2009 to 58.8% males
in 2002 (Table 1). The number of males produced
per year did not differ {X:6 = \A,P> 0.05) from
the number of males expected assuming a 1 : 1 ratio
(Table 1). There w as a tendency to produce more
females following periods of high rainfall (Fig. I ),
particularly in 2004 and 2009. when nestling
survival was high (Table 1). However, there was
a 50:50 sex ratio in 2007 following the highest
annual rainfall of 1.065 mm. Overall, the annual
nestling sex ratio w-as not related < R: = 0.4 1 3: F \ 5
- 3.5, P = 0.12) to environmental quality as
indicated by rainfall (Fig. 1).
The frequency of offspring gender was not
associated with date of hatching (X\ = 1.8. P =
0.88). Twenty-two nestlings hatched in the early
period of which 54.5% were male; 28 nestlings
hatched in the middle period with 39.3% males,
and 14 nestlings hatched in the late period with
57.1% males. There was no association of nestling
sex ratio with hatching order (X‘\ - 0.68, P =
0.61). However, 51.7% of first-hatched nestlings
were males and 53.6% of second-hatched nestlings
were males whereas third-hatched nestlings were
only 33.3% males (Table 2). A nominal logistic
regression showed no effect of rainfall prior to egg-
laying. hatch date or hatch order on nestling sex
(Whole Model X\> = 3.7. P = 0.92)
DISCUSSION
We found no evidence of modification of brood
sex ratio by the Lilac -crowned Parrot for the
variables evaluated. Our results did not support
the local resource hypothesis, although we
observed a tendency to produce more females
following periods of high rainfall when there was
high nestling survival. The date of hatching
hypothesis was also not supported by our results.
However. Lilac-crowned Parrots exhibit high
synchrony in nest initiation (Renton and Salinas-
Melgoza 1999), which may limit the influence of
hatching date on brood sex ratio. We found no
significant association of sex ratio with hatching
order, although our data indicate a slight female-
bias in third-hatched nestlings. The sexually
dimorphic Common Kestrel {Falco tinnunculus )
and Audouin’s Gull ( Ichthyaetus audouinii ) both
produce more males in early clutches and fewer
males later in the season (Dijkstra el al. 1990,
Genovart el al. 2003). There may be a tendency for
Lilac -crowned Panels to produce more female
offspring in years of high nestling survival by
producing larger clutches with a slight female-bias
in third-hatched nestlings; a larger sample size may
be required to detect significant associations.
One possible explanation for the lack of
evidence in our study is that the factors evaluated
do not affect the costs or benefits associated with
rearing either males or females (Radford and
Blakey 2000). The factors we evaluated have been
associated w ith sex ratio manipulation in strongly
dimorphic parrot species (Trew ick 1997, Heinsohn
et al. 201 1 ). but they may not result in differential
costs or benefits in monomorphic species like the
Lilac-crowned Parrot or the Yellow-naped Ama¬
zon (South and Wright 2002). In addition,
restrictions imposed by chromosomal sex-determi¬
nation could prevent females from altering the
primary sex ratio of their offspring (Pike and Petrie
2003; but see Heinsohn et al. J997. Genovart et al.
2003). However, some studies suggest this con¬
straint can he overcome, although the mechanisms
are not well understood (West and Sheldon 2002.
Korsten el al. 2006).
ACKNOWLEDGMENTS
Research and CITES export permits were provided by
the Secretaria del Medio Ambicntc (SF.MARNAT) in
Mexico and CITES import permits by the U.S. Fish and
Wildlife Service. S. M. Pease conducted this project while
participating in the NMSU-Howard Hughes Medical
Institute Research Scholar Undergraduate Research Schol¬
ars Program. We are grateful lor logistical and financial
support from the Fundacion Ecologies de Cuixmala,
Denver Zoological Foundation, World Parrot Trust (to K.
Renton), and NSF grant IOS-0725032 and REU supple¬
ment IOS-0940689 (to T. F. Wright). We thank Elizabeth
Hobson and Erie Pease for helpful comments on this
manuscript.
LITERATURE CITED
Addison, B.. A. S. Kitaysky. and J. M. Hipfner. 2008.
Sex allocation in a monomorphic seabird with a single-
egg clutch: test of the environment, mate quality, and
female condition hypotheses. Behavioral Ecology and
Sociobiology 63-135-141.
Bidden. A. E. and S. R. Beissinger. 2004. Against the
odds? Nestling sex ratio variation in Green-rumpcd
Parrotlets. Behavioral Ecology 15:607-613.
BlELOCK, S. H. 1986. Climate of Chamela, Jalisco, and
trends in the south coastal region of Mexico. Archives
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THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 2. June 20/2
for Meteorology, Geophysics and Bioclimatology B
36:297-316.
DiJKSTKA, C, S. Daan. AMD J. B. Bi kf.r. 1990. Adaptive
seasonal vanation in the sex ratio of kestrel broods.
Functional Ecology 4:143-147.
Fawcett, T. W„ B. Kiuper. F. J. Weissing. and I. Pen.
2011. Sex-ratio control erodes sexual selection,
revealing evolutionary feedback from adaptive plas¬
ticity. Proceedings of the National Academy of
Sciences of the USA 38:15925-15930.
Genovart. M.. D. Oro. X. Ruiz, R. Griffiths, P.
Monaghan, and R. G. Nager. 2003. Seasonal
changes in brood sex composition in Audouin's Gulls.
Condur 105:783-790.
Han, J.-l.. J.-H. Kim, S. Kim. S R. Park, and K.-J. Na.
2009. A simple and improved DNA test for avian sex
determination. Auk 126:779-783.
Heinsohn. R.. S. Leoge. and S. Barry. 1997. Extreme
bias in sex allocation in Lr leans parrots. Proceedings of
the Royal Society of London, Series B 264: 1 325 1 329.
Heinsohn. R.. N. H. LaNGMOre, A. Cockbi'RN. and H.
Kokko. 201 I. Adaptive secondary sex ratio adjustments
via sex-specific infanticide in a bird. Current Biology
2LI744-1747. DOl 10. I016/j.cub.20l 1.08.064
Korsten. P„ C. K. M. Lessei.es, A. C. Maikman. M. van
der Velde, and J. Komdhur. 2006. Primary sex
ratio adjustment to experimentally reduced ’ male
UV attractiveness in Blue Tits. Behavioral Ecology
17:539-546.
Pike. T. \\. and M. Petrie. 2003, Potential mechanisms of
avian sex manipulation. Biological Reviews of the
Cambridge Philosophical Society 78:553-574.
Radford. A. N. and J. K. Blakey. 2000. Is variation in
brood sex ratios adaptive in the Great Tit
major l? Behavioral Ecology 1 1 294-298.
Renton, K. 2001 Lilac-crowncd Parrot diet and iood
resource availability: resource tracking by a pm*
seed predator. Condor 103:62-69.
Ren ton. K. 2002. Influence of environmental vanabilitv on
the growth of Lilac-crowned Parrot nestlings. Ibis
144:331-339.
Renton. K. and A, Saunas-MelGOZA. 1999 Nesting
behavior of the Lilac-crowned Parrot. Wilson Bulletin
111:488-493.
Renton, K. and A. Saunas-MelGOZA. 2004. Climatic
variability, nest predation, and reproductive output of
Lilac-crowncd Parrots (Amazana finschi ) in tropical
dry forest of western Mexico. Auk 121:1214-1225
SasvAri. L. and I. Nishiumi. 2005. Environmental
conditions affect offspring sex-ratio variation ami
adult survival in Tawnv Owls. Condor 107:321-
326.
South, j. M. and T. F. Wright. 2002. Nestling sex ratios
in the Yellow-naped Amazon: no evidence tor
adaptive modification. Condor 104:437-440.
I REWICK. S. A. 1997. On the skewed sex ratio of Ac
Kakapo Strigups hahroptilus'. sexual and natural
selection in opposition? Ibis 139:652-663.
Pig vers. R. I.. and D. R. Willard. 1973. Natural selection
ol parental ability to vary the sex ratio of offspring.
Science 1 79:90-92.
West. S. A. and B. C. Sheldon. 2002. Constraints in the
evolution of sex ratio adjustment. Science 295: 1685-
1688.
The Wilson Journal of Ornithology 1 24(2):396— 399. 2012
Multiple Male Feeders at Nests of the Veery
Matthew R. Halley1 2 and Christopher M. Heckscher1
ABSTRACT.— We present the first documentation of
nestling care by multiple male feeders at nests of the
Veery ( Catharus fuscescens) in a Mid-Atlantic Pied¬
mont forest in northern Delaware. This is only the
second confirmation of this behavior in a Nearetic-
neotropicul migrant songbird. Five of six nests (83%)
were anended by a male that concurrently fed nestlings
at a second or third nest. Three of six nests (50%) were
attended by one female and two males. No females were
observed at more than one nest. We monitored >140
Veery nests at our study site since 1998. and believe the
dense breeding habitat and single-brooded nature of the
ware , Agneulti.ro and Natural Resources. D
ware State University. Dover. DE 19901. USA
Corresponding author: e-mail:
matthewhalley@gmail.com
Veery have inhibited our ability to confirm this
behavior prior to 201 1. Our data suggest this behavior
is widespread in our study population. Received 25 July
2011. Accepted 30 November 2011.
Avian mating systems that feature multiple male
feeders attending a single-female brood tire rare but
taxonomieally widespread, and documented for uni'
14 species representing nine families (Brown l1--
Hartley and Davies 1994. Ligon 1999. Goetz et i
2003). This type of behavior is especial!}' rare anw-
long-di stance migrant songbirds. Only Smith -
Longspur (Calcar ins pictus) (Briskie et al. IW
and Bicknell’s Thrush ( Catharus bickttelli) (Goetz a.
al. 2003) in North America feature provisioning by
SHORT COMMUNICATIONS
397
TABLE 1. Methods of observation for six nests of the
Veery. each attended by a single female (A-F). in a
Delaware Piedmont forest, 2011.
Female
S of Males
Method
Time (hrs)
A
2
Video
16.9
B
1
Direct
<1.0
C
1
Video
6.3
D
2
Both
10.1
E
2
Direct
<1.0
F
1
Video
18.7
multiple male feeders despite engaging
in annual
long-distance
migration.
Modes of parental care
among the Turdidae that
involve more
than two
adults per nest are only known from 3% ot the
species (Cockburn 2006). We present the first
documentation of multiple male feeders at nests of
the Veery (C. fuscescens), a Nearetic-neotropical
migratory thnish long considered to be monogamous.
METHODS
Research was conducted at White Clay Creek
State Park, New Castle County. Delaware (39 44'
N, 75 45' W), on the floodplain of a Middle-
Atlantic Piedmont forest (Heckscher 2004) during
May and June 2011. We monitored six Veery
nests (Table I) from time of discovery until
Hedging or failure with field observations and
use of a compact digital video camera (Oregon
Scientific ATC2K, Tualatin, OR, USA). The
small video camera was placed <1 m from the
nest in each case, covered in camouflage, and
concealed in natural vegetation. Adult Vecries
were handed with unique color combinations and
subsequently identified on film or via binoculars.
All six nests were in dense forest understory
dominated by the invasive shrub Rosa muUiflora.
Nests were located using behavioral cues, most
often during the nestling phase, as adults made
regular trips to the nest with food, Only one nest
was found and monitored prior to hatching.
RESULTS
We observed 1 1 adult Vecries provisioning
nestlings at six nests (Fig. I ). All females (n = 6)
fed a single brood while males ( n - 5) were
observed provisioning nestlings at one (2 of 5
males), two (2 of 5), or three ( 1 of 5) nests. Five of
six broods (83%) were attended by a male that was
detected provisioning nestlings at a second or third
nest. Three of six broods (50%) were attended by
Males Females
FIG. 1. Males (1-5) and females (A-F) with their
respective parental contributions at six Veery' nests (black
circles) in a Piedmont forest in Delaware. Solid lines
represent feeding behavior that was captured on video or
observed in the field.
multiple male feeders. We observed only one male
and one female feeder at one nest (17%).
We examined 52 hrs of video footage from four of
the six nests (Table 1; mean ± SD = 13.0 ± 5.8 hrs;
range = 6.3-18.7 hrs). Adult feeders for nests lacking
footage were identified in the field using binoculars.
Only four nests were filmed for >6 hrs and our
findings may underestimate the incidence of multiple
male feeders at these nests. These males may also
have attended additional nests that were not observed.
On the morning of 20 June, MRH observed a
Cooper's Hawk ( Accipiter cooperii) approach
within 10 m of a monitored nest with mature
nestlings (<24 hrs from Hedging). All three adult
feeders, previously identified from video footage,
were observed vigorously defending the nest site,
calling emphatically and making diving flights in
the direction of (he hawk, which subsequently
retreated. A similar defense by multiple males
was also observed at a second nest on 27 June
(also with nestlings <24 hrs from fledging).
Defensive behavior involving three adults was
observed at two of the three nests (67%) that were
atiended by multiple male leeders.
DISCUSSION
Our confirmation of multiple male feeders at
Veery nests is the first for this species and only
the second report for a Nearctic-neotropical
migratory songbird. Provisioning strategies ob¬
served in our study are consistent with descrip¬
tions of the variable polygynandrous mating
system of congeneric Bicknell s Thrush (Goetz
398
THE WILSON JOURNAL OF ORNITHOLOGY • Vo/. !24. No. 2. June 2012
TABLE 2. Distances (m) among six Veery nests in a Piedmont forest in Delaware, 2011. Nests A. D. and E were
visited by multiple male feeders. Nests A-E were visited by a male that also attended another nest. Nest F was attended bv a
socially monogamous pair.
Nest
A
B
c
D
E
F
A
-
169.1
127.1
55.9
80.1
357.4
B
169.1
-
290.2
168.2
216.1
526.5
C
127.1
290.2
-
126.8
147.9
244.3
D
55.9
168.2
126.8
—
134.8
370.4
E
80.1
216.1
147.9
134.8
__
332.9
F
357.4
526.5
244.3
370.4
332.9
et al. 2003) including: (I) males attending
multiple nests, (2) multiple male feeders at
single-female nests, and (3) a monogamous pair.
We monitored >140 Vccry nests al our study site
since 1998, but provisioning by multiple males was
not confirmed until 2011. .Several observations
suggested that Veeries at our site may have engaged
in this behavior in previous years, but confirmation
did not occur prior to use or video cameras. Our
ability to confirm the presence of multiple male
feeders was likely diminished by dense understory
vegetation at nest sites (Hcckscher 2004) and the
single-brooded nature of this species (Heckscher
2007). These observatioas suggest multiple males
provisioning single broods and provisioning simulta¬
neously at multiple nests is widespread in our
population in at least some years. Parental care
strategies may exhibit annual fluctuations in frequen¬
cy and distribution (Brown 1987. Davies 1992).
Multiple male provisioning strategies at our study site
may be facultative (i.c.. influenced by factors that
vaiy from year to year, including breeding synchrony,
sex ratios, density ot breeders, and availability of
suitable habitat). Males that were detected provision¬
ing at multiple nests did not necessarily provision at
the nearest available nest (Table 2), but asynchronous
nestling periods do not make it possible to rule out
nest proximity as a factor influencing helping
behavior.
Veeries at our study site have a social
dominance hierarchy among males dependent on
age or time spent in the population (Heckscher
2007). Territorial aggression among male Veeries
is common (Dilger 1956, Heckscher 2007), unlike
Bicknell’s Thrush (Ritnmer et al. 2001. Goetz
et al. 2003). However, Heckscher (2007) found
dominant males tolerated nests of subordinate
males within their territories while maintaining
nests ol their own and continuing to defend
against adjacent territorial males. This resulted in
overlapping home ranges among male Veeries, a
feature that has been shown to facilitate polyan-
drous mating behavior in other species (Davies
1992, Goetz et al. 2003). Aggressive behavior
described in the context of intraspecific territorial
exclusion (e.g., Dilger 1956) may also have a role
in establishment of relationships among males
that provision at the same nest (MRH. unpubl.
data). Our discovery of multiple male feeders for
a single clutch provides a new context for
interpreting foundational studies of Veery behav¬
ioral ecology including intraspecific hostile inter¬
actions (Dilger 1956) and use of the vocal
repertoire in communication (Heckscher 2007 1.
Ihe close phylogenetic relationship between
Bicknell’s Thrush and the Veery (Ellison 2001.
Outlaw ct al. 2003. Winker and Pmett 2006). and the
general similarities between nestling care in these
species, warrant a re-evaluation of hypotheses
regarding the evolutionary history of parental care
in Cailtanis thrushes. The evolutionary origin of this
behavior is unlikely to bo explained by ecological
constraints experienced by BickneU's Thrush alone,
such as harsh montane weather (Goetz et al. 2003) or
food shortage (Strong et al. 2004). as Veeries breed at
lower elevations in broadleaf forests that lack these
extreme conditions. Future studies of the pooriy-
known Gray-cheeked Thrush (C. minimus) and the
Ruddy-capped Nightingale Thrush (C Jruntzii)
may help define whether parental care among these
closely-related species is (1 ) recently evolved, (2)
plesiomorphic within the bicknelli clade (Outlaw ct
al. 2003), or (3) derived from a more distant
Caiharus ancestor. Future studies of Veery breed¬
ing ecology may clarify or reveal the role of
hierarchies, genetic relatedness among multiple
male feeders, and extra-pair paternity within the
mating system of this secretive forest thrush.
ACKNOWLEDGMENTS
This study was conducted with the support of the Center
for Integrated Biological and Environmental Research.
SHORT COMMUNICATIONS
399
College of Agriculture and Related Sciences, Delaware
State University. We thank Nicholas McFadden, the staff of
White Clay Creek State Park, and the Delaware Division of
Parks and Recreation for their cooperation.
LITERATURE CITED
Briskie. J. V., R. Montgomerie, T. Poldmaa. and P. T.
Boag. 1998. Paternity and paternal care in the
polygynandrous Smith’s Longspur. Behavioral Ecolo¬
gy and Sociobiology 43: 1 8 1 - 1 90.
Brown. J. L. 1987. Helping and communal breeding in
birds: ecology and evolution. Princeton University
Press. Princeton, New Jersey. USA.
Cockbl'RN, A. 2006. Prevalence of different modes of
parental care in birds. Proceedings of the Royal
Society of London. Series B 273:1375-1383.
Davies, N. B. 1992. Dunnock behaviour and social
evolution Oxford University Press. Oxford, United
Kingdom.
Dilger. W, C. 1956. Hostile behavior and reproductive
isolating mechanisms in die avian genera Catharus
and Hylocichla. Auk 73:313-353.
Ellison, W. G. 2001. Population structure and gene flow in
two long-distance migrant birds, the Bicknell’s Thrush
(Catharus bicknelli) and Veery (C. fusccsccns). Disser¬
tation. State University of New York at Albany, USA.
Goetz. J. E„ K. P. McFarland, and C. C. Rimmp.r. 2003.
Multiple paternity and multiple male feeders in Bick¬
nell’s Thrush ( Ciitluiivs bicknelli). Auk 120:1044-1053.
Hartley, I. R. and N R. Davies. 1994. Limits to
cooperative polyandry in birds. Proceedings of the
Royal Society of London. Series B 257:67-73.
Hi c ksc her. C. M. 2004 Veeiy nesi sites in a Mid-Atlantic
Piedmont forest: vegetative physiognomy and use of
alien shrubs. American Midland Naturalist 151:326-337.
HkckscHER, C. M. 2007 Use of the Veery- (Catharus
fuscescens) call repertoire in vocal communication.
Dissertation. University of Delaware, Newark, USA.
I uiON. J. D. 1999. The evolution of avian breeding systems.
Oxford University Press. Oxford. United Kingdom.
Outlaw. D. C. G. Voelker, B. Mn a, and D. J. Girman.
2003. Evolution of long-distance migration in and
historical biogeography of Carbarns thrushes: a
molecular phylogenetic approach. Auk 120:299-310.
Rimmer. C. C, K. P. McFarland, W G. Ellison, and
J. E. Goetz. 2001. BicknelFs Thrush ( Catharus
bicknelli). The birds of North America. Number 592.
Strong. A. M.. C. C. Rimmer. and K. P. McFarland. 2004.
Effect of prey biomass on reproductive success and
mating strategy of Bieknell's Thrush (Catharus bick¬
nelli). a polygynandrous songbird. Auk 121 :446-451.
Winker. K. and C. L. Pruett. 2006. Seasonal migration,
speciation, and morphological convergence in the
genus Catharus (Turdidae). Auk 123:1052-1068.
The Wilson Journal of Ornithology 1 24(2): 399-402, 2012
Nestling Diet of Eastern Meadowlarks in East-central Illinois
Susan Linn Ostrand12 and Eric K. Bollinger1 3
ABSTRACT. — We observed Eastern Meadowlark
(Stumelia magna) nests in Conservation Reserve Pro¬
gram grasslands in east-central Illinois to examine the
influence of tile surrounding agricultural landscape on
nestling diets. Esophageal ligatures were applied to 3-
and 6-day old nestlings to examine food items brought to
the nest. The most common items were spiders (44% of
total volume; primarily wolf spiders [Hogna spp.J),
followed by orthopierans (23%; crickets, grasshoppers,
and katydids), and lepidopteran larvae (18%, primarily
cutworms). Adult Eastern Meadowlarks foraged more
often than expected in soybean fields. Received 8 August
2011. Accepted 21 November 201 1.
1 Department of Biological Sciences. Eastern Illinois Uni¬
versity, Charleston. IL 61920. USA.
2 Current address: 663 Winding View. New- Braunfels.
TX 78132. USA.
3 Corresponding author; e-mail: ckhollinger@eiu.edu
Grassland ecosystems in the Midwestern Unit¬
ed States have been reduced and fragmented,
largely due to expansion of rowerop agriculture
(Herbert 1995. Askins et al. 2007, Walk et al.
2010). Wildlife depending on these habitats
consequently has been affected, including grass¬
land birds, which have typically exhibited dra¬
matic population declines in the last 50 years
(Bollinger and Gavin 1992, Askins 1993, Herbert
1995, Vickery and Herbert 2001, Sauer et al.
2008). The remaining grasslands lend to occur in
small, scattered patches surrounded by large tracts
of agricultural land, negatively affecting area-
sensitive grassland birds (Ribic et al. 2009). Many
birds have been shown to use rowerop agriculture
(Bollinger and Caslick 1985b; Best et al. 1995,
1998; Boutin et al. 1999; Kershner et al. 2004;
Walk et al. 2010) for multiple reasons including
both foraging and nesting. Relatively little
400
THE WILSON JOURNAL OF ORNITHOLOGY • Vo/. 124. No. 2, June 2012
information is available regarding the interactions
between grassland birds and rowerops (such as
corn and soybeans) that have the potential to be
mutually beneficial (e.g., Bollinger and Caslick
1985a).
Eastern Meadowlarks (Stumella magna) inhab¬
it a wide variety of grassland habitats throughout
the Midwest (Bollinger 1995, Lanyon 1995.
Kershner 2001, Ribic and Sample 2001, Walk
et al. 2010). preferring to forage on the ground
and primarily feeding on arthropods (Beal 1948.
Lanyon 1995). Nestling diets of Eastern Mead¬
owlarks have not been closely studied. However,
movements of adults have been monitored using
radiotelemetry, indicating they routinely forage in
rowerops. especially soybeans (Kershner 2001,
Kershner et al. 2004). These findings suggest
further study of the importance of grassland
patches within a rowerop agricultural land matrix
is warranted. We examined (he nestling diet of
nesting Eastern Meadowlarks in grasslands adja¬
cent to corn and soybean fields.
METHODS
Study Area. — We conducted research in eight
Conservation Reserve Program (CRP) fields
ranging in size from 1.35 to 20.80 ha. These
fields were planted primarily with redtop (Agros-
tis alba) and orchard grass ( Dactyl is glome rata).
All CRP tracts were bordered on most sides by
corn and soybean fields with some small forest
fragments and wooded hedgerows.
Nest location.— We located nests using die
rope dragging technique (Higgins ct al. 1969).
Each nest was marked 5 m to the north with
flagging tape. We recorded nest status and
monitored each nest every third day until fledgina
or nest failure, noting the date, the number of eggs
or nestlings, female presence, and condition of
eggs (warm or cold).
Nestling Diet.— We assessed types of foods fed
to nestlings using esophageal ligatures. This
technique was performed at each nest twice (3-
and 6-day old nestlings) during the 10-day nestling
period. One person removed all of the nestlings
after a parent had been observed leaving a nest and
brought them to an area at least 100 m from the nest
to apply ligatures. Ligature materials consisted of
10.2-cm cable ties (Mellot and Woods 1993).
These were fastened around the necks and adjusted
so individuals could breathe but not swallow food
items. Nestlings were returned to the nest after
igature application (~J min/bird), and left for a
period of 20-60 min or until two foraging trips of
adults had been observed. Nestlings were once
again removed from the nest, and food was
transferred from their esophagus and placed into
a vial of 80% ethanol. Food items from each nest
were placed into separate vials. Volumes wete
measured by liquid displacement (Bollinger and
Caslick 1985b). Mealworms were given to each
nestling to replace the lost meal and nestlings were
subsequently returned to the nest. We combined
data from the different age classes to increase
sample sizes.
RESULTS
We collected 29 ligature samples from 19
different Eastern Meadowlark nests between April
and August 2002. Spiders (Araneae). including
egg sacs, represented the largest volume of food
items (44%) as well as the largest number of
individual food items (53%). The most common
lamily of spiders was Lycosidae (wolf spiders,
primarily Hogna spp., 80% of spider specimens).
Other lamilies included jumping spiders (Salt-
icidae), 10%; crab spiders (Thomisidae), 4%; orb
weavers (Araneidae), 4%; and sac spiders (Gna-
phosidae), 2%. Orthopterans comprised the sec¬
ond largest volume of food items (23%, 13.5% of
food items) including crickets (Gryllidae). 46% of
orthopterans: grasshoppers (Acrididae). 31%;
and katydids (Tettigonidae), 23%. Lepidoptera
larvae followed closely with 18% of the specimen
volume (14.6% of items), consisting mostly of
cutworms (Noctuidae), 73% of lepidopterans:
and sullur butterfly caterpillars, (Pieridae), 27%.
Adult lepidopterans were not found in our ligature
samples. Other taxa were Coleoptera (mostly
Carabidae and Scarabidae), 10.8% (15.6% of
items), Homoptera (Cicadidae), 2.0% (1% of
items), and Hemiptera (Pentotomidae). 1.9%
(2.1% of items).
DISCUSSION
Composition of Nestling Diet.— Previous stud¬
ies examining the diet composition of adult
Eastern and Western ( Stumella neglecta) mead¬
owlarks revealed several dietary preferences.
Orthopterans composed the largest proportion of
animal matter, whereas beetles and caterpillars
also were commonly found in the stomachs of
these birds ( Beal 1948. Bent 1958). Spiders were
occasionally identified, but they were not ob¬
served in large numbers and contributed little to
overall prey percentages (Beal 1948). However.
SHORT COMMUNICATIONS
401
prey items fed to nestlings during our study
indicated Eastern Meadowlarks exhibited clear
preferences for arachnids when feeding their
young. Spotted Flycatchers (Muscicapa striata)
have also been observed to feed nestlings prey
items deviating from their usual diet (Davies I ‘>77 ),
possibly due to travel time pressures during active
brood rearing. Possible time constraints resulting
trom nestling nutritional and brooding require¬
ments could also exist for meadowlarks during the
breeding season. Spiders were also the primary
invertebrates fed to nestling Eastern Bluebirds
(Sialia sialis) and Great Tits (Purus major)
iRoyama 1970. Pinkow'ski 1978); this was attributed
to tlieir relatively soft body parts and appendages
(Pinkowski 1978) as well as their higher caloric
values compared to most orthopterans and annelids
(Colley 1961. Van Hook 1971).
CONSERVATION IMPLICATIONS
Nesting meadowlarks in our study commonly
foraged in soybean fields (21% ol Imaging trips;
Linn 2004). Arachnids in our ligature samples are
suggestive of soybean agroecosystems as likely
food sources for nestlings (Ferguson cl al. 1984,
Carter and Rypstra 1995). Thus, soybean fields,
if they provide a large amount of arachnid prey
items, benefit Eastern Meadowlarks. However,
spiders are thought to be important for natural pest
removal, and foraging meadowlarks may actually
have a negative economic impact in soybeans.
Whether or not economically significant amounts
of these arthropods are being consumed by
meadowlarks and other birds should be investi¬
gated further.
ACKNOWLEDGMENTS
Wolf spiders (primarily Hogna spp.) comprised
the largest number and volume of items fed to the
nestlings. One possible explanation for the large
quantity of Lycosidae could be that wolf spiders
are often relatively large and commonly occupy
surface habitats in many different terrestrial
ecosystems (Marshall and Rypstra 1999). making
them more likely to be detected by ground-
We thank N. C. Hudson. E. U. Grissom. J. B. Towey,
p. C. Enslrom. and E. I. Greig for field assistance. We thank
Eastern Illinois University's (EIU) Council for Faculty
Research, the graduate school of EIU. and the Champaign
County Audubon Society's Kendeigh Memorial Student
Research Fund for financial support. P. V. Switzer. T. A.
Nelson, and S. J. Meiners helped with manuscript review and we
are grateful to R. C. Funk for help wiUi arthropod identification.
foraging meadowlarks than other spider taxa. Size
and ease of detection of available prey influence
avian food selection (Bryant 1973). The majority
of the spiders were females carrying egg sacs and,
because female wolf spiders are invariably larger
than males, their size and prominent egg sacs
could also make them more conspicuous to
foraging meadowlarks.
The second and third largest percentage of
prey items were orthopterans and iepidopteran
larvae, common foods of adult meadowlarks
(Beal 1948) and easily found in surrounding
grasslands and soybean fields throughout the
breeding season. Cutworms were also common
food items fed to young Eastern Bluebirds
'Pinkowski 1978). Few hemipierans and homop-
lerans were fed to nestling meadowlarks during
the breeding season. The scarceness of these taxa
could result from these prey types being more
difficult for nestlings to digest or could have
greater handling times, thus decreasing their
caloric value (Einlen 1966, Pinkowski 1978).
The immature gut of developing birds can lead to
less efficient means of obtaining proper nourish¬
ment ( Karasov 1990), and the possibility of
feeding nestlings more soft-bodied arthropods
could potentially aid in brood survival.
LITERATURE CITED
ASKINS. R. A. 1993. Population trends in grassland,
shrubland. and forest birds in eastern North America.
Current Ornithology 11:1 -34.
Askins, K. A., F. CliAVr.z-RA.MlRt/.. B. C Cole, C. A.
Haas. .1. R. Herkert, F. U. Knopf, and P. D.
Vickery. 2007. Conservation of grassland birds in North
America: understanding ecological processes in different
regions. Ornithological Monographs Number 64.
Beal, p-. E. L. 1948. Some common birds useful to the
farmer. Conservation Bulletin IS. USD1. Fish and
Wildlife Service. Washington. D.C., USA.
Bent, a. C. 1958. Life histories of North American
blackbirds, orioles, lanagers. and allies. Dover Publi¬
cations, New York, USA.
Best. L. B.. K. E. Freemark, and J. J. DinsmciRE. 1995. A
review and synthesis of habitat use by breeding birds
in agricultural landscapes of Iowa. American Midland
Naturalist 134:1-29.
Best. L. B.. H. Campa, and K. E. Kemp. 1998. Avian
abundance in CRP and crop fields during winter in the
Midwest. American Midland Naturalist 139:311-324.
BOLLINGER. E. K. 1995. Successional changes and habitat
selection in hayfield bird communities. Auk 1 12:720-
730.
Bollinger, E. K. AND J. W. CASLICK. 1985a. Northern corn
rootworm beetles near a Red-winged Blackbird roost.
Canadian Journal of Zoology 63:502-505.
Bollinger. E. K. and J. W. Casuck. 1985b. Red-winged
Blackbird predation on northern corn rootworm
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beetles in field com. Journal of Applied Ecology
22:39-48.
BOLLINGER. I:. K. AND T. A. Gavin. 1992. Eastern
Bobolink populations: ecology and conservation in
an agricultural landscape. Pages 497-5(16 in Ecology
and conservation of neotropical migrant landbirds
(J. M. Hagan III and D. W. Johnston. Editors).
Smithsonian Institution Press, Washington, D.C., USA.
Boutin. C.. K. E. Freemark. and D. A. Kirk. 1999.
Farmland birds in southern Ontano: field use, activity
patterns and vulnerability to pesticide use. Agriculture,
Ecosystems, and Environment 72:239-254.
Bryan i, D, M 1973. The factors influencing the selection
ot food by Ihe House Martin ( Delichon urhica |L|)
Journal of Animal Ecology 42:539-564.
Carter. P. F. and A. L. RYpstra. 1995. Top-down effects
in soybean agroecosystems: spider density affects
herbivore damage. Oikos 72:433-439.
Davies, N. B, 1977. Prey selection and the search strategy of
the Spotted Flycatcher ( Musckapa striata ): a field study
on optimal foraging. Animal Behaviour 25:1016-1033.
Emlen, .1. M. 1966. The role of time and energy in food
preference. American Naturalist 100:611-617.
Ferguson. H. J.. R. M. McPherson, and W, a. Allen.
1984. Ground- and foliage-dwelling spiders in four
soybean cropping systems. Environmental Entomolo¬
gy 13:975-980.
Goi.ley. F. B 1961 Energy values of ecological materials.
Ecology 42:581-584.
Herkf.rt. J. R. 1995. An analysis of Midwestern breeding
bird population trends: 1966-1993. American Midland
Naturalist 134:41-50.
Higgins. K. F.. L. M. Kirsch, and 1. J. Ball. 1969. A
cable-chain device for locating duck nests. Journal of
Wildlife Management 33:1009-1011.
Karasov. W. H. 1990. Digestion in birds: chemical and
physiological determinants and ecological implica¬
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Kershner. E. L. 2001, Conservation of grassland birds in
an agricultural landscape: the importance of habitat
availability and demography. Dissertation. University
of Illinois, Urbana. USA.
Kershner. E. L., J. W. Walk, and R. E. Warner. 2004.
Breeding-season decisions, renesting, and annual
fecundity of female Eastern Meadowlarks ( Stumella
manna) in southeastern Illinois. Auk 121:796-805
1-ANYON, W. E. 1995. Eastern Meadowlark {Stumella
manna). The birds of North America. Number 160.
Linn, S. A. 2004. Impacts of agricultural landscapes on the
breeding biology and behavioral ecology of grassland
birds. Thesis. Eastern Illinois University. Charleston.
USA.
Marshall. S. D. and A. L. Rypstra. 1999. Patterns m the
distribution of two wolf spiders (Araneac: Lycosidaei
in two soybean agroecosystems. Population Ecology
28:1052-1059.
Mellot. R. S. and P. F. Woods. 1993. An improved
ligature technique for dietary sampling in nestling
birds. Journal of Field Ornithology 64:205-210.
PtNKOWSKI. B. C 1978. Feeding of nestling and tledglrng
Eastern Bluebirds. Wilson Bulletin 90:84-98.
Rime. C. A. and D. W. Sample. 2001. Associations of
grassland birds with landscape factors in southern
Wisconsin. American Midland Naturalist 146:105-121.
Rime'. C. A.. R. R. Koford, J. R. Hkrkert. D. H. Johnson.
N. D. Niemuth, D. E. Naugle. K. K. Bakkfr. D. W.
Sample, and R. B. Renfrew, 2(X)9. Area sensitivity in
North American grassland birds: patterns and process¬
es. Auk 126:233-244.
Royama, T. 1970. Factors governing the hunting behavior
and selection of food by the Great Tit (Parus major
I-)' Journal of Animal Ecology 39:619-668.
Sauer. J. R„ J. E. Hines, and J. Fallon. 2008. The North
American Breeding Bird Survey, results and analysis
1966-2007. Version 5.15.2008. USGS. Patuxent
Wildlife Research Center. Laurel, Maryland.
USA.
Van Hook Jr.. R. I. 1971. Energy and nutrient dynamics
ol spider and orthoptera populations in a grassland
ecosystem. Ecological Monographs 41:1-26.
VICKERY. P. D. and J. R. Herkert. 200l. Recent advances
in grassland bird research: w here do we eo from here?
Auk 118:11-15
Walk, J. W.. M. P. Ward. T. J. Benson. J. L. Deppe, S. A.
Lischka, S. D. Bailey, and J. D. Brawn. 2010.
Illinois birds: a century of change. Special Publication
31. Illinois Natural History Survey. Urbana. USA.
SHORT COMMUNICATIONS
403
The Wilson Journal of Ornithology 1 24( 2):403— 405. 2012
Agonistic Interactions Between Two Foraging Anhinga Females in
Southeastern Brazil
Ivan Sazima1-3 and Giulia B. D'Angelo2
ABSTRACT— Darters (Anhingidae) are among die
most territorial Pelecanit'ormes. but most of the observed
aggression is between nudes and limited primarily to the
breeding season. We observed three instances of
agonistic interactions between two female Anhingas
( Anhinga anhinga) foraging in a pond of an urban park in
southeastern Brazil. A foraging resident female chased
another female as soon as it caught sight of the latter
approaching, which caused the intruder to dive and
retreat. The resident female vocalized toward the site
where the intruder disappeared while still in the water.
The resident then vocalized front a perch from tintc to
time toward the pond while drying its feathers. We
played back its recorded call and the bird vocalized
toward us suggesting this vocalization was territorial.
Agonistic behavior at foraging sites merits further
observation to leam whether it is restricted to particular
individuals and/or periods. Received 21 October 201 1.
Accepted 21 January 2012.
Darters (Anhingidae) are territorial species of
Pelecanit'ormes, although they may associate with
other aquatic birds (Orta 1992, Frederick and
Siegel-Causey 2000). The Anhinga (Anhinga
anhinga ) forages mostly solitarily in South Amer¬
ica (Haverschmidt 1971, Sick 1997). Agonistic
interactions among Anhingas have been recorded
at perches and breeding sites with males being
more aggressive than females (Orta 1992. Freder¬
ick and Siegel-Causey 2000). Aggressive interac-
lions between females at sites other than breeding
areas and perches arc unrecorded to date to our
knowledge. We report on agonistic interactions
between two Anhinga females foraging in a pond
of an urban park in southeastern Brazil.
OBSERVATIONS
We observed Anhinga behaviors at the urban
park Parque Ecoldgico 'Prof. Hermogenes de
Freitas Leitao Filho', Campinas (—22 54’ S, 47
Museu de Zoologia. l/'niversidadc Estadual dc Campi¬
nas. 13083-970 Campinas. Sao Paulo. Brazil.
' Programa de Pbs-Graduayao cm Biologia Animal. Uni-
versidade Estadual de Campinas, 13083-970 Campinas. Sao
Paulo, Brazil.
’ Corresponding author: e-mail: isazima@gmail.com
04' W), Sao Paulo, southeastern Brazil. Females
arc easily distinguishable from males as the latter
are black with silvery to white streaks and spots
on upper back, scapulars, and wing-coverts,
whereas the former are duller with head, neck,
and breast huffy (Frederick and Siegel-Causey
2000). We watched Anhingas in the morning or
afternoon with the naked eye and through a 70-
300 telephoto zoom lens mounted on a SLR
camera from a distance of 3-15 m from 7 January
to 31 March 2011. We used ad libitum and
behaviour sampling rules (Martin and Bateson
1986), both of which are adequate for rare
behaviors and/or opportunistic records, throughout
the observations. Vouchers of digital photographs
are on file at the Museu de Zoologia da
Universidade Estadual de Campinas (ZUEC).
Vocalizations were recorded with a Marantz
PM 1 3-671 digital recorder and a Scnnheiser ME-
67 microphone at 24 bit and 48 kHz resolution. The
recorded vocalizations are at the Fonoteca Neo¬
tropical 'Jacques Viclliard', Universidade Estadual
de Campinas, Brazil.
We observed a female Anhinga interacting with
another female on three occasions (16. 22, and 29
Jan 2011). One of the females was mated to a
male that occasionally foraged at the same site, as
both attended the same nest. We observed this
female ('resident' hereafter) several times in the
previous year and no aggressive behavior toward
any bird in the pond was recorded at the time.
This female was selectively foraging for small
fish in January at a particular site (22 48' 37" S,
47 04' 30” W; Fig. 1 ) near a small bridge from
which people threw pieces of bread for domestic
waterfowl and fish (Sazima 2007). This resident
mostly foraged at the water surface near the
floating bread (which attracted small fish that
stayed close to the surface), and it scanned the
neighborhood visually. As soon as the foraging
bird observed another female (‘intruder’ hereaf¬
ter) approaching from ~50 m distant, the resi¬
dent quickly swam towards it (Fig. 2A) gaping
occasionally. If the intruder did not retreat, the
404
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 2. June 2012
FIG. 1. Section of the pond at which agonistic
interactions were observed between two female Anhingas.
Diagonally hatched rectangle = bridge; stippled line =
approximate boundary of the foraging site; dashed line =
approximate boundary of the agonistic interactions; square
= tree with nestlings. Scale = 20 m.
resident female chased it by alternating diving
with swimming, and even flapping the wings, a
behavior that caused the intruder to dive and
retreat (Fig. 2B). The resident female vocalized
while still in the water (Fig. 3A) and heading for a
perch on the bank toward the site where the
intruder disappeared. The resident vocalized from
time to time toward the pond while perched on the
bank or a branch near the foraging site waiting for
its plumage to dry (Fig. 3B). If the intruder female
again approached the foraging area, the still wet
resident female plunged into the water and chased
the intruder. The intruder was likely the same
individual, as there was another mated pair on the
opposite side ot the pond. The agonistic behavior
was similar during all 3 days. The resident female
and its mate were lending two nestlings on a tree
— 150 m from the foraging site at the time of our
observations (Fig. 1).
The resident female promptly and insistently
responded to playback of its own call, directing
its vocalization toward us. This vocalization is
a series of croaking sounds, consisting of 6-10
notes with 4601 Hz maximum frequency, 1312 Hz
dominant frequency, and 872 Hz minimum
frequency (Fig. 4). The notes last 0.1-0.33 sec
and the intervals are 0.09 to 0.13 sec in the
recorded vocalization. The sound of this vocali¬
>-
FIG. 2. (A) The resident female Anhinga (right) moves
quickly toward an intruder female (left) that approached a
highly rewarding foraging site. (B) The resident female
vigorously Haps its soaked wings while chasing the
intruder, which has just dived (concentric circles).
zation type is roughly similar to the record
XC5766 (http://www.xeno-canto.org/browse.php?
query ^anhinga).
DISCUSSION
We initially interpreted the unusual aggressive
behavior of the resident female as a type ot
territorial parental care, as it fed the nestlings with
small fishes that were abundant at the foraging
site. However, the bird continued to vocalize at
the foraging area for ~2 weeks after termination
of nesting. Tims, parental care was not the main
cause ol the aggressive behavior even if care of
young may have initiated it. Instead, we regard the
aggressiveness of the resident female as a detense
of a particularly rewarding foraging site, as the
pieces of bread supplied by people promoted and
maintained a high fish density near the bndge
(Sazima 2007). Anhingas vocalize at breeding
sites or at perches (Orta 1992, Fredenck and
Siegel-Causey 2000). although vocalization at a
foraging site seems unrecorded to date. The
resident bird’s vocalization toward its playback
SHORT COMMUNICATIONS
405
FIG. 3. (A) The resident female vocalizing in the
direction of the site where the intruder disappeared, while
swimming toward the bank. (B) The resident female
vocalizing in the direction of the pond.
leaves no doubt the calls were uttered within a
territorial context. Thus, defense of an unusually
rewarding foraging site is the most parsimonious
explanation we have for the agonistic encounters
between the two females.
Agonistic interactions between Anhinga fe¬
males seem uncommon at foraging areas, and
this behavior merits further observation to ascer¬
tain if it is restricted to particular individuals and/
or periods, or if these interactions have gone
unnoticed due to the secretive habits of these
FIG. 4. Sound spectrogram of a territorial call (#
1 1888. Fonoteca Neotropical ‘Jacques Vielliard', Universi-
dade Estadual de Campinas) uttered by the resident female
while perched on a dead branch near the bank.
birds (Haverschmidt 1971. Orta 1992, Sick 1997,
Frederick and Siegel-Causey 2000).
ACKNOWLEDGMENTS
We are most grateful to Milena Corbo and Arthur
Macarrao for recording the vocalizations with us (MC also
for the resulting sound spectrograms and help with their
description), Celso L. D'Angelo for expert advice about the
aerial image of the park. Micael Nagai for company in the
field. CNPq for earlier financial support to JS and CAPES
for a grant to GBD. and the editor and two anonymous
referees for considerably improving our paper.
LITERATURE CITED
Frederick, P. C. and D. Siegel-Causey. 2000. Anhinga
(Anhinga anhinga). The birds of North America.
Number 522.
Haverschmidt. E 1971 Birds of Surinam. Oliver and
Boyd, Edinburgh,. United Kingdom
Martin. P. AND P, Bateson. 1986. Measuring behaviour,
an introductory guide. Cambridge University Press.
Cambridge, United Kingdom.
Orta, .1. 1992. Family Anhingidae (darters). Pages 354-361
in Handbook of the birds of tlte world. Volume 1.
Ostrich to ducks (J. del Hoyo, A. Elliott, and J.
Sargatal. Editors). Lynx Editions. Barcelona, Spain.
Sa/.ima, 1. 2007. Frustrated fisher: geese and tilapia spoil
bait-fishing by the Green Heron (Butorides striata) in
an urban park in southeastern Brazil. Revista Brasi-
leira de Ornitologia 15:611-614.
Sick, H. 1997. Ornitologia brasileira. F.ditora Nova
Fronteira, Rio dc Janeiro. Brazil.
406
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124, No. 2, June 2012
The Wilson Journal of Ornithology 124(2):406-408, 2012
House Crow ( Corvus splendens) Attempt to Cooperatively Kleptoparasitize
Western Osprey ( P and ion haliaetus)
Reuven Yosef,14 Assaf Zvuloni,2 and Nufar Yosef-Sukenik1 2
ABSTRACT. — The House Crow (Conus splendens)
is a bioinvader to the Red Sea region and has been show n
to negatively impact indigenous species. We describe
attempts by House Crows to acquire an ordinarily inac¬
cessible, high quality food source by mobbing Western
Osprey (Pondion haliaetus ) in large coordinated groups.
The crows mobbed perched Osprey that had success
fully caught fish in 17b observed attempts to steal the
otherwise inaccessible food source. However, crows suc¬
ceeded in forcing Osprey to abandon fish on only seven
occasions (—4%). The crows then jointly fed on the
abandoned fish. The consistency in mobbing Osprey and
the low rate of success suggests House Crows are aware
of the energetic value of fish. Received 5 Decern her 201 1.
Accepted 3 March 2012.
Kleptopara.sitism is a behavior in which one ani¬
mal takes food or inanimate objects from another
(Brockman and Barnard 1979). The kleptoparasitc
profits by acquiring prey or objects that it could not
obtain itself, or by saving time and energy required
to obtain it. KJeptoparasitism may be intra- or
interspecific (e.g., Yosef 1991, Yosef and Yosef
2010. Yosef et al. 201 1 ). Garcia et al. (2010) sug¬
gested animals with specialized feeding methods,
or with large or high-energy food, or with extended
handling time of large or cumbersome prey, are
most likely to be kleptoparasilised.
Some kleptoparasitic species achieve their goal
by mobbing in large numbers. Mobbing is defined
as the attack initiated against a potential enemy or
predator (cf. Altmann 1956) and has been shown
to occur in many different situations for a variety
of purposes (e.g., Ostreiher 2003).
The House Crow (Corvus splendens). a bioin¬
vader to the Eilat/Aqaba region of Israel, nega¬
tively impacts indigenous and migratory avian
species (Yoset 2009) and is considered a threat to
1 Ben Gurion University at Eilat. P. O. Box 272. Eilat.
Israel.
2 Israel Nature and Parks Authority. P. O. Box 667, Eilat,
Israel.
Department ot Education, Tel Aviv University. Ramat
Aviv, Israel.
J Corresponding author; e-mail: ryosef@bezeqint.net
biodiversity (e.g.. Britton 1980. Feare and Mun-
groo 1990. Chuan Urn et al. 2003). We describe
attempts at cooperative mobbing by House Crows
that use kieptoparasitism to access a food source
that is otherwise unattainable: fresh fish caught in
the Red Sea by Western Osprey ( Pandion haliae-
tus). We investigated whether House Crows have
developed strategies similar to those of ravens (cf.
C. corns: Bugnyar and Heinrich 2003. 2005: C.
ruftcollis: Yosef and Yosef 2010, Yosef et al. 2011)
to access large, inaccessible or qualitative food
sources with minimal effort.
METHODS
Study Species. — The Western Osprey is cosmo¬
politan in occurrence and is a Holarctie breeder
(Ferguson -Lees and Christie 2001 ). It is a passage
migrant in most parts of Israel. However, at Eilat
it occurs throughout the year; these may be mostly
dispersing juveniles Hedged on islands and archi¬
pelagos in the Red Sea (e.g., Straits of Than and
Dahlak Islands; Safriel et al. 1985).
The House Crow is a bioinvader in the Eilal-
Aqaba region since the late 1970s and has estab¬
lished breeding populations on both sides of the
international boundary (Israel and Jordani. It is
a little-studied species in the region but. because
of its ability to exploit human settlements in the
desert, populations have reached pest dimensions
in Israel (Yosef 2009).
We undertook periodic observations at known
feeding perches of Western Osprey along the Israeli
shoreline between March and June 2011 at the 11
most popular perches where distances can range from
30 to I (X) m from the perched Osprey. We observed
the behavioral sequence of interactions between the
two species during 213 hrs of observation from
the shoreline. All observations were with 15 * 50
Swarovski binoculars and a 20 X 60 telescope.
OBSERVATIONS
Western Osprey successfully caught a fish on
176 (15.5%) observed occasions during spring
(Mar-Jun) 2011. We observed Osprey perch at
SHORT COMMUNICATIONS
407
specific sites on 233 occasions. Mobbing was
usually by flocks comprising 10-25 (15.9 ± 4.1
SD) crows and included calling incessantly (n =
176: 100%) and dive-bombing (n = 633 separate
attacks by 103 flocks, i.e.. in 59% of mobbing
events) the Osprey. The observed Western Osprey
stopped feeding on the fish and observed the
crows on all occasions. Western Osprey appar¬
ently tried to avoid being hit by either facing
the attacking crows (n =118; 67%) or crouching
(n = 58: 33%). Mobbing of the Western Osprey
lasted between 75 and 305 sec ( 1 87.5 ± 76.2 SD)
after which the House Crows returned to the trees
on the shore if the kleptoparasitism attempt w'as
unsuccessful. The Western Osprey abandoned the
fish and flew from the immediate area on only
seven (4%) occasions. On these occasions the
crows retrieved the fish, flew with it to the sandy
portion of shoreline, and fed on it. The size of the
House Crow flock significantly affected klcpto-
parasitizing success (/-test, P ~ 0,0014) while
duration of mobbing did not (P 0.19). However,
because neither Western Osprey nor House Crows
were marked for individual identification, we do
not know how many times the same individuals
were involved in these intra-specific interactions.
DISCUSSION
Morand-Ferron et al. (2007) emphasized the
central role of cognitive abilities in avian kleptopar¬
asitism and offered a novel perception of avian food
stealing which, in the past, was primarily seen in
terms of ‘brains’ rather than'brawn’. Our results do
not concur with their suggestions and the House
Crow resorts to ‘brawn’ and not ‘brain* in their
attempts to access a high quality food source. They
appear to recognize the freshly -caught fish as a rich
resource (which may reflect advanced cognitive
ability ), but did not display any innovative tactics to
steal the fish. This is further substantiated when we
consider that usually when a Western Osprey was
observed to catch a fish and perched to feed, it w'as
mobbed by House Crows. The Osprey perched
>200 m from the areas where crows breed or roost
in most cases. They were mobbed only when they
had caught a fish and w'hile perched relatively far
from breeding or roosting areas of die crows sug¬
gesting that crows recognized the value of fish as a
rich food resource, and the purpose of the mobbing
was to kleptoparasitize the Western Osprey to gain
food.
The reliance upon a brawn-based strategy is
surprising because corvids are considered to be
intelligent and fast-learning, and display advanced
manipulative and cognitive abilities (reviewed by
Emery and Clayton 2004). Ravens, for example,
are known to cooperatively hunt and kleptopar-
asilizc (e.g„ Yosef and Yosef 2010, Yosef et al.
2011). associate with predators to obtain food
(Stahlcckor et al. 2002), raid caches of arctic fox
( Alnpex hitfopus; Careau et al. 2007), scavenge,
supply disinformation to inter- and con-specifics
(Bugnyar and Heinrich 2003, 2005), exploit novel
and hidden food resources (Hendricks and Hen¬
dricks 201 1), or nest based on predation experi¬
ence of past seasons (Tryjanowski et al. 2004).
The uniformity in the behavior of the crow
flocks, and their lack of a strategy to kleptopar-
asiti/e Osprey, leads us to assume crows recognize
the Western Osprey, a raptor, as a potential pre¬
dator and attack it to dissuade it from approaching
their frequented areas and kleptoparasitism result¬
ed accidently wherein a mobbed individual aban¬
doned its prey. House Crows do not maintain
individual territories but are gregarious and engage
in group defense over large urban areas (RY. pers.
ohs.). However, it has not been ascertained in any
study if local populations intermingle and if they
have an encompassing strategy or restrict them¬
selves to specific neighborhoods. We assume it is
the first because every evening we observed indi¬
viduals flocking to a central fresh water drinking
site from all over the city. They also concentrated
at specific roost sites in different areas. Hence, we
were unable to ascertain whether the individuals
involved in each engagement were the same.
Ospreys are known to be kleptoparasitized by
other species (e.g.. Bald Eagle [Haliaeetus leucoce-
phalus], Prevost 1979; Parasitic Jaegers \Stercorarius
parasiticus ], Belisle and Giroux 1995; Great Blue
Herons [A idea herodias 1, Squires 1998; Northern
Crested Caracara [Caracura cheriway\, McNair et al.
2000), hut no previous study has shown cooperative
kleptoparasitism of Ospreys by House Crows. Future
studies should investigate whether this behavior is
common where the two species occur together or is
restricted to our study area. This is of conservation
importance because the Western Osprey is a native
species with low breeding densities ( Ferguson-Lees
and Christie 2001), while crows are bioinvaders and
as yet unable to routinely successfully kleptoparasi-
tize Western Osprey by mobbing.
ACKNOWLEDGMENTS
We thank G. G. Frye, J.-F. Giroux, and the editor for
improving an earlier draft of the paper.
408
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 2. June 2012
LITERATURE CITED
Altmans. S. A. 1956. Avian mobbing behavior and
predator recognition. Condor 58:241-253.
Belisle, M. and J.-F. Giroux. 1995. Predation and
klcptoparasitism by migrating Parasitic Jaegers. Con¬
dor 97:771-781.
Britton. P. L. 1980. Birds of East Africa. East African
Natural History Society. Nairobi, Kenya.
Brockman. H. J. and C. J. Barnard. 1979. Klcptoparasit-
ism in birds. Animal Behaviour 27:487-514.
Bugnvak, T. AND B Heinrich. 2003 Hiding in food-
caching ravens. Revista de Etologia Supplement 5:57,
Bugnyar, T. and B. Heinrich. 2005. Ravens differentiate
between knowledgeable and ignorant competitors.
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Viewpoint
The Wilson Journal of Ornithology 1 24(2):409-4 1 9, 20 1 2
THE ‘FIRST BASIC PROBLEM’ REVISITED: A RE-EVALUATION OF
HOWELL ET AL. (2003)
GERARD L. HAWKINS'
ABSTRACT— Howell et al. (2003) proposed modifications to the system of molt terminology lor birds developed by
Humphrey and Parkes (1959) to address a perceived inconsistency in the Humphrey-Parkes CH-P") system that Howell et
al. (200?) termed the -first basic problem' These modifications have been adopted by mainstream ornithological literature,
hut arc premature and unnecessary. The recharacterization of the preju venal and first prebasic molts, and resulting
plumages, bv Howell el al. (2003) is: (1) not supported by scientific studies, (2) inconsistent with several factors that
support classification of these molts and plumages under the H P system, and (?) contrary to the fundamental purpose ot
that system. Moreover, the H P system can be interpreted in a manner that resolves the 'first basic problem without
recharacterizing the prcjuvenal and first prebasic molts and resulting plumages. The ll-P system also can be interpreted to
Man the first molt cycle with commencement of the initial acquisition of contour feathers and provide a fixed point to start a
nomenclature of molts and plumages. The four molt strategies identified by Howell et al. (2003) may be explained by
variability in conventional first prebasic and first prealtcmule molts and are not dependent on adoption ol their proposed
modifications of the H-P system. Ornithologists arc encouraged to re-examine the modifications to the H P system
proposed by Howell et al. (2003) and to resolve existing conflicts in North American molt terminology by adopting the
proposed interpretations of the H-P system identified in this paper. Received I September 2D! I. Accepted h January 2012.
Conventional North American molt terminolo¬
gy for birds was developed by Humphrey and
Parkes (1959) to facilitate identification of
homologies among molts and plumages across
species through use of the neutral terms ‘basic’,
'alternate', and 'supplemental' rather than terms
that refer to breeding status, plumage, or season ol
the year. Humphrey and Parkes (1959:3) defined
'cycle' as the period that "runs from a given
plumage or molt to I he next occurrence of the
same plumage or moll". Under the Humphrey-
Parkes CH-P’) system adults undergo a regular,
typically complete or nearly-complete definitive
prebasic (‘adult post-breeding’ using traditional
European terminology) molt that includes the
remiges and rectrices and produces a basic
plumage each molt cycle, which is an annual
cycle in most bird species but is shorter or longer
in some species or individuals (Humphrey and
Parkes 1959, Ashmolc 1963, ienni and Winkler
1994. Pyle 2008). Adults of many species also
undergo a typically partial definitive prealtemate
(‘adult pre-breeding’ using traditional European
terminology) molt between prebasic molts that
produces an alternate plumage (Humphrey and
Parkes 1959). Typically, young undergo a partial
'Elias. Mat/.. Tieman & Herrick LLP. 1 1th Floor, 734
15th Street. NW. Washington, DC. 20005, USA;
e-mail: ghawk@emth.com
molt soon after the prcjuvenal molt, or first
prebasic (' post -ju venal') molt and. if applicable, a
first prealtemate (‘first pre-breeding’) molt that
produces first basic and first alternate plumages,
respectively (Humphrey and Parkes 1959). Young
also may undergo a presupplcmental molt in the
first molt cycle that may or may not have a
counterpart in the definitive basic molt cycle (i.e.,
the period between regular, typically complete or
nearly-complete prebasic molts), which 1 refer to
as a ‘molt cycle’ (Thompson and Leu 1994, Pyle
1997). The H-P system was quickly adopted by
most North American ornithologists (Palmer
1962, Willoughby 2004), and their described
sequence and extent of molts and plumages have
been accepted throughout the world with different
terminologies ( Dement’ ev and Gladkov 1967,
Cramp 1977).
Howell et al. (2003 ) proposed modifications to
the H-P system to address a perceived inconsis¬
tency, which they termed the 'first basic problem .
This inconsistency arises because some species or
individuals have a first prebasic molt under the
H-P system (‘conventional first prebasic molt')
while others do not (Howell et al. 2003). Species
or individuals that have a conventional first
prebasic molt subsequently acquire a second basic
plumage via a complete or nearly-complete
second prebasic molt. However, species or
individuals that lack a conventional first prebasic
409
410
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 2. June 2012
molt acquire a first basic plumage via a complete
or ncarly-complete first prebasic molt that is
equivalent with the second basic plumage and
second prebasic molt in species or individuals that
have a conventional first prebasic molt. Thus,
plumages and molts that appear to be homologous
have different names across taxa. Howell et al.
(2003) adopted a two-part solution to the ’first
basic problem’. First, they recharacterized and
renamed the conventional first prebasic molt as a
nonrecurring preformative molt because this molt
is highly variable in timing and extent within and
across avian taxa. Second, they deemed the
prejuvenal molt and juvenal plumage to be
homologous with definitive prebasic molls and
basic plumages. The result of these modifications
is the prejuvenal molt becomes the first prebasic
molt and all birds acquire a second basic plumage
~ 1 year after hatching via a second prebasic molt.
Howell et al. (2003) also provided a definition
for the 'first molt cycle', a term that was not
defined by Humphrey and Parkes (1959, 1963).
Howell et al. (2003: 639) defined the first molt
cycle as “the period between the attainment of
juvenal plumage and the acquisition of the next
basic plumage via a complete, or nearly complete,
molt that corresponds to a molt in the Simple
Basic Strategy”. This strategy is characterized by
the presence of only a prejuvenal molt followed
by cyclical complete prebasic molts. The result is
that “as a rule the first molt cycle has a duration
similar to subsequent basic [molt] cycles”
(Howell et al. 2003: 639).
Four commentaries (Jenni and Winkler 2004,
Piersma 2004, Thompson 2004, Willoughby
2004) on Howell et al. (2003) and a reply by
Howell et al. (2004) were published. Thompson
(2004) was strongly critical, while Piersma (2004)
was supportive, Jenni and Winkler (2004) and
Willoughby (2004) were supportive of the pro¬
posed recharacterization of the conventional first
prebasic molt, but maintained the modified H-P
system still does not effectively reflect phyloge¬
netic molt homologies due to the wide variety in
molts and plumages. These authors remained
advocates of the traditional, life-history-depen-
dent approach to naming molts and plumages
rejected by Humphrey and Parkes (1959). Jenni
and Winkler (2004) also were critical of the
definition of the terms ’molt’ and ’first moll
cycle' in Howell et al. (2003). Despite the
concerns raised by these commentaries, the
modifications to the H-P system proposed by
Howell et al. (2003) have been widely used in
ornithological literature, including revised species
entries in The Birds of North America Online
It currently is unclear whether ornithologists
should use conventional H-P terminology or Un¬
modified H-P terminology of Howell et al. (2003)
to describe avian molts and plumages iDitiinar.n
and Cardiff 2009). Moreover, the so-called ‘first
basic problem' identified by Howell el al. (2003)
now has a second dimension because some
ornithologists communicate about avian molts
and plumages without stating which system of
molt terminology is being used. Thus, it is
uncertain whether the terms ‘first prebasic molt’
and ’first basic plumage' refer to the 'prejuvenal
molt' and 'juvenal plumage’, respectively, as
proposed by Howell et al. (2003), or a typically
partial, postjuvcnal molt and resulting plumage
under conventional H-P terminology. Moreover,
the recharacterization of the conventional first
prebasic molt as a oncc-in-a-lifetime preformative
moll has significant consequences in identifica¬
tion of presumed homologies among molls and
plumages, particularly with respect to homologies
involving this moll.
In this article I re-evaluate the modifications to
the H-P system proposed by Howell et al. (2003).
I first discuss an interpretive issue with the
definition of ’molt’ in Humphrey and Parkes
(1959) and the revised definition of this tenn
adopted by Howell et al. (2003). Next. I evaluate
Howell et al.’s proposed recharacterization of the
prejuvenal and conventional first prebasic molts
and resulting plumages by discussing each of the
prejuvenal. conventional first prebasic. and first
prealtemate molts and resulting plumages I
maintain these modifications to the H-P system
arc premature for a variety of reasons, including
the lack of supporting evidence. These modifica¬
tions also are unnecessary in light of a proposed
interpretation of the H-P system that resolves the
'first basic problem' without recharacterizing the
status of the prejuvenal and conventional first
prebasic molts (Table I ). I also discuss the
beginning and end of the first molt cycle for
purposes of the H-P system. 1 maintain the H-P
system can be interpreted to start the first molt
cycle with commencement of the initial acquisi¬
tion of contour (or pennaceous) feathers and
provide a fixed point to start a nomenclature o!
molts and plumages (Table I). I then discuss the
appropriate way to view presumed homologies
among molts under the H-P system and the four
Hawkins • THE 'FIRST BASIC PROBLEM' REVISITED
411
TABLE 1. Proposed interpretations of the H-P system.
Issue
H-P System
Proposed interpretations
Numbering of prebasic molts and
basic plumages ('first basic
problem')
Definition of the 'first molt cycle'
Consecutive, starting with the Consecutive, starting with the conventional first
conventional first prebasic molt prebasic molt and tirst basic plumage,
and first basic plumage, if present whether or not present
(e.g., Howell el al. 2003)
None' The period starting with commencement of the
initial acquisition of contour feathers and ending
with commencement of ( 1 ) a unilormly-
complete first prebasic molt that has equivalent
timing as subsequent prebasic molts, if
applicable, or (2) the second prebasic molt
molt strategies identified by Howell et al. (2003),
which 1 maintain can be identified with conven¬
tional molt terminology.
RE-EVALUATION OF
HOWELL ET AL. (2003)
The goal of the H-P system was to provide a
system of naming molts and plumages that could
be applied broadly across taxa to reflect both
interspecific homologies (i.e., molts and plumages
that are similar because of shared ancestry) and
intraspecific homologies (molts and plumages that
occur within an individual at different stages in its
life cycle but result from a similar genetic
program or physiological process) (Humphrey
and Parkes 1959, 1963; Rohwer et al. 1992). The
truth regarding these homologies is unknown
because we cannot precisely reconstruct evolu¬
tionary history and do not have a full understand¬
ing of the genetic and physiological processes that
control molts and plumages (Thompson 2004.
Dawson 2006). However, we can make strong
inferences about interspecific and intraspecific
homologies, particularly in the case of closely-
related species, by comparing the relative timing
and extent of molts, and the color and pattern of
the resulting plumages (Rohwer et al. 1992.
Thompson 2004).
Howell et al. (2003) shared Humphrey and
Parkes’ goal of naming molts and plumages based
on presumed homologies, but their modifications
to the H-P system are primarily concerned with
placing all birds on the same numbered molt
cycles and ensuring the first molt cycle has a
duration that is similar to subsequent molt cycles.
Definition of 'Molt'
Humphrey and Parkes (1959:6) defined ‘molt'
as "the normal shedding of feathers and the
replacement of most or all of these by a new
generation of feathers". Under this and similar
definitions (e.g.. Campbell and Lack 1985,
Ehrlich et al. 1988), avian molt is a physiological
process that involves feather loss and feather
growth.
Humphrey and Parkes (1959) started their
analysis of plumage succession at the time of loss
of juvenal plumage and did not address prior
acquisitions of feathers in a subsequent article as
they intended. Humphrey and Parkes (1959) thus
did not discuss an interpretive issue with their
definition of ‘molt* in the case of the initial
acquisition of feathers (natal down or juvenal
plumage, as applicable). Under the definition ol
‘molt’ in Humphrey and Parkes (1959). taxa with
a natal down undergo a prejuvena! molt because
(he growth of juvenal plumage replaces shed
feathers (i.e., natal down). However, many taxa do
not have a natal down, including all Piciformes,
many Psittaciformes, most Coracii formes, and
some Corvidae (Jcnni and Winkler 2004), and do
not undergo a projuvcnul molt because the growth
of juvenal plumage does not replace shed feathers.
This discrepancy may he addressed by defining
‘molt’ as "the normal and regular growth of
feathers by which plumages are attained", which
is the definition of this term adopted by Howell et
al. (2003: 636) without explanation, Howell et al.
(2003) likely eliminated the requirement of
feather loss in the definition of ‘molt* to maintain
that taxa that lack a natal down have a prejuvenal
molt that is equivalent with definitive prebasic
molts. Another result of their approach is ihe
initial acquisition ot natal down occurs hy molt
even though it does not replace shed leathers.
Humphrey and Parkes (1959. 1963) emphasized
the growth aspect of the molt process and believed
that loss of the previous generation of feathers is a
412
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 2. June 20/2
relatively unimportant by-product of this process
in terms of energy expenditure. This likely is the
basis for the position of Howell et al. (2003). but it
seems premature to modify the conventional
definition of ’molt’ on this basis in the absence
of supporting evidence. Use of the term ’pre-
juvenal molt' to refer to all acquisitions of juvenal
plumage (e.g., Pyle 2008. Howell 2010) generally
appears reasonable, however, and I use this
approach except where the context otherwise
requires (see Definition of the First Molt Cycle:
page 415),
PrejuvenaJ Molts and Juvenal Plumages
Howell et al. (2003) presumed prejuvenal molts
and juvenal plumages were homologous across
species but, other than noting that prejuvenal and
definitive prebasic molts typically are complete,
they did not provide any analysis or evidence to
support their conclusion that prejuvenal molts and
juvenal plumages arc basic in nature and presum¬
ably homologous with definitive prebasic molts
and basic plumages. Humphrey and Parkes
(1959), by starting their analysis of plumage
succession with the loss of juvenal plumage,
appeared to consider the prejuvenal molt unique
and not basic in nature even if it is homologous
across species. At least four factors support this
position.
First, as noted by Howell and Corben (2000),
the prejuvenal molt is, by necessity, a more
complete, temporally compressed, and synchro¬
nous molt than definitive prebasic molts, which
may be incomplete in many species, including
most raptors, eolumbids, cuculids. owls, nightjars,
trogons, kingfishers, and woodpeckers (Jenni and
Winkler 1994; Pyle 1997. 2008). Definitive
prebasic molts, unlike prejuvenal molts, may vary
significantly in duration and be suspended for
phases of breeding, migration, or nutritional stress
(Humphrey and Parkes 1959, Payne 1972).
Second, as acknowledged by Howell et al.
(2003), the prejuvenal molt produces a unique
plumage for most birds because juvenal body
feathers typically are structurally weaker than
feathers grown in subsequent molts (Jenni and
Winkler 1994, Pyle 1997, Butler et al. 2008),
Moreover, juvenal feathers frequently differ from
basic leathers in length, shape, pattern, and color
(Alatalo et al, 1984, Jenni and Winkler 1994,
Butler et al. 2008. Moreno and Soler 201 1 ). Third,
many taxa do not have a natal down plumage that
is replaced by juvenal feathers (Jenni and Winkler
2004) and acquire juvenal plumage, unlike basic
and other plumages, without shedding feathers.
Fourth, several factors suggest conventional first
prebasic molts and first basic plumages are
homologous with definitive prebasic molts and
basic plumages. The foregoing considerations
suggest prejuvenal molts and juvenal plumages
are appropriately named and distinguished from
prebasic molts and basic plumages even if these
molts and plumages are homologous, as seems
likely.
The status of the prejuvenal molt is unknown in
the absence of a complete physiological under¬
standing of molt. However, Howell et al. 1 2003)
essentially conceded the validity of the conven¬
tional approach to this molt when they evaluated
the best way to address the ‘first basic problem'.
Having concluded it is inappropriate to start the
first moll cycle with the conventional first
prebasic molt because it is variable in timing
and extent and not basic in nature. Howell et al.
(2003) believed they had to make a choice. They
could align moll cycles by considering the
complete prebasic molt at the end of a bird's first
molt cycle to be the first prebasic molt, or they
could consider this molt the second prebasic molt
as is conventional for most birds and deem the
prejuvenal molt the first prebasic molt. Howell et
al. (2003: 642) selected the second option, not
because the prejuvenal molt is clearly basic in
nature and they could not have chosen the first
option, but because choosing the first option
“would result in a major upheaval of convention¬
al terminology' Thus, the change in the conven¬
tional view of prejuvenal molts and juvenal
plumages was an expedient way for Howell et
al. (2003) to address the ‘first basic problem' and
not based on scientific evidence.
First Prebasic Molts and Basic Plumages
Perhaps the most important modification to the
H-P system proposed by Howell et al. (2003) was
the change in the identity of the conventional first
prebasic molt to a unique preformative molt
because it is highly \ariable in timing and extent
within and across species. Howell et al. (2003)
maintained the conventional first prebasic molt i>
not homologous with subsequent prebasic molts,
and is a nonrecurring adaptation that allows birds
to get through their first molt cycle. However,
some species have a uniformly-complete conven¬
tional first prebasic molt that is equivalent in
liming with definitive prebasic molts and produc-
Hawkins • THE 'FIRST BASIC PROBLEM' REVISITED
413
TABLE 2. Examples of North American Bird species
equivalent in timing with subsequent prebasic molts.
that have a uniformly-complete conventional first prebasic molt
Species*
Source'
Anna's Hummingbird ( Calypte anna)
Williamson 1956. Pyle 1997
Nonhem Beardless-Tyrannulet (Camptostoma imberbef
Pyle 1997
1 lomed Lark ( Erenuiphila alpestrisf
Pyle 1997
Bam Swallow (llirundo rustica )b
Pyle 1997
Bushtii ( Psaltriparus minimus)*
Pyle 1997
European Starling ( Stumus vulgaris )h
Pyle 1997
Bachman's Sparrow ( Peucaea aestivalis )h
Willoughby 1986
Cassin's Sparrow (P. ettssinii )b
Willoughby 1986
Eastern Meadowlark (Stumella magnaf
Pyle 1997
Western Meadowlark (S. neglecta )b
Pyle 1997
House Sparrow {Passer domesticus)*
Pyle 1997
Eurasian Tree Sparrow (P. manumus f'
Pyle 1997
J Includes species with conventional first prebasic molts that have identical timing as subsequent prebasic molts or that occur within I or 2. rarely 3 months of the
tinting of subsequent prebasic molls due to time of hatching and presence of the prcjuvenal molt (Pyle 1997).
b Mm a first basic plumage that is indistinguishable from subsequent basic plumages.
c The Birds of North America Online.
es a plumage that is indistinguishable from the
definitive basic plumage (Table 2), There is every
reason to assume the conventional first prebasic
moll of these species is not only homologous with
definitive prebasic molts but is itself definitive in
nature.
Howell et al. (2004: 207) maintained that
complete conventional first prebasic molts repre¬
sent “one end of a continuum in which the
preformative molt replaces from one to all of a
bird's leathers”. A continuum in the extent of
conventional first prebasic molts across avian taxa
is not inconsistent with these molts being basic in
nature and homologous with definitive prebasic
molts. Moreover, the fact that one end of this
continuum consists of young that undergo uni-
formly-eomplete conventional first prebasic molts
that are indistinguishable from definitive prebasic
molts suggests this continuum represents levels of
development of conventional first prebasic molts
across species and not variability in nonrecurring
preformative molts.
Howell et al. (2003: 046) also maintained that
complete conventional first prebasic molls are
nonrecurring preformative molts because “they
do not correspond to molts in the Simple Basic
Strategy” and birds that have such molls “would
gain an extra 'basic' plumage relative to the
[Simple Basic Strategy!". All birds are consid¬
ered to reach molt maturity by means of the
second prebasic molt under the system of Howell
et al. (2003). despite significant morphological
and behavioral differences and that birds do not
uniformly acquire definitive plumage or reach
sexual maturity at the same lime in their life
cycles. This argument of Howell et al. (2003)
indicates the artificial nature of their proposed
modifications to the H-P system, which empha¬
size uniformity among species at the expense ol
ignoring real and important interspecific variation.
Howell et al. (2003: 647) acknowledged that
from an evolutionary perspective "it is most
parsimonious to consider molts and plumages
present in definitive cycles to have homologous
counterparts in the first cycle, unless good
evidence exists to the contrary”. Howell et al.
(2003, 2004) provided no scientific evidence to
rebut this position.
Howell et al. (2003) ultimately may be correct
that conventional first prebasic molls are unique
adaptations that allow birds to get through their
first moll cycle. Absent scientific evidence to the
contrary, however, it appears more reasonable to
consider conventional first prebasic molts basic in
nature as provided under the H-P system. The
variability in the timing and extent of this molt
reflects the effects of a wide variety of environ¬
mental, ecological, physiological, and behavioral
factors (Payne 1972) on the molts of young,
developing birds and the wide diversity across
avian taxa. Thus, for example, it clearly is
reasonable to presume that the conventional first
prebasic molts of the California and Massachu¬
setts populations of House Finch ( Carpodacus
mexicanus) are basic in nature and homologous
notwithstanding that they differ significantly in
414
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 2. June 2012
timing and extent (Stangel 1985). Similarly,
despite the position of Howell and Corben
(2000) to the contrary, it is reasonable to presume
the variably partial or partial to complete
conventional first prebasic molts of closely-
related species such as Calidris sandpipers are
homologous with definitive prebasic molts not¬
withstanding the varying forces acting on the
extent of these molts.
The wide variability in timing and extent of
conventional first prebasic molts is consistent
with the H-P system. Humphrey and Parkes
(1959:7) stated, as to timing, “the temporal
location of a homologous molt in the cycles of
plumage succession may vary among different
groups of birds or among individuals of a
species”. Humphrey and Parkes (1959:2) also
believed the conventional first prebasic moll was
present in some form in most birds and part of “a
fundamental pattern of plumage succession which
can be traced almost throughout the class of
Aves”. Nothing contained in Howell et al. (2003)
contradicts this position. This does not mean the
conventional first prebasic molt is present in every
bird, however. The conventional first prebasic
moll molt may not be present, for example, in any
particular individual, population, or species be¬
cause it is developmentally suppressed in re¬
sponse to environmental conditions or lost as a
result of the effects of selection (Howell et al.
2004, Thompson 2004).
Some birds exhibit atypical molt patterns that
make identification of first-cycle molts under the
H-P system extremely difficult, hut this is no less
true under the system of Howell et al. (2003).
Atypical molts include delayed, interrupted,
protracted, and continuous molts that initially
produce basic feathers and later alternate feathers,
or so-called ‘merged' molts. No one can say for
sure, but I suspect that most atypical molt patterns
are not ancestral and instead represent the effects
of selection on typical prebasic and prealternate
molt patterns. This is suggested by bird species
with individuals or populations that exhibit typical
or atypical first-cycle molt patterns (Erskinc 1971,
Howell et al. 2003, Pyle 2008), and a phyloge¬
netic analysis of the evolution of moll patterns in
Western Palearctic warblers (Svensson and He-
denstrom 1999).
First Prealternate Molls and Alternate Plumages
Howell et al. (2003) generally deemed first
piealternate molts to be homologous with defin¬
itive prealternate molts and not nonrecurring
auxiliary preformative molts. This position raises
the question how Howell et al. (2003) could
routinely conclude that some first-cycle molts art-
homologous with definitive prealtemate molts
while other first-cycle molts that are indistin¬
guishable from definitive prebasic molts in
timing, extent, and resulting plumage are not
homologous with definitive prebasic molts
(Thompson 2004). This position also appears to
be inconsistent with that of Howell et al. (2003)
with respect to conventional first prebasic molts
because the first prealtemate molt also varies
significantly in timing and extent, both across and
within species (Pyle 1997. 2008). Gulls, for
example, have first prealternate molts that vary
in extent from 0 to 1 00%. and certain large, white-
headed gull species have a partial first prealtemate
molt in some populations but not others (Howell
et al. 2003. Pyle 2008. Howell 2010). Howell ct
al. (2003), as well as Pyle (2008) and Howell
(2010), considered these molts to be alternate and
not preformative in nature despite this variability.
Plumage Color and Pattern
Perhaps the most contentious position of
Howell et al. (2003) is that plumage color and
pattern should not be used in evaluating homol¬
ogies among molts and plumages because the
physiological processes that govern plumage color
and pattern are independent of those that govern
molt. The extent of separation between these
processes is difficult to evaluate because, despite
decades of study, there is much that is not known
about the environmental, physiological, and
behavioral control of molts and plumage colora¬
tion (Thompson 2004. Dawson 2006, Kimball
2006). However, it is one thing to maintain that
different physiological processes and selective
forces may affect plumage color and pattern and
the underlying molts, which appears reasonable
and has been suggested elsewhere (Voitkevich
1966, Oring 1968, Jenni and Winkler 2004.
Willoughby 2004). and another thing to maintain
these processes are independent to an extent that
plumage color and pattern are irrelevant to molt
homology analyses. How'ell et al. (2004) appeared
to soften this position, but both Pyle (2005) and
Howell (2009) strongly maintained that plumage
color and pattern should be divorced from molt
homology analyses.
Howell et al. (2003) maintained the similar-
appearing conventional first basic and definitive
Hawkins • THE 'FIRST BASIC PROBLEM' REVISITED
415
basic plumages in many birds, including most
Passeriformes and Charadrii formes, are analogous
and not homologous. Howell et al. (2003: 637-
638) also maintained these plumage similarities
"cloud an appreciation of homologies'' between
juvenal and definitive basic plumages and their
underlying molts, which are anything but clear.
Howell et al. (2003) supported their position by
citing examples in which plumage color and
pattern, when considered in isolation, may
provide a misleading indication of the underlying
molt, i.e., shorebird species that variably exhibit
delayed plumage maturation and a tropical
African passerine whose basic plumage may
resemble its alternate plumage when conditions
are favorable for breeding. These examples do not
justify a categorical exclusion of plumage color
and pattern in molt homology analyses, or a
position that widespread similarities in conven¬
tional first basic and definitive basic plumages are
not suggestive of homologies between these
plumages and their underlying molts. Howell et
al. (2003:638) acknowledged the physiological
processes that govern molt and plumage color and
pattern “usually are coincident”, and these
processes usually produce the expected result in
terms of the color and pattern of the resulting
plumages. Thus, we may validly presume that
similarities in plumage color and pattern generally
are suggestive of underlying plumage and moll
homologies. Plumage color and pattern, as
Thompson (2004) showed hypothetically and
other ornithologists have demonstrated in actual
molt homology analyses (e.g.. Oring 1968,
Heitmever 1987, Thompson and Leu 1994), may
provide critically-important information in a molt
homology analysis. This does not mean plumage
color and pattern are infallible or should be given
priority over other relevant factors in a molt
homology analysis (e.g.. timing and extent), but
neither should they be rejected without good
reason. This analysis is consistent with the H-P
system (Rohwer et al. 1992. Thompson 2004).
Proposed Solution to the ‘First Basic Problem'
The fundamental purpose of the modifications
to the H-P system proposed by Howell et al.
(2003) was to address the 'first basic problem'.
This 'paibletn' may be addressed in a manner that
does not require recharacterization of the pre-
juvenal and conventional first prebasic molts and
resulting plumages as proposed by Howell et al.
(2003). Specifically, under the H-P system the
conventional first prebasic molt should be con¬
sidered potentially present and included for
purposes of numbering prebasic molls even when
it is absent (Fig. I ). Thus, for example, a species
of eagle that does not have a conventional first
prebasic molt commences a molt cycle 1 year
after hatching w ith a second prebasic molt and not
a first prebasic molt, which is absent and should
be noted as such in any detailed description of this
species' molts and plumages.
This approach also applies to the first pre¬
alternate molt and addresses a similar ‘first
alternate problem’. Thus, in species that have a
prcbasic-prealtcmate-prebasic definitive sequence
of molts but lack a first prealtemate molt (Pyle
2008). the prealtemate molt that occurs after the
second prebasic moll is the second prealtemate
moll despite the absence of a prealtemate molt in
the first molt cycle (Fig. I).
Definition of the First Molt Cycle
Howell et al. (2003:639) stalled the first molt
cycle with “the attainment of juvenal plumage”
because they maintained the first molt cycle under
the H-P system starts with the highly-variable
conventional first prebasic molt. Humphrey and
Parkes (1959, 1963) did not address this point,
however, and the H-P system does not require this
molt be the starting point for plumage succession.
The position of Howell et aL (2003) that the first
molt cycle starts with completion of the pre-
ju venal molt appears inconsistent with the H-P
system because, under this system, all molts are
named in reference to the incoming contour
feathers and defined by the beginning of a molt
and not its completion.
1 suggest the first molt cycle under the H-P
system should include a bird's first acquisition of
contour feathers, and thus propose that the first
molt cycle begin with commencement of the initial
acquisition of these feathers. In the case of birds
with a natal down, or all birds under the definition
of ‘molt’ in Howell et al. (2003), this starting point
is commencement of the prejuvenal molt. This
approach provides an unambiguous starting point
for the first molt cycle for all birds with the
possible exception of the Bam Ow l ( Tyio alba) and
any other Tytonidae in which natal down may
effectively constitute the juvenal plumage (Marti et
al. 2005). However, this issue is not solved by
starting the first molt cycle w ith the attainment of
juvenal plumage because one still must identify the
juvenal plumage for this purpose.
416
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 2. June 2012
(A)
Year 1 Year 2 Year 3
JFMAMJJASOND JFMAMJJASOND JFMAMJJASOND
Northern Fulmar PJ
PBI
PB2
Red-tailed Hawk PJ
PBI
PB2
Merlin (European) PJ | PB1
PB2
PB3
Merlin (New World) PJ
PBI 1 PB2
Glaucous-winged Gull PJ | PBI
PB2 PA2 PB3
Glaucous-winged Gull PJ
PBI PA] | PB2
(B)
Year 1 Year 2 Year 3
JFMAMJJASOND JFMAMJJASOND JFMAMJJASOND
Northern Fulmar
PBI
PB2 PB3
Red-tailed Hawk
PBI
PB2 PB3
Merlin (European)
PBI PFI
PB2 PB3
Merlin (New World)
PBI
PB2 PB3
Glaucous-winged Gull
PBI PA 1
PB2 PA2 PB3
Glaucous-winged Gull
PBI
PB2 PA2 PB3
(C)
Yearl Year 2 Year 3
- JFMAMJJASOND JFMAMJJASOND IFMAMIfASOND
Northern Fulmar
PJ
PB2 PB3
Red-tailed Hawk
PJ
PB2 PB3
Merlin (European)
PJ PBI
PB2 PB3
Merlin (New World)
PJ
PB2 PB3
Glaucous-winged Gull
PB2 PA2 PB3
Glaucous-w'inged Gull
PJ
PB2 PA2 PB3
FIG. 1. Diagrammatic comparison of molt cycles of Northern Fulmar ( Fulmarus glacicilis). Red-tailed Hawk (Buteo
jama, cams). European and New World populations of Merlin (Falco columbarius), and two strategies of Glaucous-winged
Gull (Lurus glaucescens). (A) Conventional molt terminology under the H-P system based on Howell etal. (2003: figure L
(B) Proposed modifications to the H-P system of Howell et al. (2003: figure 1 ). (C) The proposed solution to the ‘first basic
problem The shaded zone represents the first molt cycle. No position is taken in (C) with respect to the identity of the
partial molt in the first molt cycle of populations of the Glaucous-winged Gull that have such a molt.
My proposal to start the first molt cycle with
commencement of the initial acquisition of
contour feathers makes the H-P system more
facile with respect to species that have a
presupplemental molt that precedes the conven¬
tional first prebasic molt (Thompson 2004) and
species that have a uniform ly-complele conven¬
tional first prebasic molt (Table 2). Presupple¬
mental molts were known only for adults at (he
time Humphrey and Parkcs (1959) wrote their
article (Rohwcr et al. 1992). but a first-cycle
presupplemental moll has since been reported for
at least 16 North American passerines (Pyle 1997)
and likely is present in many more passerines
(Rohwer et al. 1992. Thompson and Leu 19941.
The end of the first molt cycle for all birds is
commencement of the second prebasic molt under
the definition of the first molt cycle in Howell et
al. (2003). This is true for the vast majority ot
birds, but some species (Table 2) have a uniform-
ly-complete conventional first prebasic molt that
is equivalent in timing with subsequent prebasic
molts, and commence the definitive molt cycle
with this molt. (The definitive molt cycle may or
may not commence the definitive basic plumage
cycle, which commences w'hen a bird first
Hawkins • THE FIRST BASIC PROBLEM' REVISITED
417
acquires the definitive basic plumage (Howell et
al. 2004. Jeruii and Winkler 2004). Thus, the first
molt cycle does not "as a rule" have a duration
similar to subsequent molt cycles as maintained
by Howell et al. (2003: 639) (Jenni and Winker
2004). All birds have the same numbered prebasic
molts and basic plumages, but not all birds have
the same numbered molt cycles.
1 propose that for purposes of the H-P system
the 'first molt cycle’ be defined as "the period
starting with commencement of the initial acqui¬
sition of contour feathers and ending with
commencement of (1) a uniformly-complete first
prebasic molt that has equivalent timing as
subsequent prebasic molts, if applicable, or (2)
the second prebasic molt". A first prebasic molt
generally will be equivalent in timing with
subsequent prebasic molts if it occurs within I
or 2. and rarely 3 months of the timing of these
molls due to time of hatching and presence of the
prejuvenal molt. Under this definition species that
have a nearly-complete conventional first prebasic
molt and a complete second prebasic molt, such as
certain grouse (Crunden 1963, Pyle 2008), do not
commence the second moll cycle with the
conventional first prebasic molt. The same also
is true for species, such as certain terns, that have
a complete conventional first prebasic molt that
occurs over a much longer period than subsequent
prebasic molts (Pyle 2008).
My proposed definition of ‘first molt cycle’
does not conform to the definition of 'cycle’ in
Humphrey and Parkes (1959) because the initial
acquisition of contour feathers is not by means of
a prebasic molt under the H-P system. However,
the H-P system surely is sufficiently flexible to
permit a common-sense modification to start the
first molt cycle with commencement of the initial
acquisition of contour feathers.
Presumed Homologies Among Molts Under the
H-P System
Presumed homologies among molts can be
properly identified once the H-P system is
properly interpreted. I suggest that under the
naming system developed by Humphrey and
Parkes (1959) numbered prebasic molts presum¬
ably are homologous with prior and subsequent
prebasic molts within species and with their
respective counterparts, and prior and subsequent
prebasic molts across species even though these
molts may vary in timing and extent. Thus, for
example, conventional first prebasic molts pre¬
sumably are homologous with each other and with
subsequent prebasic molts across species even
though some species have a uniformly-complete
conventional first prebasic molt and others have a
limited or no conventional first prebasic molt.
There are simply different levels of development
of the conventional first prebasic molt across and
within species. Similarly, second prebasic molts
presumably are homologous with each other and
with first and subsequent prebasic molts across
species even though they also vary in timing and
extent (Humphrey and Parkes 1959; Jenni and
Winkler 2004; Pyle 1997, 2008).
The Four Molt Strategies of Howell et al. (2003)
Howell et al. (2003) identified four molt
strategies of increasing complexity (i.e., simple
basic, complex basic, simple alternate, complex
alternate) and maintained they incorporate all
known patterns of plumage succession in North
American and Australasian birds. Howell et al.
(2003) used the concept of inserted molts and
plumages to describe these strategies, which are
molts and plumages that have evolved between
the prebasic molts that delineate a molt cycle.
The four molt strategies of Howell et al. (2003)
may represent the four most common types of
plumage succession, but they do not encompass
all known patterns of plumage succession or molt
strategies. For example, according to Howell et al.
(2003:646), birds that use the simple alternate
strategy have "at most" only one inserted molt in
the first molt cycle that “usually" appears
homologous with definitive prealternate molts
and is not a unique preformative molt. However,
according to Pyle (2008), species that use the
simple alternate strategy may have a preformative
(conventional first prebasic) molt and no pre¬
alternate molt in the first molt cycle (Pyle
2008:16; figure 10 C-E). This is a different molt
strategy than the simple alternate strategy as
defined and the other molt strategies identified by
Howell et al. (2003). Moreover, according to Pyle
(2008), the two first-cycle molts that characterize
species that use the complex alternate strategy
may be reduced to a single 'merged' molt, which
also is included in the simple alternate strategy
even though by definition it is both formative and
alternate in nature. The simple alternate strategy
thus includes several molt strategies.
Howell et al. (2003) incorrectly maintained it is
necessary to adopt their tw'o-pari solution to the
•first basic problem’ to identify and sort species
418 THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 2. June 2012
into their lour molt strategies. Under my proposed Ornithologists are encouraged to re-examine the
interpretations of the H-P system, there is a fixed modifications to the H-P system proposed by
point to start a nomenclature of molts and Howell et al. (2003) and to resolve existing
plumages (i.e., commencement of the initial conflicts in North American molt terminology by
acquisition ot contour leathers) and all birds have adopting the proposed interpretations of the H-P
the same numbered prebasie and prealternate system described in this paper,
molts, and basic and alternate plumages. Thus,
the four molt strategies may be attributable to
variability in conventional first prebasie and first
prealternate molts.
Further Study
Humphrey and Parkes (1959, 1963) were aware
that some bird species have molt patterns that are
difficult to describe using their molt terminology.
Subsequent studies have identified more of these
molt patterns, including the repeated wing molts
exhibited by many tern species (Bridge et al.
2007) and the continuous molts of feathers on the
head of the Field Sparrow [Spizella pusilla)
(Willoughby 1989) and the southern subspecies
of the Black-chinned Sparrow ( S . atmgularis
atrogularis) (Tenney 1997). Humphrey and
Parkes (1959. 1963) believed a thorough under¬
standing of the typical molt patterns exhibited by
the substantial majority of birds will help us
understand the evolution of atypical molt patterns.
Humphrey and Parkes < 1 959) acknowledged that
further study of molts and plumages may indicate
the need to alter or broaden the H-P system.
However, based on current knowledge of the
complicated and highly variable molt and plumage
cycles, it does not appear necessary or advisable to
do so at this time, except through adoption of the
proposed interpretations of the H-P system de¬
scribed in this paper. This approach is consistent
with the fundamental purpose of Humphrey and
Parkes ( 1959). which was to facilitate a search for
the evolutionary b;isis of av ian molls and plumages
by treating similar molt and plumage sequences in
various groups of birds as provisionally homolo¬
gous until scientific studies revealed that it was
inappropriate to do so. In contrast, Howell et al.
(2003) contradict the fundamental purpose of the
H-P system and impede the search for homologies
involving the conventional first prebasie moll by
deeming this molt a unique preformative molt.
Proponents of changes to the fundamental purpose
and presumed homologies of the H-P system bear
the burden ot providing supporting scientific
studies. Howell et al. <2(X)3) did not provide such
evidence, and their proposed modifications to the
H-P system are premature and unnecessary.
ACKNOWLEDGMENTS
I thank E. J. Willoughby, Peter Pyle, and five anonymous
reviewers lor reviewing and commenting on ihis paper
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The Wilson Journal of Ornithology 124(2):420-427, 2012
Ornithological Literature
Margaret A. Voss, Book Review Editor
AVES DE CUBA. By Orlando H. Garrido and
Arturo Kirkconnell. Illustrations by Roman Com¬
pany. Foreword by John W. Fitzpatrick. Comstock
Publishing Associates, Ithaca, New York, USA.
2011: 287 pages, 51 color plates, I figure, range
maps. ISBN: 13-978-0-8014-7691-4. $35.00 (pa¬
perback). — Cuba, as the largest island in the
Caribbean ( 105,007 km’), has 26 endemic species,
second only to Jamaica (30) in species endemic to a
Caribbean island. In addition. 61 races or subspe¬
cies inhabit the Cuban archipelago. Eight of Cuba’s
unique species occur in seven endemic genera
including Cyanolimnas (Zapata Rail). Suimoencis
(Blue-headed Quail-Dove), Xiphidiopiats (Cuban
Green Woodpecker), Ferniinia (Zapata Wren),
Teretistris (Oriente anil Yellow-headed warblers),
and Torreomis (Zapata Sparrow). The genus ToUus
is endemic to the region although the endemic
Cuban Tody multicolor) shares congeners with
the other Greater Antillean islands. Cuba also has
the world's smallest bird, the endemic Cuban Bee
Hummingbird ( Mellisuga helenae), which has a
mass ol only 1 .7 g. Another 343 species, in addition
to the endemics, are known from Cuba and its
satellite islands. Two hundred and eighty-seven
occur regularly and 152 or 41% of the total breed
on the island or associated islands. Non-breeding
species, primarily Nearctic-neotropica! migrants,
visit the island during passage (50 species) or as
winter residents (115 species) as they take
advantage ot Cuba’s position relative to North
America, just south of the Tropic of Cancer. Thus,
Cuba's aviluana. rich in numbers of species
including taxa unique to the archipelago as well
as many unique to the Caribbean, is justly
deserving of a modem field guide for Cubans anil
visitors.
Orlando H. Garrido and Arturo Kirkconnell.
both at the National Museum of Natural History
of Cuba, are uniquely qualified to write A ves do
Cuba, given their in-depth knowledge of Cuba's
avifauna as well as other aspect’s of the island’s
natural history. Much of this knowledge is
presented in the Introduction, which briefly
summarizes Cuba’s geography and the island’s
origin; its climate and habitats; fossil birds and the
origins of the avifauna; migration; history of
Cuban ornithology; tips on where to watch birds:
safety concerns in the field; and threatened
species and conservation issues. Included in the
Introduction are maps showing the island’s
provinces and key birding sites, location of Cuba
relative to neighboring islands and the Yucatan
Peninsula, and the major vegetation types of Cuba
and the Isle of Youth (formerly Isle of Pines). The
Introduction also includes a section that summa¬
rizes the key field marks required to distinguish
species within various taxa. The Introduction also
provides recommendations for using the guide
including summaries and definitions of families
and species, how birds are described for identifi¬
cation along with diagrams illustrating passerine
topography. Ornithological terms used in the
Introduction and elsewhere are defined in a
glossary at the end of the book. The various
categories used to describe each species’ status in
the species accounts are also defined in detail,
1 he species accounts arc organized phylogenet-
ically within 20 Orders and 63 families, the trails of
which are each summarized in a short synopsis,
which precedes each family’s species accounts.
The accounts summarize breeding period, egg
traits and clutch size, and nest characteristics for
each resident species. A range map depicting
distribution on Cuba and satellite islands is
provided for each resident species. Additional
range descriptions for endemic species and sub¬
species are provided in the Appendix. The species
accounts include the scientific name. Cuban and
English names, the species’ description as well a>
species with which it might be confused, descrip¬
tion ol its entire geographic range, status, habitat,
voice, and diet. Earliest and latest dates found in
Cuba are provided under status for the more
common migrants, whereas dates of occurrence
arc included where available for rare transients and
visitors. Vagrants observed only a few times and
not documented with a specimen or photo are also
described in the text. Thus, the species accounts
provide information beyond the usual minimalist
descriptions required for species identifications in
most modem field guides.
The book contains 51 color plates with 662
images by the late Roman Company, who was
420
ORNITHOLOGICAL LITERATURE
421
experienced in illustrating Cuban wildlife. Only
five species known from Cuba are not illustrated,
some of which are difficult to distinguish from
congenerics (e.g., Common Nighthawk \Chor-
tleiles minor]: Bicknell's Thrush [Cat hums bick-
nelli ]). which are already depicted, or species that
have occurred only recently (e.g.. Lesser Black-
backed Gull. Lams fuscus). Both sexes are
illustrated in the case of sexually dichromatic
species whereas adult and juvenile or immature
plumages are shown for those species with
plumage that differs with age. Some juvenile
plumages for Cuban species are illustrated for the
first time (e.g., Cuban Green Woodpecker [Xiphi-
diopicus percussus ]; Cuban Gnatcatcher [Poliop-
tila lembeyei ]; Zapata Sparrow | Torreornis in-
expectant]) as are some endemic races. Most
Nearctic-neotropical migrants are illustrated in the
plumage most commonly observed in Cuba (i.e.,
basic plumage), although alternate plumages are
also shown for those species that molt prior to
vernal migration. Illustrations of birds in flight
augment each species' depiction in perched or still
posture for most waterfowl, raptors, shorebirds,
gulls, and terns. Overall, most illustrations are
attractive, although one could quibble with the
accuracy of postures, shapes, proportions, and
color patterns of some illustrated species. How¬
ever, observers should be able to use the pictures
to identify the endemics and most of the resident
species. Observers should also have no problem
using the plates to identify species of migrant
warblers; however, migrant species that are
difficult to identify, such as shorebirds, flycatch¬
ers, vireos, and sparrows may require reference to
a North American field guide.
.-Ires de Cuba is a translation of the Field Guide
to the Birds of Cuba published by the same
authors in 2000. I am not qualified to evaluate the
quality of the translation but my comparisons of
some passages of the Spanish text w ith the earlier
English text suggests the translation is faithful to
the original. A ves de Cuba has been updated since
the English version with more recent information
reflecting taxonomic revisions resulting in an
increase in numbers of endemic species and
subspecies. Recent observations of species new
to the island list since 2000 have also been added
(e.g., Lesser Black-backed Gull) as well as a
revision of the list of threatened species and their
status. Range maps have also been revised tor
several resident species since the original English
version. The earlier version stated that it followed
the systematic sequence and species-level changes
as well as the common and scientific names
suggested by the American Ornithologists’ Union
( 1998 Check-list of North American Birds, 7th
Edition), whereas the recent Spanish version notes
the recommendations in the AOU checklist and
supplements are not strictly followed. Bird identi¬
fication based on the plates has been facilitated in
the Spanish version by using numbers and, at times,
letters for each image, which enables the reader to
match the image with the numbered species name
in the legend on the page opposite each plate. The
new plate legends not only list the scientific name
and Cuban common name for each species, but also
provide brief identification notes as well as the
page number for the corresponding species account
text, both of which were missing in the earlier
English version. The only discrepancy and minor
error that I found in the Spanish version was the
absence of small boxes in front of each species
name in the Index to enable birders to record their
Cuban observations, despite advising readers at the
end of the Introduction of its presence in the Index.
Aves de Cuba makes a valuable contribution by
providing an important summary of Cuban birds
that is accessible to Spanish speakers, especially
important for reaching a broad Cuban audience.
The earlier English version, which was a useful
compilation of Cuban ornithology when published
in 2000. has been revised and updated in this
Spanish version. The various organizations that
supported this translated version, as summarized
in the Foreword by John Fitzpatrick, should be
recognized for supporting the translation and
revision of this important work. The fact that the
Cuba's Ministry of Science, Technology, and
Environment has collaborated in distributing this
book to various organizations, agencies, and
schools throughout Cuba bodes well for ornitho¬
logical knowledge, appreciation, and conservation
in Cuba. Not only should this book be distributed
widely in Cuba, but it also belongs in the libraries
of institutions and individuals with an interest
in Caribbean birds.— JOSEPH M. WUNDERLE
JR.. International Institute of Tropical Forestry,
USDA Forest Service, Sabana Field Research
Station. HC 02 Box 6205. Luquillo. Puerto Rico
00773, USA; e-mail: jmwunderle@gmail.com
FEATHERS; THE EVOLUTION OF A NAT¬
URAL MIRACLE. By Thor Hanson. Basic Books
Publishing. New York, USA. 2011: 256 pages, 30
422
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124. No. 2. June 2012
black-and-white photographs. ISBN: 978-0-465-
02013-3 (hard cover): E-book ISBN: 978-0-0465-
02346-2. S25.99 (hardcover). — Thor Hanson
manages to weave together a great and wondrous
diversity of feather-related facts and stories,
organized around the themes Evolution. Fluff,
Flight. Fancy, and Function. Most of these themes
are self-explanatory, think down and insulation for
•Fluff, and sexual selection and cabaret for
'Fancy,' respectively. Hanson uses these themes
and manages to flit and fly among everything you
can think of relating to feathers and quite a bit
more. From purely biological subjects— Archae-
opteryx and the first birds, the origin of feathers
within dinosaurs, feather development, molt,
keratin, the up- and downsides of insulation, flight
and the evolution thereof, airfoils and wing-
assisted incline running, sexual selection, colora¬
tion. sound production, etc.— to feather-related
human activities and history — down and millinary
industries, falconry, fly-tying, feather pens, con¬
servation — it all seems to be there.
The writing is very engaging. In each chapter
Hanson winds around, alternately telling stories
from history antl/oi recent research, sprinkling in
cool biological facts, slipping into personal obser¬
vations and experience, and even reporting on a
surprising amount of do-it-yourself-at-home exper¬
imentation (often with dead birds from his freezer!).
Hanson makes his journey of discovery ours as he
introduces us to a suite of interesting characters,
some of them biologists, some of them businessmen
and women, some of them artists. Often humorous
quotes begin each chapter and draw from such
luminaries as Alfred Russell Wallace. William
Shakespeare, Lord Byron. Izaak Walton, Paul
Simon, and my personal favorite, the writers of the
movie ‘Chicken Run’. Thoughtful reflections set up
transitions between stories, and pique the reader’s
curiosity for each subsequent chapter.
There is something for everyone to learn.
Seasoned/professional ornithologists will inevita¬
bly leant something about the nexus between
feathers and human activities, perhaps in the story
about the covert (pun intended) South African
expedition to obtain ‘Barbary’ Ostriches. But even
biologists will likely learn a thing or two about the
biology ol leathers as well with so much happening
in related fields ol paleontology, development, and
coloration these days. For the budding students of
ornithology, this is an engaging and fun read
spanning all the important aspects of leather
io ogy in an easily accessible and memorable
way. Birdwatchers/-lovers will enjoy basking in
the multidimensional glory of the feather, hallmark
of our favorite creatures. For the non-biologist,
Fcoilicrs fits into the genre of topical non-fiction
that is often fun in showing the reader how
something as ‘mundane’ as a feather is actualh
brimming with fascinating details. In this way. if
you are just fascinated with all the surprising
details of how things in life fit together, you will
surely enjoy this book.
My only caveat to the book is to warn the
.scientific readers that it uses the poetic license of
someone writing for general audiences to adapt
some of the historical accounts a little to make
them flow as stories. Likewise, Hanson uses a few
analogies to explain some of the more complex
biological phenomenon that are not entireh
accurate. Thus, although this account of feathers
will greatly educate anyone who reads it about
leathers, some of the details should be checked
against the primary scientific literature before
conducting any research based on them!
I enjoyed the entire read but, perhaps mv
favorite passage was the last, which I think
summarizes the spirit of the entire book quite
well. Hanson describes a giant blown-up photo¬
graph of a puffin on display at the Smithsonian. In
the photograph, the bird is flying straight at you.
and apparently each feather and racliis on the
animal’s head is visible in crisp detail. He
describes the reaction of people rounding a comer
ol the exhibit and coming face-to-face with the
larger-then-life puffin: “They all react just as I
had: a sudden intake of breath, then the leaning in
for a closer look, the narrowing of the eyes,
the careful examination. From surprise to query
to wonder. Let the fascination begin." What
an appropriate note to end such a journey of
discovery on: with the sense that the journey
is just beginning.— KIMBERLY S. BOSTWICK.
Curator, Birds and Mammals, Museum of Verte¬
brates. Department of Ecology and Evolutionary
Biology. Cornell University, Imogene Powers
Johnson Center, 159 Sapsucker Woods Road.
Ithaca, NY 14850, USA: e-mail: Lsb6@comell.
edu
THE CROSSLEY ID GUIDE: EASTERN
BIRDS. By Richard Crossley. Princeton Univer¬
sity Press. Princeton. New Jersey. USA. 201 1: 544
pages, 10,000 color images. ISBN: 978-0-691-
14778-9. $35.00 (Cloth). — According to the press
ORNITHOLOGICAL LITERATURE
423
release, this book “For beginners, expert, and
anyone in between. The Crossley ID Guide:
Eastern Birds promises to vastly improve all
birders' abilities to identify birds." The author and
publisher claim “This book changes field guide
design to make you a better birder.. .Unlike other
guides, which provide isolated individual photo¬
graphs or illustrations, this is the first book to
feature large, lifelike scenes lor each species.
These scenes - 640 in all - are composed from
more than 10,000 of the author's images showing
birds in a wide range of views - near and far, from
different angles, in various plumages and behav¬
iors. including (light, and in the habitat in which
they live. These beautiful compositions show how
a bird's appearance changes with distance, and give
equal emphasis to characteristics experts use to
identify birds: size, structure and shape, behavior,
probability, and color. This is the first book to
convey all of these features visually - in a single
image - and to reinforce them with accurate,
concise text. Each scene provides a wealth of
detailed visual information that invites and rewards
careful study, but the most important identification
features can be grasped instantly by anyone.”
The author, Richard Crossley. is an interna¬
tionally acclaimed birder and photographer, who
has been hireling; since age 7 and. by age 2 1 , had
hitchhiked >160,000 kilometers chasing birds
across his native Britain and Europe. His love of
the outdoors and his interest in teaching, design,
and technology shaped his unique vision for the
future of birding and bird books. He is excited by
the prospect of using now technologies to bring
reality birding’ to a wide audience through many
different media. He is a spokesperson for Nikon
Sports Optics and coauthor of The Shore bird
Guide (O'Brien el al. 2006; The Shorebird Guide).
As can be drawn from the information above,
this book was promoted extensively before its
release, and within 2 days of publication there
were more than three dozen blogs on-line
providing reviews. Of necessity, these first reviews
w ere based on initial impressions of the book and,
when I received my review copy. I was as
impressed as the majority of the other reviewers
with the stunning photos and artistic composition
presented on each page. The author is to be
commended with the effort put into these outstand¬
ing and for the most part appealing compositions;
on first pass only the tiny Spruce Grouse
l Falcipeitnis canadensis) wedged in below the
large male challenged my sense of balance and
perspective. But. with any bird identification guide
- especially one that makes such great claims - it
must be tested by actually using it to assess its
effectiveness, which takes time.
Over the course of several months after
receiving my review copy. I read the introductory
materials as recommended by the author, which
suggest how the book is intended to be used. It is
not intended to be carried into the Field, but as a
guide to be studied at home before and after a day
in the field, or kept in the car as a reference. Indeed
the size of the hook, larger and heavier than Sibley
(Sibley 20(H); The Sibley Guide to Birds), makes it
impractical as a field guide. Emphasis is more on
general impressions of size and shape (G1SS). and
there are no arrows pointing to field marks.
Virtually all other bird identification guides
throughout history have implored users to read
the introduction first, hut the reality is that most
users do not. There is an innate tendency to skip
straight to the pictures. How will this impact the
effectiveness of the guide? I have also attempted to
use the guide as intended, by ‘studying’ in the
evenings, and also after coming home from the
field, from the end of spring migration and into
early winter birding in Michigan. Here 1 consider
separately how it appears the book will work tor
“beginners, experts, and anyone in between” as
claimed by the book's promoters.
Beginners want photographs. But until recent¬
ly. photographic guides simply had too many
shortcomings compared to the traditional field
guides using artwork. Kaufman (Kaufman. 2000;
Birds of North America) provided the first truly
effective photographic field guide. The organiza¬
tion of The Crossley ID Guide may appeal most to
beginners. The inside front cover provides small
thumbnail photographs of representatives of each
of the groupings the author uses to organize the
book. These groupings are a combination of
behavioral and taxonomic characters, Waterbirds
are subdivided into Swimming. Flying, and
Walking, while Lundbirds are categorized as
Upland Gamebirds. Raptors. Miscellaneous Larg¬
er Landbirds. Aerial Landbirds, and Songbirds.
Before the introduction, several pages provide
single photographs of all regularly occurring
species in the East in a size guide, which can
act as a visual index of sorts although the species
are labeled only with the four-letter banding code
and not the full species name. An excellent pair of
plates for beginners (and everyone else) to start
with are Greater (Aythya mania) and Lesser scaup
424
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 2. June 2012
(A. affinis), conveniently arranged on facing
pages. There are four larger images at the bottom,
which draws the eye first, then toward the top the
birds are farther away, smaller, and engaged in
different behaviors. What makes this pair of plates
work so well is that the same ages and sexes of each
species are shown in the same position on each
plate, and in similar poses. This allows direct
comparison of key characteristics. But not all plates
work this well. The Cooper's (Accipiter cooperii)
and Sharp-shinned (A. stria t us) hawk pair of plates
show many birds in night, which is good since that
is how many of these are seen. But there is a nice
head shot of a perched Sharp-shinned Hawk that
shows the head shape, bill proportions, and lack of
contrast between the cap and nape. There is no
similar photograph for comparison on the Cooper’s
Hawk plate. In fact, it is difficult to see the
contrasting black cap and paler nape on any of the
birds on this plate; an important field mark on
perched birds that is missing. On some plates, the
number of individuals included is impressive; but
could this be overwhelming to beginners? Add to
this the use of four-letter banding codes and you
have a potentially steep learning curve for a
beginner. It is good to challenge learners, but is it
too much? Some beginners will simply resort to
picture-matching, which can lead to errors and may
not encourage learning.
Experts will most likely dig into the traditional
difficult identification challenges, including juve¬
nile jaegers, gulls, shorebirds, fall warblers, and
Empidonax flycatchers to name a few, as well
as checking the accuracy of the range maps and
text.
After spending many years learning and using
taxonomic order in field guides, the book’s
organization can be difficult to use for more
experienced birders. Even after using the book for
several months. I find it difficult to find a species,
as the groupings arc at times ambiguous or
overlapping. For example. Common Moorhen
(Gall inula chloropus) (now the Common Galli-
nule, G. galeata) and American Coot (Fulica
americana) are not to be found among 'swimming
waterbirds' but instead among ‘walking water-
birds’ more than 100 pages farther along in the
book. I see moorhens (gallinules) swimming more
often than walking. And every one of the 65 +
birds on the coot page is either swimming or
flying! Apparently taxonomy was considered
more important in these cases, as they follow
the rails which are walking waterbirds.
So, are there any groundbreaking innovations
for difficult identifications in this guide? To me. it
does not appear so. Having all three jaeger species
on the same two-page ‘spread’ is helpful, hut
reduces the coverage of Pomarine (Stercorarius
pomarinus) and Long-tailed (5. longicaudus )
jaegers to a half-page. Juveniles are notoriously
difficult to identify, but close images of all three
species in similar poses and lighting are simply
not provided. Two juveniles and one ‘first year'
Parasitic (5. parasiticus ) are presented, one
intermediate and one light juvenile Long-tailed
arc shown, and one or two ‘first year' Pomarines
are included. The shapes of the central tail
feathers are important to identification of juvenile
jaegers, but on the Pomarine and Long-tailed
jaegers, these cannot be seen at all, and none is
shown in similar poses and lighting. The author
likes to refer to his approach as ‘reality hireling .
These two plates provide a good idea of the chaos
and confusion that can accompany watching
jaegers at a sea (or lake), but unfortunately do
not provide much clarity or learning opportunities.
The use of photographs from other contributors
tor these difficult identifications could undoubt¬
edly improve these plates by “making you a
better birder" which they fall short of doing now.
Experienced birders tend to look at range maps
in minute detail, while beginners at times ignore
them entirely! In my opinion the best range maps
to date have been in the National Geographic
Field Guide to the Birds of North America (Dunn
and Alderfer 2006). A cursory look at the range
maps in The Crossley ID Guide did not result in
any glaring errors or significant differences from
Dunn and Alderfer, but there were differences
detectable around the edges of the ranges. In
Michigan, where 1 have the most local knowledge,
the ranges of 35 species are overstated and 17 are
understated. Migration paths are not mapped, and
the topic is only briefly mentioned in the
Introduction.
Not all species get a full page, but apparently
for different reasons. The introduction states the
more common and widespread species get full-
page spreads. Relegating the Boreal Chickadee
(Poecile hudsonicus) to only a half-page short¬
changes Canadian birders who will certainly
consider this a widespread species in their large
country. The half-page treatment and the resulting
smaller map of such widespread species are
difficult to read. This bias against treating
steadfastly northern species, which are rather
ORNITHOLOGICAL LITERATURE
425
widespread, with only half-page or even quarter-
page spreads, extends also to Rock (Lagopus
nuiw) and Willow (L lagopus) ptarmigan. Quarter
pages for Ross's ( Rhodostethia rosea) and Ivory
(Pagophila eburnea ) gulls represent their relative
rarity even in eastern Canada, but 1 would still like
to have seen larger images of these beautiful
birds. Interestingly. Northern Goshawk (Accipiter
gentilis), a species likely to be seen less frequently
by eastern Canadian birders than a Boreal
Chickadee, is given a full page.
The use of banding codes to label the plates,
and within the body of the text, is potentially
contusing to all users who are not already
intimately familiar with them. As a bander myself.
I confess to not being particularly familiar with
the codes for species that I have never banded and
do not see very often in the Great Lakes (seabirds
for example), so even banders will have to study
up! One code is already out of dale with the AOU
recently splitting Common Gallinule from Com¬
mon Moorhen (Chesser et al. 201 1 ; Auk 128: 600-
613); and updates to these codes by the Bird
Banding Laboratory have tended to lag behind the
pace of AOU changes making any ‘official’
updates more complicated.
The core audience for this guide might be
"anyone in between”. The wealth of information
and dizzying array of excellent photos could
overwhelm a beginner, but may provide ample
stimulus to those wanting to learn more once they
get the basics of identification down. The incon¬
sistencies of presentation for some difficult iden¬
tification challenges may leave some "experts”
wanting. It is difficult to pinpoint what an "in
between” birder might find helpful as everyone
approaches birding in a different way with favorite
species groups ranging across the spectrum. This
guide's presentation of shore bird plumages is sure
to provide much of interest to those who decide
they want to transition from "beginner” to start to
understand the identification of these birds. Fall
warbler plumages are also treated quite well, and
the text for the warblers is on the whole very useful
and instructive. Some minor disappointments could
arise when working to distinguish a rarity from a
more common species. One example is the Black-
headed Grosbeak ( Pheurticus nielcutocephalus),
which is most often recorded in the East during
late fall and winter, yet none is shown in this
plumage to allow the more advanced or interme¬
diate birder to compare with Rose-breasted Gros¬
beak (P. ludovicianus).
The introduction notes that "expanded captions
for many of these plates” can be found on the
internet (www.crossleybirds.com). which pro¬
vides the author "the opportunity ... to include
additional identification information”. Navigating
to this web site, one first secs a considerable
amount of advertising for the book, testimonials,
several videos, and interviews with the author.
Using the technique of guesswork. I found these
plates under the main menu title 'books’, and
clicking on the selection ‘The Crossley ID Guide
- Eastern Birds’. I later discovered that clicking
on the red graphic ‘IPAGES’. which suggests
these pages are interactive (they are not), takes
you to the same page. This page contains 45
plates, plus the cover with added pop-up style
added text on the plates but not the cover. This
docs not really meet my definition of "many”,
but it is understandable that a balance is needed so
the entire book is not posted on-line. The 14 pages
of the book’s introduction are provided on the
main page as a downloadable PDF file.
There is a bias to non-passerines in this
selection of plates, as only eight are of passerines,
and 18 do not have any additional text provided as
of January 2012. This is not a browser issue as
there is no text on these plates when viewed with
Microsoft™ Internet Explorer and with Mozilla
Firefox™. Hopefully, some text will be added to
these plates in the near future, otherwise one
wonders why they are included. The additional
text provided is quite variable, from comments on
how the photo-plates were put together, rationale
for why some things were done the way they
were, details about the background location,
aspects of taxonomy, and hints about birding
techniques in general. There is additional helpful
information on some of these plates that touches
on topics more detailed than typically discussed in
a field guide, including aspects that are still not
yet worked out about assigning age or sex of
certain species, or details of molt progression.
The urge for some readers to search for errors is
irresistible with several to many individuals of the
same species on each page. Almost immediately,
blog reviewers participating in a bird version of
"Where’s Waldo?” found a hen Mallard (Anas
platyrhynehos) with ducklings erroneously placed
on the Cinnamon Teal (A. cyattoprera) page. A
few other errors have been found, but surprisingly
few considering how many images are presented.
These corrections are being posted on-line (www.
crossleybooks.com/comments-corrections/). This
426
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 2. June 2012
link is difficult to find from the main page (www.
crossleybooks.com). appearing as a text link in the
upper right side of the “expanded captions’ plates
page. One additional error that 1 found was the
Ruby-throated Hummingbird ( Archilochus colu-
bris) labeled as an immature female is actually an
adult female as evidenced by the apparent moll on
the crow n (likely photographed in August), the lack
of buff-fringing on the upperparts, and the worn
white tips on the tail feathers.
I recommend this book for the library of any
birder, beginner, expert, or in between. There is
certainly much more to like about this book than
there is to dislike. Beginners may struggle with the
overwhelming information and may be misled by
some of the photographs and sparseness of
identification information in the text, but with
effort it can be very rewarding and improve their
birding skills. Beginners may still want to bring
another more portable guide with them in the field.
Experts will be rewarded by the wealth of images
contained in the magnificent dioramas on each
page, making this book an essential addition to
their bird library, but they may not find all the.
answers for the lough identification challenges.
Everyone in between will likely find much new
information that could truly help make them better
birders. But as with any identification guide
innovation, the definitive review of the effective¬
ness ol The Cro.ssley ID Guide cannot be written
until birders ot all levels of expertise have actually
used the book over the course of months, or
even years.— ALLEN T. CH ARTIER. 1442 West
River Park Drive. Inkster, MI 48141. USA;
e-mail : amazilia3 @gmai 1 .com
HOW FAST CAN A FALCON DIVE? By
Peter Capainola and Carol A. Butler. Rutgers
University Press. Piscataway, New Jersey, USA.
2010: 220 pages, 33 figures, and 19 color plates.
ISBN: 978-0-8135-4790-9. S21.95 (paperback).—
Peter Capainola and Carol Butler present this
sufficiently researched general introduction to
birds of prey in an organized and approachable
question and answer format. Capainola is senior
scientific assistant in the Department of Ornithol¬
ogy at the American Museum of Natural History in
New York City, adjunct faculty member in the
Department of Biology at the City College of the
City University of New York, and research
associate and member of (he board of trustees of
the Long Island Natural History Museum. Butler is
a licensed psychoanalyst and mediator in private
practice, an adjunct assistant professor at New
York University in the Department of Applied
Psychology, and a docent at the American Museum
of Natural History. The book is broad in scope
addressing 85 specific questions in five chapters
dealing w'lth raptor biology and four chapters on
aspects of husbandry, falconry, and raptor conser¬
vation. The questions in each chapter address those
of greatest interest to the average reader and can be
thoroughly answered in —1.000 words or less.
Interspersed are 13 brief essays which anchor the
questions around a central topic of biology, story,
or a personal experience of Capainola.
The book’s first half is devoted to raptor
biology, addressing taxonomic classification of
the five to seven families of flesh-eating birds that
include eagles, hawks, falcons, ospreys, vultures,
and owls. A brief essay by Alan Turner, research
associate, American Museum of Natural History,
and assistant professor at Stony Brook University
describes recent findings in the evolutionary
relationship of dinosaurs and raptors. The evolu¬
tion of feathers preceded the evolution of birds:
this is well-illustrated in a figure showing feather
quill attachment sites on the fossil ulna of the
carnivorous dinosaur Velocioraptor. Chapter 1
orients the reader to the major taxonomic groups
of raptors, covering a range of life history traits,
including the structural differences between
lalcons and hawks, diet and hunting, and finishing
with referenced material on the smallest and
largest raptor species, and life spans.
Chapters 2 and 3 describe raptor physiology
and behavior with frequent references to current
research. The questions, “How fast can a raptor
fly?” and ‘“How far can a raptor fly?" are
effectively anchored by brief essays on bird
strikes and migration theory. The essay on bird
strikes takes the reader back to January 2009
when an Airbus 320 departing from New York’s
La Guardia Airport lost all engine power after
contact with a flock of Canada Geese (BranM
canadensis), thus forcing an emergency-landing
in the Hudson River. Current efforts to reduce the
frequency of these accidents are described,
including the use of trained falcons to harass
and disperse birds at Kennedy Airport. The essay
on migration theory reviews a March 2009
international conference on animal migration,
concluding that theoretical models need to be more
flexible and user-friendly to accommodate the
many variables affecting the animals' migration
ORNITHOLOGICAL LITERATURE
427
strategies in the face of environmental change. All
of the book's essays are similar as they provide
simple messages accompanied by interesting
stories or narratives. For example, a general
overview of reproductive biology (Chapter 4) is
addressed by a series of common questions such as
‘ How do birds of prey attract a mate?”. “Arc
raptors monogamous”, and “How is artificial
insemination practiced with raptors?” Answers to
each question are embedded within a narrative of
the first author’s detailed observations of a Bam
Owl ( Tylo alba) nest.
Chapter 5 deals with the dangers that confront
raptors and their defenses. It asks “What injuries
are common among wild raptors?” and then
focuses on power line structures and wind
turbines. A landmark case in Colorado led to the
development of Avian Protection Plans which use
measures to mitigate dangers to birds of prey. The
controversy of wind turbine development and
wildlife impacts is described, yet no data or
summary of major studies are covered. The
chapter ends with common questions relating to
environmental toxins in birds of prey. Overviews
are presented of Swainson's Hawk (liuleo swainsoni)
exposure to the pesticide monocrotophos used by
sunflower farmers to combat grasshoppers in
Argentina, and mercury induced reproductive
impairment in Bald Eagles ( Haliaeetus leucoee-
phalus) in Maine. Three chapters deal directly with
husbandry, falconry, and common questions relat¬
ing to the relationship between raptors and people,
such as "I lave attitudes about raptors changed over
time?” anti “Ol what value are raptors to the
environment?” The latter question addresses the
idea that raptors are apex predators and their status
in an environment indicates the condition of the
habitat. This message underscores the intention of
the book: namely, to provide a comprehensive
general introduction to raptor biology in brief,
well-referenced essays. The authors clearly avoid
more advanced concepts of evolutionary biology
and ecology in an effort to directly address the
questions posed. An appendix and full list of
references provide a rich collection of sources for
more information. — GREGORY J. NORWOOD.
Wildlife Biologist, U.S. Fish and Wildlife Serv ice,
Detroit River International Wildlife Refuge,
9311 Groh Road, Grasse lie. Ml 48138, USA;
e-mai I : Greg_Norwood @ fws.gov
Editorial News
Dr. Mary Bomberger Brown has been elected
Editor starting with the March 2013 issue of The
Wilson Journal of Ornithology (Volume 125). She
will stall receiving new manuscripts on I July
2012 in anticipation of makeup of her lirst Issue to
be sent to Allen Press on about I December 2012.
Please welcome Dr. Bomberger Brown and send
all new manuscripts after 30 June 2012 to her at
3310 Holdrege Street. School of Natural Resourc¬
es. University of Nebraska. Lincoln. NE 68583,
USA (402472-8878); e-mail: (mbrown9@ uninotes.
unl.edu). Revisions presently in process should continue
to be returned to Editor (2007-2012) Clait E. Braun
until he notifies you to send them to Dr.
Bomberger Brown which will happen once he
has received sufficient material for his last Issue
(December 2012). This Issue will he made up
and sent to Allen Press on about I September
2012. We plan to make the transition as smooth
as possible and will jointly share manuscripts
presently in the system until the transition is
completed. We thank you for your patience
during the transition and continue to look
forward to receiving manuscripts for publica¬
tion consideration in The Wilson Journal of
Ornithology.
Clait E. Braun
Editor, 2007-2012
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issue ol The Wilson Journal of Ornithology was published on I June 2012.
Continued from outside back cover
338 Predation on seeds of invasive Lantana camara by Darwin’s finches in the Galapagos Islands
Jorge Carridn-Tacuri, Regina Berjano, Giovanny Guetrero, Enrique Figueroa, Alan Tye, and
JestisM. Castillo
343 Birds caught in spider webs: a synthesis of patterns
Daniel M. Brooks
354 Environmental factors affecting nest-site selection and breeding success of the White Stork ( Ciconia
ciconia) in western Turkey
Orta( Ommq, Yildirim Agaoglu, and Orhan Gill
Short Communications
36_ Prolonged incubation and early clutch reduction of White Storks ( Ciconia ciconia)
Andrzej Wuczynski
366 Stopover site fidelity by Tennessee Warblers at a southern Appalachian high-elevation site
David F. Vogt, Mark E. Hopey, G. Rad Mayfield III, Eric C. Soehren, Laura M. Lewis, John A. Trent, and
Scott A. Rush
■' 0 Female song in the Common Yellowthroat
Conor C. Tajfi Katherine A. Littrell, and Corey R. Freeman-Gallant
3 3 Nesting density of Hermit I brushes in a remnant invasive earthworm-free portion of a Wisconsin
hardwood forest
Scott R. Loss
380 First nesting information for the Orange-eared Tanager ( Chlorochrysa calliparea )
Manuel A. Sanchez Martinez and Gustavo A. Londofio
384 Does nest-box size impact clutch size of House Sparrows?
Peter E. Lowther
38 ) An unusually synchronous double brooding attempt by a Northern Flicker pair
Elizabeth A. Goto and Karen L Wiebe
^ b Brood sex ratio of the Lilac-crowned Parrot ( Amazona finscht)
Shannon M. Pease, Alejandro Salinas -Melgoza, Katherine Renton, Patricia Escalante, and
Timothy E Wright
3% Multiple male feeders at nests of the Veery
Matthew R. Halley and Christopher M. Heckscher
99 Nestling diet of Eastern Meadowlarks in east-central Illinois
Susan Linn Ostrand and Eric K Bollinger
403 Agonistic interactions between two foraging Anhinga females in southeastern Brazil
Ivan Sazimaand Giulia B. D'Angelo
406 House Crow ( Corvus splendent ) attempt to cooperatively kleptoparasitize Western Osprey ( Pandion
kaliaetus)
Reuven Yosef, AssafZvuloni, and Nufar Yosef-Sukenik
Viewpoint
409 The ‘first basic problem’ revisited: a re-evaluation of Howell et al. (2003)
Gerard L. Hawkins
420 Ornithological Literature
Margaret A. Voss, Book Review Editor
427 Editorial News
The Wilson Journal of Ornithology
(formerly The Wilson Bulletin)
Volume 124, Number 2 CONTENTS June 2012
Major Articles
199 Post-fledging ecology of Northern Pygmy-Owls in the Rocky Mountains
Graham G. Frye and Harry R. Jageman
208 Climate change does not affect protandry in seven passerines in North America
Lisa Baubock, Abraham J. Miller-Rushing, Richard B. Primack, Trevor L. Lloyd Evans, and
Fred E. Wasserman
217 Comparison of migrant songbird stopover ecology on two islands in the Gulf of Maine
I Rebecca W. Sttomala, Sara R. Morris, and Kimberly J. Babbitt
230 A nation-wide standardized bird survey scheme for Venezuela
Gustavo A. Rodriguez, Jon Paul Rodriguez, Jose Rafael Fetrer-Paris, and Ada Sdnchez-Mercado
245 Population survey of Leach s Storm-Petrels breeding at Grand Colombier Island, Saint-Pierre and
Miquelon Archipelago
Herve Lormee, Karine Delord, Bruno Letoumel, and Christophe Barbraud
253 Apparent forced mating and female control in Saltmarsh Sparrows
Jon S. Greenlaw and William Post
265 Vccrics experience more varied acoustic competition at dawn than at dusk
Kara Loeb Belinsky, Joe! Lahman Hogle, and Kenneth A. Schmidt
270 Mating and breeding success decline with elevation for the Pacific Wren ( Troglodytes pacijicus ) in coastal
mountain forests
Lesley J. Evans Ogden, Michaela Martin, and Kathy Martin
111 Nesting ecology of the Black-capped Vireo in southwest Texas
Kathryn N. Smith, James W. Cain III , Michael L. Morrison, and R. Neal Wilkins
286 Nest and eggs of the Marsh Antwren (, Stymphalornis acutirostris ): the only marsh-dwelling thamnophilid
Bianca L. Reinert, Ricardo Belmonte- Lopes, Marcos R. Bornschein, Daiane D. Sobotka, Leandro Correa,
Marcia R. Pie, and Marco A. Pizo
292 First record of a Harpy Eagle ( Harpia harpyja ) nest in Belize
James A. Rotenberg, Jacob A. Marlin, Liberato Pop, and William Garcia
298 Provisioning of nestling Dickcissels in native warm-season grass field buffers
Kristina L Mitchell, Samuel K Riffell, L Wes Burger Jr., and Francisco J. Vilella
310 1 he effect of habitat edges on nest survival of Spragues Pipits
Stephanie L, Jones and Gary C. White
3 1 6 Population density of the Helmeted Curassow (Pauxi pauxi) in Tama National Park, Colombia
Victor Setina, Diego J. Lizcano, Daniel M. Brooks, and Luis Fab io Silveira
32 1 The Red-billed Curassow (C rax blumenbachii ): social organization, and daily activity patterns
Ana Carolina Srbek -Araujo, Luis Fdbio Silveira, and A. G. Chiarcllo
328 Descriptive anatomy of the pelvic appendage myology of the endemic Chinese Grouse ( Tetrastes
sewerzowi)
Zihui Zhang, James C. Vanden Berge, and Yue Hua Sun
Continued on inside back cover
I * Wilson Journal
S4 of Ornithology
Volume 124 , Number 3, September 2012
SEP I 0 2012
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FRONTISPIECE. Juvenile and adult Laniocera hypopyrra. Original painting by Tomas Sigrist.
S^UDELPH^
Wilson Journal
of Ornithology
Published by the Wilson Ornithological Society
VOL. 124, NO. 3 September 2012 PAGES 429-650
The Wilson Journal of Ornithology 1 24(3):429 — 435. 2012
GAUDY JUVENILE PLUMAGES OF CINEREOUS MOURNER
(LAN IOC ERA HYPOPYRRA) AND BRAZILIAN LANIISOMA
( LANIISOMA ELEGANS)
FERNANDO MENDON^A P'HORTA." GUY M. KIRWAN.2 AND DANTE BUZZETTP
ABSTRACT.— Wc describe the juvenile plumages of the Cinereous Mourner (Laniocera hypopyrm) and the Brazilian
Laniisoma (Laniisoma clegans ). Both /.. hypopyrm and L. elegans possess a dramatically conspicuous plumage as juveniles
in contrast to the generally cryptic plumage pattern exhibited by most juvenile birds. They are predominantly covered by
cinnamon-orange leathers with black terminal spots, contrasting with the nest and the predominant colors of their
environment. This Colorful plumage presumably makes them more at risk front predation by visually oriented animals (e.g.,
raptors and primates), during one ot the most vulnerable phases of their life, and strongly suggests these plumages function
as a true, or lalse (mimicry), signal ol * unprof itubi lily’. Previous knowledge concerning the phylogenetic relationships
between these two genera, and the juvenile plumage patterns of other species placed in the Tityridae indicate this shared
character in L. hypopyrm and L elegans represents a synapomorphy within this chide, thereby providing additional
evidence of their relationship. Received 13 December 2011. Accepted I May 2012.
The neotropical genera Uttnoceru and Lanii-
sonut are strictly forest birds (Slot/ et al. 1996).
The genus Laniocera comprises two species.
Cinereous Mourner (L. hypopyrra), which is
widely distributed over the greater part of Amazo¬
nia with a geographically separate population in the
central Atlantic Forest, and the Speckled Mourner
(L rufescens), which occurs over Middle America
and northwest South America (Ridgely and Tudor
1994. Fitzpatrick et ul. 2004). Laniisoma is usually
Departamento de Gcnetica e Biologia Evolutiva,
Instituto de Biociencias, Univcrsidadc dc Sao Paulo. Ruu
do Matao 277. 05508-090, Sao Paulo, SP. Brazil.
■Research Associate. Field Museum of Natural History.
1400 South Lakcshore Drive, Chicago. IL 60605. USA.
Ruu Alvaro Rodrigues 163, sala 4. 04582-000, Sao
Paulo. SP. Brazil.
4 Corresponding author; e-mail: fmhorta@usp.br
considered to be a monospecific genus (e.g.. Snow
1982, 2004), although some authorities have
separated its Andean and Atlantic Forest popula¬
tions at the specific level. We treat Laniisoma
elegans as a polytypic species following Kirwan
and Green (201 1, contra the IOC: Gill and Donsker
2012) that is discontinuous!)' distributed in the
Brazilian Atlantic Forest as well as even more
disjunctlv in the foothills of the Andes, from
southwest Venezuela south to northern Bolivia
(Ridgely and Tudor 1994. Snow 2004).
The taxonomic affinities of Laniocera and
Laniisoma have been the subject of controversy
and speculation (e.g., Traylor 1979. Prum and
Lanyon 1989. Sibley and Ahlquist 1990. Fitzpa¬
trick et al. 2004. Snow 2004). Prum and Lanyon
(1989). in a phylogenetic study of what they
termed the ‘ Schiffomis group', used morpholog¬
ical characters and were the first to identify a
429
430
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124. No. 3, September 2012
monophylelic group formed by Schiffornis. lut-
niocera, and Laniisoma. The evolutionary rela¬
tionships among these three genera were subse¬
quently confirmed by Barber and Rice (2007)
based on a molecular phylogeny of the Tityridae,
as well as by the more inclusive phylogenetic-
study of Tello et al. (2009). The clade comprising
Schiffornis. Lantisonia, and Lanincera was strong¬
ly supported by both studies, and was grouped by
Barber and Rice (2007) under the subfamily
Laniisominae. These studies suggested that Lani-
soma and Lanincera were sisters with Schiffornis
being sister to these two genera.
Other characters also support recognition of the
subfamily Laniisominae. There arc some similar¬
ities between known nests among Laniisominae
species, hut these have not been described for all
species (or even genera), preventing a more
complete understanding of the evolution of these
characters. However, available information sug¬
gests nests of Lanincera spp. (only that of L.
hypopyrra is known) and Schiffornis spp. are quite
similar. Only the nest of Thrush-like Schiffornis
(Schiffornis turdina ) has been described in detail
to date, but some data are available for Greenish
Schiffornis (.S', vires cells). All nests described
have been characterized basically as large, bulky
cups of dry leaves (Skulch 1969. Londono and
Cadena 2003. Snow 2004). However, the nest of
Laniisoma remains undescribed. The eggs of S.
turdina are similar to those of L. hypopyrra in
coloration, but this similarity cannot be interpret¬
ed as an indication of evolutionary affinity
because this character is highly homoplasic
(Londono and Cadena 2003).
The juvenile plumages of many neotropical
bird species are relatively well known. The
juvenile plumages among species of Tityridae.
as in the great majority of birds, are inconspicu¬
ous. The juvenile, even in Schiffornis. described
for S. turdina. resembles the adult (Wetmore
1972, Kirwan and Green 2011). Contrasting with
this general pattern we describe the colorful
juvenile plumages of Lanincera hypopyrra and
Laniisoma elegant, compare them with other
species of Tityridae, and discuss their evolution¬
ary and ecological significance.
METHODS
The description of the juvenile plumage of
Laniocera hypopyrra is based on a specimen
collected on 6 September 2002 by FMH in the
understory ol a disturbed terra finite forest, at
Igarape Mutum, Juruti. Parii. east Amazonian
Brazil (02 36' S. 56 13' W). The specimen
(Frontispiece. Fig. I) is housed at the Museu
Paraense Emilio Gocldi Belem. Brazil (MPEG
56.746). We describe the previously unknown
juvenile plumage of Laniisoma e. elegons, based
on an observation by Jeremy C. Minns (in litt. to
GMK, May 2008) in the Atlantic Forest at the
Parque Estadual da Serra do Mar. Nucleo Santa
Virginia, Silo Luiz do Paraitinga, Sao Paulo
(23 23' S. 45 08’ W). southeast Brazil, on 30
December 1997. We also recapitulate a descrip¬
tion of the nestling (pilllus) of L. e. buckleyi .
based on the two syntypes (Figs. 2. 3) of this
taxon at The Natural History Museum. Tring,
UK (BMNH 1888.1.20.337 and BMNH
1 888. 1 .20.338). both of which were collected by
Clarence Buckley at Pindo. Ecuador, and de¬
scribed by P. L. Sclater to illustrate plumage
progression in Laniisoma. Pindo is an untraced
locality, speculated by Paynter (1992) to be the
Rio Pindo (03 50' S. 79 45' W) in Pastaza. This
remarkable plumage also was illustrated in Sclater
and Salvin (1880: plate 16) and Snow (1982:34.
plate 2).
RESULTS
Laniocera hypopyrra. — The L. hypopyrra spec¬
imen (MPEG 56.746) possesses typical adult
flight feathers: the remiges and rectrices being
primarily gray, while the median and greater
wing-coverts, tertials. and rectrices are adorned
with pale cinnamon spots on their tips. The entire
body, except for the flight feathers, is covered by
bright orange feathers with black terminal >pots
(Fig. I ). while the head is covered by a crest also
formed of orange feathers with black terminal
spots. A remarkable feature of the crest is the
feathers in which there are distal extensions,
composed by up to six orange filaments 15 to
22 mm long, possessing white distal and proximal
portions (Frontispiece. Fig. 1). The crest, includ¬
ing these filaments, reaches 40 to 48 mm. The
same structure is exhibited by some of the dorsal
feathers. Subadults (and juveniles) of L. hypo¬
pyrra exhibit a few. irregular, bright orange
feathers with black terminal spots in a seemingly
random fashion across their underpans, as well as
parts of the upperparts. especially when younger
(Kirwan and Green 2011).
Laniisoma elegans. — The two syntypes of L. c.
buckleyi are basically identical to each other.
They are very similar to L. hypopyrra in some
d'Horta el al. • JUVENILE PLUMAGES OF LA NIOC ERA AND LAN 1 ISOM A
431
FIG. I. Ventral (A) and dorsal (B) view of juvenile specimen of Laniocera liypopyrra.
plumage features, mainly in the upperparts. The
plumage of the dorsal region is mostly cinnamon,
as well as the head and throat with black sub¬
terminal bars and small white tips to the feathers.
The rest of the underparts arc primarily dark gray
to blackish barred off-white, especially broadly
over the breast with cinnamon-orange Huffy
feathers on the flanks, and especially in the
ventral region. The wing-coverts are very dark
olive -green, marked with a few irregular rufous
spots, while the tertials and flight feathers (which
were no longer in pm) are broadly fringed brighter
olive-green. Filamentous down feathers similar to
those observed in L liypopyrra sprout to 20-
26 mm from the head and body, form noticeable
tufts in places, and are either black with white
tips, on the head, or cinnamon with white tips,
over the back (Figs. 2, 3). .1. C. Minns observed an
adult (perhaps subadult) female L. e, elegans,
which was subsequently joined by a fledged
juvenile of the same species. He described the
latter bird as being the same size as the adult or
subadult, but the entire body was mottled dark
green-brown, which color seemed almost black in
some light, and rufous. The mottling took the
form of large asymmetric patches, while Minns
noted the feathers on the head and around the base
ot the bill were erect and spiky.
DISCUSSION
Evolution of Juvenile Plumage. — Adults of
Laniocera and Laniisoma exhibit significant
432
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124, No. 3, September 2012
FIG. 2. Dorsal (A) and ventral (B) view of nestling specimens of Lcmiisoma elegans (Guy M. Kirwan /© The Natural
History Museum. Tring. United Kingdom).
differences in some morphological traits (e.g.,
plumage), which resulted in earlier misinterpreta¬
tions concerning their taxonomic affinities (Snow
2004). However. Prum and Lanyon (1989). based
on a morphological phylogeny. suggested Lanio-
cera and Laniisoma are sister taxa with the genus
Schiffomis sister to the Laniocera-Laniisoma clade.
This hypothesis was corroborated by two molecular
phylogenies (Barber and Rice 2007, Tello et al.
2009). A similarly bulky nest occurs in several
species although nesting is incompletely known for
all taxa (Londono and Cadena 2003).
The juvenile/immaturc plumage usually resem¬
bles that of the adult female in all of the other
species currently placed in the Tityridae, i.e.,
Tityra spp., purpletufts ( fodopleura spp.). becards
(Pachyramphus spp.). Whitc-naped Xenopsaris
( Xenopsaris albinucha). Myiobiu s spp., Tereno-
triccus spp.. royal- flycatchers (< Onychorhynchus
spp.), Sharpbi 1 1 (Oxyruncus cri status), and the
Schiffomis spp.
Not all ol these taxa are universally accepted
to be part of the Tityridae with, for instance
Oxyruncus cri status, at limes being accorded its
own family, Oxyruncidae (e.g., Kirwan and Green
201 I. Remsen et al. 201 I ). Many of these species
present juvcnile/immalure plumages that are even
more inconspicuous than those of females,
exhibiting darker ( Tityra spp.), browner (Xenop¬
saris albinucha ), or more greenish (Barred
Becard. Pachyramphus versicolor) plumage. The
differences between juveniles and females in
other species, are chiefly reflected in the most
colorful tracts of plumage, for instance Black-
tailed Myiobius ( Myiobius atricaudus). in which
the juvenile lacks yellow in the coronal patch, or
in Oxyruncus cristatus. in which juveniles lack
any red or orange in the crown. The only group
that presents conspicuous marks in their plumage
is the genus lodopleura. Juveniles of two of the
three species — White-browed Purpletuft (/. isa-
bellae ), and Buff-throated Purpletuft (/. pi pro ) —
possess rather conspicuous, white- or buff-tipped
feathers, hut do not resemble the juveniles of L
hypopyrra and L. elegans. The juvenile of the
Dusky Purpletuft (/. fusca) is presently unknown,
although the nest has been recently described, and
is identical to those of the other two species
(Ingels and Vinot 2010). We suspect the juvenile
of this species is unlikely to differ greatly from the
d'Horta et at. • JUVENILE PLUMAGES OF LA NIOC ERA AND LAN I ISOM A
433
P 2 S 1880.P1.XVI
J ClUu] eraan» Ktk. Haniaart trap
PT1L0CHL0R1S BUCKLEY], ad ajoudl.
FIG. 3. Image of pullus and adult Laniisoma elegans. originally published in the Proceedings of the Zoological Societv
,8y councsy of Biodiversi,y Heri,agc L,b^- *4 of its
434
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 3. September 2012
pattern exhibited by the other two species of
lodopleuro. Juveniles, as far as is known,
resemble females even in Schiffomis. the most
closely related genus to Laniocera and Laniisoma ,
although Kirwan and Green (201 1) speculate that
Varzea Schiffomis (5. major) with drop-shaped
bluish-gray spots on the greater wing-coverts
perhaps represents the juvenile plumage. Thus,
the general pattern of juvenile plumage observed
in Tityridae, as for most birds, is less conspicuous,
contrasting dramatically with those plumages we
describe for L livpopyrra and L. elegans.
The evolutionary relationship between L. hypo *
pyrra and L. elegans. when considered with respect
to juvenile plumages of other Tityridae, strongly
suggests the described state is a synapomorphy of
the clade Laniocera- Lav i i soma. Thus, we expect
the first plumage (juvenile) of Laniocera rufescens
should possess a similar plumage pattern. This
species’ nest has not been found (Fitzpatrick et al.
2004. Kirwan and Green 2011), but there are
descriptions of so-called juvenile plumage in the
literature. Some authors have suggested the
juvenile is grayer on the head with black fringes
to the greater and median wing-coverts, and
randomly black-spotted body-sides (Restall et al.
2006), while the immature is reported to resemble
the female, albeit with more prominent wing and
underparts markings, a grayish wash to the crown,
foreneck, lower back and rump and, at times wilh
some sparse black spotting on the breast with dull
gray bands extending from the neck-sides to the
undertail coverts (Welmore 1972. Hilty and Brown
1986. Fitzpatrick et al. 2004 ). We suspect that all
of the descriptions concerning non-adult plumages
of L. rufescens refer to plumage states older than
juvenile given the documented juvenile plumages
of L. hypopyrra and Laniisoma elegans described
in this paper.
Ecological Function. — Coloration among bird
species is often subject to differences, occasionally
extreme, dependent on sex. season, and age. The
general pattern related to plumage of immatures,
regardless of sex. is characteristically dull, or
inconspicuously marked, and closely resembling
the plumage of the adult female (Kilner 2006).
Predators can threaten birds of all ages, but they
pose the greatest threat to eggs, nestlings, and
young juveniles (Dumbacher and Pruett-Jones
1996), which are more vulnerable than adults.
1 he evolution ol the inconspicuousness of juvenile
plumage is considered to be a consequence of
selection for crypsis (Kilner 2006) in response to
predation pressure by visually oriented predator}'
species (e.g.. raptors and primates).
The juveniles of Laniocera hypopyrra and
Laniisoma elegans. in contrast to the general
pattern of plumage color observed in juvenile
birds, possess highly conspicuous plumages,
while adults of both species are either very
inconspicuous or less conspicuous, respectively.
Snow (1982) suggested the nestling of Lanii¬
soma elegans had evolved to appear like moss
covered by fruits, and subsequently postulated
this remarkable plumage represents an adapta¬
tion to the species using an exposed nest site
(Snow 2004). However, we consider the patterns
observed in the juveniles of these two species
(and the nestling of Laniisoma) strongly suggest
either a chemical defense (toxic and/or unpalat¬
able) or Batesian mimicry (e.g.. of a large, hairy
caterpillar). A general pattern of conspicuous
colors, exhibited by some birds, may function as
a signal of Ymprofitability’ to predators (Baker
and Parker 1979). Chemical defense (toxic and
unpalatable) in some taxa is correlated with
aposematic coloration (Cott 1940, Colt and
Benson 1970. Guilford 1990, Dumbacher and
Pruett-Jones 1996). Some non-toxic or palatable
species also present morphological and behav¬
ioral characters similar to those of toxic or
unpalatable species by Batesian mimicry (Dia¬
mond 1982. Borloloti 2006). Additionally, it has
often been suggested that warning colors can
also have a disruptive (Tullberg et al. 2005). or
a distractive function (Stevens and Merilaita
2009). Further work is needed to test the
alternative hypothesis regarding the ecological
role of juvenile plumage of Laniocera and
Laniisoma.
ACKNOWLEDGMENTS
Personnel from CNEC Engenharia Ltd. supported
FMH’s fieldwork. We are grateful to Manuel Santa
Brigida who prepared the specimens collected during
the same fieldwork, and Alexandre Aleixo from MPEG,
who provided the specimen loan. Jeremy C. Minns is
warmly thanked for sharing his observations of the
juvenile of luiniisoma elegans. GMK is grateful to Robert
Pry s Jones, Mark Adams, and Hein van Grouw at The
Natural History Museum, Tring. for permission to study
relevant specimen material housed there. We are grateful to
Tomas Sigrist, who kindly ereated the illustration of
Laniocera hypopyrra, and the Biodiversity Heritage Library
for allowing us to reproduce the image of Laniisoma
elegans. Clait E. Braun. John M. Bates, and an anonymous
referee provided useful comments on the submitted
manuscript.
d'Horta el al. • JUVENILE PLUMAGES OF LANIOCERA AND LANIISOMA
435
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The Wilson Journal of Ornithology 124(3):436-445, 2012
TEMPORAL AND SPATIAL PATTERNS IN ABUNDANCE OF
THE WEDGE-BILLED WOODCREEPER ( GLYPHORYNCHUS SPIRURUS)
IN LOWLAND ECUADOR
JOHN G. BLAKE12 AND BETTE A. LOISELLE'
ABSTRACT. — Glyphorynchus spirurus (Wedge-billed Woodcreeper) is one of the most common birds in the understory
of many tropical forests of Central and South America bin few studies have focused on its abundance and distribution. We
use data from mist nets and direct observations over a 10-year period to examine patterns of abundance and distribution on
two 100-ha plots (Harpia, Puma). - 1.7 km apart in lowland forest of eastern Ecuador. Birds were captured in mist nets
(96 nets/plot) that were open for -6 hts/day for 1 day each in January and February; direct observations were made along
transects within each plot during February (7 yrsl and April |4 yrs). We recorded 861 captures (447 recapturesi on Harpia
and 963 captures (540 recaptures) on Puma: capture rates < birds/ 100 mist-net hrs) were slightly higher on Puma, largely j
result of the greater numbers of recaptures. Number of individuals captured per year did not differ between plots. Mean
(± SE) recapture distance w ithin a year was less on Harpia (94.5 £ 6.1 m) than on Puma (121.6 ± 7.3 m) but recapture
distances between years did not differ between plots ( 108 and 97 m. respectively lor Harpia and Puma). Number of captures
had a clumped distribution with some nets capturing many more individuals than others, number of captures per net was not
correlated with captures at nearby nets. We recorded 490 Glyphorynchus during observations on Harpia (Feb samples) and
e84 on Puma. Number ol observations was greater on Harpia during 6 of 7 years. Numbers of observations had clumped
distribution patterns on both plots; significant autocorrelations likely rc-flcctcd the difficulty of delecting individuals by
voice when >50 in from a transect. Comparisons with published data from other sites in Central and South America
indicate considerable spatial variation in abundance but reasons for geographic variation in abundance need further
investigation. Received 5 February 2012. Accepted 6 May 2012.
The Wedge-billed Woodcreeper ( Glypho¬
rynchus spirurus-. Glyphorynchus hereafter) is
the smallest of the woodcreepers (Furnariidae).
It is widely distributed from southern Mexico to
western Ecuador, northern Bolivia, and Amazonia
to eastern Brazil (Hiity and Brown 1986, Ridgely
and Tudor 1994). typically in mature forest
but also in second-growth habitats (Blake and
Loiselle 1991. 2001; Borges and Stouffer 1999).
Glyphorynchus feeds on insects taken from the
bark of trunks or branches, foraging alone, in
pairs, or in mixed-species flocks (Hiity and Brown
1986); it often forages in moss on trunks (English
1998).
Glyphorynchus is typically one of the most
frequently captured species in mist nets (Blake
and Loiselle 2009) and some (e.g., Remscn and
Good 1996, Maria and Remsen 1997) have
suggested its capture frequency reflects behavior
rather than abundance. This suggestion apparently
derives from an earlier paper (Gradwohl and
Greenberg 1980) in which Glyphorynchus was
described as having large and overlapping home
langes. That conclusion may not be representative
P 0DCBox' MOa;;!' u MV"'e Et’°logy :,nd Conservation.
3261 I USA. ’ erS,ly 01 F|orida- Gainesville. FI.
2 Corresponding author; e-mail. john.blake@ufl.edu
436
of the ecology and spacing patterns of the species
in other forests, particularly where densities are
higher than in central Panama. Glyphorynchus
density (estimated from observations and map¬
ping) varies widely among geographic regions,
from —6 to 10/100 ha (Panama: Karr 1971.
Robinson ct al. 2000; Peru: Terborgh et al. 1990)
to >50 (French Guiana: Thiollay 1994) or 100/
100 ha (Ecuador: English 1998). Thus, frequent
captures of Glyphorynchus in mist nets may
indicate the species is abundant in some regions,
including Ecuador (Blake 2007. Blake and
Loiselle 2009).
Feu studies have focused on the ecology or
behavior of Glyphorynchus. despite its abundance
in the understory of many tropical forests.
Stratford and Stouffer (2001) examined patterns
of feather growth in Glyphorynchus to learn if
fragmentation affected its growth (it did not) and
several studies have examined occurrence of
parasites and lice (e.g.. Price and Clayton 1989.
McQuistion and Capparella 1997. Valim et al.
201 1). A variety of studies focused on mixed-
species flocks included information on Glypho¬
rynchus (e.g.. Gradwohl and Greenberg 1980.
English 1998) but have not had the woodcreeper
as the primary focus. Glyphorynchus has also
been included in studies that estimated survival
i ates of tropical birds; the frequency of captures
Blake and Loiselle • VARIATION IN GL YPHOR YNCHUS ABUNDANCE
437
and recaptures provides the data needed for such
estimates (Jullien and Clobert 2000, Blake and
Loiselle 2008). Glyphorynchus has figured prom¬
inently in studies that used molecular approaches
to examine patterns of diversification (e.g.. Bates
2000, 2002; Mila et al. 2009; Thomassen et aJ.
2009).
The major goal of our study was to provide
information on temporal and spatial patterns of
Glyphorynchus abundance from a lowland forest
site in Ecuador. We used netting and observation
data to examine spatial variation in abundance (we
use the term abundance to refer to numbers of
birds, whether based on captures or observations)
at both within and between-plot (100-ha plot)
scales, movements (based on recapture informa¬
tion). patterns of habitat use (based on captures and
observations), and temporal changes in these
metrics. Specifically, we examined whether Gly-
phorynchus was randomly distributed across
two 100-ha study plots or whether it displayed a
clumped distribution pattern indicative of responses
to local habitat differences; whether abundance is
relatively stable across years; and whether patterns
of abundance (both spatial and temporal) are similar
on two 100-ha plots in the same area of lowland
forest. Our results provide a unique perspective on
the distribution and abundance patterns of an
important neotropical species.
METHODS
Study Site.— We conducted our research at
Tiputini Biodiversity Station (TBS), Orellana
Province, Ecuador (—00 37' S, 76 10' W;
190-270 m elevation). TBS was founded in 1994
by Universidad San Francisco de Quito (USFQ)
on a tract of undisturbed lowland rainforest within
the — 1. 7-million ha Yasum Biosphere Reserve,
one of the most biologically diverse regions of the
world (Bass et al. 2010). The station and nearby
areas support a variety of habitats including terra
lirine and vdrzea forest, palm (e.g.. Manritia
flexuosa) swamps and other wetlands, as well as
areas of natural succession that follow treefalls,
windthrows. or other natural disturbances. The
mean annual precipitation at Yasum' Research
Station. —30 km WSW of TBS, is —3,100 mm
(http://w wav. biologia.pucc.edu.ec/natura.plip ?c= 337).
Wet months are from April through June: January
and August are relatively dry with January often
very dry (pers. obs. l.
Two —100-ha plots (Harpia and Puma; -I X
1 km each) were established in terra firme forest
during 2001. Both plots were gridded (100 X
200 m grid lines) and marked W'ith tagged, 1 .5-m
tall PVC tubes every 50 m along each grid line.
The Harpia plot ranges from 201 to 233 m in
elevation and is characterized by dissected upland
forest. The Puma plot has less topographic relief
overall, although the range in elevation is similar,
from 209 to 235 m. Both areas experience partial,
temporary inundation ( — 5 to 10 ha. depending on
the height of the flood) when small streams fill
and overflow their banks as the Tiputini River
rises; Puma has more areas that fill with standing
water after heavy rains.
Points at 50-m intervals within each plot were
classified into one of six habitat categories
(mature upland forest, mixed upland forest,
palm-hardwood swamp, palm swamp, second
growth, gap) based on a subjective evaluation of
the dominant habitat type within a 25-m radius of
that point in 2005. Most of the habitat types have
remained the same throughout the study despite
some changes in habitats around points (e.g., as a
result of treefalls).
Sampling Methods: Captures. — Birds were
captured with mist nets (12 X 2.6 m. 36-mm
mesh) set at ground level. Nets were arranged in a
series of eight sets of 1 2 nets on each plot (96 nets
per plot). Each set of 12 nets formed a rectangle
(100 X 200 in) with nets set — 50 m apart; max¬
imum distance between nets on a plot was
—900 m. Nets on the two plots were —1.7 km
apart at their closest point. Barlow and Peres
(2004) concluded, based on recaptures of marked
individuals, that plots 500 m apart in the Brazilian
Amazon were spatially independent; <1% of
birds were recaptured between plots in their study.
We recorded six recaptures (all species combined)
between plots (<0.1% of total captures; >13,000
captures) and have reobserved only a few' color-
banded individuals between plots. Each set of nets
was operated for 1 day (—0600 to 1230 hrs) in
January (peak of breeding for many species) and
March (late breeding season for many species),
starling in March 2001 and ending in March 2010.
All captured birds were banded with numbered,
aluminum leg bands. Mist nets, as with any
sampling method, are subject to biases, but
because both plots in this study were sampled
the same way. any biases associated with mist
nets are similar on both plots.
Sampling Methods: Observations. —We used
direct observations to sample birds during Februarv
(2002-2006. 2009. 2010) and April (2002-2005);
438
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 3. September 2012
we primarily use data from February as that month
was sampled more regularly. We use the term
observation to refer to both visual and auditory
records of individuals: the great majority of
observations were auditory. Locations ot all birds
seen or heard were noted on scale maps ot the plots
as one of us (JGB) w alked slowly with many stops
along transects. - 1.0- 1.4 km was covered during
a morning; starting positions were distributed
throughout the plots and rotated between monthly
samples to ensure, as much as possible, that all
parts of the plots were covered early in the morning
when vocal activity was greatest. Each plot took
— 12-13 days to cover: transects were not covered
more than once during a given sample. Total effort
expended (i.e.. number of hrs and number of km)
was equivalent between plots and among samples.
Observations started well before light and contin¬
ued for up to 3 hrs of the morning. Periods of rain
occasionally interrupted or ended counts early.
Statistical Analyses: Capture Data. — Sample
effort (number of mist-net hrs. where one mist net
open 1 hr equals one mist-net-hr or I mn/hr)
varied slightly among samples. Consequently,
some comparisons of number of captures were
based on captures per 100 mn/hr. We used all
captures or only individuals (recaptures omitted)
depending on the comparison. Capture rates
(birds/100 mn/hr) and number of individuals
captured per year were compared between plots
using paired /-tests. We used Pearson's correlation
coefficient to test if annual variation in captures
was similar between plots. We used coefficients
of variation and variance-ratio tests to compare
variation in capture rates between plots. Mean
recapture distances were calculated for individu¬
als with > three captures; individual means were
used to calculate plot means (individuals as
replicates). Mean recapture distances per individ¬
ual were compared between plots using /-tests.
Comparisons of mean between-year recapture
distances were based on the distance between
the last capture location in I year and the first
capture location in the subsequent year.
Spatial distribution of captures (i.e.. clumped,
random, uniform; also for observations) was
evaluated using Program PASSaGE Version
2.0.10.18 (Rosenberg and Anderson 2011). PASS¬
aGE computes means and variances from counts
(e.g., number of coptures/net) and calculates a
series of indices to describe patterns of variation.
We used the Index of Dispersion (ID: based on
the variance-to-mean ratio) as an indication of
whether distribution of captures was clumped (ID
> 1.0). random (ID = 1.0). or uniform (ID < 1.0).
Departure from random distribution was evaluated
with a Chi-square test (Rosenberg and Anderson
20! 1 ). We also provide values of Morisita’s Index,
the scaled probability that two points chosen at
random are in the same quadrat (or from the same
mist net): higher values indicate a more clumped
distribution.
We used PASSaGE to calculate spatial auto¬
correlation indices (i.e.. correlograms: Moran’s I)
to examine if number of captures at one location
was correlated with captures at nets at different
distances (using 50-m increments, the closest
distance between nets). Moran's 1 (Moran 1950)
ranges from 1 to - I with an expected value of -0
for large sample sizes and no spatial autocorrela¬
tion. Significance levels of correlations were
examined with permutation tests.
Net locations were classified by habitat and we
used Chi-square tests to examine if number of
captures differed among habitats with expected
numbers based on the number of nets in different
habitat categories.
Statistical Analyses: Observation Data. — Num¬
ber of observations per year (Feb samples) was
compared between plots using paired /-tests.
Variation across years was compared between
plots with correlation analyses. We used several
approaches in PASSaGE to examine distribution
patterns of observations. We created a 50 X 50-m
(0.25 ha) grid overlay for each plot (i.e.. 400 grid
cells per plot) and counted the number of
observations per grid cell; we selected 50-m grid
si/e as that corresponds to the mean distance
between nets. We calculated dispersion indices
(ID) for each plot based on the distribution of
counts among cells, as was done for number of
captures per mist net. We used these same grid¬
cell data to calculate correlograms and Moran's 1
to examine spatial autocorrelation among cells.
Significance of correlations was examined with
permutation tests.
We used second-order statistics (Ripley's K-
function; Rosenberg and Anderson 2011) to
evaluate patterns of clumping based on all
observations within the plot. Second-order statis¬
tics are based on the co-occurrence of pairs of
points and answer the question: are there more
points within a given distance from a specified
point than one would expect by chance (Rosen¬
berg and Anderson 2011). If true, points are
spatially aggregated. Ripley's /f-function is a
Blake and Loiselle • VARIATION IN GLYPHORYNCHUS ABUNDANCE
439
TABLE 1. Numbers of Glyphorynchus captured (Cap.), recaptured (Rec.), and observed (Obs.) on two 100-ha plots.
Tiputini Biodiversity Station. Ecuador, 200 1 20 1 0. CR = capture rate expressed as captures/ 1 00 mn/hr (one mist net open 1 hr
= 1 mn/hr). Numbers are for February/March when iwo values are listed for Obs. but for February il only one value is given.
Year
Harpia
Puma
Harpia
Puma
Cap.
CR
Rec.
‘Tr Rec.
Cap.
CR
Rec.
<3> Rec.
Obs,
Obs.
2001*
55
9.2
1
2
53
8.1
2
4
2002
89
7.6
41
46
85
7.9
42
49
61/61
50/38
2003
80
6.3
49
61
83
6.7
42
51
63/66
32/54
2004
109
7.9
63
58
107
9.0
58
56
64/80
52/61
2005
98
8.1
52
53
121
10.2
76
63
62
82
2006
91
7.9
52
57
95
8.2
55
58
93
62
2007
86
7.4
40
47
77
6.8
45
58
2008
87
7.7
46
53
123
10.8
76
62
2009
88
7.3
57
65
119
10.2
66
55
82
49
2010
78
7.3
46
59
100
8.7
78
78
65
57
* Only one misi-net sample. March.
common way to characterize point patterns; tests
for deviation from random are based on Ripley’s
L-hat (0 = random. <0 = clumped. >0 =
uniform). Significance of E-hat values were based
on permutation tests implemented with PAS-
SaGE. Calculation of the K statistic was corrected
for edge effects (Rosenberg and Anderson 201 1 ).
We compared numbers of observations within
25-m radius circles around net sites based on the
habitat types associated with each net site, as
described for captures. Results are given as means
and SE. unless otherwise noted.
RESULTS
Capture Data. — We recorded 861 captures of
Glyphorynchus on Harpia (414 individuals, 447
recaptures) and 963 captures (423 individuals, 540
recaptures) on Puma (Table 1 ). Overall capture rate
per year was slightly higher on Puma (mean = 8.7 —
± 0.45) than on Harpia (7.7 ± 0.23; paired /-test, zl
r = 2.23, df = 9, P = 0.052). The difference in ^
capture rates was largely a result of greater numbers t5
of recaptures on Puma (569r of total) than on Harpia ™
(5257- ); number of individuals captured per year did ^
not differ between plots (paired /-test, / - 0.21 . df = ^
9. P = 0.84). Capture rates were fairly consistent ££
across years but were somewhat more variable on q!
Puma (CV = 16.3) than on Harpia (9.6; variance
ratio test for capture rate y = 3.67. P = 0.082).
Capture rates were not well correlated between plots
(/' = 0.27, P = 0.45).
Most individuals were captured only once or
twice (Fig. 1) with decreasing numbers captured
multiple times. Most had moved 0 to 150 m from
the previous capture (i.e.. recaptured in the same
net or in nets up to three sites away; Fig. 2);
few individuals were recaptured >250 m from
the previous location although occasional, longer
recapture distances were recorded. The mean dis¬
tance between capture sites within a year (i.e.,
within the same month or between months) was
less on Harpia than on Puma (/ = 2.85, df = 448,
P < 0.005; Fig. 3); mean recapture distance from
I year to the next had less variation between plots
(/ = 1.16, df = 512 ,P = 0.25).
Captures were not evenly spread among all nets
within a plot (Fig. 4) with most nets capturing ~4
to 14 birds. All nets on each plot captured at least
one individual, indicating Glyphorynchus oc¬
curred throughout most of each plot. Captures
Number of captures per individual
FIG. I. Number of captures per individual: approxi¬
mately half of all Glyphorynchus were captured only once
on two study plots at Tiputini Biodiversity Station. Ecuador.
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 3. September 2012
440
Recapture distance categories (m)
FIG. 2. Percentage of recaptures at different distances
from the original capture site. Zero distance indicates
capture in the same net. Nets were -50 m apart.
per net had a clumped or clustered distribution on
each plot (Indices of Dispersion - 2.19, 2.44, P <
0.001 on Harpia and Puma, respectively; corre¬
sponding Morisita’s Index values were 1.13 and
1.15, respectively). Number of captures per net
had no correlation with captures at nearby nets
despite the clumped distribution pattern. Correlo-
grams had a significant positive correlation only
at 525 m on Puma (Moran's I = 0.076. P = 0.04
at 525 m; Bonferroni corrected significance for
total correlation = 0.75) and no significant
correlation at any distance on Harpia (Bonferroni
significance for total correlation = 1.0).
Number of captures per habitat category (4
types were represented by nets on Harpia; swamp
FIG. 3. Means (± SE) for recapture distances within
and between years on each of two study plots at Tiputini
Biodiversity Station. Ecuador. Betwcen-year capture dis¬
tances based on the distance between the last net the bird
was captured in 1 year to the net it was first captured in
during the second year. Values in parentheses are range of
recapture distances.
Number of captures per net
FIG. 4. Number of captures per net on each of two 100-
ha study plots (96 nets/plot) at Tiputini Biodiversity
Station. Ecuador.
habitats not represented) did not differ from
expected with expected values based on the
proportion of net sites within each habitat
category (x; - 0.9, df =3 , P > 0.75). There
were fewer captures than expected in swamp
habitats on Puma and more than expected in
mixed-upland forests (xz 17.7, df = 4, P =
0.001; f = 11.0, df = 3, P = 0.029 if swamp
habitats are excluded from comparison).
Observation Pat a. —We recorded 490 Glypho-
rynchus during February samples on Harpia (mean/
sample = 70 ± 4.7) and 384 on Puma (mean = 55
± 5.7; Table 1). The number of observations was
greater on Harpia during 6 of 7 years (paired /-test.
t = 2.36. df =6 . P = 0.057). Observations per
sample were somewhat less variable on Harpia
(CV = 17.8) than on Puma (CV = 27.7; variance-
ratio lest Fbx, = 1.53, P = 0.31) and were not
correlated across years between the two plots (r =
0.08). Number of observations per sample was not
correlated with number of captures during the same
year on Harpia (r = 0.18) but was to some extent
on Puma (r = 0.67).
Observations were not evenly distributed
throughout either plot (Fig. 5); Glyphnrynchus
was not recorded in ~-28% of cells on Harpia and
~40% on Puma. Combining cells with six or
more Glyphorynchus observations (to avoid cells
with <5 records), the distribution of cells with a
given number of observations (0, 1. 2. 3. 4. 5. >5)
differed between the two plots ij2 = 19.8, df = 6.
P = 0.003). mostly a consequence of the greater
number of cells without any observations in Puma.
The difference in distribution was not significant
Blake ami Loiselle • VARIATION IN GL YPH OR YNCH US ABUNDANCE
441
0123456789
Number observations per grid cell
FIG. 5. Number of records per 50 X 50-m grid cell on
each of two 100-ha study plots (400 grid cells/plot) at
Tiputini Biodiversity Station, Ecuador.
between plots (y/ = 8.28. df = 5, P = 0. 142) when
cells with no observations were omitted. Number
of observations per grid cell had a clumped or
clustered distribution on each plot (Indices of
Dispersion = 1 .94. 1 .96. P < 0.00 1 . on Harpia and
Puma, respectively; corresponding Morisita's In¬
dex values were 1.49 and 1.67. respectively).
Second-order analyses (using a 10-m distance
increment and correcting for edges) indicated
numbers of observations were clumped at distances
up lo —70-80 and from • — 1 00 to 150 m from a
point on both plots. Corrclograms showed a
significant negative autocorrelation at 0-50 and
300-350 m and a positive correlation at 200-250
and 400-450 m on Harpia (Bonferroni corrected
significance for total correlation - 0.068): signi¬
ficant negative correlations on Puma occurred at
0-50 and 200-250 m and positive correlations at
100-150 and 500-550 m (Bonferroni significance
for total correlation = 0.009).
DISCUSSION
Glyphorynchus is one of the most widespread
and abundant species in the forest understory at
Tiputini Biodiversity Station (Blake 2007. Blake
and Loiselle 2009) but shows considerable
variation in abundance over time and space.
Numbers of Glyphorynchus seen during annual
counts indicated greater variation in abundance
than did numbers of birds captured. The two
methods also differed in that count data indicated
somewhat greater variation on Puma than on
Harpia but the reverse was true for captures. In
neither case, however, was variation significantly
different between plots. It is perhaps not surpris¬
ing that extent of temporal variation did not differ
substantially between plots given that plots are in
relalively close proximity. Glyphorynchus clearly
varies in abundance from I year to the next but
there was no consistent trend in numbers, either
up or down. Thus, our results are similar to those
of Stratford and Stouffer (2001 ) who reported no
significant variation in capture rates over 9 years
at their study site in Brazil.
Variation in abundance across years might be
related to changes in survival rate or reproductive
success or to changes in behavior that might alter
the likelihood of capture or observation. Annual
survival of Glyphorynchus al our site is —0.6
(Blake and Loiselle 2008) and a recent reanalysis
of 12 years of data provided no indication of
significant annual variation in survival i Blake and
Loiselle. unpubl. data). We do not have data on
reproductive success and are not able to tell if
annual variation in abundance is related to
changes in demographic parameters. Temporal
patterns in local abundance may. in some cases,
reflect habitat shifts in response to seasonal
changes in resources (Beja et al. 2010) but it is
not likely that Glyphorynchus undertakes signif¬
icant shifts in habitat (e.g., terra fume to varzea)
given their relatively small home ranges and
recapture distances. Changes in moisture may
affect microclimate conditions and cause some
species to shill their use of microhabitats,
potentially affecting probability of capture (Kan*
and Free mark 1983). Monthly rainfall has varied
during the course of our study but there was no
significant correlation between rainfall and num¬
bers of captures (based on an analysis of rainfall
data from Yasuni Research Station). The relative¬
ly low level of variation in abundance across years
(Table 1) suggests more random effects, such as
daily changes in weather or behavior, might
account for temporal variation in numbers of
captures and observations. It is not likely temporal
variation was the result of methodological issues
as sampling methods were the same across years
in our study.
Glyphorynchus varies in abundance at several
spatial scales; within plots, between plots, and
over w ide geographic regions. All nets captured at
least one individual (Fig. 4). but there were large
differences in total captures per net, indicating
Glyphorynchus activity was concentrated in
specific areas of the plot. Captures per net
provided no evidence of spatial autocorrelation
(i.e., captures at I net were nor correlated with
captures at nearby nets), suggesting activity levels
442
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124, No. 3. September 2012
and. likely, abundance can vary over relatively
short distances, perhaps in relation to abrupt
changes in habitat that occur on the plots (Sheth
et al. 2009). Observations also indicated consid¬
erable small-scale variation in abundance with
few or no individuals recorded in some areas ol
each plot (Fig. 5). Clumped distributions could, as
with nets, reflect differences in habitat suitability.
For example, Clyphorynehus was rare or absent in
some of the wetter habitats, accounting for some
of the spatial variation in abundance.
Observed spatial variation in abundance might
be partially explained by sampling methods,
particularly for observational data. Observations
cover a greater proportion of each plot than do
mist nets but Clyphorynehus vocalizations are
relatively weak and individuals are not likely to
be equally detectable at all distances from transect
center lines (i.e.. probabilities for detecting
individuals may decline away from transects).
Distance effects may account for some of the
autocorrelation and clustering patterns in the
count data.
It is clear, based on recaptures of marked
individuals, that many individuals confine most of
their activity to relatively small areas. This is
evident based both on recaptures within a year
(e.g., from Jan to Mar) and between years; many
recaptures are from the same or adjacent nets (i.e..
50 m from the original location) (Fig. 3).
Differences in patterns of abundance between
plots could arise for several reasons. Puma, for
example, has more areas with apparently less
suitable habitat (e.g.. dense vine tangles, swamps),
which might account for the fact there were more
areas on Puma with few or no observations
(Fig. 5). Harpia tends to be more uniformly terra
firtne although there still were areas without
records. Differences in availability of suitable
habitat might account for the greater within-year
recapture distances on Puma relative to Harpia
(Fig. 3). Individuals might move over longer
distances in search of suitable sites or might have
larger home ranges; either could lead to longer
recapture distances.
Relatively long movements associated with
large home ranges or territories have been
suggested to account for the frequent number of
captures ol Clyphorynehus in mist nets (e.g.,
Marra and Remsen 1997). Some longer-distance
movements (i.e.. >500 m) occurred at our site
(Fig. 3) (as also reported by English [ 1 998 1 at a
nearby site) and may represent exploratory
movements, as individuals typically moved back
to original capture locations. However, move¬
ments of recaptured individuals in our study
generally were relatively short (Fig. 2), indicating
relatively small home ranges. It we assume that
average recapture distance (Fig. 3) indicates the
diameter of a circular home range, home ranges
would be 0.7 ha in Harpia and 1.2 ha in Puma. If
wc use the recapture distance as the radius ol a
circular home range, these values would be 2.8
and 4.7 ha, respectively, for the two plots. Home
ranges, in either case, would be relatively small
and similar to or smaller than reported for many
other species in Amazonian forests (e.g.. Terborgh
et al. 1990). Johnson et al. (2011). for example,
reported a territory size of 5.2 ha for Glyplw-
rynehus in terra firtne forest in Brazil,
Approximately half of all individuals were not
recaptured (Fig. I ) and may represent transients
or young of the year, birds that are not likely to be
recaptured. An analysis of apparent survival rates
(Blake and Loiscllc 2008) indicated transients
likely were an important component of Gfypho-
rynchus population dynamics. In other cases,
individuals may be captured when on the edge
of their home range with most of the range beyond
the normal area covered by nets. Thus, with nets
opened at a particular location for only two
mornings per year, it is perhaps not surprising that
some individuals are not recaptured. It is not
uncommon for individuals of many species to not
be recaptured for many years (unpubl. data).
Glyphorynehus abundance also varies substan¬
tially at larger scales of comparison, whether
abundance is represented by captures or observa¬
tions. Capture rates at our study site are the
highest of which we arc aw'are. even when
compared to sites where Glyphorynehus is among
the most frequently encountered species. Beja
et al. (2010) reported Glyphorynehus to be most
frequently captured in terra ftrme forest in central
Amazonia and, although capture rates were not
given, the data provided suggest a capture rate of
~0.7 birds/ 100 nin/hr. Similarly low rates (~0.6-
1.15/100 mn/hr) have been reported from other
South American sites such as the forest fragments
project near Manaus (Bierregaard 1990. Stratford
and Stoulfer 2001). Slightly higher capture rates
of Glyphorynehus were reported in control and
logged forest plots in Brazil (—1.1 to 2.3 birds/
100 mn/hr; Wunderle et al. 2006) and primary
(2.4 birds/100 mn/hr) and logged forest (1. 3-1-9
birds/100 mn/hr) in Venezuela (Mason 1996).
Blake and Loiselle • VARIATION IN GLYPHORYNCHUS ABUNDANCE
443
Capture rates also vary substantially in Central
America. Glyphorynchus was infrequently cap¬
tured in Kan’s (1990) long-term studies along
Pipeline Road. Panama, and none was captured in
Schemske and Brokaw's ( 1981 ) study in the same
area. In contrast, Glyhphorynchus was more
common in Comarca de Kuna Yala. Panama with
capture rates varying from 2.4 (50 m elevation)
to 0.9 (850 m) per 100 mn/hr (Blake 1989).
Glyphorynchus also was one of the most fre¬
quently captured species in Costa Rica (e.g..
Blake and Loiselle 1991, 2000, 2001), where
capture rates ranged from 0.7/100 mn/hr in second
growth to —2.7 in old-growth forest at 50 m and
4.7 in forest at 500 m.
Observation data indicate even greater variation
in abundance among sites than capture data.
Densities of Glyphorynchus were low in central
Panama along Pipeline Road (8/100 ha; Robinson
et al. 2000), in agreement with the very low
capture rates, and in Manu, Peru, where densities
were approximately the same or lower (2.75 pairs/
100 ha; Terborgh el al. 1990). Capture rates were
not available for the Peru site but Glyphorynchus
was ranked second in numbers of captures (Karr
et al. 1990). Densities were somewhat higher
(16.5 pairs/ 1 00 ha) in a plot in the forest frag¬
ments project north of Manaus (Johnson et al.
2011) and ranked about fourth in number of
captures. Similarly. Thiol lay (1994) reported
densities from 28 to 36 pairs/100 ha in French
Guiana with Glyphorynchus the most frequently
captured species. English (1998). working close to
our study site, estimated Glyphorynchus densities
at — I /ha. the highest recorded by any study, and
in agreement with our capture rates which are the
highest reported.
Overall density of entire bird communities does
not. however, appear related to Glyphorynchus
density or capture rate. The Panama site, for
example, has the highest total density of birds
(Robinson et al. 2000) but one of the lowest
densities and capture rates for Glyphorynchus.
Total density at the Manaus site (Johnson ct al.
201 1) is less than in Peru (Terborgh et al. 1990)
but density and capture rate of Glyphorynchus
were higher in the former site, although Glypho¬
rynchus ranked slightly higher among captures in
the latter site (4 vs. 2).
An evaluation of factors that might cause
geographic variation in abundance is beyond Ihe
scope of this paper. Habitat, foraging sites,
resource abundance, abundance of ecologically
similar species (Poletto et al. 2004), and environ¬
mental conditions all might influence the number
of individuals in a given region, but few data are
available to allow examination of their influence.
Rainfall and strength of the dry season may have
an influence on Glyphorynchus abundance. The
three sites with the highest abundances (whether
by capture rate or territory mapping) were Costa
Rica, French Guiana, and Ecuador (2 sites). All of
these sites have rainfall of at least —3,000 mm per
year and no strong dry season. The other sites in
Venezuela. Brazil. Peru, and Panama have rainfall
of — 1 .700 to —2.600 mm per year and have more
pronounced dry seasons; Glyphorynchus abun¬
dance was lower in these sites. Glyphorynchus
often forages in moss growing on tree trunks
(English 1998) and it is possible that lower
rainfall and more pronounced dry seasons may
limit this foraging option.
Glyphorynchus is one of the most abundant
birds in the understory of wet tropical forests of
Central and South America. Its abundance varies
both spatially (at both local and geographic scales
of analysis) and temporally (i.e„ across years).
Spatial variation likely is linked to habitat
preferences at a local scale and, perhaps, with
rainfall or other environmental factors at larger
geographic scales. Future studies that examine
movements in relation to foraging behavior or
studies that examine reproductive success and
foraging behavior in different geographic regions
may lend further insight into the population
dynamics of this common neotropical species.
Similar studies on additional species may reveal
whether patterns shown by Glyphorynchus are
unique or shared by other species.
ACKNOWLEDGMENTS
We are grateful to the individuals who helped establish
the 100-ha study plots or assisted in collecting field data:
Javier Andy. Renata Duraes, Jeanne Fair, Alvaro Garcia.
Jose Hidalgo, Kimberly Holbrook. Franklin Narvaez,
Jcndry Narvaez. T B. Ryder. J.-C. Rodriguez, Tina
Sommers, and W. P. Tori. We also thank the staff of the
Tiputini Biodiversity Station, especially Jaime Guerra.
Diego Mosquera, Consuelo de Romo. David Romo, Kelly
Swing, and all others who have made our visits to the site so
rewarding. The National Science Foundation (IBN
02.15141). National Geographic Society 17113-01), Fulb-
right U.S Scholars Program, University of Missou ri-St.
Louis, and University of Florida provided fundinc. Work at
Tiputini Biodiversity Station was conducted in accordance
wtlh research permit # 13-tC-FAU-DFN (and renewals),
Ministeno del Ambiente. Distrito ForesfaJ Napo. Tena
Ecuador.
444
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 3. September 2012
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The Wilson Journal of Ornithology 124(3):446 453. 2012
REPERTOIRE SIZE AND SYLLABLE SHARING IN THE SONG OF
THE CLAY-COLORED THRUSH (' TURDUS GRAYI)
LUIS E. VARGAS-CASTRO,1-2-3 NATALIE V. SANCHEZ.1 AND GILBERT BARRANTES1
ABSTRACT.— Sons- repertoire size and extent of song sharing provide information about social interactions that occur
in songbird species. We recorded the songs of eight male Clay-colored Thrushes (Turd us grayi ) m San Jose. Costa Rica
during the 2008 breeding season. We classified 695 songs and 5,032 syllables using visual inspection of spectrograms and
spectrogram correlation analysis to measure repertoire size and syllable sharing among a local group ot males. Mat
repertoire size was 10-17 syllable types. Males shared on average 28 ± 15% (SD) syllable types from their repertoires with
other males, but a larger proportion of syllable types remained unique to particular males. Extent ot repertoire sharing and
distance between singing males were not related. Presence of shared and individually unique syllables in the repertoires
indicate that imitation, and perhaps improvisation, contribute to development of the song ot Clay-colored Thrushes.
Received 21 February 201 1 . Accepted 14 April 2012.
Bird song is used in territorial defense and
female attraction (Krebs et al. 1978. Catchpole
1987. Catchpole and Slater 1995). Some songbird
species accomplish both purposes with a single
song or phrase type throughout their lives
(Kroodsma 1996). but in many species the song
repertoire is much larger ranging from a few
(Krebs et al. 1978) to hundreds (Todt and Hultsch
1996) or even thousands of song types (Kroodsma
and Parker 1977).
Songbird species also differ in the extent of
song sharing between individuals of a given pop¬
ulation (Johnson 2006, Nicholson et al. 2007).
Song sharing within a population is thought to be
a result of learning, in which young individuals
produce accurate imitations of previously heard
adult con-specific songs (Marler 1970. Marler and
Peters 1981. Kroodsma 1982). Usually, only pan
of the repertoire is shared among individuals
(Catchpole and Slater 1995). Thus, repertoire size
and extent of song sharing arc behavioral
characters that provide information about social
interactions and the song learning process of a
songbird species (Baker et al. 1986. Searcy and
Andersson 1986. Beecher et al. 2000. Beecher and
Burt 2004).
Thrushes (Turdidae) in general are known for
their long, varied, and melodious songs. The song
ot Clay-colored Thrushes ( Tardus gmvi) consists
of a sequence of syllables highly variable in length.
Our objectives were to: ( 1 ) describe the temporal
structure of songs of the Clay-colored Thrush, (2)
' Escuela de Biologui. Universidad dc Costa Rica. 2060
San Pedro. San Jose. Costa Rica,
Current address: Department of Biology. University of
Miami. Coral Gables. FL 33146, USA.
Corresponding author; e-mail: luissum@gmail.com
identify individual repertoire size, and (3) estimate
the extent of syllable sharing between neighboring
males to better understand the social interactions
that occur among neighbors of this thrush.
METHODS
Study Area. — We conducted this study on the
campus of the Universidad de Costa Rica (UCR),
San Jose Province, Costa Rica (09 56' N, 84 02' W;
1,200 m asl). The campus has large open areas
with scattered trees and bushes near a stream that
crosses the campus. There arc also two old-second
growth forest patches of 1 and 0.5 ha. respectively.
Female Clay-colored Thrushes nest principally on
trees in open areas or human-made structures, while
males defend a small territory around the nest.
Procedures. — The Clay-colored Thrush breeds
from March to June at this location. We recorded
songs of eight adult males from March to May in
2008, of which four were banded with a unique
combination of colors and another had a unique
mark on his chest. We recorded one banded male
on 4 different days, three other males (2 of which
were banded) on 3 different days, and the rest of
the males (2 were marked) during a single day.
Some males w ere unbanded, but w e were able to
identify each male through time by its territory
location and presence of individual syllable types
in its repertoire. We obtained most songs between
0450 and 0930 hrs, but we also used recordings
from other times of the day.
Song Recording. — We used a Sony M-635VK
tape recorder and a Sennheiser ME66/K6 shotgun
microphone to record songs. We digitized the
recordings at a sample rate of 44.1 kHz and a
resolution of 16 bits with Adobe Audition 1.0
software (Adobe Systems Inc., San Jose. CA.
446
Vargas-Castro et a!. • SONG OF THE CLAY-COLORED THRUSH
447
Male B
a a
b
b
h H\i mi
- f /it
p* V*
V'« v*
i 2
3
4
5
6
7
Male D
V
/
r
\
Mi
c
*
N
- - - 1 - - - 1 -
1 2
3
4
5
6
7
Male F
✓
6 i 2
3
4
5
6
7
>
o
c
0
3
cr
0
5
4
3
2
1
0
Time (sec)
FIG. 1 . Spectrograms of the songs of three male Clay-colored Thrushes recorded during 2008 in San Jose, Costa Rica.
Each of these songs is composed of 10 syllables in total, but males may sing songs ranging from one syllable to more than a
hundred syllables. Songs with equal number of syllables usually vary in syllable sequence. The songs of male B, D, and F
have 8, 9, and 10 different syllable types, respectively. Lower case letters a. b. and c indicate syllables of the same types.
Syllables are 0.29 ± 0.07 sec in length arid separated by comparable silent intervals of 0.28 ± 0.07 sec in length (mean ±
SD. a = 8 males, 54-125 syllables from 10 random songs/male were measured). Syllables have a sound frequency range of
1 100 to 5400 Hi and complex frequency modulations that may include buzzes or trills.
USA) to produce .wav sound files. We used
Raven Pro 1.4 software (Cornell Laboratory of
Ornithology. Ithaca. NY. USA) for sound spec¬
trogram production and analysis.
Song Measurements. — Each song is composed
of a sequence of syllables, which are the minimal
structural units of a song (Fig. I ). Some syllables
are single notes that appear as a eonlinous trace in
the spectrogram, but other syllables tire comprised
of multiple notes. Consecutive songs in a song
bout are separated by silent intervals >1 sec. We
measured the number of syllables per song, song
duration, inter-song silent intervals, and song
tempo (number of syllables/sec) in 695 songs
(range: 44-150 songs/male). We randomly select¬
ed 10 songs from each male to measure syllable
duration and inter-syllable silent intervals.
The song of the Clay-colored Thrush, as in
other thrushes, contains two syllable categories:
whistles (or loud syllables) and soft syllables. The
latter in other thrushes have been termed ‘hisselly’
or 'whisper' elements (Grabowski 1979, Rasmus¬
sen and Dabelsteen 2002. Johnson 2006). Soft
syllables are sung at a lower amplitude and have a
more complex structure than whistles. A given
male Clay-colored Thrush sings at least two times
as many soft syllable types as whistle syllable
types (LEV. unpubl. data). Soft song in other
songbird species is used in close-range commu¬
nication, primarily during aggressive interactions,
courtship displays, or both, depending upon the
species (Dabelsteen et al. 1998. Searcy and
Beecher 2009). However, soft syllables are rare
in the spontaneous 'loud' songs that we analyzed
here. We recorded a total of 5.188 syllables of
w hich 5,032 were whistles and only 3% were soft
syllables. Thus, we included soft syllables in the
song-level measurements but we excluded them
from the syllable repertoire size estimation and
syllable sharing analysis.
448
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 3. September 2012
N
X
>
o
c
CD
3
c r
CD
3
2
1
A**
cp
Dp
.0 0.2 0.4
0.6 0.8
i.o
Ck
Fk
•0 0.2 0.4
0,6 0'8
1.0
Ei
Ai
Di
0 0.2 0.4
0.6 0.8 1
Time (sec)
.0 1.2 1.4
p: * " ,, JTTV Sy“aD,e typeS between malc ^ay-colored Thrushes during the 2008 breeding season in San Jose. Costa
Shi/! ? hP shared among the repertoires of males C and D, syllable 'k' is shared between males C and F. and
- 0 (h A 'rv arnd7ny ma E’ A' and D' Mcan Spectrogram correlation values are: Cp-Dp - 0.86, Ck-Fk = 0.76. Ei-Ai
- 0.66, Ai-Di = 0.70, and Ei-Di = 0.69.
Syllable Repertoire Size.— We printed spectro¬
grams of the recordings using a fixed scale and
visually identified each syllable type to produce a
cataiogue of the repertoires of all males. Clear
* terences 111 frequency-temporal pattern of
the different syllables facilitated the visual
classification process (Fig. |). Wc measured
repertoire size as the total number of different
syllable types in the songs of a given male. We
also constructed cumulative plots of new syllable
types per every 10 recorded syllables to verify that
we had obtained complete repertoires.
Syllable Sharing. — We based identification ol
shared syllables between males by the similarity
ol the frequency-temporal patterns (Fig. 2) using
a similar procedure as other studies analyzing
Vargas-Castro et al. • SONG OF THE CLAY-COLORED THRUSH
449
syllable or song type sharing (Mundinger 1982,
Hughes et al. 1998. Molles and Vehrencamp
1999, Rasmussen and Dabelsteen 2002, Nicholson
et al. 2007). We printed spectrograms of each
syllable type in the repertoire of all males and
mixed them into a single syllable pool. Three
different observers blindly looked for matches
between syllable types. A pair of syllables from
two different males was considered to be a shared
type only if all observers agreed on that match,
We re-examined similarity of shared types
using the spectrogram correlator tool of Raven
Pro 1.4 software (Cornell Laboratory of Ornithol¬
ogy, Ithaca. NY, USA). The correlator compares
two syllables to each other and provides a
correlation value based on the similarity of the
frequency-temporal pattern of the sounds. We
applied a 900-6,000 Hz band pass filter and
selected the normalize and linear power options in
the correlator configuration settings. We random¬
ly selected 10 different renditions of that syllable
type from each male for each pair of shared
syllables, and ran the correlator using those sets of
renditions to obtain 100 correlation values. We
used the largest number of renditions available if
the number of renditions of a given syllable type
sung by one male was ■ 10 (2 cases). We also
selected 10 syllables for each pair of males at
random from both males and compared those
random sets to obtain 100 additional correlation
values. Mean spectrogram correlations of shared
and random syllables were later analyzed in a
paired comparison.
We calculated the proportion of repertoire
sharing between pairs of males using the formula:
2Ns/( R i + R2), following McGregor and Krebs
(1982). N„ is the number of shared syllable types
among two males and R| and R> are the repertoire
sizes of each male, respectively. Wc substraeted
the proportion of repertoire sharing from I to
obtain a dissimilarity measure of the repertoires
between pairs of males.
Statistical Analysis. — We used a paired /-test to
examine w'hether males have as many types of
shared syllables as indiv idual syllables (exclusive to
each male) in their repertoires. We used a /-test to
examine if the relative frequency of individual and
shared syllables in the songs was not different from
that expected by the proportion of individual and
shared types in the repertoires. All tests were two-
tailed; assumptions of normality and homogeneity
of variance w ere met (Zar 1996). We conducted a
Mantel test using repertoire dissimilarity values and
distance between song perches to test if males that
were closer to each other shared a higher proportion
of their repertoires (Sokal and Rohlf 1995). The P-
value of the Mantel lest correlation was calculated
from 9.999 permutations. We used R 2.14.0 (R
Development Core Team, Vienna, Austria) to
conduct statistical tests.
RESULTS
The song of Clay-colored Thrushes consists of
a sequence of syllables that is highly variable in
length. Overall variation of number of syllables
per song (mean = 7 syllables. CV range = 30-
94 07), song length (mean = 4.07 sec. CV range -
31-101%), and silent intervals between songs
(mean = 3.94 sec, CV range = 58-131%) was
high within and across individuals, but song
tempo had low variation (mean = 1.9 syllables/
sec. CV range = 7-1 1%) (;? = 8 males. 44-150
songs/malc).
Wc identified 91 different syllable types from
all birds. Male repertoire size ranged from 10 to
17 syllable types (Table I ). The cumulative plots
of syllable types all clearly reached asymptotes,
demostrating that complete repertoires were
detected for all males during the time of the study
(Fig. 3). Males sang a given syllable type only
once during the study period in few cases.
Only single syllables were shared among males
rather than complete songs. There were 51
matches considered as shared syllable types
between pairs of males by at least one observer.
Seventeen of these 51 possible matches were
identified as shared types by all three observers
(Table I). These final matches consisted of 13
different syllable types. Comparisons within pairs
of males showed that mean spectrogram correla¬
tions were constantly higher for shared types than
for random syllables (Table 2).
Most of the males (6/8) shared syllables with
three or more males (Table 1 ). Males shared on
average (,± SD) 4 ± 2 syllables, which corre¬
spond to 25 ± 16% of their repertoires (Table I).
Repertoires were composed of more individual
syllable types (syllables exclusive to each male)
than shared syllable types (t7 = 4.689, P = 0.002)
(Table I ). The frequency of individual and shared
syllables in songs did not differ from that
expected by chance according to the proportion
ol individual and shared types in the repertoires
(/7 = 0.047, P = 0.96) (Fig. 4). Males that had
closer song perches did not have more similar
repertoires (Z = -0.03 6. P = 0.48) (Table I ).
450
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 3. September 2012
TABLE 1. Distance (m) between territories (upper half) of eight male Turdus grayi (A-H) and number of shared
syllables between males (lower half) during the 2008 breeding season in San Jose. Costa Rica. Male syllable repertoire size
is shown in parenthesis.
Male
A (12)
B (II)
C (14)
D (13)
E (10)
F (17)
G (12)
H (17)
A
55
149
209
271
32
135
125
B
0
_
96
181
325
29
84
75
c
0
0
_
140
420
118
68
33
D
2
0
1
—
452
181
205
124
E
1
0
1
1
—
303
394
395
F
1
0
2
1
1
—
113
93
G
0
0
1
0
0
0
—
82
H
1
0
3
1
0
0
0
—
Totals3
4
0
7
5
2
4
1
5
" Tolal number of different shared syllable types. A male may share the same syllable type with more than one other male.
DISCUSSION
Songs of Clay-colored Thrushes are highly
variable in length and number of syllables within
and between males. Variation between males in
song length and syllable number could be the
result of individual differences in neuromuscular
development that constrain song duration and
performance (Lambrechts 1996, Suthers et al.
1999). For example, male Zebra Finches (Taenio-
pygia guttata) with longer and more complex
songs have greater reproductive success (Wood-
gate et al. 2012). Thus, song length and syllable
number are traits that could provide females with
valuable information regarding male quality. In
turn, variation in song length (Weary et al. 1988)
and song tempo (Cooper and Goller 2006) within
males could be affected by the motivational slate
of the singing bird. However, song tempo in our
study was considerably steady.
Male Clay-colored Thrushes have a repertoire
of 10-17 syllable types. This repertoire size is
within the range that has been observed for other
thrushes of the genus Tardus, which have
repertoires composed of 6 to 25 syllable types
Number of recorded syllables
breech n e ' season* San inlfr Kp*™ire sjf ^ number of recorded syllables of Clay-colored Thrushes during the 2001
breeding season m San Jose. Costa Rica. The solid gray line indicates mean repertoire size = 13 syllable types (« =
Vargas-Castro et al • SONG OF THE CLAY-COLORED THRUSH
451
TABLE 2. Mean spectrogram correlations lor shared
syllable types and one set of random syllables from the
songs of eight male Turdus grayi by male pair. Each value
represents die average of 100 spectrogram correlations,
except for male pairs A-F and D-H, which are based on 1(1
and 70 correlations, respectively.
Shared type
Male pair
First
Second
Third
Random
A-D
0.75
0.70
—
0.33
A-E
0.66
—
—
0.18
A-F
0.68
—
—
0.34
A-H
0.70
—
—
0.29
C-D
0.86
—
—
0.31
C-E
0.64
—
—
0.10
C-F
0.64
0.76
—
0.27
C-G
0.60
—
—
0.27
C-H
0.62
0.55
0.65
0.35
D-E
0.69
—
—
0.21
D-F
0.55
—
—
0.30
D-H
0.63
—
—
0.29
E-F
0.73
—
—
0.16
(Rufous-backed Thrush [7'. rufopalliatus] in Gra-
bowski 1979, American Robin |7'. migratorm \
in Johnson 2006. Japanese Thrush IT", cardial in
Tooru 2006). Common Blackbirds (T. me rid a ) in
contrast have a larger repertoire of motifs
(Rasmussen and Dabelstcen 2002) than the syllable
repertoires of Clay-colored Thrushes, bid this
species has a different song structure.
The repertoire of the Clay-colored Thrush is
composed of a set of individually unique syllabic
types and a smaller number of syllable types lhai
arc shared with neighbors. A larger fraction of
individual syllables comprising the repertoires
probably facilitates individual recognition (Falls
1982, Beecher et al. 1994), although unique
re
>»
)
C
c
o
t:
&
o
CL
FIG. 4. Proportion of individual (white) and shared
(gray) syllables sung by each male Clay-colored Thrush
during 2008 in San Jose, Costa Rica. Total number of
recorded syllables is at the base of each bar.
syllables or song types may not be necessary to
accomplish individual recognition (Weary and
Krebs 1992). Individual syllables could be
invented, improvised or learned elsewhere (Mar-
ler and Peters 1982, Payne 1996, Kroodsma et al.
1999). Johnson (2006) observed that most of the
elements (75-82%) in the repertoires of hand-
reared American Robins were acquired by inven¬
tion. The high and similar proportion of individual
syllables that we found in the repertoires of Clay-
colored Tlmtshes suggests that at least part of
these syllables are invented as well.
Shared syllables in mrn reflect social learning
among neighboring males (Payne 1981. Baptista
and Peirinovich 1984. Beecher and Burt 2004).
Only single syllables were shared among males,
suggesting that syllables arc the unit of imitation.
Shared song components are maintained through
time in a local population if vocal learning occurs
early in life (e.g.. as nestlings) followed by short
natal dispersal or if song learning occurs after
young males disperse and interact with local
neighbors in a new area (Kroodsma 1974, Lynch
1996, Payne 1996), Generally, the extent of re¬
pertoire sharing decreases with increasing dis¬
tance between territorial males (Bertram 1970.
McGregor and Krebs 1982). However, we did not
find a relationship between repertoire sharing and
song perch distance. Such a relationship would
not be expected if Clay-colored Thrushes disperse
relatively long distances before setting up their
First territory. Unfortunately, natal dispersal dis¬
tance of Clay-colored Thrushes is only known
for one male that we found defending a territory
about 130 m distant from where it was banded
as a nestling. Alternatively, Clay-colored Thrush¬
es could follow a different pattern of repertoire
sharing with increasing distance, similar to that of
Common Blackbirds and Common Nightingales
( Luscinia megarhynchos). which are more likely
to share components of their repertoires with other
males at intermediate distances (>100 m) rather
than with closer neighbors (Hultsch and Todt
1981).
Local repertoire sharing has an important role
in territory possession (Beecher et al. 2000) and
song discrimination by females (Searcy 1990.
Searcy et al. 2002). The relative importance of
song sharing in C lay-colored Thrushes for differ¬
ent social functions needs further investigation.
Future research on population dynamics, espe¬
cially natal dispersal, as well as on the critical
period for song learning is required to better
452
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. September 2012
understand song development and function in this
and other species of thrushes.
ACKNOWLEDGMENTS
Wc thank W. A. Searcy. Karla Rivera-Caceres, and two
anonymous reviewers for providing helptul comments on
an early draft of the manuscript. We also thank Vice-
rrectoria tie Admmistracion of the Universidad de Costa
Rica, especially Oficina de Seguridad y Transito for helping
us with logistics and permits to conduct the study. MICIT/
CONICIT provided financial support of activities related to
this investigation. Dean Hawthorne helped with Raven's
detector and correlator. All procedures in the present study
comply with the current laws of Costa Rica.
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The Wilson Journal of Ornithology 1 24(3):454— 466, 2012
SILVEREYES ( ZOSTEROPS LATERALIS) SONG DIFFERENTIATION IN
AN ISLAND-MAINLAND COMPARISON: ANALYSES OF A COMPLEX
CULTURAL TRAIT
MYRON C. BAKER1-2
ABSTRACT. — Members of the genus Zosterops are known for their colonizing ability and extensive phenotypic
differentiation on numerous islands. There have been morphological and biochemical analyses of some Zosterops
populations, but little study has been devoted to patterns of vocal communication signals, known to be important pre-mating
barriers in many bird species and in possible diversification of taxa. I report on the song system ol one subspecies of
Zosterops in a mainland population and an island population 15 km distant. I used both a traditional subjective classification
of song elements and the multivariate procedure of linear discriminant analyses (I DA) of measured sound features. The
syllables constituting songs exhibited a low level of stereotypy, disallowing a lexicon of syllable "types' to be constructed
for individuals or a population, New syllables were continuously produced as a bird uttered more and more songs, possibly
indicating an extremely large repertoire or an open-ended generation of vocal innovations. I.DA indicated songs ot the
island population were moderately differentiated from and less variable than those of the mainland. This type of song
system creates a problem for research on vocal signals, whether directed at comparisons between birds in a local area or
between populations. I made a preliminary effort to address this problem and discuss mv results in the framework of
Zosterops and its propensity for evolutionary diversification. Received II October 2<>l I . Accepted 6 March 2012.
Phenotypic divergence on islands has long held
interest for students of evolutionary biology
(Darwin 1859, Mayr 1963, DeSalle and Temple¬
ton 1988, Grant 1999), stimulating empirical
and theoretical work on adaptation and speciation
(Grant 1968, Barton 1989. Mayr and Diamond
2001). Comparing phenotypic differentiation
of isolated populations on different islands or
between mainland and island populations has
been more clearly suggestive of causal processes,
such as founder effect, ecological selection, or
genetic drill (Kaneshiro 1980. Mayr 1982, Baker
et al. 2006. Parker et al. 2010). Historically,
studies ot island biotas emphasized patterns of
morphological evolution, but more recently in¬
clude molecular evolution (c.g., Slikas et al. 2000;
Clegg et al. 2002a, b: Moyle et al. 2009; reviewed
by Grant 2001, 2002). However, behavioral
components of the phenotype, especially those
involved in mating, have received much less
attention in island studies.
Research on mating signals of birds has con¬
tributed a number of findings that raise questions
on the possible contribution of learned behavior
patterns and social selection to genetic differen¬
tiation of populations (West-Eberhard 1983.
Biology Department, Colorado State University. Fort
Collins, CO 80523, USA; and School of Animal Biology.
University of Western Australia, Crawley, WA, Australia
Current address: I27N Ambrosini Uane. Femdale, CA
95536, USA; e-mail: mcbaker@colostate.edu
MacDougall-Shackleton and MacDougall-Shack-
lelon 2001, Slabbekoorn and Smith 2002, Price
2008, Servedio et al. 2009). Acoustic features of
learned vocal signals, for example, are frequently
correlated with morphological patterns of popu¬
lation differentiation, giving rise to the question of
their role, if any, in speciation (Grant and Grant
1989, Lachlan and Servedio 2004. Price 2008).
Regardless of how a vocal difference arose in an
island population upon or following colonization
(founder effect, drift, selection), if it is a signal
involved in mating, the production of the
differentiated form of the signal could have a
role in evolutionary sequelae (c.g., reproductive
isolation, genomic divergence) that would be
tested, and possibly reinforced (Butlin 1989) in
the event of subsequent contact with new
immigrants.
Much of what we know about adaptive ra¬
diation of species on islands, particularly the
correlated vocal communication traits, we owe to
the extensive studies of Darwin's finches on the
Galapagos Islands (Grant 1999, Podos 2001 1. An
equally famous example of bird speciation is the
genus Zosterops, a highly speciose group of some
85 species (Gill and Donsker 2012) distributed
widely in the world, but especially known for
having colonized numerous islands throughout the
Indian Ocean and tropical Pacific. Many of these
species and subspecies are island endemics (Mees
1961, Pratt et al. 1987). The possibility that social
selection may be important in Zosterops is
relevant to the ‘great speciator’ status of this
454
Baker • SILVEREYES SONG EVOLUTION
455
taxon (Diamond et al. 1976, Warren et al. 2006).
The unusually high rate of Zosterops diversifica¬
tion in species and subspecies, together with rapid
expansion and colonizing ability (potential gene
flow), presents something of a paradox: i.e., how
can one explain a high rate of differentiation from
island to island (e.g.. as little as 2 km: Mavr and
Diamond 2001) in a genus with an apparently
exceptional dispersal capacity? Could learned
mating signals have an isolating effect and serve
to repel new attempts to colonize an island with
an established population?
Zosierops appears to be an ideal taxon with
which to examine patterns of evolutionary differ¬
entiation in association with possible diversifica¬
tion of reproductive communication signals. Local
populations are commonly dense with singing
males during an early dawn chorus of —30 min. A
given male's song is —5-7 sec but can range up to
10 sec with noticeable spaces between successive
songs, which are produced at a rate of five or so
songs per min and consist of a series of discrete
sound units usually referred to as notes or
syllables (1 use the latter term). A song sounds
like a warbling sequence of similar syllables not
possessing any obvious syntactical variation to the
human listener. Ecological studies and research on
vocal communication behavior of Zosterops are
scant with only a handful of studies reporting on
ecology or behavior, and most have been
conducted on a single island without comparison
to other island or mainland populations. Thus,
knowledge of song structures across the genus is
lacking.
These factors led me to conduct research on an
island population (Woody Island) and an adjacent
mainland population 15 km distant (near Esper-
ance) of Zosterops in Western Australia. The
objectives were to: ( I ) compare the populations to
see if they differed in song traits, and (2) explore
methodology that could be used in an extensive
survey of Zosierops island endemics. Choice of
the study areas was based upon two factors. First,
they were relatively near where 1 lived. Second,
given the species reputation for colonizing ability
(and banding-recovery data from mainland loca¬
tions) the 15-km distance between the island and
mainland populations seemed trivial. Therefore, if
the two study populations differed vocally it
would be consistent with the hypothesis that a first
step in behavioral isolation is differentiation in
reproductive communication signals. The two
target populations of the present paper are
considered conspecific; there has been no evidence
collected to address their morphological or molec¬
ular differences, nor are there data on possible
exchanges of birds between them. Exchanges
between any Zosierops populations on different
islands remain undocumented. Work on Zosterops
populations occupying islands elsewhere indicated
inter-island distances of 8-12 km or less separate
morphologically differentiated forms (e.g., Mees
1961).
METHODS
General Biology, Study Locations, and Sam¬
pling of Vocalizations. — Most Zosterops are
known as White-eyes or Silvereyes for the
characteristic white-feathered eye ring and tend
not to exhibit sharply defined plumage patterns
having more or less gray green to yellow green
upper parts, green or brownish sides, and gray or
yellow below. They are socially and genetically
monogamous (Robertson et al. 2001). breed in
dense colonies (11-30 pairs/ha: Catterall et al.
1982). and males sing intensely for somewhat
<30 min in the pre-dawn. 1 and a field assistant
(M. S. A. Baker) tape recorded a mainland
population sample of Zosterops lateralis gouldi
(Johnstone and Stori 2004; Z. /. cliloronotus in
some treatments) occupying coastal scrub habitat
(low sclerophy llous shrubs/heath) near the town
of Esperance, Western Australia on two succes¬
sive mornings during the pre-dawn chorus of the
breeding season (Nov 2004). 1 recorded a second
sample in similar habitat on two successive
mornings, within a few days of the Esperance
sample, on Woody Island, a 240-ha island 15 km
offshore from Esperance in the Recherche Archi¬
pelago in the Southern Ocean. The second
morning of recording of both populations began
where recording the previous morning had ended.
No searching for nests was conducted to follow
breeding status. The song of Z lateralis has often
been described as a ’'sequence of warbling notes"
but. a wide variety of songs has been described in
onomatopoeia (Pratt et al. 1987) among different
island populations of Zosterops in the tropical
Pacific; many of these verbal descriptions hold
little resemblance to "a sequence of warbling
notes".
Birds were not marked, which would have been
of limited help as most singing was under dim
pre-dawn light when the recording occurred, and
reading color bands would have been uncertain or
impossible. I moved continuously through the
456
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 3. September 2012
habitat to ensure recording of different birds,
sometimes skipping the neighbor of the bird just
recorded if there was noticeable movement.
Territory measurements were not conducted, but
the distance from one singing male to the next was
on the order of 10-15 m, and studies elsewhere
found territory sizes of —900-1,500 in2 (Catterall
et al. 1982). The small territories made it
relatively easy to keep track of the location of a
bird previously recorded as attention was placed
on the next subject. However, the high density
created some problems as singing was both loud
and frequent during the dawn chorus and often
songs of an individual being recorded had parts
overlapped by another. It had been previously
noted in a different location that Silvereyes utter
songs independently of one another (i.e., no
alteration, etc.; Slater 1991, 1993). The birds
appeared to be well habituated to people, perhaps
from the frequent tourists near these habitats and,
together with the low light conditions. I was able
to get close to singing birds. These conditions
were optimal for near-field recording, but it was
difficult to obtain songs free of overlapped
syllables.
Recordings were made with a Marantz cassette
deck (PMD222, Marantz America Inc., Itasca, IL.
USA) connected to a Sennhciser ME62 micro¬
phone (Sennheiser Corp.. Old Lyme, CT, USA)
mounted in a 45-cm parabolic reflector. A
constant frequency marker and known click rate
(Seiko SQ-44. Seiko Instruments. Maidenhead,
UK) were recorded before and at random times
during a recording session so that tape speed
could later be checked for accuracy. No changes
in tape speed were found at the time of digitizing
the songs for acoustical analyses.
Acoustical Analyses. — Vocal recordings were
digitized with Sound Blaster Audigy 2NX (Crea¬
tive Technology Ltd., Creative Labs Inc., Milpitis,
CA, USA ) with 16 bit accuracy at a rate of 44. 1 kHz
to a personal computer. The favorable recording
conditions provided good quality sounds, but low
frequency noise (below -300 Hz) was filtered
out. Sound spectrograms were produced with Real
Time Spectrogram (Model 5129 Version 2.3:
Kay Elemetrics Corp (now KayPentax). Lincoln
Park, NJ, USA) with settings of 256 points, and
Hamming Window weighting. I used Sound
Analysis Pro software (Version 1.04: Tcherni-
chovski et al. 2000, Baker and Loguc 2003,
Tchemichovski and Mitra 2004) following digiti¬
zation to quantify the spectral features of the
syllables constituting songs. Sound Analysis Pro
creates spectral derivatives of a sound, such as a
song syllable, and automatically extracts measure¬
ments of a set of acoustic variables (Fee et al. 1998.
Ho et al. 1998). The values of each acoustic
variable were averaged over a succession of narrow
and overlapping windows of time (data window
9.27 ms, advance window 1.36 ms) over the
duration of the given syllable. Six variables were
quantified for eaeh syllable examined by Sound
Analysis Pro: sy llable duration, pitch, fm (frequen¬
cy modulation is the change in frequency with
time), am (amplitude modulation is the change in
sound power with time), goodness of pitch (how
much of the sound energy is concentrated in the
pitch), and Wiener entropy (a measure of the
breadth and evenness of a sound: pure tones have
low entropy, white noise high entropy). Mathe¬
matical and verbal descriptions of these features
are provided in Tchemichovski et al. (2000) and
Tchemichovski and Mitra (2004).
Analysis Strategy. — The only published research
providing a detailed description of song of any
Zosterops is that of Slater (1993) (Capricorn
Silvcreye, Z. lateralis chlorocephalus ), and initially
I thought I would be able to follow the analysis
approach used in that study. Slater’s study,
however, turned out not to be an appropriate model:
it did not present actual sound spectrograms of
songs hut instead made line drawings of syllables to
create a catalog of syllable ‘types', a method that
can be an impediment to comparative studies. I
tried to follow this methodology by examining
sound spectrograms of songs, and systematically
comparing syllables looking for matches, but found
that syllables w ere difficult to sort into categories of
'types': there was a great deal of variation and
grouping and splitting often had a highly arbitrary
aspect to it, The population (and subspecies) studied
by Slater (1991. 1993) may have exhibited more
stereotypy in song elements than the populations I
recorded, hut without a published presentation of
actual spectrograms of syllable ‘types', and the
variants subsumed in these categories, a compari¬
son of Slater's results to my data was impossible. It
became necessary to formulate a different method
for comparing population samples of Zosterops
songs for the purposes of my research.
I present a typological classification to demon¬
strate the problem, based upon sound spectro¬
grams. to show the great diversity of song
elements and, evidently, an essentially continuous
generation of new syllables constituting Silver-
Baker • SILVF.REYES SONG EVOLUTION
457
eyes' songs. I found there are some stereotyped
syllables repeated now and then in an ongoing
stream of songs from an individual, and syllable
sequences recur occasionally, but the syllables did
not constitute a finite repertoire expressed by a
given bird. Extreme complexity of song struc¬
tures. including hundreds of syllable types in the
songs of an individual, and individual song
repertoires of hundreds or thousands (some likely
unbounded), have been described in songbird
species (Wiidenthall 1965, Kroodsma and Parker
1977, Kroodsma 1980, Kroodsma et al. 1999,
Huntsman and Ritehison 2002, Price and Yuan
201 1 ). This vocal variation can be limiting or too
often effectively preclude the study of geographic
variation in specific birds. The Eastern Bluebird
(Sialiu sialis ), an example of these kinds of
songbirds (Huntsman and Ritehison 2002), dem¬
onstrated the more songs recorded, the more song
types are found, even after assaying many
hundreds of songs of an individual (i.e.. plotting
the cumulative number of song types identified
versus the number of songs uttered did not reach
an asymptote).
My unsuccessful attempt to categorize the large
variety of song elements of the Zosterops
recorded into a relatively fixed repertoire of
syllables, and my lack of confidence in the
typological classification approach, led me to
consider an alternative method of analysis. This
alternative is based upon the use of linear
discriminant analysis to create a way to compare
the song syllables of individual birds and of
population samples of birds' songs. I used a
syllable-level analysis for two reasons. First, I
assumed my results would be most comparable to
the only other detailed examination of Zosterops
songs (Slater 1993), which used the syllable in
analyses, and second because previous studies of
several songbird species (although not Zosterops)
had demonstrated that syllables w'ere the units of
transmission during the song learning process
(Marler and Peters 1977, 1988; Kroodsma and
Picker! 1984).
Statistical Analyses. — Measurements of the
acoustic features of song syllables were examined
by linear discriminant analysis (LDA) using
STAT1STICA software (Version 5.1. StatSoft
Inc. 1995) or MINITAB (Version 13. Minitab
Inc. 2000), Post-hoc assignment probabilities
from LDA were obtained by jack-knifed cross
validation. Correlation matrices lor LDA were
judged for sampling adequacy with the Kaiser-
Meyer-Olkin (KMO) test, and their ‘condition’
was examined with Bartlett’s Sphericity Test
using PARANAL (Budaev 1997). Basic statistics
(means, etc.) were calculated with MINITAB.
RESULTS
I recorded 10 birds in the Esperance (mainland)
population and obtained 69 good quality songs
(mean = 6.9 songs/bi id) and on Woody Island, 19
birds and 102 songs (mean = 5.4 songs/bird). The
acoustic features of the constituent song syllables
0/ 1.728: i.e., those not overlapped) w'ere
measured with Sound Analysis Pro. All songs
were prepared as sound spectrograms and exam¬
ined visually. Initially, at least, this visual
appraisal began with the goal of sorting the
constituent syllables into categories (types) for a
given population. The potential use of such a
lexicon of syllable types would allow calculation
of sharing among birds in a population and. for
my primary use, to compare song characteristics
between island and mainland samples. This
approach has often been used and works well
for many songbird species in which individual
vocabularies arc of small or modest size and
consist of stereotyped syllables. 1 found it to be
impossible to apply in my song samples, as
indicated in my initial analysis.
I selected the 13 songs recorded from a single
Woody Island bird for the initial analysis by
visual classification of song syllables and exam¬
ined the constituent syllables sequentially. This
bird was selected because it was recorded with
none of its syllables overlapped by another singer,
and it had the longest sequence of such songs in
the samples. The first four of the 1 3 songs of this
bird are illustrated (Fig. I ). indicating by numbers
the 55 different kinds of syllables I categorized by
visual examination in the total 102 syllables, and
the cases I judged to be recurrence of certain of the
syllable types. Many syllabic types appeared to be
discretely different but. in some cases, shapes alone
were misleading. Syllable types 1 0, 12, and 34 for
example, were grouped in my first pass through the
songs, but closer examination and subsequent
measurements revealed they differed consistently
on the frequency scale (decreasing -400-500 Hz
from type 10 to 12. and u similar decrease from
type 12 to 34). Similar problems arose in different
renditions of syllable 47, which covered a range of
frequencies, or the small but apparent differences
between syllables 35 and 53. Completing the
syllable-by-syllable examination of the 13 songs
Frequency (kHz)
458
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 3. September 2012
Song 1
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1 i 1 234 567 89 10 9
'u, V \«a k ^ \ y* ^ s/
11 12 13 14 15 16 3 16 17 18 12
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cr
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The Wilson Journal of Ornithology 1 24(3):467 -477, 2012
AGE-DEPENDENT ORIENTATION TO MAGNETICALLY-SIMULATED
GEOGRAPHIC DISPLACEMENTS IN MIGRATORY AUSTRALIAN
SILVEREYES ( ZOSTEROPS L. LATERALIS )
MARK E. DEUTSCHLANDER.M JOHN B. PHILLIPS,1 2 AND URSULA MUNRO3 4
ABSTRACT. — Geographic relocations of migratory passerines have shown that adults can compensate for physical
displacements; juveniles on their first migration, however, use an innate clock-and-compass strategy and are unable to
compensate for displacement. We examined the effects of changes in magnetic inclination and intensity on orientation of
adult and juvenile Australian Silvcreyes i Zosit rops I lateralis) to learn if geomagnetic cues are used by a migratory
passerine for geographic positioning. Silvcreyes, captured in breeding areas in Tasmania, were physically transported to a
location along their migratory route and assessed tor orientation during autumn migration. Adults and juveniles exhibited
seasonally appropriate, northeasterly orientation 1 1‘> and 23 east ol magnetic North, respectively) when tested under the
natural geomagnetic field. Birds were then exposed to changes in the magnetic field that simulated either southern (SimS)
or northern iSimN) locations near the beginning and end. respectively, ot their migratory route. Inexperienced juveniles
continued to show seasonally appropriate orientation (3 and 358 . respectively) in both SimS and SimN magnetic fields.
Adults, in contrast, exhibited changes in orientation but only when the experimental magnetic field w as consistent w ith a
geographical displacement that should require compensatory orientation (i.e., SimN). Adults exposed to a SimS magnetic
field continued to show season ally-appropriate orientation to the North (O'). However, adults exposed to magnetic fields
simulating locations beyond their wintering areas (SimN) altered their orientation significantly, orienting bimodally and
perpendicular (123 -303 ) to their seasonally appropriate migratory direction. These results are consistent with the
presence of an age- or experience-dependent magnetic geographic position sense in migratory Australian Silvereyes.
Received 20 February 2011. Accepted 4 March 2012.
Juvenile migratory birds to accomplish their
first migration have been shown to rely on a
‘vector strategy' that combines an innate direc-
(ional ‘compass’ heading with a temporal ‘clock’
program that affects migration distance (Helbig et
al. 1989; Berthold 1990a, b; Helbig 1991 1996;
Mouritsen 1998, 2001). However, age-dependent
recoveries of geographically displaced migratory
birds suggest adult passerines are able to use a
different orientation strategy than juveniles; adult
migratory birds can reorient to compensate for
displacement in both North-South and East-West
directions (e.g., Perdeck 1958; Mouritsen 2001,
2003; Thorup et al. 2007: Chernetsov et al. 2008).
These field experiments demonstrate adults can
perceive their position, but they reveal little
information about the cues used by birds to do so.
Birds and many other organisms possess a
magnetic compass sense to obtain directional
information (reviewed in Wiltschko and Wiltschko
1 Department of Biology. Hobart and William Smith
Colleges. Geneva, NY 14456. USA.
Department of Biological Sciences, Virginia Technical
Institute and State University, Blacksburg. VA 24061.
USA.
Centre of Environmental Sustainability. School of (lie
Environment, University of Technology, Sydney, P, 0. Box
123. Broadway. NSW 2007. Australia.
4 Corresponding author; e-mail; deutschlande@hws.edu
1995). In addition, some animals may be able to
sense gradients in the geomagnetic field to derive
geographic-position information (reviewed in
Freake et al. 2006), Specific values of the
geomagnetic field can serve as an innate ‘sign
post' or ‘releasing mechanism' for migrants to
change their migratory behavior at appropriate
locations, such as al stopover sites or migratory
boundaries. For example, when exposed to grad¬
ually decreasing values of magnetic intensity and
inclination, juvenile European Pied Flycatchers
(FicednUi hypoleuca) shift their autumn orientation
from southwest to southeast in magnetic fields that
simulate those of southern Spain, as would freely
migrating conspecifics. Southeast reorientation
towards Africa prevents the birds from migrating
over the Atlantic Ocean (Beck and Wiltschko
1988).
Use of the geomagnetic field as a ‘sign post'
does not require that birds recognize their
position; instead, specific geomagnetic field
values elicit an appropriate ‘programmed’ change
in the animal's behavior, orientation or otherwise,
and can affect both adults and juveniles. For
example, juvenile Thrush Nightingales ( Luscinia
luscinia ) increase feeding rates in a magnetic Held
simulating a stopover site in northern Egypt
(Fransson et al. 2001. Kullberg cl al. 2003). True
map-based navigation (Griffin 1952). in contrast.
467
468
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 3. September 2012
requires an animal to ascertain its position along a
gradient by comparing the local value of a map
component to a 'home' or familiar value, such as
a breeding site. Bi-coordinate positioning (i.e..
distinguishing both latitude and longitude) re¬
quires perception of two non-parallel gradients
(e.g., Wiltschko and Wiltschko 1995. Phillips
1996). Geomagnetic intensity and inclination vary
mainly along a north-south axis in many geo¬
graphic regions, and geomagnetic information
alone may provide birds w ith only a unicoordinate
map limited to latitudinal information (Mouritsen
2003). Moreover, migratory birds would likely
have to learn the pattern of magnetic gradients
within their 'home' or migratory range to
accommodate regional and temporal variation in
the geomagnetic field (Phillips and Deutschlander
1997, Frcake et al. 2006). Thus, consistent with
geographic displacement experiments (e.g., Per-
deck 1958). juvenile migrants on their first
migration would not be expected to use a
magnetic map.
Direct tests of the involvement of geomagnetic
cues in map-based navigation are few and. in most
cases, involve homing behavior in non-avian
species (reviewed in Freake et al. 2006). Geo¬
graphic displacements need to be simulated by
altering only the geomagnetic field to test for
the role of geomagnetic cues in positioning and
orientation. Only tw'o studies (Fischer et al. 2003,
Henshaw et al. 2010) have directly examined the
effect(s) of geomagnetic displacements on migra¬
tory passerines, specifically Australian Silvereyes
( Zosterops 1. lateralis) and Lesser Whitethroats
( Sylvia curruca ). Adults that had made at least
one migration prior to the experiments in both
studies were exposed to magnetically-simulated
geographic displacements while en route to a goal
(i.e., wintering areas for Australian Silvereyes and
breeding areas for Lesser Whitethroats). Both
species exhibited remarkably similar orientation
responses. Birds exposed to a 'magnetic displace¬
ment southward towards the origin of their
migratory flight continued to orient towards the
north, their seasonally appropriate direction. Birds
exposed to geomagnetic values found beyond
their goal became relatively disoriented. These
results are consistent with migratory birds using
spatial variation in the geomagnetic field to perceive
position, but the lack of redirected orientation
owards their goal leaves many unanswered ques-
tmns about the function of the magnetic field in
geographic-positioning. Moreover, juveniles were
not tested in either experiment to be sure their
magnetic compass sense was unaffected by the
experimental magnetic fields and to ensure that
other 'innate' navigation processes (such as 'sign
post* navigation) were unaffected.
We exposed both juvenile and adult Australian
Silvereyes to magnetic field values simulating
different geographic positions during autumn
migration. A simulated northern displacement
(SimN) w'as produced by decreasing both mag¬
netic inclination and total intensity to values
found to the north of the normal wintering range
for the Tasmanian population of Silvereyes. A
simulated southern displacement (SimS). pro¬
duced by increasing magnetic inclination and
total intensity, provided magnetic field values
near, or to the south, of the origin of their autumn
migratory journey in Tasmania. Our goal was to
learn if the effect of the experimental magnetic
displacements is both age- and displacement-
specific. We used larger changes in the magnetic
field than used previously (Fischer et al. 2003) to
ensure locations that were specified were well
outside the range of this subspecies. Juveniles
should be unaffected by the simulated displace¬
ment treatments and should continue to orient
north- northeast (NNE). their typical autumn
direction, if geomagnetic values do not affect
their magnetic compass or serve as innate 'sign
posts’. The orientation of adults, unlike juveniles,
should depend on the simulated displacement.
Adults in the SimS group should perceive their
location to be south of their breeding area and
should continue to orient in the seasonally
appropriate migratory direction to the NNE. SimN
adults should perceive their geographic position
as being to the north of their normal winter range
and should exhibit a change in behavior that
consists of reorientation towards specific over¬
wintering sites, dispersal to search for new over¬
wintering sites, or cessation of migratory behavior
consistent with termination of migration.
METHODS
Forty Australian Silvereyes were captured in
breeding areas prior to autumn migration near
Hobart. Tasmania (42 54' S. 147 18' E). Silvereyes
of this subspecies migrate in autumn, mainly during
dawn and dusk (Funnell and Munro 2007) to
wintering sites on the Australian continent ranging
from southeastern South Australia to southern
Queensland (Lane and Battam 1971. Griffioen
and Clarke 2002); the majority of the population
Deutschlander el al. • AGE-DEPENDENT GEOMAGNETIC POSITIONING
469
TABLE I. Values (nT = nanoTesIa) for total magnetic
intensity and magnetic inclination during holding and
iesting of Australian Silvcreyes. The birds in the SmiN
and SimS groups were held in different rooms and the
ambient values of the geomagnetic field vary slightly. The
ambient field values of the testing room also varied slightly
from each holding room.
SimN group
SiinS group
Control (ambient) — holding
54.000 nT
55.5(H) nT
field
60.25
60.8(1
Control (ambient) — testing
52,500 nT
52.5(H) nT
field
59.25
59.25
Average control field value
53,250 nT
54.000 ill
59.75J
60
Experimental — holding field
42.9(H) nT
68.800 nT
51.4(1
67.50
Experimental — -testing field
43,150 nT
69.135 nT
50.50
67.00
Average experimental field
43.025 nT
68.968 nT
value
50.95
67.25
moves northward along the southeast coast, although
some birds move westward overwintering in south¬
eastern South Australia (Funnel! 2007). Eighteen
birds were juveniles (or hatch-year) based on skull
pneumatization, which had not migrated, and 22
were adults (or alter hatch-year), which presumably
had previously migrated to and from wintering areas.
The birds were transported by airplane to
Sydney, New' South Wales (NSW) and then to
Armidale, NSW (30 30' S. 1 5 1 40' E), where all
experiments occurred from April through early
June. Silvcreyes were randomly divided into two
groups, each containing similar numbers of adults
and juveniles, and held in two adjacent rooms al
ihe University of New England’s animal care
facility. Birds were housed in pairs in non¬
magnetic. stainless steel cages (700 X 360 X
360 mm: Mascot Wire Works. NSW Australia)
placed in the center of each room within a
Merritt’s cube-surface coil for magnetic field
manipulations (Kirschvink 1992). Solid food (a
high-protein diet consisting of hard-boiled egg,
buttermilk curd. Madeira cake, fish food, meal¬
worms, and apple), fresh water, and artificial
nectar (38.5% w/v honey with a vitamin supple¬
ment) were provided ad libitum. The photoperiod
in the holding rooms was changed weekly to
match the natural photoperiod in Armidale. NSW.
All Silvcreyes were released into the wild
following our experiments.
Orientation Tests. — These tests were conducted
in a separate building, — 1 00 m from the animal
care facility. Tests began 30 min before sunset
and lasted for 90 min, Birds were transported to
and from the test room in a light-tight box. Each
evening, 10 Silvcreyes were tested individually in
funnel-shaped, aluminum cages (Emlen and
Hmlen 1966) covered with translucent ‘white’
Perspex tops. A single incandescent bulb centered
above the test room provided diffuse illumination.
Each funnel was lined with typewriter correc¬
tion paper (formerly I ipp-Ex. B1C Deutschland
GmbH. Eschbom, Germany) to record bird
activity. Birds hop on the Tipp-Ex paper within
Emlen funnels leaving scratch marks as a record
of where and how often they hop on the paper
(Emlen and Emlen 1966). The number of
scratches on the Tipp-Ex paper was recorded for
each of 24 15 -sectors, starting at 0-15 . 16-30°.
to 346-360 . The total number of scratches on the
Tipp-Ex paper was used as an estimate of nightly
activity, or migratory restlessness. A bird that left
<35 scratches was classified as inactive and no
orientation was recorded for that night. Nightly
orientation (mean angular direction, a; and
vector length, r) was calculated from the distri¬
bution of scratches in the 24 sectors. Vector
length provided an indication of the nightly
concentration of orientation between 0 and 1; a
larger r value indicated greater clustering in the
distribution of scratches.
Control Tests and Experimental Simulations. —
The orientation of each bird was tested on five
nights prior to exposure to the experimental
magnetic field in the ambient magnetic field of
Armidale (‘control period’; Table 1). Median
activity, median concentration, and mean vector
were recorded for each individual for the control
period from five nightly bearings (Table 2). The
design of our experiments required active, goal-
oriented birds w'ilh clear Orientation towards their
wintering areas; thus, individuals that did not
exhibit seasonally appropriate orientation, defined
a priori as a mean vector between 240 clockwise
to 120 . during control tests were eliminated from
further experimentation. Tasmanian-breeding Sil-
vereyes are partial migrants; some individuals
may not migrate and would not show northward
autumn movements. Four birds with mean vectors
during the control period of 223 and 159° (2
adults) and 158 and 148 (2 juveniles) were
omitted from experimental tests.
Birds were exposed to an altered magnetic Held
using a vertically aligned cube-surface coil
(Kirschvink 1992) around their holding cages
470
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 3. September 2012
TABLE 2. Median activity, median concentration, and mean vector ( ot and r lor angle and vector length, respective!))
for Australian Silvereyes prior to and during exposure to magnetic fields simulating North (SimN) and South iSimS)
locations. For birds w hose distribution of nightly bearings were axially-oriented, v and r values are indicated in italics and
the i value is given as the strongest end of the bimodal axis, as defined by which end of the axis was nearest to the greater
number of nightly bearings. Birds that were active on only one or two nights (indicated by NA rather than sample si/e.
n) during displacement tests were omitted from further analyses.
Control:
before displacement
Sim Field:
during displacement
Bird
n
Median activity Median concentration
aC't
r
n
Median activity
Median concentration a( t
r
SimN adults
A1
5
129
0.28
37
0.77
6
140
0.18
337
0.55
A2
5
200
0.26
II
0.51
6
113
0.16
287
0.15
A3
5
222
0.19
45
0.93
6
109
0.41
129
0.59
A4
5
821
0.41
289
0.63
6
462
0.56
278
0.52
A5
5
499
0.18
348
0.61
6
456
0.24
92
0.61
A6
5
262
0.20
10
0.50
6
295
0.13
94
0.18
A7
5
641
0.24
40
0.53
6
702
0.38
319
0.31
A8
5
288
0.14
80
0.93
6
298
0.17
301
0.58
A9
5
483
0.1 1
17
0.88
5
323
0.14
325
0.62
A10
5
175
0.24
21
0.82
NA
SimN juveniles
Jl
5
111
0.28
43
0.49
6
201
0.20
10
0.83
J2
5
88
0.28
103
0.40
3
69
0.33
51
0.77
J3
5
909
0.19
9
0.62
6
372
0.10
37
0.59
J4
5
1,151
0.26
60
0.27
4
64
0.40
349
0.55
J5
5
514
0.23
14
0.30
4
41
0.30
312
0.62
J6
5
396
0.17
47
0.86
6
57
0.33
356
0.96
J7
5
510
0.1 1
25
0.49
6
176
0.25
335
0.55
J8
5
202
0.28
356
0.54
6
126
0.30
311
0.48
SimS adults
All
5
254
0.34
331
0.71
5
322
0.33
21
0.56
A12
5
284
0.20
29
0.43
5
168
0.25
15
0.67
A13
5
564
0.19
83
0.88
5
380
0.30
139
0.58
A14
5
608
0.27
8
0.57
5
206
0.39
0
0.51
A15
5
179
0.25
29
0.52
5
1 16
0.24
354
0.96
A16
5
901
0.14
318
0.77
5
252
0.31
10
0.64
A17
5
206
0.32
36
0.54
5
316
0.28
110
0.31
A18
5
225
0.34
38
0.24
5
92
0.37
343
0.68
A19
5
275
0.39
5
0.78
5
208
0.46
301
0.56
A20
5
586
0.49
I
0.73
5
599
0.43
322
0.57
SimS juveniles
J9
5
233
0.27
48
0.71
5
131
0.34
41
0.40
J 10
5
201
0.22
356
0.56
5
160
0.21
334
0.79
Jl 1
5
958
0.27
66
0.57
6
958
0.22
23
0.77
J12
5
412
0.21
304
0.68
5
412
0.17
23
0.71
J 13
5
688
0.38
17
0.64
6
184
0.45
15
0.45
J14
5
63
0.36
13
0.96
3
95
0.55
334
0.96
J15
4
90
0.3 1
17
0.77
NA
J16
5
96
0.26
19
0.85
NA
after control tests. Each holding room was used
tor one of two experimental treatments. One
gioup was exposed to values of magnetic intensity
and inclination that simulated displacement, or
locations, to the north towards the equator and
beyond their normal wintering areas (simulated
north or ‘SimN" group: Table 1, Fig. 1). The
‘SimS’ group was exposed to magnetic held
values that simulated displacement, or locations,
to the south, towards breeding areas in Tasmania
(Table I, Fig. 1 ). The values of magnetic intensity
or inclination for both the SimS and SimN groups
Deutschlander et al. • AGE-DEPEN DENT GEOMAGNETIC POSITIONING
471
Juveniles
FIG. 1. Orientation of Australian Silvereyes in the natural geomagnetic field (C and D), the simulated North
displacement magnetic field (SimN shown in A and B). and the simulated South displacement magnetic field (SimS shown
in E and F); juveniles (A. C, E) and adults (B. D. F) are shown on the left and right, respectively. Small solid dots show
individual nightly bearings for all birds tested in the specified condition and each line with a solid dot on the end represents
the mean vector for an individual bird (as given in Table 2 by ot and r): all data are plotted with respect to magnetic north
(mN = 0 ). The mean unimodal orientation of each group is shown graphically by the 95% confidence ellipse on each plot
( Hotelling's one-sample test). The gray arrowheads outside each circle show the significant mean angular direction for each
distribution. Dotted lines on the map show the geographic locations of the SimN average magnetic intensity, SimN average
magnetic inclination, and SimS average magnetic inclination (SimS intensity is not on map): gray area shows the
approximate winter range for Tasman ian-breeding Silvereyes.
ilid not correspond (Fig. I ) to any one geographic
location due to the method used to change the
magnetic Field (Fischer et al. 2003). The SimN
values of intensity and inclination specify differ¬
ent magnetic ’latitudes' towards the equator with
an inclination value on the Australian continent
and an intensity value to the north of Australia.
The SimS value of magnetic inclination corre¬
sponds to locations in southern Australia. How¬
ever. the SimS value of magnetic intensity does
not exist at that region of the earth.
Birds were tested for orientation after at least
6 days of exposure to the experimental magnetic
fields. A cube-surface coil similar to that used in
the holding rooms generated the experimental
magnetic fields in the testing room (Table J).
Each bird was tested for 5-6 nights ( ‘displace¬
ment period"). Birds were returned to their
holding cages between tests and w ere continually
exposed to the SimN or SimS fields. The only
time a bird was not exposed to the altered
magnetic Held was during the 1 0-15 min transport
472
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 3. September 2012
between the holding and testing rooms. Only
about half of the birds in each treatment group
could be tested on a given night, and birds from
the two groups were tested alternately on
successive nights: thus individual birds were
tested once every four nights.
Median activity, median concentration, and
mean vector were calculated lor each bird from
its nightly bearings (as in the control period) to
examine the orientation ol birds exposed to the two
experimental treatments (Table 2). Three birds that
were inactive ( <35 scratches) for four or more
nights during the displacement period were not
used for statistical comparisons (Table 2). as
reliable mean vectors could not be calculated from
fewer than three nights of activity.
Magnetic Field Measurements and Manipula¬
tions.— Magnetic fields were measured using a
Cesium magnetometer (Model #757010. Seintrex
Ltd.. Concord. ON. Canada) operated with a TM4
interface (Geophysical Technology Ltd.. University
of New England. Armidale. Australia). Changes
in the geomagnetic ITdd were accomplished by
altering only the vertical component of the magnetic-
field. which simultaneously changed both total
intensity and inclination (Fischer et al. 2003).
Altering the vertical component of the magnetic
field did not change the horizontal alignment or
declination of the magnetic field.
A 2-irr. four-element. Merritt's cube-surface
coil (Kirschvink 1992) was oriented vertically in
each holding room to either add to or subtract
from the vertical component of the geomagnetic
field for SimS or SimN' conditions, respectively.
Each coil was powered by one channel of a
current-regulated two-channel power supply. A
vertically aligned. 2.1 -nr. four-element. Merrilfs
cube-surface coil was used to alter the magnetic
field in the testing room. A two-channel power
supply (one channel for SimS and one for SimN)
was used to provide current to the coil. Current
was applied to both coils to match the magnetic
fields during testing as closely as possible to the
holding fields (Table 1).
Statistical Analyses. — We ascertained the over¬
all orientation ot each group of birds (each age
class for each simulated displacement), using one-
sample Hotelling's test, which considers both
bearing and length of each bird’s mean vector
(Batschelet 1981 ). The I fotel I ing's test generates a
95% confidence ellipse for the mean orientation
ol any significantly oriented sample (Fig. I). We
also examined the change in mean angular
direction between the control and displacement
tests (A direction = displacement mean bearing
minus control mean bearing for each bird) and the
change in mean vector length (A length =
displacement vector length minus control vector
length for each bird) to evaluate the effect of
simulated displacement on individual orientation.
We compared the changes in direction and in
vector length between different treatment groups
with noil-parametric Wileoxon Rank Sum tests on
each set of independent variables.
Median nightly activity and median concentra-
lion were measured before and during simulated
displacement for each individual (Table 2). These
median values for activity and concentration were
used in two repeated measures ANOVAs (using
the GLM procedure of SPSS 1 1.0. 2001) to
ascertain if birds changed migratory behavior
between the control and displacement periods (the
‘within-subjeets’ factor, which we designated as
'time') and to learn whether activity or concen¬
tration varied as a function of age or type ol
displacement (the 2 'be tween-subjects' factors).
The distribution of median values for activity and
concentration was tested for normality using a
one-sample Kolmogorov-Smirnov test. Data were
transformed where appropriate to conform to
requirements of parametric analysis. Data were
back-transformed for presentation (Fig. 2). All P
values are two-tailed.
RESULTS
Control Orientation. — Juvenile and adult Silver-
eyes in the ambient magnetic field of Armidale
oriented towards the north-northeast (NNE) with
mean hearings of 23 and 19 . respectively (one-
sample Hotelling’s test, r = 66.3 and 131.2. P '
0.005 for both samples). Thus, both age groups of
birds exhibited seasonally appropriate orientation in
the local geomagnetic field (Table 2: Fig. 1C. D).
Juvenile Orientation During Exposure to SimS
and SimS Magnetic Fields. — Juveniles in both
SimN (Fig. 1 Aland SimS displacements (Fig. IE)
were well oriented with mean bearings of 358 and
3 (r = 57.4 and 85.5, P < 0.005 for both sam¬
ples). Most juveniles in both experimental mag¬
netic fields oriented slightly counterclockwise ol
their control directions with a slight increase in
mean vector length (Table 2). However, neither
treatment resulted in a significant difference in
orientation from that exhibited during the control
period: the two groups of juveniles did not differ in
their deviations from their control direction or in
Nightly concentration Nightly activity
Deutschlander el al. • AGE-DEPENDENT GEOMAGNETIC POSITIONING
473
Test period
Key
R>] SimN Adults
SimS Adults
Pi] SimN Juveniles
f7"] SimS Juveniles
Control Displacement
Test period
FIG. 2. Distribution of median nightly activity and median nightly concentration of activity (from Table 2) for juvenile
and adult Australian Silvereyes during both the control and simulated displacement (i.e., ‘displacement’) tests for the SimN
and SimS groups. Boxes show the interquartile range with the median represented by the transecting line. Whiskers show
the distance from the end of the box to values that are <1.5 box lengths from the box borders (the points plotted with an
open circle are outliers within 1.5 to 3 box lengths from the box border).
474
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 3. September 2012
changes in iheir mean vector length (Wilcoxon
Rank Sum test. W = 33. P = 0.14 for both
comparisons).
Adult Orientation During Exposure to SitnN
and SitnS Magnetic Fields. — SimS adults contin¬
ued to orient towards the north with a mean bearing
of 0° ( r = 12.7. P < 0.05; Fig. 1 F). The distribution
of adults exposed to the SimN magnetic Held was
not significantly oriented to the north or in any other
uni modal direction if = 2.6. P > 0.05; Fig IB).
SimN adults were bi modally oriented along a mean
axis of 123 -303 (/’ =- 30.2. P < 0.05, on doubled
angles), roughly perpendicular to their seasonally
appropriate migratory direction to the NNE exhib¬
ited in control tests. Adults exposed to the SimN
magnetic field deviated more from their control
direction than SimS adults ( W = 70.5, P = 0.013);
SimN adults also had shorter mean vector lengths
compared to SimS adults (W = 64, P — 0.035).
Nightly Activity and Concentration of Orienta¬
tion. — Median activity and median concentration
were not normally distributed and were trans¬
formed using the lOgwi of activity and the square
root of concentration, respectively. Both variables
fit the requirements after transformation for
ANOVA (Kolmogorov-Smirnov Test after trans¬
formation; activity; Z = 0.65 and 0.53 with P-
values of 0.79 and 0.95, respectively, for the
control and displacement periods; concentration:
Z = 0.70 and 0.50 with F-values of 0.72 and
0.97).
A significant three-way interaction was ob¬
served for median nightly activity among time
(the within-subjects factor that reflects the com¬
parison between the control and displacement
periods), age. and type of displacement (Repeated
measures ANOVA. interaction: FUN — 4.435. P =
0.044; Fig. 2), All four groups during the control
period had similar activity levels. Each group's
activity decreased during the simulated displace¬
ment (time: FlJ9 = 16.64. P = 0.0003; Fig. 2).
However, juveniles in the SimN displacement
exhibited a greater decrease in activity than any
ol the other three groups, which is reflected by the
significant statistical interaction among time, age.
and type of displacement.
Each group of birds exhibited an increase in
median nightly concentration between the control
and the displacement periods (Repeated measures
ANOVA. time: FtM = 4.973, P = 0.034; Fig. 2).
There was a weak between-subjects effect of
displacement independent of time (FU2y = 4.165.
P - 0.05). Birds assigned to the SimS group.
regardless of age and whether the tests were
during the control or simulated displacement
periods, had higher concentration values (or were
less dispersed in individual nightly orientation)
than birds in the SimN group.
DISCUSSION
Only adult Silvereyes exposed to the SimN
magnetic field altered their orientation; SimN
adults exhibited axial (or bimodal) orientation
along a WNW-ESE axis roughly perpendicular to
their seasonally appropriate NNE direction. How¬
ever, adults exposed to the SimS magnetic field,
and juveniles exposed to both the SimN and SimS
fields, continued to show seasonally appropriate
northward orientation that was indistinguishable
from the orientation exhibited during control tests.
Thus, changes in magnetic intensity and incliiw-
lion affected orientation ( 1 ) only in adults, which
have previous migratory experience, and (2) only
when the magnetic field change was consistent
with geographical location(s) that were beyond
the goal, in this case, iheir wintering area.
The change in orientation of SimN adults was
not accompanied by a specific change in either
activity or in the concentration of nightly activity,
indicating the ‘motivation’ of the SimN adults to
orient (i.c., migratory restlessness) did not differ
from the other three groups. All birds, regardless
of age or simulated displacement, had a decrease
in nightly activity during the displacement period;
this would be expected as migratory restlessness
diminishes towards the end of migration or as the
birds become acclimated to repeated testing.
ANOVA indicated a weak interaction between
test condition and age for activity, reflecting that
SimN juveniles exhibited a greater decrease in
activity compared to the other three groups; this
change in activity was not associated with a
change in the orientation of SimN juveniles. The
decrease in activity was least pronounced in SimN
adults (Fig. 2). the only group that exhibited a
significant change in orientation when exposed
to the simulated displacement. The nightly con¬
centration of orientation increased ti.e.. less dis¬
persion around the individuals' mean nightly
direction) in all four groups during the displace¬
ment period. This might suggest all birds became
better oriented, but an increase in concentration
could be the result of a decrease in the nightly
activity of birds.
We included hatch-year juveniles with no
migration experience; juveniles possess a magnetic
Deutschlander et al • AC.E-DEPENDENT GEOMAGNETIC POSITIONING
475
compass and are presumed to have an innate
knowledge of the species-specific migratory direc¬
tion. The SimN (and SimS) magnetic fields used did
not affect orientation of juveniles; this finding rules
out an effect of the experimental magnetic field on
the Silvereve's magnetic compass sense or on some
pre-programmed, innate navigational mechanism.
The change in orientation of SimN, but not SimS,
adults is consistent with evidence for a geographic
position sense perhaps mediated by iron-mineral
deposits associated with the trigeminal nerve
(Semm and Beason 1990, Beason and Semin
1996, Munro et al. 1997, Wiltschko et al. 2006.
Falkenberg ct al. 2010),
Fischer et al. (2003), using smaller changes in
magnetic intensity and inclination, found adult
Silvereyes exposed to a SimN magnetic field
failed to show consistent orientation. Reanalysis
of these same data revealed an initial easterly
orientation in adults, similar to some of our SimN
adults, followed by a shift to a more southerly,
albeit statistically insignificant, direction (Freake
et al. 2006). Stringent tests of a magnetic map
hypothesis, or true navigation, require exposing
animals to geomagnetic values outside their
normal migratory range to examine if they are
able to orient towards their goal without using
route-based cues or familiar landmarks (Yeagley
1947, 1951; Gould 1980; Moore 1980; Walcott
1980; Wall raff 1991; Phillips 1996). The mag¬
netic field values used by Fischer et al. (2003), at
least for inclination, were arguably within the
normal wintering range for Zo.sierops I. lateralis.
We applied a change in the magnetic field
approximately double in magnitude (—24%
change in vertical intensity rather than 12%) used
by Fischer et al. (2003). The values of inclination
and intensity for our SimN magnetic field were
clearly beyond the northern-most latitudes to
which Silvereyes migrate (Fig. I, and Lane and
Battam 1 97 1 >. However. SimN adults in our study
did not show' a reversal from their normal NNE
orientation as might be expected to compensate
for 'over shooting’ their normal overwintering
sites.
The lack of a goal-oriented response in SimN
adult Silvereyes is puzzling, hut may be due to an
inadequate understanding of how birds use
geographic variation in the magnetic field for
positioning. There are several possible explana¬
tions for these findings. (1) Adults possess a
magnetic map, but are confused by disparate
locations specified by inclination and intensity
(Fig. I). This explanation seems unlikely because
SimS birds were also exposed to values of
inclination and intensity that did not specify a
single geographic location or latitude. (2) Adults
possess a magnetic map, but their ‘goal’ (i.e.,
wintering site) is not sufficiently specific to result
in redirection of orientation. The magnetic field
characteristics experienced by the SimN birds
represent values beyond the northernmost latitude
for wintering Australian Silvereyes, particularly
for those that breed in Tasmania (Lane and
Battam 1971). but the birds should only reorient
southwards if they exhibit high fidelity for a
particular winter territory or range of latitudes.
Unfortunately there are no published data on
wintering site fidelity for Australian Silvereyes.
(3) Both inclination and intensity vary along the
same NNF.-SSW axis in eastern Australia and
adults may use magnetic intensity and/or inclina¬
tion to derive only one geomagnetic coordinate
for latitude. Displaced birds may need celestial
information to identify their longitude from
magnetic declination (Akesson et al. 2005,
Thorup and Rabol 2007) or they may search
longitudinally for familiar geographical land¬
marks to locate their east-west position (Mour-
ilscn 2003). (4) Adults may Use geomagnetic
spatial variation as a 'sign post’ rather than a map.
Northern values of magnetic inclination or
intensity for Silvereyes may be a navigational
marker to cease oriented migration or to disperse
randomly or longitudinally. Only adult Silvereyes
responded to the SimN field, and use of ‘sign
post’ geomagnetic cues is clearly age- or experi¬
ence-dependent if this explanation is correct. (5)
Finally it is possible that birds exposed to abrupt
magnetic field changes, which result in novel
magnetic position ‘signatures’, may disperse in an
attempt to perceive the gradient in the magnetic
field; gradual magnetic field changes may
allow birds to better compensate (Henshaw et al.
2010).
Our results are consistent with an age- or
experience-dependent, geomagnetic geographic
position sense. The reorientation of SimN adults,
perpendicular to their seasonally appropriate
migratory direction, does not allow us to distin¬
guish between map-based navigation or ‘sign
post' navigation by adults. SitnN adults did not
reorient towards the south, and we cannot
conclusively state whether they have a geomag¬
netic-based 'map' for true goal-oriented naviga¬
tion. The birds' behavioral response indicates
476
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 3. September 2012
spatial variation in the magnetic field has an
important role in migratory orientation of adults
that is likely involved in geographic positioning.
ACKNOWLEDGMENTS
We lhank H. A. Ford and the Zoology Department for
hosting MED’s visit to the University of New England.
Mark Stewart from Geophysical Technology Ltd. for
providing technical support and access to the magnetom¬
eter. D. C. Droney for statistical advice in analyzing activity
and concentration data. Rachel Muheim for assistance in
creating Figure I and for comments on the manuscript, and
R. C. Season and C. D. Galvani for editorial assistance. We
also thank Wolfgang and Roswitha Wiltschko for discuss¬
ing the interpretation of our experimental findings. Funding
was provided by a grant from the National Science
Foundation to .IBP (1BN02-I6957). The experiments
comply with the current laws of Australia and we followed
the 1991 “Guidelines for the use of animals in research"
(Animal Behaviour 41:1 83- 1 86).
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The Wilson Journal of Ornithology 1 24(3):478-486, 2012
RESTORATION OF MOVEMENT PATTERNS OF THE
HAWAIIAN GOOSE
STEVEN C. HESS,1 *-6 CHRISTINA R. LEOPOLD,-’ KATHLEEN MISAJON,3
DARCY HU.4 AND JOHN J. JEFFREY5
ABSTRACT. — We used visual observations of banded individuals and satellite telemetry from 2007 to 201 1 on Hawaii
Island to document movement patterns of the Hawaiian Goose (Bronra sandvicensis), commonly known as Nene. Visual
observations of numbered leg bands identified >19% and Sl0% of 323 geese at one of two breeding sites and one of two
distant non-breeding areas during 2007-201 1. We used satellite telemetry to document movement patterns of 10 male Nene
from 2009 to 201 1. and log-linear models to quantify the magnitude and individual differences in altitudinal migration. Two
subpopulations of Nene moved 974.4 m (95% Cl ± 22.0) and 226.4 m (95% Cl ± 40.7) in elevation between seasons on
average, from high-elevation shrublands during the non-breeding season of May-August, to lower-elevation breeding and
molting areas in September-April. Traditional movement patterns were thought to be lost until recently, but the movement
pattern we documented with satellite telemetry was similar to altitudinal migration described by early naturalists in Hawaii
prior to the severe population decline of Nene in the 20th century. Received II January 2011. Accepted 14 April 2012.
The Hawaiian Goose, commonly known as
Nene (Branta sandvicensis ), was reduced to near¬
extinction in the late 1940s with an estimated 30
wild and 1 1 captive individuals on Hawaii Island
(Smith 1952, Kcar and Berger 1980). Causes of
their precipitous decline were unregulated hunt¬
ing, habitat destruction, and several introduced
predatory mammal species. Feral cats (he! is
cants), dogs (Canis familiaris). and small Indian
mongooses ( Herpestes auropunctatus ) prey on
adults; leral pigs (Sits scrofa) and rats (Ramis
spp.) depredate nests (Banko 1992). Decades of
captive propagation and releases into the wild
have resulted in a population of -2.000 Nene
throughout the Hawaiian Islands, although most
island populations are not yet self-sustaining;
predation remains high and breeding success low
(USDI 2004). Most captive-raised geese were
released above 1,524 m because low-elevation
habitats had been profoundly altered and the
remaining wild Nene were observed at high-
1 Pacific Island Ecosystems Research Center, U.S.
Geological Survey. KTIauea Field Station. P. O. Box 44.
Hawaii National Park. HI 96718, USA.
’Hawaii Cooperative Studies Unit. University of
Hawaii. Hilo. P. O Box 44. Hawaii National Park. HI
96718. USA.
‘U.S. National Park Service, Division of Resources
Management. P. O. Box 52, Hawaii National Park. HI
9671 8. USA.
OfWSpNnknal Service' Paci,lc Wcst Regional
USA P' °' B°X 52' nawai‘' National Park. Ill 96718.
967J83^uSAfrey Ph0'°8raphy' P ° 40. Pcpeekeo, HI
"Corresponding author; e-mail: shess@usgs.gov
478
elevation (Kcar and Berger 1980, Black et al.
1997, Banko ct al. 1999). One consequence of the
mid-20th century population bottleneck may have
been loss of traditional movement patterns.
Altitudinal migration was described in Nene
prior to its severe population decline (Henshaw
1902, Perkins 1903). These movements consisted
of breeding anti molting in low-elevation grass¬
lands in September-April, and flights to high-
elevation shrublands during May-August (Banko
et al 1999). However. Nene that were reintro¬
duced throughout Hawaii Island from captivity
did not exhibit altitudinal migration patterns
for many generations after the population began
to recover (Black ct al. 1997, Woos and Black
2001). Altitudinal migration became re-estab¬
lished among several Hawaii Island subpopula¬
tions in the late 1990s (Hess 2011). but little was
known about movements in the remote interior o!
the island. Two subpopulations, one near Hilo and
another in the KTIauea region of Hawaii Volca¬
noes National Park, remained relatively isolated
from all others, exhibiting little regular seasonal
movement or genetic interchange.
Altitudinal migration patterns of Nene prior to
human contact are unknown, although subfossil
remains have been found as high as 2.683 ni (J- G.
Gitfin. pers. comm.). The selective pressures on
Nene likely changed with arrival of Hawaii's
original human inhabitants (Paxinos et al. 2002b)
and. more dramatically with arrival of Western¬
ers; thus, historical and current regimes may not
be representative of conditions under which Nene
evolved. Re-establishment of traditional movement
patterns may be beneficial to the species: (I)
Hess et al. • MOVEMENTS OF THE HAWAIIAN GOOSE
479
altitudinal migration may allow Nene to track
availability of food resources not otherwise
seasonally available (Black ct al. 1997), (2)
migration may enhance survival during the non-
breeding season by avoiding non-native predators
in breeding areas. (3) Nene may be able to avoid
multiple anthropogenic hazards by occupying
undeveloped high-elevation areas during the non¬
breeding season, and (4) there may be elevation-
related environmental factors such as thermal
constraints or humidity that affect the physiology
of developing ova. embryos, and goslings (Ravel¬
ing 1978. Cooper et al. 2005), We used visual
observations of banded individuals and satellite
telemetry to document seasonal movements of
Haw'ai'i Island Nene that have re-established
traditional movement patterns. Our objectives were
to: ( 1 1 identify locations used and the exchange of
geese among breeding and non-breeding areas, and
(2) understand the magnitude of elevation change
and potential differences among individuals and
breeding subpopulations by modeling altitudinal
migration patterns.
METHODS
Study Area.— Nene primarily moved among five
study areas across Hawai’i Island (19 37' N, 155
28' W): the Kahuku unit of Hawai i Volcanoes
National Park (Kahuku: 2.000-2.700 m elevation):
Hakalau Forest National Wildlife Refuge (Hakalau
Forest NWR; 1.800 ni ): KTpuka ‘Amahou Nene
Sanctuary (2.000 m); Kulani Correctional Facility
(Kulani: 1.580 m); and the Big Island Country
Club golf course (BICC; 640 m) (Fig. I). Long¬
term mean annual precipitation was 975 mm at
Kahuku, 2,479 mm at Hakalau Forest NWR. and
567 mm at BICC. The predominant ground cover
at lower elevation sites was non-native kikuyu
grass ( Pennisetum clandesiinum). Higher-elevation
shrublands were dominated by native species in¬
cluding pukiawe ( Le/necophylla tameiameia ) and
’ohelo ( Vaccinium reticulation) with sparse ground
cover of native hair grass ( Desc/tantpsia nubigena).
Hakalau Forest National Wildlife Refuge and
Kulani were formerly natural wet forest areas
unsuitable for Nene, but had been convened to
several species of non-native pasture grasses for
grazing except for small areas of native shrubland.
Breeding and molt occurred where Nene were
re-established after 1991 and 1996 at BICC
and Hakalau Forest NWR. respectively. The other
locations were used during the non-breeding
season.
Observational Data. — Visual observations of
numbered leg bands were compiled to ascertain
the proportion of Nene that moved among study
sites. Nene had been banded by the Hawai‘i
Division of Forestry and Wildlife (DOFAW) at
BICC and Hakalau Forest NWR as part of
ongoing management efforts. We recorded all
identifiably banded Nene front 2009 to 201 1, and
obtained comparable data from DOFAW during
2007-201 1. Observations were collected regularly
at Hakalau Forest NWR during 2009-2010. BICC
during 2007-2011. and opportunistically at Ku¬
lani. and at remote areas of Kahuku. and the
vicinity of KTpuka ‘Ainahou during 2009-201 1.
Satellite Telemetry.— Two cohorts of Nene
were outfitted with Platform Transmitter Terminal
(PTT) units equipped with Global Positioning
System (GPS) capability (Microwave Telemetry.
Columbia, MD. USA). PTTs measured 57 X 30 X
20 mm and were attached dorsally with a double-
threaded backpack harness made of Teflon®
ribbon (Bally Ribbon Mills. Bally. PA, USA).
PTT units were fitted only on males to reduce
potential interference w'ith breeding and because
mates are generally monogamous and travel
together throughout the year: eight of 10 males
were paired with females al time of capture.
Transmitter packages weighed s3% of each
bird's body mass. Capture, handling, and trans¬
mitter attachment procedures were approved by
the University of Hawaii IAC-UC Protocol 08-636.
Candidate None for satellite telemetry must have
been observed at Kahuku and must have nested
either at Hakalau Forest NWR or BICC.
The first cohort of five males in 2009 was fitted
with 40-g battery-powered PTT units programmed
to take global positioning system (GPS) locations
at 0000 and 1000 hrs HST. The second cohort of
six males in 2010 and 2011. including one from
the 2009 cohort, was fitted with 45-g solar-
powered PTTs for a total of 10 sludy subjects.
Solar-powered PTTs were programmed to take
GPS locations at 0000. 1000. 1400. and 1900 hrs.
All PTT units uploaded data to satellites every
3 days (CLS America Inc.. Upper Marlboro. MD,
USA). We conducted stationary trials for PTTs
prior to attachment and 95% of GPS locations
were horizontally accurate ±15 in.
Statistical Analyses.— Locution coordinates
were matched with a 10-m digital elevation model
of Hawai'i Island to document movement and
elevation (ESRJ 1999). Data consisted of Nene
identity and origin, elevation, and ordinal date.
480
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 3. September 2012
155°W
Hakalau
BICC
Mauna ,
Kea
Kipuka
Ainahou
Kailua
Kona
Kulani
Mauna
Loa
Kilauea
Kahuku
Kipuka
| Nene
E ISO ■
i. 120 -
§ 90 -
g. 60 -
jjj 30 -
Eel
lllllnnllnfln
J FMAMJ JASOND
location * . M°L.Vt;nien °‘ ‘S, ™“‘C N5nC’ with satellite transmitters during 2009-2011 on Hawaii Island from breeding
breeding ill JT , (gray ;intl Big Island Country Club (BICC) golf course (white circles- to non-
2(ordinul date)2. Parameters
and 9 5% Cl were estimated using PROC REG
(SAS Institute 1999).
RESULTS
Observational Data. — Visual observations dur¬
ing 2007-2011 identified 323 uniquely-banded
None at two breeding sites and three non-breeding
sites (Table I). One hundred and sixty geese
Hess et al. • MOVEMENTS OF THE HAWAIIAN GOOSE
481
TABLE 1 . Exchange of 323 individually-marked Nene between breeding and non-breeding locations on Hawaii Island
from 2007 to 201 1 based on visual observations of leg bands. Entries to the right ot the diagonal indicate the number of
individuals observed at two sites expressed as a percent of the grand total. Total observed indicates the total number of
banded Nene observed at each site. Nene originated from breeding sites al Hakalau Forest National Wildlife Refuge
(HFNWR) or Big Island Country Club golf course (BICC).
Breeding
Nun-breeding
BICC HFNWR
Kahuku
Kipuka 'Ainahou
Kulani
Breeding
BICC
_
9.6
9.4
10.0
5.6
HFNWR
31
—
19.8
19.2
0.9
Non-breeding
Kahuku
30
64
—
1.6
5.9
KTpuka ‘Ainahou
32
62
5
—
0.9
Kulani
18
3
19
3
—
Total observed
141
183
101
100
28
(49.5%) were observed at >1 site. While 101
Nene from BICC and Hakalau Forest NWR were
observed at Kahuku during the non-breeding
season, only one remained at BICC and Ihree
remained at Hakalau Forest NWR during the non¬
breeding season. More than 19% of all marked
geese were observed at Hakalau Forest NWR
during the breeding season and al Kahuku or
KTpuka 'Ainahou during the non-breeding season;
^10% were observed at BICC and Kahuku or
KTpuka ‘Ainahou.
Satellite Telemetry.— Transmitters functioned
for a sufficient length of time to capture data
across multiple seasons for nine of the 10 geese,
producing 9.607 GPS locations (Table 2), Bat¬
tery-powered transmitters functioned 65-102 days,
but solar- powered transmitters functioned 129
to >614 days. Nene repeatedly traveled from
Kahuku to BICC. the two most distant sites,
between sunrise and 1000 hrs. a minimum dis¬
tance of 67 km over the summit of Mauna Loa
(4,039 m). hut —90 km on the more likely route of
travel (Fig. I). Eight of 10 males from both
breeding sites dispersed over a broad area on the
remote southeast slope of Mauna Loa. most of
which was inaccessible to us by road.
The southernmost terminus of movements was a
small area at Kahuku known as KTpuka Nene.
noted as an important location by Smith ( 1952: I ):
"In the Kau Territorial Forest Reserve on Mauna
Loa. there is an area at an elevation of 6.500 feet
[—1.980 m| doited with small, shallow, permanent
pools and covered w ith an open ohia ( Metrosideros
eollina) forest with a ground cover of lush grass
and sedges. On maps of Hawaii, this area is labeled
Kipuka Nene, a name given it by the ancient
Hawaiians testifying to its habitation by Nene for
centuries. (Kipuka means an isolated patch of
vegetation surrounded by recent lava flows.) In
former years, the forest rangers frequently saw
geese in this location during patrols in the winter
months. In 1948. a ranger saw a flock of 17 Nene,
and in January 1949. three were observed. Since
then, no Nene has been seen, yet the ranger has
continued to make his monthly patrols in the same
routine manner." A major lava flow in 1950
altered the surrounding landscape, but left KTpuka
Nene intact aside from the loss of permanent pools
and gradual changes in plant communities.
The greatest mean difference in elevation for
BICC Nene was 974.4 m (95% Cl ± 22.0),
whereas Hakalau Forest NWR geese differed
226.4 m (95% Cl ± 40.7) between molting and
non-breeding seasons. Two Nene that originated
at BICC ranged ^2.281 m in elevation, from 199
to 2.568 nt, and 481 to 2.762 m. Log-linear
modeling of the five geese that provided data from
all three seasons resulted in significant relation¬
ships between ordinal date and elevation for
each (F2.tm ~ 177.76; P < 0.001; Table 3). We
interpreted the exponent of the intercept (exp|/?0J)
to represent the estimated base elevation of each
individual with 95% Cl. The magnitude of
seasonal elevation change for these live geese
differed according to origin, largely because the
Hakalau Forest NWR breeding location was near
the upper elevation limit (Fig. 2).
DISCUSSION
The movement pattern we documented with
satellite telemetry was similar to that reported by
early naturalists in Hawaii prior to the effects of
profound changes in habitats and introduced
mammalian predators (Baldwin 1945). Henshaw
(1902: 105) wrote: "It has been stated and seems
to be the general impression that the nene rears its
TABLE 2. Identities, origin, sample period, number of locations, minimum, maximum, and mean elevation (± 95% Cl) by season of 10 male Nene with satellite transmitters on
Hawai'i Island. Nene originated from Hakalau Forest National Wildlife Refuge (HFNWR) or Big Island Country Club golf course (BICC). Dashes indicate no data during a season.
482
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124, No. 3. September 2012
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young in the uplands where it is found in summer,
but such is not the fact. The greater number,
probably all. leave the upper grounds beginning
early in the fall, and resort to lower altitudes, from
about 1.200 feet [—360 m| downwards." Perkins
(1903: 437) also reported: "As is well-known the
Goose, like many other native birds, changes its
abode at different seasons of the year, being no
doubt chiefly influenced by the food-supply. In
the summer months it affects the open upland
region, which is covered with a scrubby vegeta¬
tion and traversed by many lava flows, such for
instance as parts of the plateau between the three
great mountains of Hawaii, at an elevation of four
or five thousand feet [ - 1.220- 1.525 m| above the
sea."
Two breeding subpopulations of Hawaii Island
None have resumed traditional movement patterns
similar to those reported by early naturalists
(Henshaw 1902. Perkins 1903, Smith 1952).
There was a strong pattern of full and partial
altitudinal migration; this pattern was opposite
that of many tropical bird species which typically
move from higher elevation breeding ranges to
lower elevation non-breeding ranges (Loiselleand
Blake 1991, Johnson and Maclean 1994. Ornelas
and Arizmcndi 1995, Hobson et al. 2003. Boyle
2010). Nene spent the breeding and molting
seasons at lower elevation areas from September
to April, and moved to higher elevation areas
during the non-breeding season in May to August.
Previous research found no evidence ot any
regular migration in a subpopulation of Nene in
the Kflauea region of Hawai'i Volcanoes National
Park ( Woog and Black 2001 ), which had limited
interchange with the subpopulations we studied.
We predict that pair bonds will form between
young Nene from Hakalau Forest NTVVR and BICC
w hile at non-breeding locations of Kahuku and
Klpuka ‘Ainahou, thereby reinforcing both move¬
ment routes and contributing to greater genetic
exchange between these breeding subpopulations.
However, it is unlikely Nene will colonize other
lower elevation grassland nesting sites without
translocation because of strong natal philopatry
and site fidelity (Banko et al. 1999).
Altitudinal migration is well documented in
continental tropical bird species, although rarely
in island species ( Berthold 200 1 . Boyle 2008, Cox
2010). Typically, altitudinal migration involves
annual return movements of forest-dwelling birds
from lower elevation non-breeding areas to higher
elevation breeding sites (Loiselle and Blake 1991,
Hess el al. • MOVEMENTS OF THE HAWAIIAN GOOSE
483
TABLE 3. Log-linear model results of elevation and ordinal date for five male None with satellite transmitters during
2009-2011 on Hawai'i Island. A linearized exponential function took the form: In(elcvation) = h0 + />|(ordinal date) +
/^(ordinal date)2. None originated from Hakalau Forest National Wildlife Refuge (HENWR) or Big Island Country Club
golf course i BICC).
Transmitter
Origin
Expife,)
,>5r} Cl l.xpl/x,)
f.xp(|/iil ordinal dale)
Expl|/'il ordinal dale’)
F-value
R:
90843/49
HFNWR
1.243.9
1.185.5-1.305.1
1 .006
1 .000
177.76
0.284
90848
HFNWR
1.846.7
1.828.1-1.865.6
1.002
1.000
293,94
0.396
90853
BICC
62.3
53.1-73.2
1.035
0.999
719.86
0.616
90847
BICC
264.2
237.7-293.6
1.019
1.000
432.85
0.491
90850
BICC
260.4
237.8-285.2
1.020
1.000
637.00
0.587
Johnson and Maclean 1994, Ornelas and Arizmendi
1995. Hobson et al. 2003). Factors affecting these
movements may include responses to changes in
resource availability, predation, parasites, or storms
(Boyle 2008, 201 o’; Boyle et al. 2010). Aseasonal
climate conditions within elevation zones of the
tropics may produce unimodal patterns in these
factors with little variation: however, orographic
effects may cause greater seasonal variation in
phenology over relatively short distances between
elevation zones (van Schaik et al. 1993). Phyloge¬
netic conservatism and physiological constraints
may also have a role in persistence of seasonal
movements (Sutherland 1998, Boyle and Conway
2007).
Other Hawaiian forest bird species, most
notably Tivvi ( Vestiaria coccinea) and 'Apapane
(Himatione sanguined), are also known to make
high-elevation forays during September-Novem-
ber (Fancy and Ralph 1997. 1998: Hess et al.
2001) when Nene begin their descent to breeding
areas. This contrary movement pattern in Nene
raises the question: why would one tropical bird
species make altitudinal movements in the
opposite direction of most other species? Migra¬
tion routes and long-distance movements are
culturally transmitted from adults to goslings in
many goose species, including Nene (Sutherland
1998. Banko et al. 1999). which may allow for
more evolutionary flexibility in resource tracking
than in birds with innate migratory behavior
(Pulido 2007. Sol et al. 2010).
Food resources may remain one of the most
important factors associated with movements to
productive low-elevation grasslands during the
breeding season. Many parts of the Hawaiian
Islands receive the greatest annual precipitation
during November, which contributes to substan¬
tial fresh growth of grasses that Nene use lo
improve body condition prior to nesting, for
gosling development, and during molt (Baldwin
1945. Banko et al. 1999). Grassland sites are
managed year-round at Nene breeding locations,
thus movements are not necessary to obtain
seasonally abundant grasses. It is also not clear
which factors arc associated with Nene moving to
higher elevation non-breeding areas. Henshaw'
(1902:104) noted that upland food: “...consists of
pualele ( Sonchns ole ravens), tender grasses and
several kinds of berries, especially the ohelo
( Vaccinium reticulation >. puakeawe ( Cvathores
\Lcpiccophyllu\ tameiameiae), and the strawberry
( Fragariu chilenxis |sic]). In summer when the
latter abound in the upper districts, the geese
become very fat...” Strawberries are now rare
and upland ground cover is often patchy barren
lava unlike the dense grass cover of lower
elevations, although peak production of ‘ohelo
berries occurs during the non-breeding season
(Wagner el al. 1999).
There is no indication that development of ova,
embryos, or goslings is limited by physiological
constraints at higher-elevations but productive
breeding areas at Hakalau Forest NWR. although
frequent heavy precipitation may affect gosling
survival during cooler months. Nene are unique as
they arc the only Northern Hemisphere goose that
breeds during September-Febniary (Johnsgard
1978). There is no indication that phylogenetic
conservatism may have a role in the seasonal
timing of migration, yet continental species such
as Canada Geese ( Brant a canadensis) from which
Nene evolved —890.000 years ago (Paxinos et al.
2002a) begin long-distance migrations that rough¬
ly correspond to the timing of Nene movements.
Other potential factors such as the altitudinal
distribution of parasites have not been quantified
in Nene. but migration patterns art* consistent with
seasonal storm avoidance (Boyle et al. 2010).
Frontal storm systems are generally less common
484
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124. No. 3. September 2012
J FMAMJ JASOND
Month
J FMAMJ JASOND
Month
du L'™ ! H locations - 900/goose) plotted by ordinal date for five male Nene with satellite transmitters
(Cirdest Hn T ' f™ra HakalaU Forcsl NWR («l«are symbols) and Big Island Country Club golf course
(crc.es, . Lines represent the est.mated annual elevation distribution of each male based on loe-Iinear modeling
in higher elevation areas during the non-breed
season than during the period when Nene brt
(Armstrong et al. 1983).
The community of predatory mammals tr
either in composition and abundance between I,
and high-elevation areas, but no data are available
quantity this pattern. We noted daily movements
Kahuku during the non-breeding season consist!
with a pattern of predator avoidance, roosting at the
Klpuka Nene site with smooth-texture lava sur¬
rounded by flows of rough-texture lava that would
present considerable barriers to wide-ranging mam¬
mals such as feral dogs. Thus, the severe terrain ot
high-elevation environments may provide opportu¬
nities to escape from predators. There are also few
anthropogenic hazards in high-elevation areas.
Hess el at. • MOVEMENTS OF THE HAWAIIAN GOOSE
485
The net effect of movements to high-elevation
areas during the non-breeding season may be
enhanced survival. Lowland breeding sites may
confer higher long-term reproductive success, al¬
though this is largely dependent on the intensity of
predator control. Measures of indiv idual fitness may
be able to disentangle the multiple factors associated
with benefits of migration. Re-establishment of
lowland breeding sites appears to have a central role
in recovery of range-wide traditional movements in
Nene, and remains an important conservation
priority for this species (USD1 2004). Restoration
of endangered tropical species throughout the
entirety of their altitudinal range may be important
for re-establishing behaviors including seasonal
movements, and may benefit species recovery.
AC KNOW LF. DO M ENTS
Funding for this project was provided by Park Oriented
Biological Support and the Natural Resources Preservation
Program of the National Park Service and the L'.S.
Geological Survey. We acknowledge Hawui'i Division ol
Forestry and Wildlife, Three Mountain Alliance. Ilakalau
Forest National Wildlife Refuge, Big Island Country Club,
and Hawaii Volcanoes National Park for data and access to
field sites. The LJ.S. Army Pdhakulou Training Area
provided satellite transmitters for this research. We also
thank K. W. Brinck, L. S. Elliott. E T. Polhemiis, and II. Sin
for assistance and two anonymous reviewers for many
helpful comments. Use of trade, product, or firm names in
this publication is for descriptive purposes and docs not
imply endorsement by the U.S. Government.
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The Wilson Journal of Ornithology 124(3):487 496, 2012
ECOLOGY AND HABITAT SELECTION OF THE MAGELLANIC
PLOVER ( PLUV1ANELLUS SOCIALIS)’. A LITTLE-KNOWN
PATAGONIAN SHOREBIRD
CARMEN LISHMAN1 : ' AND ERICA NOL1
ABSTRACT.— We studied the ecology and habitat selection ol the Magellanic Plover (Pluvianellus socialis) in southern
Patagonia during two austral summers. We searched for the presence ol this rare species along the shores of 33 privately-
owned lakes and portions of Lago Argentino across 12,000 knr of steppe habitat in Santa Cruz Province, southern
Argentina anti compared characteristics of occupied and unoccupied lakes. Aeolian lunette size was a significant predictor
of occupancy. Most lakes had only a single pair of breeding birds, although one had 14 pairs. No lake feature successfully
predicted number ol breeding pairs per lake. Territories were on cobbled beaches on the side of the lake with Aeolian
lunettes, and at sites significantly closer to small streams and further from vegetation than random sites. Nest sites within
territories had significantly less clay than unused sites. Clutch size was small 1 1 2) while hatching success was moderate
1 70% ). Future studies of this species should focus on adult and juvenile survival, and the development of a demographic
model that assesses the long-term stability of the population. Received 12 February 201 1. Accepted 21 March 2012.
Northern tundra and wetland habitats support
diverse and. at times, dense populations of breeding
shorebirds (Melinite et al. 2007). Studies of areiie-
breeding shorebirds largely inform our understand¬
ing of shorebird biology (Colwell 2010). However,
shorebirds also breed throughout tlte world wherev¬
er suitable habitats exist (e.g.. prairies, steppes,
agricultural fields, river beds, beaches). Many ol the
species that breed outside of arctic habitats occur al
low densities and are. partially as a consequence,
poorly studied (e.g., Madagascar Plover \Chara-
tlrius thoracicus\\ Long et al. 2008). Habitats of
these species are also often inaccessible (e.g..
Diademed Plover | Phegornis itiitchellii | which
breeds at altitudes >3,000 m in inaccessible habitats
of the central Andean cordillera: Johnson 1964).
Few of the 15 species of South American breeding
shorebirds have been studied in any detail (Piersma
et al. 1997, St. Clair et al. 2010).
The Magellanic Plover (Pluvianellus socialis)
is a rare shorebird that breeds on the shores ol
lakes and rivers of Patagonia in southern South
America (Jehl 1975. BirdLife International 2012).
It is listed as near threatened on the IUCN Red
List (BirdLife International 2012). Population
estimates suggest fewer than 1,000 individuals
(Jehl 1975) with a more recent value of 'fewer
than 10.000’ (BirdLife International 2012). Few
systematic evaluations of this species' breeding
Department of Biology, Trent University, Peterborough.
ON KVJ 7B8. Canada.
Current address: 1336 Queen Street. Halifax, NS B3J
2H5. Canada.
'Corresponding author; e-mail:
carmen.lishman@gmail.com
success or habitat use have been conducted either
al landscape or local scales (Jehl 1975: Piersma
et al. 1997; lmbertj 2003: Ferrari et al. 2003,
2008).
We report results of a regional survey of the
Magellanic Plover in southern Patagonia. Argen¬
tina, including a habitat selection study at three
scales. We assessed characteristics of this species’
habitat within Santa Cruz Province, Argentina at
the scale of lakes, territories, and nest sites. Out-
goal was to provide specific habitat information in
the center of the species’ geographic range to
assist in more accurately assessing global popu¬
lation si/.e. We also compared habitat character¬
istics between successful and unsuccessful nests,
and provide an estimate of detection probability
for this species on lakes searched on multiple
occasions.
METHODS
Field Procedures.— We studied Magellanic
Plovers during two consecutive breeding seasons
in austral spring and summer from August 2006
to March 2007 (hereafter 2006) and during the
summer. December 2007 (hereafter 2007) in
southern Santa Cruz Province. Argentina (48 lo
52 S). The semi-arid Patagonian steppe region
is characterized by a cold (average 7.2 C). dry
(<200 nun annual rainfall) climate with strong
(average 35 ktn/hr. gusting to 150 km/hr. Ferrari
et al. 2003) persistent westerly winds (Soriano
1983). The flat grassland landscape supports
many endorheic lakes (i.e., lakes within basins
that do not drain to the ocean, hereafter ’lakes’)
that vary in salinity, size, and geomorphologic
48 7
488
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 3. September 2012
wintering sites of Magellanic ' ^ 1° SOUthcm Argcnlina during the breeding season (circles) and tl
-arched in 2006. «"*> « shown with dotted rectangles around at
mool^T"1 (Sonano 1983’ Quirts and D,
)■ Many lakes have a large area devoic
vegetation on the windward side of the lake ha
i y-three lakes were surveyed, and 35 of il
were searched in both seasons. In addition. 4
e shoreline of Lago Argentine (50 19' S,
initiate' f 7(!U Rm freshwaler that at
muiates f,-0,1, Andean glaciers) was searched ,
day hCt‘fy Calafalc- A11 >^es in the study
but on Sv,Und Unve«etated shorelines, and
were on' o" :", ^ Nacio"aI Monte Le
cond season aL4>7Wned ^ ranches- The
—40% «r i 1 ~° 7, was Particularly dry ;
season were "surte"'1' U'rOUghl1111 ,he 2C
ary. Surveys were also conduct
along 12.5 km of the banks of three rivers
(big. 1 ): 6 km of the Gallegos River (51 37' S.
69 36 W) west from the ruta 3 bridge at Gtier
Aike. 2 km of the Santa Cruz River (50 00' S.
68 55' W) west from the village of Cmdte Luis
Piedra Buena, and 4.5 km of the Chico River
(48 46’ S. 70 15' W) southeast of the village ol
Gobemador Gregores.
Observers (2-3) walked parallel transects
around the perimeter of a lake, or along the banks
ol a river to locate breeding pairs of plovers
stopping every 100-150 m to complete a 360
scan using a 40X spotting scope. Behavioral
cues were used to ascertain breeding status when
individual plovers were located. We observed two
Lishman and Nol • MAGELLANIC PLOVER HABITAT SELECTION
489
different sets of behavioral patterns. Transient
birds would walk or fly long distances (e.g.. 500 m
to 2 kin) within the lake area, forage for extended
periods of time (>2 hrs), and neither associate
with other birds, nor exhibit territorial behaviors.
Territorial birds vocalized in the presence of
an observer or conspecific. were aggressive with
conspecifics and. at times with other species
( Charadrius falklandivus: but see Jehl 1975),
associated strongly with a male (copulating,
following, or giving joint territorial displays),
and/or incubated a nest or brooded and fed a
chick.
We recorded the location of each plover
encountered on the shoreline of lakes, using a
Global Positioning System (GPS) (Garmin Inter¬
national Inc.. Olathe, KS. USA). The spatial
distribution of observations of territorial birds was
examined using Program Garmin Mapsource®.
Locations within 200 m of one another were
classified as a single territory, based on previous
observations that pairs were spaced along lake-
shores every 200-300 m (Jehl 1975. Ferrari el al.
2008). The validity of classifying clumps of
observations as a territorial pair was confirmed
by observations of territorial disputes at territory
boundaries and by stability of territory locations
on successive visits within and between the two
field seasons. The number of territories per lake
was calculated for 18 occupied lakes that were
searched thoroughly in both seasons.
Nests were considered successful if one or more
eggs hatched, young were seen, or small eggshell
fragments were found in the nest cup (Mabee
1997) and the parents were still on territory. They
were considered unsuccessful if we found no eggs
or adults on territory (Mabee 1997). We presumed
predation was the cause of failure if eggs and
young were absent. Eggs crushed inside the scrape
were considered trampled. We used the Mayfield
(1961 1 method and Johnson’s ( 1979) alternative to
incorporate exposure days (days between nest
visits) and number of total nest losses to calculate
daily nest survival.
Magellanic Plover habitat was described at
three spatial scales: lake, putative territory, and
nest (microhabitat). We did not measure actual
territory sizes and assume our measurements at
the scale of 200-m radius around nest sites and/or
feeding areas of pairs of plovers, represent broadly,
territories of this species, given the average dis¬
tance between adjacent pairs. Wc considered all
endorheic lakes in the known geographic distribu¬
tion in Santa Cruz Province, Argentina (Ferrari
el al. 2003) as available at the lake scale and
searched 53. based on road accessibility. Lakes
were considered occupied if individual Magellanic
Plovers were observed at least once during the
2006 and/or 2007 breeding season. We used data
from 22 lakes searched on five occasions (Aug,
Oct. Nov. and Dec 2006. and Dec 2007) to estimate
monthly detection probability, using the occupancy
model of Program MARK (White and Burnham
1999).
We examined satellite images from Google
Earths and measured lake perimeter, total area
and size of aeolian lunettes using the "distance
ruler’. The high water line of the lakes, clearly
visible on satellite images, delineated the lake
perimeter. The aeolian lunette's shape w'as approx¬
imated to that of a rectangle. Lunette area was
calculated using the equation: area (in ha) = length
(m) X width (m) X 0.0001 ha/m2. Elevation of the
shoreline weis taken from the digital elevation
model (DEM) provided by Google Earth®.
Electrical conductivity was measured by CL to
approximate salinity on a subset of 22 lakes that
were visited from 14 to 20 December 2007 using a
Eutech ECTestr 10 high'M tester (Oakton Instru¬
ments, www.instrumart.eom/Oakton) to the near¬
est 0. 1 mS/cm. Measurements >19.9 rnS/cm were
nol detected by this device. The measurement was
taken by directly immersing the device’s probe
in the hike water at the shoreline on 12 lakes.
Lakes that were dry Of = 10) were measured by
dissolving 10()-ml hike bottom sediment in 100 ml
distilled water and immersing the probe in this
solution. Salinity metrics were binomial in
distribution with all readings between 0 and
0.8 mS/cm (freshwater) or >19.9 mS/cin (saline).
Salinity measurements W'cre confirmed by taste.
A 300-m buffer at the high water line of the
lake delineated the available area at the territory
scale. Wc measured 33 sites within that area used
by Magellanic Plover and 33 available sites along
the lake shores (used and available, respectively).
A territory was considered used if a nest or chick
was found and the location of the nest or chick
defined the center of the used territory. Unused
sites at this scale were chosen using randomly-
selected angles and distances (0-200 m) from
the center of evenly spaced point s around the
perimeter of the lake. The next appropriate
randomly generated distance was used if the
unused site w'as outside of the designated
490
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 3. September 2012
available area (i.e., >300 m from the waterline or
inside the inundated area of the lake).
Cover types were categorized as: clay, vegeta¬
tion. gravel (<5 cm), cobble (>5 cm), sand, or
wrack (organic material washed up from wave
action). Percent cover in a I -nr quadrat was
measured at 5-. 15-, 30-. and 45-m distances from
the center of the territory. These quadrats were
arranged in a spiral pattern. 90 from one another
and from the territory center. Distance to lake-
shore was measured to the highest waterline of the
lake, distance to vegetation was measured to the
nearest location with >50% vegetation cover
within I nr, and distance to nearest channel was
measured to the nearest location where freshwater
flowed into the lake (formed by overland flow
during precipitation or from a groundwater
spring).
The available area for nest placement was
delineated as an area -200 m in diameter
centered on a nest site (i.e., within the presumed
territory of nesting birds). Potentially available
sites at this scale were selected at a random
orientation (between 0 and 359 ) and distance
(between 0 and 100 m) from a nest using two
random number lists. A digital photograph of each
microsite, including a I -nr quadrat marked at Id¬
em intervals centered on the nest, was taken from
1.7 m above the ground. Microsite photographs
were digitally overlayed with a 10 X 10-cin grid
in Program Jasc Paintshop Pro© by Corel
Corporation (www.corel.com). One of the six
cover types used in the mcsoscale analyses within
each grid cell was recorded and summed; the total
of all cover types equaled 100%.
Statistical Analyses.— We tested for an associ¬
ation between salinity and occupancy using
Fisher’s exact test. Multiple logistic regression
was used to test candidate models for the separate
and combined effects of lake perimeter, aeolian
lunette size, and elevation on the binary response
variable of lake occupancy (unused = 0, occupied
- 1). Akaike’s Information Criteria (AIC),
rCn1^ed foI disPersion and small sample size
i 1 u and Akaike s weights (H7) were used to
select the most parsimonious model (Burnham
and Anderson 2002). The most important param¬
eter was identified by summing Akaike’s weights
‘hC pilrame,er °f in.eresi
(Burnham and Anderson 2002).
ofir;:^ ?drest c°vcr ^ p^m m 0.05). Occupancy was
significantly associated with lake salinity as only
two of 17 freshwater lakes were occupied
whereas 12 ol 14 saline lakes were occupied
(Fisher’s exact test. P < 0.0001).
1 he size of the aeolian lunette was important in
all top models at the lake scale and had the highest
importance variable (Swr = 1 .00, Table I ). This
variable was the only one to have a parameter
estimate that did not include zero (estimate =
1.515. 95% CJ = 0.67-2.86), indicating a higher
probability of occupancy by Magellanic Plovers
on lakes with large than small aeolian lunettes.
Generally, occupied lakes had perimeters of 950 m
oi greater and contained aeolian lunettes of at
least 2 ha (Fig. 2).
Territory Use.— Lake was included as a random
effect in GLMM models at this scale. The model that
resulted from backward stepwise parameter removal
included two parameters with significant (ot < 0.05)
P- values: Vegetation at 5 m (intercept ± SE: 2.187 ±
0.61, parameter estimate: - 1.91 1 ± 0.567, / = 3.37
p < 0.0022) and vegetation at 15 m (parameter
estimate: -3.42 ± 1.155, / = 2.96, P = 0.0049).
Both parameters indicated increasing the percent
cover ol vegetation within 15 m of the center point
decreased the probability of territory use.
The model for distance to vegetation and
distance to channel was highest-ranking, alone
describing 66% of variation in territory occupa¬
tion (Table 2). The sum of Akaike’s weights tor
each variable indicated distance to vegetation and
distance to channel (both I \vi = 1,00) were
considerably more important than distance to lake
(Im1/ = 0.34). The parameter estimate lor distance
to vegetation was positive and distance to channel
was negative, indicating the probability of teni-
tory use increased wdth increasing distance from
vegetation and decreasing distance to freshwater
channels (Fig. 3).
Nest Site Use. — Nests were directly on the
substrate, close to the shore, and on the side of (he
lake with aeolian lunettes. No nests had obstruc-
tions (e.g., logs, vegetation) other than cobble
near them. The most parsimonious model describ¬
ing nest site characteristics included the additive
ellects of percent clay and percent cobble (>c/ =
0.37, Table 3). The model including percent clay
features ( lakeshore. vegetation, ^nd "fresh water rcgress,on dcscbbing the effect of proximity to three geographic
Sample size («), number of parameters (kj AkaikeTl" V,rma, ^ tenilory occuPaiK\V by Magellanic Plovers,
sample size (QA1C, difference in OA1C fAOAIC ) an > h"™" (A,C>' A1C cor"*ted for dispersion and small
^ll^andidate mode, ^ ~ ££* — ^
Lishman and Nal • MAGELLANIC PLOVER HABITAT SELECTION
493
500 -i
450 -
400 -
350 •
£ 300 -
0)
C 250
TO
Q 200
Lakeshore Vegetation Freshwater channel
FIG. 3. Mean and 95% confidence intervals of distance to three features (endorheic lakeshore. vegetation, and
freshwater channel) of Magellanic Plover, v comparing used (gray bars) and randomly-selected available territories
(open bars).
was second with a weight of 27%, and percent
clay cover was present in all of the five most
parsimonious models (Tabic 3, AA1C, < 4).
Percent clay had the highest importance value
(I"'/ = 0.73) with cobble as the next most
important value (Vvt7 = 0.37). Percent day was
lower at used than available sites, and percent
cobble was slightly higher (median. 23-75%
quartiles) used: clay = 0 (0—3.5), eobble = 2
(0-8); unused: clay = 42.5 ( 1.5-92.5). and cobble
= o (0-0).
Nest Success and Habitat— We found 20 nests
in 2006 and four in 2007. Average clutch size was
1.2 eggs ( 19 nests contained a single egg, 6 con¬
tained 2 eggs). Seventeen nests were monitored
repeatedly in 2006 by visiting every 2 to 8 days.
Seventy percent of monitored nests were success¬
ful with one or both eggs hatching ( 12/17). Four
nests were depredated and one nest was trampled,
presumably bv grazing livestock, which frequent¬
'd the aeolian lunettes. The Mayfield estimate
of daily survival was 0.975 (// = 17) with nest
success over the 24-day incubation equal to
55.0%. Twenty-six chicks (17 in 2006, 9 in
2007) were banded and followed to fledging (1 1
fledged of 26 banded, 42.3%). Chicks fledged
between 28 and 35 days after hatching. One chick
banded in 2006 bred in 2007 on a neighboring
lake 12 km distant. One banded chick was
observed at the Rio Gallegos mudflats, 30 km
from the breeding site, three months after it left
the nest area. Successful and unsuccessful nests
did not differ in proximity to lakeshore, vegeta¬
tion, freshwater channel, or in microsite percent
cover variables (Wilks' Lambda, P > 0.05).
DISCUSSION
The breeding range of the Magellanic Plover
extends over 7 of latitude in southern South
America. The major breeding area appears to be
centered in southeastern Santa Cruz Province
based on our observations and those of others
(Jehl 1975, Ferrari et ai. 2008). We found pairs
with evidence of breeding on about a third of the
494
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 3. September 2012
TABLE 3. Model selection for conditional logistic regressions describing the effect of percent substrate cover on
probability of microsite use by breeding Magellanic Plovers. Sample size (n), number of parameters (k), Akaike's
Information Criterion (AIC), AIC corrected for small sample size (A1C, ). difference in AIC, (AAIC,.). and Akaike's weight
(h7) are reported for the top five models (AAIC, < 4) and constant model of lb candidate models describing the effect of
substrate cover on microsite occupancy of the Magellanic Plover.
Model
n
k
AIC
AIC.
AAIC,
wi
Clay, cobble
50
3
14.186
20.708
0.000
0.37
Clay
50
2
17.055
21.310
0.602
0.27
Clay, vegetation
50
3
1 7.040
23.562
2.854
0.09
Clay, gravel, cobble
50
4
15.492
24.381
3.673
0.06
Clay, cobble
50
3
1 8.065
24.587
3.879
0.05
Constant
50
1
34.657
36.74 1
16.033
0.00
lakes throughout the accessible portion of this
area. The inaccessible interior of the province is
likely to have similar proportions of occupied
lakes. Lakes with plovers were large (with large
perimeters), and contained large aeolian lunettes.
All nests were on the windswept shorelines of
lakes with lunettes, and on the side of the lake
with the lunette. The substrate created by strain
winds was predominantly clay and cobble and. oi
these shorelines, both adults and their nests wen
extremely cryptic.
Plovers occupied sites further from vegetatioi
than unused sites at the territory scale allowing
for good visibility by breeding pairs. Thus, lik«
Charadrius plovers (Nguyen et al. 2003), thi
species probably nests in open habitats to maxi
mize predator detection, while minimizing visibil
ity of adults, nests, and eggs (Graul 1973. Solis an<
De Lope 1995. Nguyen et al. 2007). Most occupies
lakes were saline, although we did find nests ant
successfully Hedged young on two Ireshwate
lakes, suggesting the species can nest successfully
using food derived from freshwater sources.
We did not lmd any pairs nesting on rive
banks. Previous reports of their occurrence then
(Ferrari et al. 2003) suggest a larger sample o;
nvers, as well as a thorough survey of potential l\
suitable habitats on Tierra del Fuego needs to be
conducted to modify current estimates of popula
tion size. Our lack of ability to find a relationship
between number of territories (e.g.. abundance
and any lake measure that we used suggests
predicting which lakes might be occupied will be
aided by oar research, but predicting abundance
close n™'" d'ffifUl1' For examPlc- 'wo lakes in
close proxtmuy had 14 and I pair, respectively
and we were enable to visually assess any
'“Tnib t CharaCterisli‘:s 0<£ lunette
' Sal,mty- shaPe °r major ecological differ¬
ences). One variable we did not quantify and was
unavailable on the satellite image was the number
of small streams entering occupied lakes. Plovers
at the territory scale nested near freshwater sources,
and we often observed breeding plovers feeding
where streams entered the lakes; this may be an
important variable for future study. Ideally, finding
a characteristic that can be measured via remote
sensing that correlates with abundance, will allow
more accurate estimates of population size. Cur¬
rently. we are unable to reline the global population
estimates of between 1.000 (Jehl 1975) and 10.000
(Birdl.ife International 2012) individuals.
Magellanic Plovers within occupied territories
avoided placing nests on clay substrates. Avoid¬
ance of vegetation in nest-site selection and place¬
ment of the one or two eggs directly on gravel or
cobble rather than clay are probably additional
anti-predator adaptations (Solis and De Lobe
1995; Nguyen et al. 2003, 2007). Clay retains
moisture better than gravel or cobble, and nests on
this substrate could cool unnecessarily when
adults are not in attendance,
Poor detection due to a highly cryptic plumage
has been a critical issue for research on this
species (Ferrari et al. 2003). Surveys using our
technique ot parallel walking, repeated monthly,
detected 90% of pairs, in part, due to vocaliza¬
tions given by breeding individuals.
We documented reproductive success at 20
nests. Hatching success was higher than those
reported for other under-studied South American
shorebirds (11.6%. Charadrius wilsonia. Ruiz-
Gucrra et al. 2008; 46%. C. Jalklandicus. St. Clair
et al. 2010), and may be a result of the highly
cryptic nests ot the Magellanic Plover. None cl
the habitat variables that we measured were linked
lo nest success, but our sample size was small,
i effecting low densities of this rare species across
Lishman and No! • MAGELLANIC PLOVER HABITAT SELECTION
495
a large geographic area. The species also has low
fecundity (<1 fledgling/adult female/nest at¬
tempt). Further demographic research should be
conducted to estimate annual nest success (e.g.,
with marked populations to learn if birds renest >.
and both juvenile and adult survivorship. These
data can be supplemented with broader geograph¬
ic surveys to estimate population si/.e and
stability. Identifying the characteristics that pro¬
mote high abundance at particular lakes, and
protecting these sites will be critically important
to this species' conservation.
ACKNOWLEDGMENTS
We thank the many individuals who provided field and
logistic support in Santa Cruz, Argentina: Santiago Imberti,
Martina McNamara, German Montero, Rita Lope/. Karen
Clark, Monica Sejas. Sebastian Alvarado, Marina Ganehc-
gui. Rosario Lovcra, William Lishman. Martin Vindel.
Leslie Najgcbauer. and Franco Pa/.. We arc grateful for
private land access provided on the following ranches
(csrancias in Spanish, or Ea,): Ea. Killik Aikc Norte, La.
t.os Po/os. Ea. La Angelina, Ea. Tres de Enero. Ea. Otern
Atke, Ea. Rupai Pacha. Ea. Morro Chico. Ha. Glen Cross,
Ea. Los Luiscs, Ea. El Bosque. Ea. La Martina. Ea. La
Leona, and Ea. Don Raul. We thunk those who provided
suggestions lor early drafts and data analysis: Joe Noceru.
Unit Nguyen. Koji Tominagu. Ken Abraham, Jim Schaefer.
Santiago Imberti, Silvia Ferrari. Carlos Albrieu. and Anne
Corkery. We also thank .1. R. Jehl Jr. and C. D Duncan for
comments and suggestions on this manuscript. This study
was made possible by Trent University, Universidud
National de la Patagonia Austral, and the Natural Science
and Engineering Research Council of Canada.
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The Wilson Journal of Ornithology 124(3):497-505, 2012
BEHAVIORAL ACTIVITIES OF MALE CERULEAN WARBLERS IN
RELATION TO HABITAT CHARACTERISTICS
PETRA BOHALL WOOD1 4 AND KELLY A. PERKINS’ '
ABSTRACT. — Activities of 29 male Cerulean Warblers (Setophaga cerulea) were quantified on two sites in West
Virginia during May-June 2005. Singing and foraging were the most common of 1 1 observed behavioral activities (81 .6%),
while maintenance and mating behaviors were uncommonly observed. Male activity differed among vegetative strata (P =
0.02) with lower- and mid-canopy strata used most often {10% of observations), especially for foraging, perching, and
preening. The upper-canopy was used primarily for singing, particularly within core areas of territories and in association
with canopy gaps. Foraging occurred more than expected outside of core areas. Males were associated with canopy gaps
during 30 ft of observations, but the distribution of behavioral activities was not significantly related (P = 0.06) to gap
presence. Males used 23 different tree species for a variety of activities with oaks t Quercus spp.) used most often on the
xeric site and biack cherry ( P rumis serntina ) and black locust ( Rohinia pseudoacacia) on the mesic site. Tree species used
for singing differed between core and non-core areas f P - 0.0(H)! ) but distribution of singing and foraging activity did not
differ among tree species (P = 0.13). Cerulean Warblers appear to be flexible in use of tree species. Their use of different
canopy strata for different behavioral activities prov ides an explanation for the affinity this species exhibits for a vertically
stratified forest canopy. Received 31 August 2011. Accepted If) January 2012.
Quantifying behavioral activities (Altmann
1974) can provide useful insights into a species'
habitat needs (Graham 2001, Fleischer et al. 2003,
Aborn and Moore 2004). Habitat characteristics of
Cerulean Warblers ( Setophaga cerulea) have been
examined extensively (e.g., Weakland and Wood
2005. Barg el al. 2006, Roth and Islam 2008,
Bakermans and Rodewald 2000. Hartman el al.
2009) bui few studies have quantified behavioral
activities relative to habitat. Barg et al. (2006)
studied allocation of singing, foraging, and
perching behaviors by male Cerulean Warblers
among tree species and canopy height while
Gabbe el al. (2002) anil George (2000) examined
foraging preferences among tree species.
Canopy gaps and a heterogeneous canopy
structure are thought to be important resources
tor Cerulean Warblers (Oliarnyk and Robertson
1996, Jones and Robertson 2001. Weakland and
Wood 2005. Wood et al. 2006. Roth and Islam
2008). Cerulean Warblers often placed nest sites
within 30 m of a canopy gap in Ontario (Olinaryk
and Robertson 1996) and gap densities were three
U.S. Geological Survey. West Virginia Cooperative
Fish and Wildlife Research Unit. West Virginia University,
03 Percival Hall. P. O. Box 6125. Morgantown. WV
26506, USA.
West Virginia Cooperative Fish and Wildlife Research
knit. Division of Forestry and Natural Resources. Wcsi
Virginia University, 313 Percival Hall, P. O. Box 6125.
Morgantown, WV 26506. USA.
Current address New York Natural Heritage Program.
625 Broadway. 5th Floor. Albany. NY 12233. USA.
4 Corresponding author; e-mail; pbwood@wvu.edu
times greater within core areas of territories than
at random locations (Perkins 2006). Singing and
foraging are two activities that may relate to gap
presence. Gaps provide rich foraging opportuni¬
ties for passerines (Noss 1991. Rotenberry et al.
1995, Smith and Dallman 1996). Higher insect
abundance in gaps resulted from increased
amounts of foliage in response to more light
available to tree crowns surrounding canopy gaps
(Blake and Hoppes 1986). Thus, Cerulean War¬
blers may spend more time near gaps to exploit
prey resources. They also may use song posts near
gaps for greater song projection due to reduced
attenuation and reverberations off foliage (Barg
2002).
Mixed mesophytic (Hinkle et al. 1993) and
Appalachian oak {Quercus spp.) (Stephenson et
al. 1993) forests have high tree species diversity,
and Cerulean Warbler use of specific tree species
for singing and foraging has been documented
throughout their range (Gabbe et al. 2002,
Rosenberg et al. 2002. Barg et al. 2006, George
2009). Timber harvesting as a habitat manage¬
ment tool for this species is being considered
(e.g., Hamel et al. 2004, Wood et al. 2005,
Bakermans and Rodewald 2009), but a better
understanding of tree species used by Cerulean
Warblers for all behavioral activities is needed
before timber harvesting is applied extensively.
We quantified behavioral activities of male
Cerulean Warblers during the breeding season in
north-centra] West Virginia. Specific objectives
were to; (1) identify Cerulean Warbler behaviors
and time allocated to each, and (2) examine if
497
498
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124, No. 3, September 2012
activity varied by vegetative strata, within core
areas of territories, in association with canopy
gaps, or among tree species.
METHODS
Study Area. — Lewis Wetzel Wildlife Manage¬
ment Area (LW) in Wetzel County near Jackson-
burg. West Virginia. USA. is 5.41 8 ha in size with
elevations of 224-476 in. Two ridges. Hart Ridge
(—49 ha) and Snake Ridge (—45 ha), were
surveyed for Cerulean Warblers during the 2005
breeding season. Both ridges predominantly
consisted of mature, —70-80 year-old, second-
growth forest of mixed mesophytic and Appala¬
chian oak forest types. However, the two ridges
differed in vegetative structure and tree species
composition, partly as a result of past agricultural
activity on Hail Ridge.
Hart Ridge was mostly mesie and common tree
species were sugar maple (Acer saccharin,,).
northern red oak ( Quercus ruhra), tulip poplar
(Liriodendron tuUpifera ), white ash (Fraxinns
americana), hickory ( Carya spp.), black cherry
(P/7/m/.v serotina ), black walnut (Juglans nigra),
black locust (Rohinia pseudoacacia), and red
maple (A. rubnmi). Canopy openings included a
partially open-canopy trail that followed the
ndgeline. three maintained wildlife openings
0. 7-0.32 ha in size on broad sections of the
ridge, and treefall gaps.
Snake Ridge had a xerie ridge-top with rocky
soil and xenc or mesic side-slopes. Co-dominant
ree species on the ridge-top were chestnut oak
(Q ' pn,u,s) and scafIeI oak ( Q . coccinea). Other
common species were several hickory species
northern red oak. black oak ((7. velutina), white
oak (Q. alba), white ash. basswood (Tilia
americana ) tulip poplar, sugar maple, red maple
SnlCUpm T magnolia Magnolia acuminata).
bnake R,dge had no recent anthropogenic dist¬
ances at the time of the study but had treefall
Saps.
systematically searched
2005 d„H °r.: 5",8"’g males ,n June
8 n'°m!,ng <060(M 130 We waited
- min before record, ng locations of males to reduce
ob^"d;h?nspicurs ioraiions' we
survey burs, '""T durin8 » 30-min
allows sufficient time for a male to traverse its
entire territory if it chose to do so, and provides
biologically independent locations (Barg et ul.
2005). We used a survey in analyses if a male had
at least eight unique flagged locations or 15 min of
observation during the 30-min survey period.
We recorded activity at the first second of each
minute the observer had the bird in view. One
observer counted down the seconds with a stop
watch while a second observer watched the bird
through binoculars and identified the activity ai
the first second of each minute. No activity was
recorded it the observer did not have the bird in
view when the minute turned.
We classed activity into 1 1 categories (Table It.
Foraging included all food-related activities such
as gleaning insects, hopping along a branch
actively searching for prey, and one observation
°1 u male beating a caterpillar against a twig.
Hopping was recorded as a separate activity when
the bird had its head up while moving along the
branch and appeared to be using this behavior as a
means ol locomotion instead of a foraging strategy.
Wc defined perching as a bird observed sitting still
and not singing, whereas a bird lhai was perched
and singing was recorded as singing. Dancing
was a unique behavior where the male Cerulean
Warbler elevated his wings slightly without
opening them and moved them buck and forth in
a wiggling motion that may function as a courtship
display (R. P. Detimers and M. R. Lutmerding.
pers. comm.). Other behaviors, witnessed <3 times
each, were fanning tail feathers, fluffing out
feathers, and fluttering wings while perched. These
behaviors were included in analyses as singing if
observed while the bird was singing and otherwise
included as perching.
We recorded tree species and vegetative strata
tor each activity when possible. We recorded tree
•species and vegetative strata hut not activity type
when the male was obscured by vegetation but its
location was known. W'e categorized vegetative
strata as understory, midstory, lower-canopy , mid-
canopy, und upper-canopy. Each strata represent¬
ed 20% increments that were visually estimated
beginning at the forest floor through the upper
canopy layer. Field personnel practiced estimating
•strata before sampling began to ensure consisten¬
cy among personnel.
Mapping. — We revisited flagged male locations
in late June through July to obtain coordinates of
each flagged location using global positioning
system (GPS) units. Coordinates were corrected
Wood and Perkins • CERULEAN WARBLER ACTIVITIES
499
TABLE 1. Number of observations (n) of male Cerulean Warblers (CERW: 20 on Hart Ridge, 9 on Snake Ridge) by
activity and vegetative strata in Wetzel County, West Virginia, May-June 2005.
Harl RiUgc Snake Ridge
n
%
n
%
Activity
Singing
381
64.6
209
77.7
Foraging
94
15.9
17
6.3
Perching
36
6.1
15
5.6
Flying
39
6.6
13
4.8
Hopping
4
0.7
2
0.7
Preening
21
3.6
11
4.1
Bathing
1
0.2
0
0.0
Interaction with CERW female
10
1.7
0
0.0
Dancing
2
0.3
1
0.4
Aggressive interaction with CERW male
1
0.2
1
0.4
Interspecific interaction
1
0.2
0
0.0
Vegetative strata
0-20% ( understory)
10
1.6
1
0.4
21-40% (midstory)
76
12.2
27
10.3
41-60% (lower-canopy)
214
34.4
118
44.9
61-80% (mid-canopy)
209
33.6
76
28.9
81-100% (upper-canopy)
113
18.2
41
15.6
using GPS Pathfinder software and were accurate
to 0.5-4.5 m with the majority of points accurate
to 3 in and points on the ridgetop accurate to 0.5-
1.5 m. We used coordinates of the male locations
and fixed kernel methods (Barg el al. 2005) to
calculate 95% kernel home range estimates
(territories) and 50% kernel estimates (core areas)
with the animal movement extension (Hooge and
Eichenlaub 2000) in ArcView 3.2 using the least
squares cross-validation method. Canopy gaps
present on each study site were digitized based
on Held sketches. GPS points collected on gap
boundaries in the field, and 2003 aerial photo¬
graphs (Perkins 2006). Canopy gap, territory, and
core area shaped les were overlaid onto 2003
aerial photographs in UTM NAD83 State Plane
West Virginia north using ArcGIS 9.0 (Perkins
2006). We classified the location of each activity
as inside or outside of the core area for each
territory. We also classified the location of each
activity in relation to canopy gaps. Locations that
were within I m of a canopy gap were considered
to be associated with a gap.
Statistical Analyses.— We summarized loca¬
tions into activities, vegetative strata, and tree
species on the two ridges and used Pearson Chi-
square tests of independence in SAS Version 8
ISAS Institute 1999) for statistical analyses.
Expected values in each cell are the product of
row observations and column observations, divid¬
ed by total observations (Winkler and Hays 1975).
We used Fisher's exact test when sample size was
loo low for Chi-square tests. We considered
differences significant at l‘ ~ 0.05.
We combined data from the two ridges to
examine if male activity (singing, foraging, per¬
ching, preening) differed among vegetative strata,
within versus outside of territory core areas, and
associated versus not associated with canopy
gaps. We also examined whether vegetative strata
used for singing or foraging differed within versus
outside of core areas and in association with
versus not associated with gaps.
We examined use of tree species separately for
each site because the two ridges sampled had
different tree species composition. We compared
the distribution of singing and foraging activity
among the nine most frequently used tree species
on Hart Ridge to examine if different tree species
were used for different activities. Availability of
tree species was assumed to be equal for each
activity. Activity was not compared among tree
species on Snake Ridge because individual cell
counts within the Chi-square were too low for
a valid test. We compared singing use of tree
species between core and non-core areas of
territories for both sites combined. We made no
conclusions about preferential use of tree species.
500
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 3. September 2012
TABLE 2. Activities of male Cerulean Warblers among vegetative strata, in core areas of territories, and in association
with canopy gaps, Wetzel County. West Virginia, May-June 2005. The standardized residual (SR) values farthest from zero
indicate the greatest differences between observed and expected values (numbers of observations) of individual cells,
Vegetative strata
Core area use
Gap use
Activiry
Midstoty Lower-canopv Mid-canopy Upper-canopy
Core
Non-core
Assoc.
Not Assoc.
Singing
Observed
62
193
Expected
62.0
205.3
SR
0.00
-0.86
Foraging
Observed
15
47
Expected
12.7
42.1
SR
0.64
0.76
Perching
Observed
6
25
Expected
5.6
18.5
SR
0.18
1.52
Preening
Observed
1
13
Expected
3.7
12.2
SR
-1.40
0.23
173
94
282
175.7
79.0
261.4
-0.20
1.69
1.28
35
10
31
36.0
16.2
48.7
-0.17
-1.54
-2.53
15
1
19
15.8
7.1
21.2
-0.21
-2.29
-0.47
15
2
14
10.4
4.7
14.8
1.41
-1.24
-0.21
212 162 332
232.7 157.9 336.1
-1.35 0.33 -0.23
61 33 59
43.3 29.4 62.6
2.68 0.66 -0.45
21 11 29
18.8 12.8 27.2
0.50 -0.50 0.34
14 3 25
13.2 9.0 19.1
0.22 -1.99 1.36
We calculated standardized residuals for each
cell with the equation ([observed-expected |/v ex¬
pected) lor each significant Chi-square test (Rey¬
nolds 1977, Newman and Waters 1984, Smith
and Iverson 2004). The farther the value of the
standardized residual from zero, the more impor¬
tant the difference between the observed and
expected cell value was to the outcome of the test.
Values > ±1, especially those approaching ±2,
are considered important while values near zero
indicate little difference between observed and
expected values (AcaStat Software 2004, Smith
and Iverson 2004).
KUisUL TS
We collected observations of activities, ti
species, and vegetative strata for 20 Cerule
Warbler males on Hart Ridge and 9 on Sna
Ridge. We obtained sufficient locations to deli
eate territories for 14 males on Hart Ridge a
seven males on Snake Ridge.
Singing was the most common of the
act,vm„ rec°rdcd Mowed by foraging (1
ote I). These two activities comprised 81.6%
surhrVatl°nS at b°th sites‘ Maintenance behavic
-uch as preening and bathing were rare
served. Matmg and territorial behaviors (dan
ng, interaction with female, aggressive intera
wi,h —<•) 1.7*
observed one instance of an interspecific interac¬
tion when a Cerulean Warbler male was chased by
a male Scarlet Tanager ( Piranga olivacea).
The majority of observations on both sites
(70%) occurred in the lower- and mid-canopy
strata (Table I ). Mules rarely were delected in (lie
understory stratum and this class was omitted
from analyses. Activity differed among vegetative
strata (x* = 20.18. df = 9. P = 0.02). The upper-
canopy was used more frequently than expected
tor singing and less than expected for foraging,
perching, and preening (Table 2). The lower-
canopy was used more frequently than expected
lor perching and the mid-canopy for preening.
Activity differed between core and non-core
areas (yj = 17.64. df =3 ,P = 0.0005). Foraging,
which had the strongest difference between
observed and expected cell values, occurred more
often than expected outside of core areas and less
than expected within core areas (Table 2). Singing
was observed more than expected within core
areas and less than expected outside of core areas-
Perching and preening occurred equally among
core and non-core portions of the territory.
Use of vegetative strata for singing differed
between core and non-core areas ()(; = 10.94. dl
3- P = 0.012) and in association with canopy
gaps (x: = 26.87, df = 3, P < 0.001 ). Singing in
the upper-canopy was observed more often than
Wood and Perkins • CERULEAN WARBLER ACTIVITIES
501
TABLE 3. Use of vegetative strata for singing and foraging in core and non-core areas of territories and for singing
in association with canopy gaps by male Cerulean Warblers, Wetzel County, West Virginia, May— June 2005. The
standardized residual (SR) values farthest from zero indicate the greatest differences between observed and expected values
(numbers of observations) of individual cells.
Vegetative strata
Singing
Foraging
Singing
Core
Non-core
Core
Non-core
Gap
No Gap
Midstory
Observed
24
31
1
8
15
40
Expected
30.3
24.7
3.1
5.9
18.8
36.2
SR
-1.14
1.26
-1.18
0.85
-0.88
0.63
Lower-canopy
Observed
83
78
9
30
37
124
Expected
88.6
72.4
13.3
25.7
55.0
106.0
SR
-0.60
0.66
-1.18
0.85
-2.43
1.75
Mid-canopy
Observed
72
60
19
12
49
83
Expected
72.7
59.3
10.6
20.4
45.1
86.9
SR.
-0.08
0.09
2.59
-1.87
0.58
-0.42
Upper-canopy
Observed
61
27
1
8
48
40
Expected
48.4
39.6
3.1
5.9
30.1
57.9
SR
1.80
-2.00
-1.18
0.85
3.27
-2.36
expected within core areas and less than expected
outside of core areas (Table 3). Mid-story singing
locations occurred more than expected outside
of core areas and less than expected within core
areas. Lower- and mid-canopy singing locations
were observed equally in core and non-core
areas. Singing locations in the upper-canopy were
associated with canopy gaps more than expected
(Table 3).
Use of vegetative strata for foraging differed
between core and non-core areas (x2 = 1 6.54.
df = 3, P = 0.0009). We detected the greatest
difference between observed and expected values
in the mid-canopy strata (Table 3) where foraging
occurred in this stratum more frequently than
expected within core areas and less than expected
in non-core areas.
Males were associated with canopy gaps during
34% (/, = 234 of 685) of observations on Hail
Ridge and 19% (// = 54 of 278) of observations
on Snake Ridge. Activity associated with canopy
gaps did not differ front that away from gaps (x2
= 6.98. df = 3. P = 0.07; Fisher’s exact test P =
0-06; Table 2).
We observed Cerulean Warbler males using 23
different tree species on the two sites (Table 4)
for a variety of activities. Oaks were used most
commonly on the xeric site (Snake Ridge)
whereas black cherry and black locust were used
most often on Hart Ridge. Singing and foraging
activity did not differ among tree species on Hart
Ridge (x2 = 12.42. df = 8. P = 0.13). We
recorded too few foraging observations on Snake
Ridge to make this comparison. The distribution
of tree species used for singing differed between
core and non-core areas on Hart Ridge (x~ =
28.29. df = 6. P < 0.0001) and on Snake Ridge
(X2 = 18. 16. df - 2, P < 0.000 1 ). Males used
black cherry on Hart Ridge and species of hickory
(Table 4) on Snake Ridge more in core areas than
non-core areas (Fig. 1).
DISCUSSION
The Cerulean Warbler is a canopy associated
species. They forage by gleaning insects off
leaves and twigs in the forest canopy, place nests
in the forest canopy at heights up to 30 m, and
sing in the canopy (Hamel 2000a. b). However,
data regarding canopy levels exploited for sing¬
ing, foraging, and other behaviors are limited.
Barg et al. (2006) reported higher mean singing
heights (15 m) than foraging heights (12.8 m) in
Ontario. We found that activity type varied among
vegetative strata, which may help explain Ceru¬
lean Warbler preference for a vertically stratified
canopy. Singing occurred more than expected in
502
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 3. September 2012
TABLE 4. Number of observations of male Cerulean Warblers (20 on Hart Ridge, 9 on Snake Ridge) by activity (sing,
forage, all activities combined) and tree species in Wetzel County. West Virginia. May-June 2005.
Hart Ridge
Snake Ridge
All
All
Tree species
Sing
Forage
n
%
Sing
Forage
n
*
Ash. White/Green (. Fraxinus spp.)"
48
9
80
10.5
10
1
23
6.8
Black Cherry ( Primus serotinaf
86
27
160
21.0
0
Black Locust ( Robinia pseudoaeacidf
66
17
128
16.8
0
Black Walnut (Jug Ians nigraf
45
9
82
10.8
2
4
1.2
Hickory (Carya Spp.)"
9
2
55
7.2
23
3
47
14.0
Mockcrnut Hickory (C. tomentosa)
2
1
6 .
0
Pignut Hickory (C. glabra)
1
3
3
2
5
Shagbark Hickory (C. ovata)
1
0
Unknown spp.
6
1
45
20
1
42
Oak (Quercias spp.)
Chestnut Oak (0. prinus)
0
49
1
57
17.0
Northern Red/Black Oak (Q. rubra/
19
1
42
5.5
26
1
55
16.4
vatutina)"
Scarlet Oak ( Q . coccinea)
0
3
1
17
5.1
White Oak (Q. alba )
0
3
12
3.6
Unknown spp.
0
9
1
12
3.6
Maple ( Acer spp.)
Red Maple (A. ruhruni)"
16
1
33
4.3
5
6
1.8
Sugar Maple (A. saccluirrum)"
33
10
84
1 1.0
5
1
28
8.3
Unknown spp.
0
2
0.6
Tulip Poplar (Liriodeiulron tuHpiferaY
29
15
80
10.5
17
2
30
8.9
American Beech {Tagus grandifolia)
0
I
1
0.3
Apple l \lalus sylvestris)
1
2
0.3
0
Basswood (Tilia ament-ana)
5
8
l.l
7
14
4.2
Black Gum (Nyssa ss-lvatica)
0
1
1
2
0.6
Cucumber Magnolia ( Magnolia acuminata)
1
3
0.4
6
4
17
5.1
Elm (Ulmus spp.)
1
0.1
2
2
0.6
Redbud ( Cards canadensis)
1
0.1
0
Sassafras ( Sassafras albidurn)
1
1
2
0.3
1
0.3
Sourwood (Oxydcndntm urboreum)
0
6
6
1.8
Used in Chi-square analysis comparing tree use for singing vs. foraging on Hart Ridge.
the upper-canopy where advertisement behavior
tor mating or territory defense would be impor¬
tant. Conversely, foraging, perching, and preening
occurred less than expected in the upper-canopy,
perhaps in an attempt to remain inconspicuous
while performing these activities. These three
behaviors occurred most often in the lower-
canopy and mid-canopy strata where individi
would be less vulnerable lo aerial predation.
Cerulean Warblers spent the majority of t
time engaged in singing activities and sing
occurred more frequently than expected wii
core areas of territories, similar to that reportec
Barg et al. (2006). Cerulean Warbler territo
are often clustered fHamel 2000a, Roth and Isl
007) and most territories mapped on our st.
sites had multiple neighbors. Males frequently
moved to a new singing location to counter-sing
in closer proximity to an adjacent male that
approached a common territory boundary. This
behavior was so pronounced for some individuals
that edges of territory boundaries often over¬
lapped. Thus, core areas may serve as strategic
locations for territorial defense among multiple
neighbors especially where densities are high.
Barg et al. (2006) reported higher song-f**1
densities within core areas and suggested core
areas may be selected primarily for characteristics
related to enhanced song projection. Our finding
that males singing within core areas used the
upper-canopy more than expected supports tfu's
hypothesis because higher locations within core
Wood and Perkins • CERULEAN WARBLER ACTIVITIES
503
Black
Black
Black Red Oak
Sugar
Tulip White Ash
Chestnut Hickory
Red Oal
Cherry
Locust
Walnut group
Maple
Poplar
Oak spp.
group
Hart Ridge
Snake Ridge
FIG. 1. Percent occurrence of male Cerulean Warbler observations among tree species most often used for singing in
core compared to non-core areas of territories on two sites in Wetzel County. West Virginia. May-June 2005.
areas may enhance song broadcast to neighbors.
Barg (2002) hypothesized that song-posts would
be near canopy gaps or in trees with less dense
foliage where song attenuation and reverberations
olf foliage were reduced. We found that singing
behavior near canopy gaps occurred more than
expected in the upper-canopy. We also detected
no effect of the proximity to canopy gaps on
singing, foraging, and perching activities, even
though canopy gap densities were highest within
core areas (Perkins 2006). Core areas are likely
selected for a combination of complex reasons.
Male Cerulean Warblers foraged more than
expected outside of core areas. Similarly, core
areas did not serve as foraging centers for
Cerulean Warblers in Ontario (Barg et al. 2006).
h appears that males use core areas primarily as
singing locations and may forage within them
only opportunistically. However, males foraging
within core areas used the mid-canopy strata
more than expected. They may forage higher
within than outside of core areas simply because
singing occurred at higher canopy levels and the
primary purpose of core areas appeared to be lor
singing.
Use of different tree species is quite variable
across the range of the Cerulean Warbler,
although the importance of oaks, hickories, and
maples is often noted in the Appalachian region
for singing and foraging (Rosenberg et al. 2002).
Barg et al. (2006) found that, for IS males in
Ontario, the five most commonly used tree species
for singing, foraging, and perching were sugar
maple (36.5%), bilternut hickory (C. cordiformis ;
30.0%), white ash (12.1%), oaks (8.1%), and
American elm (Uhnus americana ; 5.7%); males
preferred sugar maple and bittemut hickory as
song-posts. Foraging males preferred hickories in
Illinois (Gabbe et al. 2002) and sugar maple,
chestnut oak. and species of hickory in the central
Appalachians while avoiding the red oak group
(George 2009). Use of tree species varied between
our two study sites, primarily as a result of
differences in tree species composition. Oaks and
hickories occurred less often on our mesic site and
male Cerulean Warblers instead used cherries,
locusts, and walnuts. Barg ct al. (2006) found the
distribution of tree species used lor song-posts
differed between core and noncore areas; males in
noncore areas predominantly used sugar maples
(34.4% of observations) whereas in core areas
they predominantly used bitternut hickories
(36.8% of observations). They suggested that
male Cerulean Warblers appeared to be selecting
trees for song-posts that had delayed development
of leaves. We similarly found hickories used as
singing locations within core areas at our xeric
site, while males at our mesic site used black
cherry within core areas. Cerulean Warblers
appear to be flexible in use of tree species for
504
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124. No. 3. September 2012
various behavioral activities; however, at oak/
hickory dominant sites it would be important to
retain these species if timber harvests are planned.
ACKNOWLEDGMENTS
Funding lor this project was provided by the Wildlife
Diversity Program of the West Virginia Division of Natural
Resources (WVDNR). Access to the study site was provided
by WVDNR. We thank Wheeling Jesuit University for field
housing. J L. Eells. M. R. Lutmcrding, L. M. McKenzie, B. L.
Miller, and J. L. Saville provided field assistance. T. J. Boves,
J. W. Edwards. S. P. Olcott, and S. H. Stoleson provided
helpful reviews of earlier drafts of this manuscript. This study
was performed under the auspices of West Virginia University
ACUC protocol #04-0302. Use of trade names or products
does not constitute endorsement by the U.S. Government.
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The Wilson Journal of Ornithology 124(3):506-512, 2012
MICROHABITAT NEST COVER EFFECT ON NEST SURVIVAL OF THE
RED-CRESTED CARDINAL
LUCIANO N. SEGURA.1’3 DIEGO A. MASSON,2 AND MARIELA G. GANTCHOFF1
ABSTRACT.— We evaluated the influence of microhabitat vegetation cover on Red-crested Cardinal (Panaris
coronata) nest survival in natural forests in central eastern Argentina by monitoring 106 nests for 1,262 exposure day
Daily nest survival rates increased with vegetation cover above the nest and decreased linearly as the breeding sea'on
progressed. Increased concealment above the nest helped hide and protect nests from predators (mainly aerial predator-.
Earlier nesting attempts in the breeding season were more successful than those later in the season. This is the first study to
evaluate the effect of microhabitat vegetation cover on daily nest survival rates of a south temperate passerine. We highlight
the importance of microhabitat nest concealment on nest success of the Red-crested Cardinal. Received 23 October 2011
Accepted 23 March 2012.
Predation is a major ecological force influenc¬
ing biological systems al a multitude of levels
(Fontaine et al. 2007). Nest predation has been an
important factor in the evolution of avian life
histories (Skutch 1985, Ricklefs 2000) and nest
site selection (Lima 2009, Martin and Briskie
2009) as egg and chick predation are the main
causes of nest failure in birds (Ricklefs 1969,
Martin 1993b, Lima 2009).
Nest predation rates of numerous bird species
are affected by the physical features of a nesting
site (Martin 1993b, Liebezeit and George 2002,
Gjerdrum et al. 2005, Eggers et al. 2006, Fontaine
and Martin 2006). Many studies have reported
vegetation cover in the immediate vicinity of a
nest provides greater concealment and lower
accessibility to predators, which results in higher
survival rates (Kelly 1993. Martin 1995, Hewlett
and Stutchbury 1996, Flaspohlcr et al. 2000
Liebezeit and George 2002, Weidineer 20(P
Wmter et al. 2005. Kdleher and O’Halloran
-007. Rangel-Salazar et al. 2008, Kerns et al.
2010; but see Vergara and Simonetti 2004).
Nest site selection likely affects nesting success
(Eggers et al. 2006). Many bird species do not
choose nest sites randomly with respect to
;eQ~, characteri-s,ic*s ( Martin and Roper
988 Holway 199!. Knopf and Sedgwick
cant vegeU,lon cover frequently has a signifi-
‘ T™,0n/'!dll0r foraging success (Stinson
nlsfj Ir '982)- SmM bi|-‘ls choose
nest sues offertng more protective cover given a
y Evolueidn,
Buenos Aires. CM’SFOA ft. -n ^'a U"lversidlui *
’Bacullad de OcfciS ^ Al*e",in“'
"S«- * fa Pb,a. ^\Un,V?*“W
C°™"8 . - a.
506
simulated increase of predation risk (Eggers et al
2006). Birds have been observed to change nest
microhabitat following predation to more con-
eealed locations (Lima 2009). The type of nesi is
also important, as cavity and closed nests are
likely to be more protected from both enviwit-
mental conditions and nest predators than open
nests (Ricklefs 1969, Martin and Li 1991
Robinson ct al. 2000).
Most studies of nesting success have been
conducted in cither north temperate or tropical
areas (Martin 1996). Some authors have inferred
that birds in the Southern Hemisphere have higher
nest predation rales than in north temperate areas
based on the presence of certain life-history traits
(reviewed in Martin 1996). The contrasts between
tropical and temperate birds still remain large!)
unresolved (Martin 1996. Ricklefs 2000. Farcin
et al. 2005). Vegetation cover has been identified
as an important influence on predation risk in bird
species of north temperate and tropical areas. M
little is known about how these factors ntf)
influence reproductive biology and nesting sue
cess ol birds in south temperate regions
Mezquida and Marone 2002. Vergara and Sinn-
netti 2004).
The Red-erestcd Cardinal (Parociria coronal -
is (he basal species of the Thraupidae (Davalo)
and Porzecanski 2009), an emblematic group “
neotropical birds. It is distributed from centra,
eastern Argentina to southern Brazil. Parage
eastern Bolivia, and Uruguay (Ridgely and Tuck
2009). Cardinals inhabit semi-open forests iS'A
1997), and build open-cup nests (~13 cm widen"
i he tree canopy in small forks or thorny branch
between 2 and 6 m height (Segura 2011). The;
breed from early October to late February. nesting
"i three different tree species: primarily in Tala
Segura et al. • MICROHABITAT EFFECT ON NEST SURVIVAL
507
(Celtis tala), and secondarily in Coronillo ( Scutia
hiixifolia) and Molle (Schinus longifo/ius ) (Segura
and Arturi 2009).
Our objective was lo evaluate the influence
of surrounding vegetation cover on nest survival
of Red-crested Cardinals in natural forests of
central eastern Argentina. We hypothesized that
increased nest cover reduces susceptibility to
predation, and predicted higher microhabitat
cover would have a significant positive influence
on nest survival.
METHODS
Study Site.— We conducted the study at 'Es-
tancia La Matilde' (35° 20' S, 57G IT W) in
central eastern Buenos Aires. Argentina. The
study site was a flat area of 400 ha within the
Biosphere Reserve Parque Costero del Sur (MAB-
I'NESCO). It is semi-open grassland with several
low chains of woodlands, mainly dominated by
native tree species including Celtis chrcnhergiana
(Tala, deciduous). Scutia hiixifolia (Coronillo.
evergreen), and Schinus longifo/ius (Molle).
Red-crested Cardinals are present in the study
area during the reproductive and non-rcproductive
seasons (Segura and Arturi 2012). Potential
terrestrial nest predators in these forests arc
white-eared opossum {Did d phis albiventris).
lesser grison ( Galictis cuja ). snakes ( Philodryas
'PP), and small rodents. Potential aerial nest
predators are: Guira Cuckoo ( Guira guira).
Chi mango Careara ( Milvago chi man go), and
Narrow -billed Woodcreeper ( Lepidocoktptes an-
gustirostris).
Nest Monitoring.— We collected data over three
consecutive breeding seasons from 2005 to 2008.
monitored 106 Red-crested Cardinal nests
annually from October through February by
extensively searching among suitable nesting
habitat. We monitored the nests daily during the
egg laying and hatching stages, and every 2 days
tinting incubation and nestling stages. Nesting
attempts that did not reach egg laying stage (i.e.,
nests in construction) and nests abandoned during
egg laying or incubation were not considered in
the analysis. Nests that failed due to Philornis
ectoparasitism (Segura and Reboreda 2011) were
not considered. We examined nest contents on
each visit, by taking all eggs or chicks from the
nest (Segura 2011 provides details of the null
effect of nest monitoring on nest success). We
checked nests until fledglings had left the nest or
until depredated. We considered a nest successful
if at least one young fledged. Nests with signs of
predation or where chicks disappeared before the
earliest possible Hedging date were considered
depredated. The entire breeding cycle was 27 days
(egg laying + incubation + nestling stages; Segura
2011).
We recorded physical characteristics of vege¬
tation cover in a 50-cm radius around the nest
immediately after fledging. We measured the
presence of leaves and branches at intervals of
10 cm in a horizontal straight line in each of the
four cardinal directions centering on the nest, and
also 50 cm vertically above and below the nest.
These measurements were taken twice at each
nest, at the northern and southern side of the nest
separately. We recorded the absence (0 = 0%),
weak presence (1 = 1-50%), and abundant
presence (2 = >50%) of leaves and branches
covering the nest in each 10-cm interval. We
calculated (he average for horizontal, above, and
below measurements. We assumed vegetation
cover surrounding the nest did not change
throughout the breeding cycle (27 days). There
was no significant association between our
measurements of cover and date of the breeding
season (Spearman's rank correlation; horizontal:
p = - 0.04. P - 0.66; above: p = 0.01 . P = 0.94;
and below: p = —0.01, P — 0.95).
We included date of the season and year as
additional variables to control for intra- and inter¬
annual variation. Age of the nest was included as
a variable to control for intra-nesting cycle
variation- We also included physical characteris¬
tics of the nest site that may influence nest
survival: (1) tree species where the nest was built
(Tala and Coronillo trees). (2) nest height from
the ground (m), and (3) nest location within the
forest (‘center’ if the nest-tree was in the center of
the continuous chains of forest parallel to the
river, 'border' if it was in the border of the chains
of forest, and ‘patches' if it was in small isolated
forest patches more distant from (lie river).
Data Analysis. — We estimated daily survival
rates (DSR) using Program MARK (White and
Burnham 1999. Dinsmore et al. 2002). Encounter
histories were coded following Dinsmore et al.
(2002). We calculated the number of days in each
encounter history relative lo a date prior to the
earliest initiated nest (I Oct = day 0). We used
Akaike's Information Criterion adjusted for small
sample sizes to compare models based on log-
likelihood values (Burnham and Anderson 2002).
We built all models without standardizing
508
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 3. September 2012
TABLE I . Support for models predicting daily survival rates for microhabitat at Red-crested Cardinal nests at Estancia
La Matilde, Argentina (2005-2008).
Model
Deviance
AAIC,
k
Wt
S (above + date)’*'
448.3
0.00
3
0.716
S (above)
452.2
2.01
2
0.252
S (horizontal)
457.4
7.07
2
0.029
S (date)
458.6
8.27
2
0.021
S (site)
459.5
9.61
4
0.009
S (tree)
459.8
9.51
3
0.006
S (age)
460.5
10.23
2
0.004
S (below)
461.4
11.04
2
0.002
so
463.4
11.07
1
0.000
u" AIC, value of ihe top model =
= 454.35.
Deviance difference between each model and the saturated model in -2 log likelihood: AAIC, = difference between each model and the lop model in
Akaike's Information Criterion corrected for small samples (AIC, ); k number of parameters in the model; ti, - Akaike weight, a measure of each model’sielati'e
support within the set ot candidate models. S(. ) is the general model that assumes constant DSR among nests and over time, Stbelowl. Sthorizontal). and Siahc'c1
are the models for the microhabitat cover below, horizontal, and above nests, respectively. S(agc) is the model where DSR has a linear relationship with age of the
nest. S(tree) is the model including the tree species Where the nest was built. Stsitel is the model including the nest location within the forest. Stdatel is the mod;
where DSR has a linear relation with date of season.
covariates and with the logit-link function
(Dinsmore et al. 2002). The list of candidate
models was based on combinations of factors that
a priori may affect Red-crested Cardinal nest
survival. We ranked and compared models using
AAICc (estimated as ihe relative difference
between the top ranked model and each other
model). We considered models with AAICc < 2
to be equally parsimonious (Burnham and
Anderson 2002. 2004). We also examined
whether the suspected effect of vegetation cover
on nest survival was consistent across tree
species (interaction tree X cover). We report
parameter estimates from the single best model
when the top model was strongly supported (tr, >
0.70) (Burnham and Anderson 2002). We report
95% confidence intervals for each parameter
based on the unconditional variances. We
obtained daily survival estimates from the
logistic-regression equation of the best-supported
model. Survival probabilities were the result of
daily survival rate over the assumed duration of
breeding cycle (27 days). Reported values are
means ± SE.
RESULTS
Thirty-four nests produced at least one fiei
ling (resulting in an overall apparent nest-survi
rate of 0.32) while the rest of the nests w
depredated (68%. n = 72 nests). The total num
ot success! ul nests did not differ between seast
(Chi-square: fa = 2.82. F = 0.24). Nests w
bmlt in Tala (n - 68 nests. 64%) and Coroni
(/? 38 nests, 36%) at a height of 3.6 ± (). |
(range = 1 .5-6.8 m). Microhabitat nest cover
(i.e., leaves and branches covering the nest) was
42.1 ± 1.9% for horizontal measures. 51.1 ±
1.8% for above, and 29.4 ± 1.6% for below
measures. Sixty-four nests (60%) were in the
border of the chains of forest, 23 nests (22%) were
in the small isolated forest patches, and 19 nests
( 1 8%) were in the center of the continuous chains
of forest.
We monitored nests over a 131-day interval
(from 16 Oct to 24 Feb) for 1.262 exposure days.
Nest cover above and date within season were
important covariates in modeling DSR (Table 1).
Models including horizontal and below nest
cover, age of the nest, tree species, and site had
a lower AlCc value than the null model, but did
not contribute significantly to the best model
(Table I). The AICc values of the rest of the
co variates were higher than the AICc's null model
and they were rejected. Interaction tree X cover
showed that effect of vegetation cover on nest
survival was consistent across both tree species.
The best fitted model contained the additive
effects of nest cover above and date throughout
the season (wi = 0.72; Table 1). DSR improved
with increasing nest cover above and when
decreasing the date throughout the season (Ta¬
ble 2; Fig. 1).
DISCUSSION
Vegetation cover surrounding the nest and date
ol reproduction within the breeding season had a
significant effect on predation risk of Red-crested
Cardinal nests. These results suggest increased
Segura el al. • MICROHABITAT EFFECT ON NEST SURVIVAL
509
TABLE 2. Estimated coefficients and precision for the top additive model (Table 1
crested Cardinal nests.
) explaining daily survival of Red-
95% confidence interval
Parameter
Estimate (p) ± SE
Lower
Upper
Intercept
Date throughout the season
Cover above nests
1.161 ± 0.444
-0.008 ± 0.004
1.058 ± 0.319
0.291
-0.228
0.431
2.032
-0.002
1.685
concealment helps hide and protect nests front
predators, and earlier nesting attempts within
the reproductive season are more successtul than
those later in the season.
Daily nest survival rates improved significantly
in relation to increased nest cover above, possibly
because of lower accessibility and less visibility
of eggs and chicks. Vegetation above the nest had
a significant impact and we speculate the main
predators access nests from above (e.g., aerial
predators such as the Guira Cuckoo, Chi mango
Caracara, or Narrow-billed Woodcreeper). and not
from the tree trunk li.e., terrestrial predators such
as mammals or snakes). The main key for aerial
nest predators to find nests is probably visual, and
the more visual barriers, the less likely a predator
might detect a nest (Watts 1989).
Dense tree-canopy seems to provide more
protection and Coronillo trees should offer high
quality nesting sites and he chosen more fre¬
quently than Tala trees, which have less leafy
canopies, However. Red-crested Cardinals nested
more frequently in Tala than Coronillo trees
Segura and Arturi 2009). Some authors have
suggested that open nesting birds should have a
balance between the advantages of high conceal¬
ment and the need to maintain visibility from the
nest i.e,. the advantages to avoid predators by
covering the nest and disadvantages associated
with too much concealment (Gotmark ct al. 1995.
Wilson and Cooper 1998). Red-crested Cardinals
appear to use this balance, selecting sites with
higher cover above the nest to avoid predators
and. at the same time avoiding building nests in
too concealed sites that may reduce visibility from
the nest when predators (or conspecifics) ap¬
proach the nest. Another possible disadvantage is
that nest sites that arc too covered may have low
ventilation and luminosity, which may increase
the frequency of ectoparasites (Love and Carroll
1998. O'Connor et al. 2010).
The date within the breeding season also had a
significant effect on nest survival, indicating the
earliest nests (initiated in Oct/Nov) are less likely
to fail than those initiated in January and
February. These results are consistent with studies
which also found seasonal variation in Passer¬
iformes (Hochachka 1990, Jehle et al. 2004. Grant
et al. 2005. Moreno et al 2005: but see Burhans
et al. 2002). The decline in nest success with date,
as Grant et al. (2005) suggested, could be the
result of an increase in predator abundance and
movement later in the reproductive season by
post-reproductive adults and dispersing juveniles.
The cumulative probability of nest survival was
0.17 for a nest initiated in the middle of the
breeding season ( 1 Dec) in a site with 50% cover
above the nest. The Red-crested Cardinal has
higher nest predation rates than north temperate
birds (Martin 1993a), but similar predation rates
to south temperate buds (Merino/ and Reboreda
1998, Mezquida and Marone 2001. Astie and
Reboreda 2006, Delhey el al. 2010. De Marsico
and Reboreda 2010, Di Giacomo et al. 2011). Nest
predation appears to be higher in several South
American than North American locations, and
predation might have had a stronger influence on
the evolution of birds’ life-history traits in South
America. South temperate birds should have
strategics that allow them to maximize their
reproductive fitness given high predation rates.
Segura (2011) reported that, after a predation
event, each pair of Red-crested Cardinals at this
same study site rapidly made another reproductive
attempt in the same territory. Nest intervals in
Red-crested Cardinals are as short as 6 days from
nest loss to initiation of the next clutch (Segura
2011). and the breeding season is long, from
October to February. This allows Red-crested
Cardinals to have at least 6-8 reproductive
attempts in a single season (Segura 201 1).
This is the first study to evaluate the effect of
microhabitat vegetation cover on daily nest
survival rates for a south temperate passerine.
Little is known regarding breeding biology and
bird predator communities in south temperate
510
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124. No. 3. September 2012
Nest cover (%)
HO 1. Daily survival rate (DSR) of Red-crested Cardinal nests related to the percentage of cover above nesls in
different periods of the breeding season (15 Oct: early nests, 1 Dec: half of the season, and 15 Jan: late nests).
areas, and future studies should focus on this
issue. We highlight the importance of microhab-
itat nest concealment on nest success of Red-
crested Cardinals, and suggest considering these
patterns in future conservation and management
of this species’ natural populations, as well as
other bird species with similar life-history traits.
ACKNOWLEDGMENTS
w c are grateful to Luis del Sotlo and Emiliano Torres I
allow ing us to conduct this study in Estancia l.a Madid,
We thank Facundo D. Sallo. Facundo Gandoy. Emilia
Depino, R. E. McNutt. Danielle Castle. S. A. Fee, Kathle
Masterson. A. E. Formoso. D. I Isaldo, R. F. Jensen. Tobi
Mika. R. H. Crandall. M. M, Kalamaras. Rachel Buxtc
Amy Nixon. Leigh Marshall. Y. S. Obed, and M. .
Diferdmando for help in data Collection and nest monitc
mg We are also grateful to M. C. Dc Mars.co and Ig
Berkunsky for helpful suggestions about Program MAR
Ne thank iwo anonymous reviewers for helpful cummer
on a previous version of this manuscript. LNS w
Inveof h> a fell?wshiP Consejo Nacional ,
L' “auo,lcs Cientificas y Tecnicas (CONICET).
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The Wilson Journal of Ornithology 124(3): 5 13-51 7. 2012
NEST-SITE CHARACTERISTICS AFFECT PROBABILITY OF
NEST PREDATION OF BULL-HEADED SHRIKES
SACHIKO ENDO1 :
ABSTRACT — I investigated the relationship between the probability of nest predation and nest-site characteristics: 1 )
nest heiaht above around. (2) number of branches attached to a nest, and (3) number ot thorny branches around the nest tor
a population of Bull-headed Shrikes (Lunius bucephalus) breeding in Japan. Thn ty-eight nests were located during 0
and 2CKW of which 16 were lost to predation. 14 were successful in Hedging young, tour were, abandoned two were
parasitized, and two may have been partially depredated, although the actual reason is unclear. Ne.ther n^t he.ght nor the
number of thomv branches was correlated with breeding success. However the number of branches wa negatively
correlated with probability of nest predation. The primary predators were bch ev ed to be birds, based on physisa
depredated nests. A high density of branches around nests of Bull-headed Shrikes may ensure they are not easily discovered
and depredated by predators. Received 26 September 201 1. Accepted 4 February 2012.
Nest predation is the major cause ot breeding
failure for many bird species (Ricklefs 1969.
Martin 1993). Nest-site characteristics along with
nest defense behavior are the most important
factors related to nest predation (Collins and
Col lias 1984. Caro 2005). Previous studies have
reported that features such as extent of nest
concealment and nest height affect nest predation
(Caro 2005). For example, greater nest cover
reduces the probability that a predator will Imd a
nest (Col lias and Collias 1984. Martin and Roper
1988). Similarly, nest height reduces accessibility
for some terrestrial predators, which may lind it
difficult to access elevated nests (Collias and
Collias 1984). Thus, nest-site characteristics can
strongly affect the success of many breeding birds.
Branches supporting a nest may also function to
reduce predation in shrub-nesting species, as high-
density branches could conceal a nest. Similarly,
branch density may also reduce access by
predators. However, there has been scant inves¬
tigation into the predator-deterring effects ot
branches. In addition, the features ol branches,
such as those with thorns, may affect access lor
nest predators. Some species select thorny plants
for nesting (Lack and Lack 1958. Gawlik and
Bildstein 1990, Yosef 2001), but the effect of
thorns is unknown.
Bull-headed Shrikes (. Lanins bucephahts) build
an open-cup nest in shrubs or bushes (Yamagishi
Department of Lite Science, Faculty of Science. 3 olio
University. Miyama 2-2-1. Hunabashi. Chiba 274-8510.
Japan.
: Current address: Department of Life Science, Faculty of
Sciences. Rikkyo University. Nishi-lkebukuro 3-34-1.
Toshima, Tokyo 171-8501. Japan: e-mail:
s.endo@rikkyo.ac.jp
1981. Takagi and Abe 1996). Their nests on the
study area were made with twigs, dead herbs, and
pieces of polyethylene tape. 1 investigated the
relationship between nest-site characteristics and
the probability of nest predation by measuring and
correlating the following variables with nest
predation: (I) nest height above ground. (2)
number of branches supporting a nest, and (3)
number of thorny branches around the nest.
METHODS
This study was conducted in the meadowlands
and cultivated fields at Karuizawa (36 31' N,
138 59' E: 920 m asl) in Nagano, Japan in 2008
and 2009. Bull-headed Shrikes in this study area
begin to nest in early April and continue until late
July. They are socially monogamous and the
average dutch size was six eggs (n - 14, range
= 3_8 eggs). The incubation period was ~ 15 days
(a — 5 range = 14—16 days), and the nestling
period was ~ 1 5 days (n = 14. range = 13-16 days).
Each nest was visited at 3- to 5-day intervals
until either nest failure or Hedging could be
confirmed. Nest visits were conducted when
parents were away from their nests to minimize
the effect of human disturbance. Successful nests
were defined as those in which at least one chick
Hedged. Failed nests were classified as: (1)
depredated if all of the eggs and nestlings
disappeared before the estimated date of Hedging
(day 15 after hatching), (2) deserted if all eggs and
nestlings were found dead in the nest, or (3)
parasitized by an interspecific brood parasite
(Common Cuckoo. Cuculits canorus). Daily
survival rate was estimated using the Mayfield
Method (Mayfield 1961, 1975: Johnson 1979;
Klett and Johonson 1982). I calculated daily
513
514
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124. No. 3. September 2012
mortality rates for nests in each 5-day age class,
and nest survival probability for each reproductive
period. Two nests parasitized by Common
Cuckoos were excluded from analysis because
they did not meet the requirements for analysis
using the Mayfield Method.
I measured three nest-site characteristics fol¬
lowing nest predation or Hedging to avoid
disturbing nest sites and parental behavior during
the breeding period. Measurements of character¬
istics of depredated nests were not affected by
predator activity as >90% of the depredated nests
were not affected by predators as the nests were
completely intact. I measured nest height from
the ground to the bottom of the nest using a
measuring pole. Bull-headed Shrikes build an
open-cup nest and branches attached to the side
and/or below support the nest. I counted branches
that were attached to at least one point of the nest,
It was difficult to evaluate whether a branch
supported a nest, and I defined supporting
branches as those attached to at least one point
of the nest. The number of thorny branches was
counted in the same way. 1 defined the number of
branches as the sum of the numbers of thorny and
non-thomy branches, as I wanted to examine both
the effects of the density of branches and the
effect of thorns.
Potential predators were Carrion Crows (Cor-
vus co rone). Large-billed Crows (C. macro-
rhynchos). Japanese rat snakes ( Elaphe climaco-
phora). Japanese weasels ( Mustek/ itatsi ). rats
( Rattns spp. ). mice ( Apodemus spp.), and domes¬
tic cats {Pelts catus). I examined evidence of
predators at depredated nests because predation
was not directly observed in most cases. I
assigned predation to mammals if the nest
structure was damaged and to birds or reptiles if
the nest was intact (Yosef 1994. 2001).
Data were analyzed using a Generalized Line
Mixed Model (GLMM) with a binomial err
structure and a logit link function (success =
predation = 0). Two nests in which a fraction ,
nestlings Hedged were excluded from lab
analysis because partial predation might huv
occurred. A tull model included three fixed term
i.e.. nest height, number of branches, and numb,
of thorny branches and one random term, i.e
research year. Likelihood ratio tests were used I
test each fixed term. The effect of the breedin
period during which predation had occurred o
nest-sue characteristics was analyzed using
Generalized Linear Model (GLM) with a binomu
error structure and a logit link function (the period
that predation occurred; egg period = I. nestling
period = 0). Likelihood ratio tests were used to
test each of the fixed terms. The R 2.12.1
statistical package (R Development Core Team
2010) was used for all analyses.
RESULTS
Thirty-eight nests were observed during the 2-
year study period ( 1 3 nests in 2008 and 25 nests ia
2009). Fourteen nests (36.8%) were successful
and 16 (42,1%) were depredated. Nest predation
was equally likely during either the egg or
nestling stage: eight of 30 nests in the egg stage
were depredated, compared to eight of 22 nests in
the nestling stage (// - 0.065. P = 0.80). Twelve
ot the depredated nests (75%) were completely
intact after predation and four were damaged
Four nests were deserted and two were lost to
brood parasitism. Two nests may have been
partially depredated, although the actual reason
is unclear. The nest survival probability was 52%
(325 nest-days, 13 losses) during the incubation
period and 67% (280 nest-days. 7 losses) during
the nestling period.
Neither nest height (Fig. 1A) nor number of
thorny branches (Fig. 1C) was significantly cor¬
related with nest success (Table I ). There was no
etlecl ol nest-site characteristics on the breeding
stage in which predation occurred (GLM. nest
height: x' - 0.13, P - 0.72; number of branches:
X“ = 0.32, P = 0.57; number of thorny branches:
X' = 1 11. P = 0.29). However, the number of
branches was negatively correlated with the
probability of nest predation (Table 1: Fig. IB).
The number of branches attached to the nest
ranged Irom three to 21. Depredated nests were
attached to approximately eight branches (» = 16.
range = 3-18). whereas successful nests were on
~14 branches (n = 14. range = 8-21).
DISCUSSION
Nest predation ( 16 of 24. 66.7%) was the main
cause ol nest tailure of Bull-headed Shrikes in this
study area. I found that high-density of branches
attached to a nest reduced the risk of nest
predation of Bull-headed Shrikes. There are two
possible explanations for this effect. First, branch¬
es may impede predators from preying on nests,
because a predator with a large body may find it
dilticult to move through the branches. Second,
numerous branches may serve as cover that
conceals the nest from predators. It appeared that
Endo • NEST-SITE CHARACTERISTICS OF BULL-HEADED SHRIKES
515
(A)
(B)
(C)
Number of thorny branches
FIG. 1. The relationship between nest outcome (successful = 1. depredated = 0) and nest height (A) number of
branches (B,. and number of thorny branches (C) (n = 30). Upper open bars ind.cate the number of successful nests, and
lower open bars indicate the number of depredated nests.
516
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 3. September 2012
TABLE 1. Analysis (Generalized Linear Mixed Model) of factors possibly affecting nest
Shrikes (n = 30).
predation of Bull-headed
Explanatory terms
df
P
Estimate ± SE
Nest height
0.34
1
0.56
Number of branches
1 1 .36
I
0.0006
0.38 ± 0.13 *
Number of thorny branches
0.10
1
0.75
Significant values arc highlighted in
bold. Research years (0.00
— 0.00) were included as random terms.
birds or reptiles were the main predators based on
physical evidence at depredated nests. I identified
Carrion Crows as egg predators based on two
video recordings and the main predators in this
study area are most likely birds. Predators that use
visual cues to detect nests do not easily discover
well-concealed nests (Lima 2009). Thus, a high
density of branches around a nest may ensure that
nests ol Bull-headed Shrikes are not easily
discovered and depredated.
Nest concealment affects the probability of nest
predation for many passerines (Martin and Roper
1988, Flaspohler et al. 2000). Nest success
increased with nest concealment of Red-backed
Shrikes {Lanins collurio) (Muller et al. 2005).
Nest concealment on the horizontal and/or vertical
planes has been used as an index for nest cover in
previous studies (Holway 1991. Burhans and
Thompson 2001). High-density branches support¬
ing a nest provided underside and lateral cover for
nests in mv study. This branch cover likely made
it difficult for ground predators to find nests
which suggest branch cover may reduce nest
predation by mammals. My results suggest that
concealment from below the nest should receive
more attention as an important nest-site charac¬
teristic.
Previous studies have suggested that thorns
could reduce nest depredation (Lack and Lac
1958, Col lias and Collias 1964). Loggerhea
Shrikes ( Lanins hulovicianns) in South Carol in;
USA nested more frequently in red ceda
( Junipems virginiana) trees, which may hav
more needles than any other species of tree
shrikes in north-central South Carolina that nestei
in red cedar trees fledged one additional youn;
per nest than shrikes nesting in other types of tree
(Gawlik and Bildstein 1990). Two recent fieh
studies have suggested that presence of thorns die
not correlate with the probability of nest predatiot
(Barnard and Markus 1990. Mezquida ant
Maione 2002). Similarly. I found no effect ol
thorny branches on nest depredation. Mezquida
and Marone (2002) suggested that thorns do not
function as anti-predator devices for some bird
species, because their main predators also m.i>
nest in thorny plants. Thus, the effect of thorns, it
any, may depend on the type of nest predators.
Nest height did not correlate with nest preda¬
tion in this population of Bull-headed Shrikes A
study of Bull-headed Shrikes in Hokkaido by
Takagi and Abe ( 1996) reported that effect of nest
height on nest predation varied depending upon
when a female laid the first egg. Nest height did
not affect nest predation of shrikes which started
nesting earlier in the breeding season, but had a
positive effect for later nesting birds. This
difference between the two sites suggests that
effect of nest-site characteristics on nest predation
varies across different environments. Variable
effects may be due to differences in the types of
predators present, which may vary in their
susceptibility to different nest defenses, or
because shrub species used as nest sites may
differ geographically as for Loggerhead Shrikes in
North America (Gawlik and Bildstein 1990).
Forty-six percent of nest sites selected by Bull-
headed Shrikes in Hokkaido were in dwarf
bamboo (Sasa kurilensis ), and 25% were in
deciduous shrubs. However, deciduous shrubs
accounted for 60% of nest sites in Karuizawa
(S. Endo. unpubl. data). It is likely that accessi¬
bility for predators differs between dwarf bamboo
and deciduous shrubs because dwarf bamboo have
smooth trunks with no strong branches, whereas
deciduous shrubs have rough trunks and many
branches. The type of tree in which a bird nests
may affect its reproductive success, as has been
found for the American Robin ( Tardus mi grown -
its) (Schmidt and Whelan 1999). However, the
probability of nest success did not differ among
nest shrub types used by Loggerhead Shrikes in
southwest Idaho, USA (Woods and Cade 1996i.
Bull-headed Shrikes that attached their nest' to
more branches had a higher probability of breeding
success in my study. However, despite the
Endo • NEST-SITE CHARACTERISTICS OF BULL-HEADED SHRIKES
517
beneficial effect of attaching to more branches, not
all Bull-headed Shrikes build nests using a high
number of branches. There are two explanations.
First, nest-sites in shrubs with many potential
branches are limited for Bull-headed Shrikes
breeding in this study area. Second, there may be
a trade -off between using many branches around the
nests and other factors concerning nest success. For
example, an incubating female in a nest with greater
concealment may have more difficult) seeing an
approaching predator, leading to higher female
depredation. McLean et al. (1986) found that nest
exposure increased the strength of parental mobbing
behavior. Thus, there may be a trade-off between
nest concealment and parental behavior.
My study demonstrated that number of branch¬
es surrounding a nest function as a screen to
conceal and camouflage Bull-headed Shrike nests
from predators. Future studies should consider the
role of branches surrounding a nest as a defense
against nest predation.
ACKNOWLEDGMENTS
I am grateful to Toshilaka Suzuki for helpful comments
and discussion on this study and the manuscript, and David
Wheatcroft, Shin Matui, Keisuke Ualu. and two referees for
helpful comments on the manuscript. 1 also thank Hiroshi
Hasegawa and members of the Laboratory of Animal
Ecology, Toho University for helpful discussions,
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The Wilson Journal of Ornithology 124(3):5 18-524. 2012
CAPSAICIN AS A DETERRENT AGAINST INTRODUCED
MAMMALIAN NEST PREDATORS
SHANE M. BAYLIS,1 4 PHILLIP CASSEY,- AND MARK E. HAUBER' '
ABSTRACT.— We investigated use of capsaicin, a chemical that evolved as a mammal -directed fruit-consumption
deterrent for chili ( Capsicum annum) fruits as a nest-predation deterrent. Capsaicin is unpalatable to mammals, but
apparently undetectable by birds, and has been used as a selective mammal-repellent in several commercial applications,
e placed nmtanon thrush (Turdus spp.i nests containing model and real eggs in a suburban site near Auckland. New
ealand. The majority of observed predation attempts in our experiments were attributed to introduced rats (Ramis spot
used on comparisons of tooth-marks on damaged plaster eggs and tooth-marks made with rat skulls. Predation rau-von
imitation eggs seated with adhesive chili powder were lower than predation rates on eggs in other treatments (W = 201.
17 H e l g "on-adhesive adhesive paprika (capsaicin-free chili powder), non-adhesivc paprika, and
n reated eggs. Successive replicates of the same experimental paradigm in the same site revealed the predation rate on all
* deCI'eaSe,ci W,th Placement of imitation ncs,s and eggs. These results Support the potential Vtdu
use ol capsaicin-heated nests to deter mammalian predators of natural bird nests. Received 15 July 2011. Accept S
The time spent as an egg. hatchling, or juvenile
by birds is a period of high vulnerability to
predation (Weatherhead and Blouin-Demers
2004). Reproductive losses of focal nesting birds
or populations due to mammalian nest predation
are typically controlled by the use of poison baits,
often used just prior to the breeding season, in a
lorm to target a particular predator species, but
often affecting others as collateral damage (Eraser
and Hauber 2008). For instance, widespread aerial
releases of 1080 bait in New Zealand, mainly
targeting brush-tailed possum (Trichoswus vulpe-
cula) as a tuberculosis reservoir, also have a
significant negative impact on introduced rat
populations and secondarily poison ermine (Mus-
lela emiinea), all ol which are major nest predators
of native birds (Innes et al. 1995, Murphy ct al.
1999). The primary conservation benefit of poison
baits is that predator numbers are diminished when
native birds are at the greatest risk of nest
predation, leading to markedly increased Hedging
and recruitment rates (Powlcsland ct al. 1999). The
wide-scale application of poison baits is frequently
unpopular with opponents observing the poisons
are non-specific and may affect non-target animals,
including pets and even protected avian species
(Fraser and Hauber 2008). Thus, narrowly targeted
'School ol Biological Sciences. University of Auckland
Auckland. PB 92019. New Zealand.
School of Earth and Environmental Sciences. Univer¬
sity of Adelaide, SA 5005, Auslralia
'Department of Psychology, Hunter College of ,he City
University of New York. NY 10065. USA.
‘Corresponding author; e-mail:
shane.m.baylis@gmail.com
518
and/or non-lethally toxic alternatives to traditional
baits should be useful, particularly near areas of
human habitation.
Capsaicin is the active ingredient in ‘hot’ chili
peppers, responsible for the immediate ‘spicy’
sensation upon ingestion and the further ‘burning’
stimulus immediately following gut passage, as well
as the similar ‘burning* feeling associated with
prolonged skin contact (Szallasi and Blumberg
1999). Capsaicin is thought to have evolved as a
selective seed-predation deterrent by the chili
(Capsicum annum) plant, although there are some
cultivars that produce fruits lacking capsaicin,
including sweet paprika (Tewksbury and Nablian
2001 ). Hot* C. annum fruits are extremely offensive
to potential mammalian seed predators in the plant's
native range; the obvious evolutionary, ecological,
and cognitive consequence of the noxious ’hot' taste
is that mammals do not willingly consume fruits or
seeds of C. annum (Tewksbury and Nabhan 2001).
Avian seed dispersers, and birds in general, are
unaffected by capsaicin with Curve-billed Thrashers
(7 oxnstatna curvirostre) recorded as important
dispersers of viable C annum seeds, as well a11
being major consumers of its fruits (Tewksbury and
Nabhan 200 1 ).
Several practical uses have been made of the
deterrent capacity of capsaicin against mammals. It
has been recently patented as a selective deterrent,
when mixed with commercial seed mixes, against
squirrels (Sciurus spp. ) in bird feeders in North
America (Blumberg 1998), as well as being
investigated as an agent to protect longleaf pine
(Pinus palustris) seeds from predation by mice
(Nolte and Barnett 2000). It is also used to protect
Baylis et al. • CAPSAICIN AS A NEST PREDATION DETERRENT
519
poultry feed from mice and ruts (Jensen et ul. 2003),
as mammals are deterred by the application of
capsaicin to items they would otherwise consume.
We consider from a cognitive perspective that
capsaicin treatment may cause predation deterrence
on focal avian nests in two ways. First, capsaicin
treatment may result in behavioral responses from
direct trigeminal irritation (Clark 19%). Second,
once predators have been exposed to capsaicin, it
may deter further predation attempts as a learned
aversion (Kimball et al. 2009). Deterrence, in the
case of a learned av ersion, may not be specific to
capsaicin-treated eggs and may generalize to items
that resemble the olfactory, tactile, and/or visual
cues of those treated with capsaicin.
We investigated the possibility of applying
capsaicin as a selective avian nest-predation
deterrent against invasive mammals in N'ew
Zealand using artificial nests. We predicted nests
treated with capsaicin-containing chili powder
would be less appealing to mammalian predators
than untreated nests, or treated with non-pungent
paprika. We also investigated the effect of
attaching chili powder to eggs using an adhesive
to see if this would be necessary to prevent
weather-related loss of chili powder over time
tinder field conditions.
METHODS
Study Area. — Our study area was the New'
Zealand Bush section of the Auckland Regional
Botanic Gardens (ARBG) in Auckland, New
Zealand (37 00' S, 174 54' E). The New Zealand
Bush of ARBG covers 1.48 ha in a narrow, I -km
long strip. The ARBG is in a suburban area,
surrounded to the east and south by housing, to the
west by motorways and on- and off-ramps, and to
'he north by Totara Park, a 216-ha area of mixed
hush and open grassland. Rat control through
poisoned bait stations is undertaken by commercial
contractors in Totara Park, but not within ARBG.
Field Procedures.— We constructed imitation
(artificial) nests (// = 60) resembling those of
European thrushes ( Turdus spp.) and placed them
"i the ARBG during the 2009-2010 austral
summer. We used imitation thrush nests because,
in areas without poison control of mammals,
introduced Turdus spp. are the most common nest
cup-nesting wild birds; most New Zealand native
and endemic bird species arc also cup nesters
(Marchant et al. 1990-2002). Imitation nests each
contained three eggs: two imitations, and one real
egg of King Quail ( Excalfactoria chinensis).
acquired from a local breeder as unincubated
(freshly laid) eggs and stored at 4 C prior to use.
Each nest contained eggs of only one experimen¬
tal treatment type.
Imitation Nests and Eggs. — We constructed
imitation nests by hand. Nests consisted of a dar¬
kened (painted dark-brown using a mix of Fas
Student Acrylic black, brown, and sap green)
cardboard base formed into a shallow cone (radius
= 80 mm; depth = 50 mm) (Fig. I ). These were
stuffed with dried, autoclaved lawn clippings just
prior to placement. We primarily anchored nests into
trees by wedging them between branches in the same
manner as real Turdus spp. nests in New' Zealand
(Igic et al. 2009); each nest was also attached to the
tree by a tie-wire incorporated into its base structure.
The tie-wire served the dual purpose of stabilizing
nests, and preventing them from being removed by
larger nest predators or extreme weather.
We cast imitation eggs (length = 23.7 mm;
width = 18.8 mm; mass = 4.94 g) in plaster-of-
Paris from moulds taken from real eggs of captive
King Quail. All imitation eggs were constructed
with a length of string protruding from their sides
(following Boulton and Cassey 2006) so they
could be tied to the nest structure to prevent
removal by predators (Fig. 1). We painted imita-
tion eggs using water-based paints (mixed from
Golden fluid acrylics™ in Raw Umber, Raw
Sienna, Phthalo Green. Primary Cyan, and Titan
Buff colors) to visually match Turdus spp. eggs as
judged by a mammalian (human) eye. We also
painted the real quail eggs used in the same
manner to avoid influencing predation patterns
with a paint effect.
Treatments.— We manipulated eggs with one of
five treatments: untreated, powder chili, powder
paprika, adhesive chili, and adhesive paprika.
Paprika served as a conspecific plant control for
capsaicin-containing chili powder (Heiser and
Smith 1953). Paprika is derived from cultivars
of C. annum with either no capsaicin (Ayuso et al.
2007), or only low levels of capsaicin (Peusch
et al. 1996) in their fruit and. at most, is only
mildly pungent (Peusch el al. 1996). We tested the
paprika used in our experiment for pungency
using the oral test of Seovillc (described in
Szallasi and Blumberg 1999), and found it not
to be ‘hot’ -tasting, even undiluted. Thus, paprika
served as a control for the visual and tactile
stimuli provided by chili powder relative to the
capsaicin content itself. We acquired both paprika
and chili commercially in local food stores.
520
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124, No. 3. September 2012
aviirTrt -nr-vt >' ^ un*!’eated imitati°n nest. B - typical depredation damage to imitation eggs. The leftmost egg shows
dZdation Zs ^ ^ C = *** of a typically-painted imitation egg. D = rat
away by predators (Bouton L^CaTsey 2006). Im',at,0n egss were anch°red 10 ”*» strings to not be earned
Bayliset al. • CAPSAICIN AS A NEST PREDATION DETERRENT
521
We left untreated eggs without any modification,
and these were placed bare in the imitation nests.
W e placed powder chili-treated eggs in the nest and
chili powder was sprinkled directly over the eggs at
a volume of 5 mL of powder per nest. Powder
paprika-treated eggs were placed in nests and
paprika was sprinkled over them, also at a volume
of 5 mL powder per nest. Adhesive-treated eggs
had either chili or paprika powder directly adhered
using raw albumen and vitellus from store-bought
Domestic Chicken ( Gal Ins gal l u.s) eggs. This was
chosen as an adhesive because, once dry, it is hard
and weatherproof, and because egg contents are a
plausible substance inside natural nests. Imitation
eggs were immersed in a well-mixed bowl of
albumen and vitellus, buried in a container of
powder, removed from the container, and allowed
to air dry at room temperature.
Blocking Experimental Design. — It was not
logistical^ feasible to use larger numbers of nests
for sufficient statistical power concurrently within
the geographic confines of ARBG. and we used a
Randomized Complete Block Design (RCBD;
McIntosh 1983. Montgomery 2005) with three
blocks. We placed the three blocks sequentially
over the same region within the study area. Blocks
each contained 20 nests, including four of each of the
live treatment types. We placed these nests in a
random order and randomized within each block.
Randomization Scheme. — We established a
'ransect line through the New Zealand Bush
section of ARBG and used random numbers
(generated in Microsoft Excel) to assign distance
along and from the transect for nest placement.
'Ve randomized the order of treatments within
each block. We placed nests as close as possible
10 the pre-allocated site wherever it was not
possible to place a nest precisely following the
protocol (for example, due to the presence of a
■>rnall pond).
Data Collection.— We left nests in the field for
1 1 days during the austral breeding season
I spring/summer: Nov 2009-Feb 2010), which is
‘‘bout equal to the incubation period ( 10-12 days)
*or introduced Common Blackbirds (Tardus
writ la) in Australia and New Zealand (Magrath
1992). We considered an egg to be depredated it it
had tooth marks (in the case of imitation eggs) or
"as broken (in the case of real eggs) or removed
'Dm the nest. The color contrast between the
Painted exterior and the while plaster-of-Paris
interior of the imitation eggs allowed tooth marks
to be easily identified (Fig. 1). We recorded
predation events for each study egg. allowing
statistical analysis of partial-nest predation (Hau¬
lier 1998).
We visually inspected depredated eggs and
compared the predator's marks with tooth imprints
from skulls of museum specimens of introduced
rats (R. ratios and R. norvegicus). ermine, possums,
and house mice (Mas musculus) in New Zealand
(Boulton and Cassey 2006). We could easily
identify predators to genus using this method,
although differentiating between the two rat species
was not feasible. We used the width of the tooth-
gouges and the presence of paired furrows in the
imitation eggs (presumably carved by paired rat
incisors, which are much less prominent in possums
and ermine, and much narrower in mice) as key
attributes in the identification.
Statistical Analysis —We checked the data for
any effect of egg type (imitation or real) on
survival time using nonparametrie Wilcoxon
signed-rank tests. We performed Kaplan-Meier
survival analysis, following Venables and Ripley
(2002), on the number of days of survival per egg
with block as a blocking factor. We tested for
differences in hazard function between treatment
groups using the 'efron' technique (Venables and
Ripley 2002). We conducted two separate tests.
Wc first looked for significant differences in
hazard rate between any two treatment groups
once egg type and block were considered using a
two-tailed test. Second, based on a priori
reasoning, we performed a one-tailed, single
comparison test to test the hypothesis that
adhesive capsaicin-treated eggs should experience
a lower hazard rate than eggs of other treatment
groups once egg type and block were considered.
There was technical pseudoreplication in this
experiment, as it was necessary to treat all eggs
within the same nest in the same manner. Thus,
we also analyzed the mean survival time (i.e.. the
mean number of days that eggs survived) within
each nest as the response variable, as this response
metric bypasses the non-independence of eggs
within nests. We considered nests as independent
data points in the second analysis, although
nearby nests may have been visited and depre¬
dated by the same individual mammals. We
modeled the effects of block on mean survival
time of nests using ANOVA, and tested the
residuals from the ANOVA model using a
Wilcoxon signed-rank test to examine if the mean
survival time of adhesive capsaicin-treated eggs
exceeded the mean survival time of the other
522
THE WrLSON JOURNAL OF ORNITHOLOGY • Vol 124. No. 3. September 2012
treatments. We used n. < 0.05 for all statistical
analyses, and conducted all analyses in R 2.10.1
(R Development Core Team 2010).
RESULTS
One hundred and four (58%) of the 180 eggs
were depredated. Sixty-seven of 120 (56%)
imitation eggs were depredated, compared to 37
of 60 (62%) real eggs. Predation rates were not
different between real and imitation eggs ( W =
4,000; n = 180. P ~ 0.2). Each block contained
60 eggs of which 20 (4 of each treatment group)
were real and 40 (8 ol each treatment group) were
imitation eggs. Fifty eggs (83%) in block one, 31
(52%) eggs in block two, and 23 (38%) eggs in
block three were depredated.
Predator type could only be ascertained for
imitation eggs. Forty (59%) of the 67 depredated
imitation eggs had rat tooth-marks, II (16%) had
avian peck-marks, four (6%) were dragged from the
nest but left unmarked, and 12 (18%) were broken
from the end of their strings and lost from the nest,
preventing predator identification. One egg had
both rat and mouse tooth-marks, and this was the
only egg with non-rat mammalian tooth marks.
Adhesive paprika-treated (z = 2.458, n - 180.
P = 0.013) and untreated (z - 2.586. n = 1 80, P =
0.009) nests had higher hazard rates than adhesive
capsaicin-treated nests in the all -comparisons test.
Hazard rales were higher for the first block than the
second (z = 4.255, n = 180. P < 0.001) or third
(z - 5.907. n = 180. P < 0.001) block. Hazard
rates were higher in the second block than the third,
but this contrast was not in itself significant (z =
1.652. u ~ 1 80. P — 0.099). There were no other
significant contrasts in this test.
The hazard rates for eggs treated with adhesive
capsaicin were significantly lower than for eggs
pooled across all other treatment groups (z =
2.409. n = 1 80, P = 0.016. Fig. 2) after
considering the effect of block and egg type.
Adhesive-capsaicin treated nests had greater mean
survival times than other nest treatment types
using the robust, but conservative, Wilcoxon
signed-rank test (W = 201. n = 60, P = 0.05).
DISCUSSION
Adhesively-applied chili powder significantly
reduced the rate of egg predation in imitation
nests constructed to resemble the open-cup nests
oi introduced thrushes in New Zealand, relative to
untreated eggs, eggs treated with non-adhesively
applied chili and paprika, or eggs treated with
adhesively-applied paprika. However, all artificial
nests had markedly-reduced predation when these
treatments were repealed several times in a small
area. It seems unlikely that predation likelihood
was independent for all eggs in a nest, but it .
not possible to correct for nest effects wiihm ih:
Kaplan-Meier analysis, as they were confounded
by treatmem effects. The statistical pattern'
observed in Kaplan-Meier analysis were aho
observed in the highly robust, although conser.a-
tive, Wilcoxon signed-rank test. The interpreta¬
tion of the Kaplan-Meier analysis support' our
main conclusions, although the significance
values associated with specific treatment contrasts
are probably slightly under-estimated.
Rats had been considered the most likely
predator of eggs in suburban New Zealand pnor
to this study (Brown 1997. Flux and Bradfieid
2006) and tooth marks on imitation eggs in this
study matched tooth marks obtained from museum-
specimen rat jaws in size and shape. Rats have
extensive home ranges, which often exceed Id0*m
linear dimensions and cover a variety of habitats
(Dowding and Murphy 1994, Hooker and lanes
1 995, Pryde et a), 2005 ). Thus, it is possible that one
or more chili-treated nests were within a randomly
selected rat home range, especially as the path
through ARBG doubled back on itself in several
locations. One consequence is that rats in the study
area would have had a good opportunity to learn the
majority of eggs in imitation nests were typically
indigestible and/or at times highly unpleasant to
bite into during the first block treatment.
The diet of rats in New Zealand also vanes
seasonally (Miller and Miller 1995), and our
experimental blocks are confounded by season./
effects. Eggs in imitation nests were depredated at
a much lower rate in later blocks regardless or
treatment type; thus, it would be valuable to
investigate whether rats learn to avoid nests
treated with capsaicin and. if so, how they learn
to recognize nest types, to assess whether thb
behavior can be modified to benefit native an.
endemic bird species.
The physiological side effect of applying m'
adhesive based nest-predation deterrent to die
surface ot live incubated, developing eggs was no
investigated in this study. Avian eggshells arc
known to be selectively permeable, allowing the
developing embryo to respire (Burton and Tullett
1983). Thus, adhesive paralleling of complementing
the egg's permeability characteristics would need to
he found (or developed) or the adhesive would need
Bayliset al. • CAPSAICIN AS A NEST PREDATION DETERRENT
523
>
£
3
in
c
o
t
a
2
0.
Adhesive Capsaicin
Adhesive Paprika
Powder Capsaicin
Powder Paprika
Untreated
— l
1 0
Time observed (days)
PIG. 2. Nest survival over time for the five treatment groups. Adhesive capsaicin-treated eggs had reduced predation
risk compared to other treatment types (/. = 2.409. n = ISO, P = 0.016).
to be applied to allow sufficient respiration through
the unaffected portion of the shell for normal
embryonic development. Alternatively, use of chili
powder on the rim of the nest versus the eggshell
would need to be explored before suggesting broad
scale application of this approach.
Applying the chili treatment to real eggs of wild
hirds would also require locating nests of at-risk,
native birds, and careful and skilled applicaiion of
the chili to ensure that eggs were sufficiently
treated, hut avoiding disturbing the physiological
function of the egg, altering the behavior of
parents, or alerting non-mammalian predators to
'he nest's location. It is likely far more cost-
effective to apply aerial baits to decrease predator
numbers, rather than using a large scale placement
nI artificial nests or a labor-intensive egg-treatment
method. However, use of capsaicin at known active
nests of highly endangered species might further
reduce predation by arboreal mammalian species in
situations where they are minimally affected hv
aerial or terrestrial poison baits (Howald et al.
2007. Oppel et al. 20 1 0). There are also regions and
sites where use of poison baits is not possible or
permitted, mainly due to agricultural practices,
human, wildlife, and pet exposure, or public-
opposition. These areas tend to lack predator
control. Capsaicin treatment as used in our trials
through its application to ical nests as a chemical
deterrent against predation of Ihc treated nest may
provide a physiological or a psychological deter¬
rent against nest-predation, or both. Thus, capsaicin
treatment of bird nests and eggs presents potential
new methodology to be used to decrease mamma¬
lian predation effects in areas without poison drops
and baits, and could be a valuable tool for avian
conservation management.
ACKNOWLEDGMENTS
We thank many colleagues for valuable discussions,
contributing the quail eggs, and B. J. Gill at the Auckland
Museum in particular for access to the Land Vertebrates
Collection. Funding for this project was provided by the
Human Frontier Science Program (to PC and MEH) and by
the Faculty of Science at the University of Auckland. PC is an
ARC Future Fellow.
524
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 3. September 2012
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Burton. F. CL and S. O. Tullett. 1983. A comparison of
the effects of eggshell porosity on the respiration of
domestic fowl, duck and lurkcy embryos. Comparative
Biochemistry and Physiology 75a: 1 67-1 74.
Clark. L 1996. Trigeminal repellents do not promote
conditioned odor avoidance in European Starlings.
Wilson Bulletin 108:36-52.
Dowding. J L. and E. C. Murphy. 1994. Ecology of ship
rals ( Rat i its nillus) in a Kauri ( Agathis australis ) forest
in Northland, New Zealand. New Zealand Journal of
Ecology 18:19-28.
Flux. I. and P. Rradfikld. 2006. Breeding biology of
Nonh Island Kokako ( Calaeas cinerea wilsoni) at
Mapara Wildlife Management Reserve. King Country,
New Zealand. Notornis 53:199-207.
Fraser. E. A. and M. E. Haubcr. 2008. Higher call rales
ol morepork. Ninos novaeseelundiae, at sites inside an
area with ongoing hnxlifacoum poisoning compared
with matched non-niunagcd sites. New Zealand
Journal of Zoology 35: 1-7.
Hauber. M. E 1998. Single-egg removal front an artificial
nest by the Gray Catbird. W ilson Bulletin 1 10:426-429.
Heiser Jr., C. B. and P. G. Smith. 1953. The cultivated
capsicum peppers. Economic Botany 7:214-227
Hooker. S and J. Innes. 1995. Ranging behaviour of
forest-dwelling ship rats. Rattus rattus. and effects of
poisoning with hrodifacoum. New Zealand Journal of
Zoology 22:291-304.
Howald. G. R.. C. J. Donlan. J. P Galvan. J. C. Russeli .
J. Parkes. A. Sam.vnilgo. Y. Wang. D. Veitch. P.
Genov lsi. M. Pascal, A. Saunders, and B. Tbrshy,
2007. Invasive rodent eradication on islands. Conser-
vaiion Biology 2 1 : 1258 1 268.
Igic. B,. p. Cassey. p. Samas. t. Grim, and M. E.
Hauher. 2009. Cigarette butts form a perceptually
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Eglinton Valley. Fiordland. New Zealand: a pilot study
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The Wilson Journal of Ornithology 124(3):525 530. 2012
HISTORICAL AND CURRENT STATUS OF LAUGHING GULLS
BREEDING IN NEW YORK STATE
BRIAN E. WASHBURN. 1,1 MARTIN S. LOWNEY,2 AND ALLEN L. GOSSER2
ABSTRACT. — The Laughing Gull t Leucophaem atririlla ) was extripated as a breeding bird from New York State by
1900. Recolonization of coastal New York by this colonial waterbird occurred in 1 070 w ith discovery ol 1 5 breeding pairs
in Jamaica Bay (Queens County ) New York. New York. We conducted a survey ol Long Island salt marsh habitats in 2008
in document if other breeding colonies of Laughing Gulls existed. We identified 66 individual possible breeding areas and
held vurseys were conducted in each area during June 2(MI8. Many areas appeared to provide suitable nesting habitat (i.e.,
large areas of salt marsh dominated by Spartina), but no evidence of Laughing Gull nesting was found. A better
understanding of Laughing Gull populations within the northeast coastal region and the effects of ongoing gull control near
New Y»rk airports is needed for their conservation. Received 26 September 2011. Accepted 22 March 2012.
The Laughing Gull (Leucophaem utricilltt) has
a predominantly southern breeding range, extend¬
ing from the Carribbean and the Gulf of Mexico
northward to Atlantic Canada (Burger 1996). Leu
nesting colonies of Laughing Gull exist north of
New Jersey along the Atlantic Coast of North
America. Those few colonies are in New York.
Massachusetts. Maine, and Nova Scotia (Nisbet
1971, Belant and Dolbeer 1993. Burger 1996).
Nesting habitat for Laughing Gulls varies across
their breeding range. They nest on sandy beaches
with varying amounts of vegetation from Florida
if North Carolina (Bent 1921. Burger and
Gochfeld 1985). This species is a salt marsh
obligate nester in the mid- Atlantic region (Vir¬
ginia to New York) with colony sites exclusively
in salt marsh habitats (Burger and Shisler 1978.
Montevecchi 1978. Burger and Shisler 1980).
Laughing Gulls nest on rocky islands with grassy
areas in northern New England (Nisbet 1971).
The Laughing Gull was historically confined to
'he coastal areas of Long Island in New York
Mate. This gull was a common summer resident
and breeder during the early 1800s (Giraud 1844.
Ctriscom 1923). Populations of Laughing Gulls.
s'milar toother colonial seabirds, were decimated
h.v commercial egging and plume-hunting for the
millinery trade in the mid- to late 1800s (Nisbet
1971. Buckley et al. 1978. Brinker et al. 2007).
and the species was extirpated as a breeding bird
horn New York State by 1900. The last known
USDA, Wildlife Services, National Wildlife Research
' enter. 6100 Columbus Avenue. Sandusky. OH 44870,
L'SA.
USDA. Wildlife Services. 1930 Route 9. Castleton. NY
•2033. USA.
Corresponding author; e-mail:
hhan.e.washbum@aphis.usda.gov
breeding records during that period were South
Oyster Bay in 1884. Amityville in 1887, Cedar
Island in 1888. and a lone pair in Orient in 1900
(Eaton 1910. Griscom 1923. Bull 1964. Latham
1975).
Laughing Gulls starting breeding (again) on
Long Island in the late 1970s after an absence from
New York Stale as a breeding bird for almost 80 yrs
(Buckley el al. 1978. Post and Riepe 1980). Our
study objectives were to: ( I ) review and summarize
information regarding Laughing Gull nesting in
New York State since 1900. and (2) provide a
current assessment of the distribution and the
nesting status of Laughing Gulls in New York.
METHODS
Breeding Records— We reviewed the scientific
literature, books, published reports, and other
printed materials for any and all available records
and information regarding the breeding status of
Laughing Gulls in New York Stale from the 1800s
to 2008. We contacted curatorial staff or accessed
on-line data bases for the New York State
Breeding Bird Atlas, the USGS Breeding Bird
Survey (BBS), and the New York cRird Network.
Reports and data summaries of Long Island
Colonial Waterbird and Piping Plover (Chara-
driits melodus) Survey information were obtained
from the New York State Department of Envi¬
ronmental Conservation tNYSDEC). Personal and
telephone interviews were conducted with repre¬
sentatives from the NYSDEC. National Park
Service. U.S. Fish and Wildlife Service, Town
of Hempstead, New' York City Audubon, and
other entities. All breeding records and associated
information were compiled into an electronic data
base, which we used for the summary and analysis
of Laughing Gulls breeding in New York
525
526
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124. No. 3. September 2012
(objective I) and for selecting potential sites to
examine for presence of Laughing Gulls (objec¬
tive 2).
We obtained the New York State Official Tidal
Wetlands Inventory from the NYSDEC. Geo-
referenced salt marsh maps for Long Island were
extracted using G1S (ArcGIS 9.2: ESRI. Red¬
lands. CA. USA). These maps provided an
estimate ol all salt marsh intertidal zone habitats
available to nesting Laughing Gulls. Much of the
~445 km of Long Island's shoreline is developed,
although coastal wetland habitats (e.g., salt marsh)
remain in some areas (Gornitz el al. 2002). The
largest concentrations of intertidal salt marsh
occur on the south shore, although small areas
occur on the north shore.
We combined all records (e.g.. Laughing Gull
nesting records, observations, and salt marsh
inventory) into a spatially-referenced electronic
data base using GIS. We identified and selected
66 individual sites that represented potential
locations where Laughing Gulls might be nesting
on Long Island based on the information in our
electronic data base (Fig. I ).
Field Surrey.*.— We conducted field surveys
during daylight hours at all 66 individual sites
(Fig. I) during 9-20 June 2008. We chose this
time period to coincide with the expected peak
nesting period for Laughing Gulls (Montevecchi
et al. 1979. Burger 1996). Two or more trained
individuals systematically observed all visible
habitats during the survey at each location with
the aid of binoculars and spotting scopes from all
available vantage points. The number of Laughing
Gull nests, number of Laughing Gulls observed bv
age class (individual Laughing Gulls were as¬
signed to age classes based on plumage [Belant
and Dolbeer I996|), and specific activities of all
Laughing Gulls observed were recorded dunng
each field survey. General observations were
recorded regarding the presence/absence of sail
marsh habitat, Spartina , and the perceived poten¬
tial value of the location for nesting by Laughing
Gulls based on the characteristics of the vegeta¬
tion and hydrology.
RESULTS
We found no records or information to verity
that Laughing Gulls were actively breeding in the
State of New York from 1900 to the late 1970s
(Eaton 1910. Griscom 1923. Bull 1964). Howev¬
er. accounts from this period suggested large
numbers of Laughing Gulls in breeding plumage
were observed on Long Island (Griscom 1923.
Cruickshank 1942. Bull 1964).
Laughing Gulls began breeding (again) in Neu
York State during the late 1970s after a nearly 8(|-
year absence, Buckley et al. (1978) reported the
first breeding record of Laughing Gulls in the
state since 1900 in Nassau County (Fig. 2). Pnsi
and Ricpe (1980) found a Laughing Gull nesting
colony (15 pairs) in 1978 in the Joco Marsh island
Washburn et al. • BREEDING OF LAUGHING GULLS IN NEW YORK STATE
527
complex (40 38' N, 73 47' W) in the Jamaica
Bay Unit of the Gateway National Recreation
Area in Queens County (Fig. 2). This colony
increased exponentially to an estimated 7,629
nests in 1990 (Brown el al. 2001). The Laughing
Gull nesting colony in Jamaica Bay (several
islands in Jamaica Bay in primarily intertidal
Icivv or high salt marsh) decreased by 83% during
1992-2008 to an estimated 1,280 nests in 2008
'Washburn et al. 2009). This nesting colony is
mlluenced by an integrated gull strike manage¬
ment program conducted on the adjacent John F.
kilned} International Airport (Washburn et al.
-I||,8). and loss of nesting habitat due to severe
marsh erosion and tidal Hooding (Gornitz et al.
-M2. Hartig et al. 2002. Bogcr el al. 2012).
Over 99.9% of the Laughing Gulls nesting in
York was associated with the nesting colony
'"Jamaica Bay during 1978-2007. Six additional
heeding records of Laughing Gulls were found
°ULside of Jamaica Bay (Table I. Fig. 2). These
Mtes were abandoned by nesting Laughing Gulls
a,tcr | or 2 yrs as no additional Laughing Gull
nesls 'vere found during surveys in subsequent
y«rs (Sommers et al. 1994. 1996, 2001).
We found no Laughing Gull nests or evidence
01 Laughing Gulls breeding during field surveys
a| 66 potential locations we surveyed. Seventy-
hV() Laughing Gulls (66 adults in breeding
Plumage and 6 subadults) were observed during
'he surveys, ranging from 0 to 30 individual gulls
Per survey location. Laughing Gulls were observed
loafing or perched (47%), feeding (29%), and
Hying (24%). but we did not observe any activity
that suggested these birds were nesting or near a
breeding colony.
Fifty-three of 66 locations surveyed (80%)
contained salt marsh habitat, of which 44 were
classified as low salt marshes (dominated by
Spurt ina al te mi flora) and nine sites were high salt
marsh habitat (predominantly S. patens). Common
reed (Pliragmites australis) had invaded 12 of the
66 (18%) salt marsh areas, degrading their
ecological value and making them relatively
useless for nesting Laughing Gulls.
DISCUSSION
Review of historical information, peer-re¬
viewed literature, reports, and unpublished infor¬
mation confirms the Laughing Gull was a
breeding bird in New York State (more specifi¬
cally on Long Island.) during 1978-2008. Our
findings suggest the Laughing Gull nesting colony
in Jamaica Bay was likely the only nesting colony
in New York in 2008.
Laughing Gull populations are relatively stable
or increasing within the Northeast region and
nationally in the United States, based on popula¬
tion trends from the BBS (Sauer et al. 2011) and
nest counts within coastal states from New Jersey
to Maine (summarized in Washburn et al. 2009).
The overall population index for Laughing Gulls
in the United States and in the Northeastern/Mid-
Atlantic Region during 1966-2009 showed mean
528
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124. No. 3. September 2012
TABLE I. Laughing Gull breeding records in New York State during 1978-2007 not associated with the nesting
colony in Jamaica Bay. New York.
Year
Location i Coordinates!
County
Number of nests
Source
1978
Line Island complex (40
36' N. 73 36' W>
Nassau
1
Buckley et al. (1978)
1990
North Cinder Island (40
36' N, 73 29' W)
Nassau
4
Sommers et al. ( 1994)
1991
North Cinder Island (40
36’ N, 73 29' W)
Nassau
4
Sominers et al. ( 1994)
1995
Young's Island (40 55
N. 73- 09' W)
Suffolk
2
Sommers et al. (2001)
1998
Carter's Island (40 45' ]
8. 72 48' W)
Suffolk
5
Sommers et al. (2001)
2007
Tobay Marsh Islands (40
37’ N. 73 25' W)
Nassau
4
S. P. Sinkevich. pers. comm.
annual increases of 4.5 and 5.8%, respectively
(Sauer et al. 2011).
The presence of adult Laughing Gulls in
breeding plumage within apparently suitable
habitat is not a direct indication of the presence
of a nesting colony. Dolbeer and Bernhardt (2003)
reported 46% of 2-year-old and 12% of ^3-year-
old female Laughing Gulls in breeding plumage
showed no evidence of reproduction. Non-breed¬
ing gulls could be using salt marsh habitats for
foraging during summer months. The presence of
hatching-year Laughing Gulls on Long Island
during late summer and early fall does not
necessarily indicate the presence of breeding, as
northward movements prior to fall migration have
been noted (Burger and Galli 1986. Belant and
Dolbeer 1993).
Salt marsh habitats on Long Island appear to
provide suitable nesting habitat for Laughing
Gulls. Large, open tidal areas dominated by
Spartina and lacking woody vegetation and
common reed occurred in numerous locations
along the coast of Long Island. However, the
reason(s) why Laughing Gulls are not nesting on
Long Island in areas outside of Jamaica Bay are
unknown. Herring Gulls (Lams argentatus ) might
be a problem within areas along the Long Island
shoreline where this species is nesting, as
breeding Laughing Gulls have been displaced by
Herring Gulls (Burger and Slhsler 1978, Burger
1996). Human disturbance and mammalian pred¬
ators could also be reducing the quality of salt
marsh habitats for Laughing Gulls and other
colonial seabirds (Burger and Shisler 1980,
Buckley and Buckley 2000).
Erosion and degradation of salt marshes is a
significant problem along the east coast of the
United States (Gornitz et al. 2002. Hartig et al
2002. Bogeret al. 2012). Loss of coastal wetland
habitats impacts a variety of colonial nesting
waterbirds, including Laughing Gulls (Erwin et al
2006, Brinker et al. 2007). Degradation of salt
marsh habitat along Long Island could negatively
impact the existing nesting colony in Jamaica
Bay. and reduce the number and quality of other
potential nesting locations.
Common reed commonly invades salt marsh
habitats along the Atlantic Coast and in wetland
areas along the Great Lakes, converting native
plant communities into dense monotypic stands
and altering the structure and function of these
areas (Roman el al. 1984, Silliman and Bertness
2004). Expansion of common reed into wetland
habitats decreases bird diversity and negatively
impacts marsh-nesting songbirds and waterbirds
(Benoit and Askins 1999. Wells et al. 2008). The
invasion of salt marsh habitats along Long Island
by common reed is an important concern,
reducing available nesting habitat for Laughing
Gulls (New York Natural Heritage Program
2011).
The Jamaica Buy colony contains >99% of the
Laughing Gulls nesting in New York State. This
colony is influenced by an integrated gull .'trike
management program at John F. Kennedy Inter¬
national Airport (Washburn et al. 2009), severe
erosion and tidal flooding of salt marshes in
Jamaica Bay (Hartig et al. 2002). and high levels
of pollutants and contaminants in Jamaica Bay
waters (Seidemann 1991). The nesting colony of
Laughing Gulls remained viable and relatively
stable in size during 2000-2008 despite the
removal of >88.000 Laughing Gulls during
1991—2008 as pan of the integrated gull strike
management program (Washburn et al. 2008.
Washburn et al. 2009), and concurrent severe
habitat loss due to tidal flooding and marsh
erosion (Gornitz et al. 2002, Hartig et al. -001
Bogeret al. 2012). However, one extreme weathei
event (e.g.. hurricane) could completely degrade
the salt marshes in Jamaica Bay (Gornitz et al
2002) and remove this nesting site for Laughing
Washburn et al • BREEDING OF LAUGHING GULLS IN NEW YORK STATE
529
Gulls while simultaneously decreasing potential
Laughing Gull-aircraft collisions.
CONSERVATION IMPLICATIONS
The presence of well dispersed Laughing Gull
nesting colonies in New York State is an
important conservation concern (New York Nat¬
ural Heritage Program 201 1). We suggest efforts
should be conducted to establish other nesting
colonies on Long Island. Laughing Gull nesting
could be encouraged through active management
activities (e.g.. gull decoys, calls, and nest
placement) following identification of suitable
nesting habitats in existing salt marshes. This
possibility should be considered by the appropri¬
ate wildlife management agencies.
ACKNOWLEDGMENTS
We thank L. A. Tyson. L. A. Humbcrg. J. .1 Albanesc. I).
R. Nicolay, and others for field assistance. We appreciate
'he data and information provided by many individuals
lrom several agencies and groups. Financial and logistical
'uppon for this project was provided by the Port Authority
New York and New Jersey, and USDA Wildlife
Services, This research was approved by the National
Wildlife Research Center IACUC (QA-I 131 ).
LITERATURE CITED
Bmant, J. L. and R. A. Dot BEER. 1993. Population status
"t nesting Laughing Gulls in the l 'oiled Slates 1997-
D91. American Birds 47:220-224,
Hravt, J. L. and R. A, Dolbeer. 1996. Age classification
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The Wilson Journal of Ornithology 124(3):53 1-537. 2012
BREEDING BIOLOGY OF THE SOUTHERN HOUSE WREN ON CHILOE
ISLAND, SOUTHERN CHILE
SILVINA IPPL' 3 5 RODRIGO A. VASQUEZ.' JUAN MORENO.* 2 *
SANTIAGO MERINO.2 AND CAM1LA P. VILLAVICENCIO14
ABSTRACT.— We studied the breeding biology of a Southern House Wren ( Troglodytes aedon chilensis ) population
using nest boxes on Chiloe Island, southern Chile (4 1 S) to make latitudinal comparisons at the intraspecific level. There
were no significant differences in body size between adult males and females, although wings were significantly longer in
make Clutch size averaged 4.3 eggs per nest, and brood size was 3.9 nestlings. Egg size averaged 1 7.3 mm in length and
13.2 nun in width. Incubation and nestling periods averaged 16 days each. The Southern House Wren on Chiloe Island has a
larger clutch size than in the tropics, hut a smaller clutch size than populations at the same latitude in the Northern
Hemisphere. The Southern House Wren has larger eggs and a longer incubation period but a similar nestling period as
House Wrens in the Northern Hemisphere Received 23 August 201 1. Accepted 29 January 2012.
Studies of species with a broad distributional
range are valuable to gain information on the
latitudinal effects on physiology and morphology
as well as behavior and life history traits. Know¬
ledge of breeding biology is useful for testing
hypotheses about effects of latitude on clutch size,
parental care, and breeding phenology (Geffen
and Yom-Tov 2000). However, in comparison
with Northern Hemisphere species, few studies
have been conducted on the breeding biology of
South American species, where information about
natural history of numerous species is lacking
(Geffen and Yom-Tov 2000. Russell et al. 2004).
The House Wren (Troglodytes aedon: Tt'Oglo-
dytidae) has a distribution from southern Canada
to southern Chile, encompassing one of the largest
latitudinal distributions for any native passerine
species (Johnson 1998). Brumfield and Caparella
r 1 996) recommended re-elevating the three main
recognized taxonomic groups to species level: T.
aedon (Northern House Wren), T bnmneicollis
i Brown-throated House Wren), and T. muse it his
•Southern House Wren). The House Wren is cur¬
rently considered a single species (Johnson 1998.
Bird Life International 2011, Gill and Donsker
-912) and we use the common name Southern
Insiiiutode Ecologia y BiodiveiNidacl. Dcpartamento de
Gencias Ecoldgicas. l niversiclad dc Chile. La<> Palmcras
*425. Xuftoa, Santiago. Chile.
: Departanienlo de Ecologia Evolutiva. Museo Nacional
& Ciencias Naturales-CSIC. E-2SfH)6. Madrid. Spain.
Current address: lastinito de Ecologia v Biodivcrsidad.
hepartamento de Ecologia. Pontificia Tniversidad Catblica
de Chile. Alameda 340. 6513677. Santiago. Chile.
4 Current address: Max Planck Institute for Ornithology.
Department ot Behavioural Neurobiology. Eberhard-Gwin-
ner-Strasse. House 6a. D-82319. Seewiesen. Germany.
Corresponding author; e-mail: silvippi@yahoo.com
House Wren for the subspecies 7'. a. chilensis in
our study.
The Southern House Wren inhabits the austral
extreme of Chile and Argentina. It is a small
insectivorous bird and a secondary cavity nester
( Johnson and Goodall 1967. Grigera 1982,
Kroodsma and Brewer 2005). It typically inhabits
scrublands and secondary or marginal forests on
the island of Chilot4 (41 S) (Rozzi et al. 1996.
Diaz et al. 2005) and is also common in urban
areas (Diaz and Armesto 2003): it is similar to
populations of the Northern Hemisphere House
Wren (Johnson 1998). The Southern House Wren
is considered a year-round resident on Chiloe
Island (Jaramillo et al. 2003). but detection during
autumn and winter is difficult, suggesting partial
migration (S. fppi. unpub. data). The House Wien
is an ideal species model, because of its extensive
geographic range, for assessing the ellects ol lati¬
tude on intraspecific variation of breeding biology
(e.g., Young 1994). Comparisons of life-history
traits with the Northern House Wren, would be
informative due to the large amount oi informa-
tion available about the ecology and breeding
biology of the species in the Northern Hemi¬
sphere (e.g.. Kendeigh 1941; Kendeigh et al. 1956:
Drilling and Thompson 1988: Johnson and Searcy
1993. 1996; Johnson 1996; Johnson et al. 2001;
Janota et al. 2002; Johnson et al. 2008. 2009).
Several ecological and reproductive studies have
recently been conducted in South America, mainly
in Argentina (e.g.. Tuero et al. 2007. Fasanella and
Fernandez 2009. Llambfas and Fernandez 2009.
Labarbera et al. 2010. Serra and Fernandez 2011).
The objective of our study was to describe the
breeding biology of the Southern House Wren in a
southern Chilean population and to compare our
531
532
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124, No. 3. September 2012
results with studies of House Wrens from North
America, Central America, and other localities in
South America. We predicted smaller reproductive
investments (e.g., smaller clutch size) by the
Southern House Wren compared to House Wrens
in the Northern Hemisphere.
METHODS
Study Area. — The study was conducted on
Chiloe Island, southern Chile (41 52' S. 73
39 W ) at 50-100 m asl in the austral spring (Oct—
Jan) of 2002-2005. Chiloe Island is < 10 km from
the mainland and supports similar forest bird
communities (Johnson and Goodall 1967. Fjeldsfl
and Krabbe 1990). The continuous distribution of
temperate rainforests as experienced by Charles
Darwin in 1834-1835 have been cleared in large
areas ol northern Chiloe Island with remaining
fragments embedded in an agricultural landscape
(Willson and Armesto 1996).
Field Procedures.— Three hundred nest boxes
were placed in scrublands and forest edges in Scnda
Darwin Biological Station (described by Carmona
et al. 2010) and 50 at Fundo ‘Los Cisnes’ at the
northern tip of the island close to mainland Chile
(nest boxes are described in Moreno et al. 2005,
2007). Both study sites included large fragments of
regenerating evergreen forests of Drimvs winter i
Nothojagus niticla , Weinmannia tddwspenna . sev¬
eral myrtaceous species, and the conifer Podocarpu y
nubtgena (Veblen et al. 1996. Aravena et al 2002)
Nest boxes were suspended from tree branches or
fastened to tree trunks or shrub branches 150 cm
above the ground in scrublands and forest edges
with some up to 100 m within the forest. The mean
distance ± SD between nest boxes was 34 () ±
2x2 m as measured with a Global Positioning
System (GPS) (Garmin e-TREX: Olathe, KS. USA);
the mean distance among active nests (i.e., nest
boxes actually used) was 1 1 7. 1 ± 79.3 m
101-7015. Z&Y Tool Supply Co. Ltd.. Guangxi.
China). Egg volume was estimated when clutch
size was also assessed using Hoyt's (1979) equa¬
tion for egg volume; volume = 6.51 x (length >
breadth-). Nests that were depredated or aban
doned before incubation were excluded from
clutch and egg size analyses.
Adults were captured with nest-box traps when
chicks were 10-13 days of age (hatching dav =
day 0) and marked with metal leg bands (Model
1242-3. National Band and Tag Co.. Newport,
KY. USA) under the authority of Servicio
Agncola y Ganadero, Chile. We measured tarsus
length and beak length to the nearest 0.1 mm
using digital calipers, wing length (mm) as
flattened wing chord, and tail (mm) following
Svensson (1984). Adult males and females were
classified using morphology as only females have
a brood patch (Johnson 1998). Mass was recorded
to the nearest 0.1 g with a Pesola spring balance
(Baar, Switzerland). We also weighed nestlings
on the day ol adult trapping, and measured their
tarsus, beak (from lip to skull), and wing length
using the same technique as for adults.
Statistical Analyses. — We checked for normal¬
ity of data and homogeneity of variance with
Kolmogorov-Smirnov and Levene tests, respec¬
tively. We used non-paranietric statistics when
these assumptions were violated. We addressed
variation in clutch size within the breeding season
and among years using non-parameirie correlation
analysis and Kruskal- Wallis tests, respectively
( Siegel and Castellan 1988). Differences in bod)
size between males and females were evaluated
using a one-way MANOVA. We conducted this
analysis although not all variables were normal,
hut all variances were homogeneous among the
groups. This analysis is considered robust to
violation of the assumption of normality (Sokal
and Rohlf 1995). We also conducted a posteriori
univariate analyses, correcting the significance
Nest Monitoring.— Nest boxes were checked
for occupation on a weekly basis beginning in
October each year. Nest boxes occupied by
Southern House Wrens were frequently checked
to detect laying dates (date of first egg), hatching
dates (first visit when eggs were observed to
natch), and fledging dales (empty nest box) Nests
were cheeked on a daily basis 2 weeks after lav ing
of the last egg to record the exact date of hatching
Some nests were visited daily 10 days after
breadmi10 ,eCO'd fle?gi"8 dale' ES« lcnS"' and
the nearest T ^ e“s in clutch Co
nearest 0.1 mm with a digital caliper (Model
(Quinn and Keough 2002). Nested ANOVA wa
used to analyze clutch size and egg volume, and ti
investigate differences in body size of nestling
measured at 10 to J3 days of age. All analyse:
were conducted with STATISTICA 6.0 (StatSof
Inc. 2001 ) and were considered significant at P <
0.05. Values reported are means ± SD.
RESULTS
Breeding Phenology. — Laying dates of the
Southern House Wren on Chiloe Island ranged
Ippiet al. • BREEDING BIOLOGY OF THE SOUTHERN HOUSE WREN
533
TABLE 1.
Dates for first and last laying, hatching, and Hedging of the Southern
House Wren during three breeding
seasons (2002-2004) on Chiloe Island. Chile.
Season
Laying dale
n
Hatching date
n
Fledging date
n
2002-2003
8 Nov to 2 Jan
1
27 Nov to 1 Jan
5
13 Dec to 4 Jan
3
2003-2004
28 Oct to 3 Dec
18
24 Nov to 20 Dec
15
30 Nov to 18 Dec
3
2004-2005
19 Oct to 8 Jan
16
5 Nov to 15 Jan
16
8 Jan to 26 Jan
3
from mid October to January, while hatching
dates were from November to January (Table 1 ).
Hedging occurred from the end of November to
January (Table 1). Wrens were not color banded
and we have no information about polygyny in
our population. One female reared a second brood
in a neighboring nest box. ~60 m distant, hut we
have no information about the success of its first
clutch. Two males and one female bred in our
study site for two consecutive breeding seasons,
and one male for three consecutive seasons. All
bred in nest boxes that were nearby in the
previous year.
Clinch and Brood Size.— Clutch si/.e in nests
with at least one hatched egg was two and five
eggs with an average of 4.3 ± 0.7 eggs (// = 59)
(Table 2). The modal clutch size was four eggs.
There was no seasonal trend in clutch size within
year (Spearman correlation coefficient, i\ = 0. IS;
P - 0.24), and there were no differences in clutch
size among years (Kruskal Wallis; H = 1.2; P =
0.75; n = 59). The mean brood size was 3.9 ±1.1
chicks (range = 1 to 5, n = 27).
Egg Size. — Southern House Wren females laid
eggs measuring 17.3 ± 0.7 mm in length and 13.2
- 0.3 mm in width (// = 66) in 15 nests monitored
during the 2003 breeding season. Egg volume was
1-532.8 ± 103.8 mm' (n = 66). Mean egg volume
decreased with clutch size (F 1.50 = 20.4. P <
0.001 ) if only four- and five-egg clutches are
considered. The number of successful clutches
with two and three eggs was small; they were
excluded from the analysis.
TABLE 2.
Mean ± SD clutch and brood si/.e
of the
Southern House Wren during four breeding seasons
1 2002—
-005) on Chiloe Island. Chile.
Year
Dutch ± SD n
Brood sire - SD
n
2002-2003
4.2 ±0.6 11
No data No data
2003-2004
4.4 ± 0.7 21
3.9 ± 1.2
14
2004-2005
4.3 ±0.7 19
3.9 ± 1
10
2005
4.2 ± 0.7 8
4.3 ± 0.6
3
Incubation and Nestling Period— The incuba¬
tion stage, the period between the last laid egg and
first hatched egg. ranged between 14 and 19 days
(16.0 ± 1.0 day; n = 32 nests). There was no
seasonal trend in incubation period w ithin year (rs
= 0.14: P = 0.45). All eggs in the clutch hatched
within 1 day. The nestling period was 16.0 ±
1.0 days (/) = 5 nests) and was 33.8 ± 1.6 days (n
= 5) from laying to Hedging.
Chick and Adult Body Size. — Chicks were
measured between days 10 and 13 (11.4 ± 1.1)
in 24 nests (Table 3). Significant morphological
differences occurred between nestlings measured
in different days (10 to 13; /• 12.101 = 29.2: P <
0.001; 11 = 88). Univariate results revealed length
of wing (/"A hi = 1 33. 1 ; P < 0.001 ). beak (F3.61
41.9; P < 0.001), and tarsus (F3.6l = 23.2; P <
0.001 ) differed, while mass of nestlings at 10. 1 1,
12, and 13 days did not (FS 6 1 = 0.7; P = 0.54).
Mean tarsus length did not differ between adults
and nestlings measured after 10 days of age
(Fi.,26 = 0.3; P = 0.61; n = 128).
We measured 38 adults (21 females and 17
males) (Table 3), There were no significant
differences in morphological measurements be¬
tween males and females (F 5,30 = 2.4, P =
0.064). No difference was detected in body mass
(f , ,fi = 0.004; P = 0.95), tarsus length (Fu6 =
0.1; P = 0.78). tail length
w'ere described >130 years ago (Sclater and
Salvin 1879). However, little is known about
other aspects of their breeding biology (Webster
1992, Ochoa and Cuervo 1998. Jaramillo and
Burke 1999). This information should serve as a
basis for understanding the intrinsic biologic d
traits involved in differential fates of populations
to disturbance (i.e., to thrive or decline to local
extinctions), and for informing conservation
strategies. Our objective was to examine the
breeding biology and behavior of Red-bellied
Grackles in a suburban landscape in northwestern
Colombia.
METHODS
Breeding groups of Red-bellied Grackles were
observed at Alto San Miguel, along the upper
538
Ocampo et al. • BREEDING BIOLOGY OF HYPO PYRRHUS
539
FIG. 1. (A) The Alto San Miguel in the nonhem central
Andes. Depanment of Antioquia. Colombia (06 02' 05" N.
75 36' 58" W). (B) Aerial photograph depicting the end¬
points of our 2-km transect along the upper Medellin River
at Alto San Miguel where seven groups of Red-bellied
Grackles (Hypopyrrhus pyrohypogaster) were nesting co¬
operatively for at least 4 consecutive years (2006-2009).
watershed of the Medellin River in the northern
central cordillera of the Andes, Department of
Antioquia. Colombia (Fig. 1 ). The region is in the
lower montane wet forest’ life zone at an
elevation of 1,800 to 2,100 m: the mean annual
temperature and precipitation is 16 C and
TOGO mm, respectively (Espinal 1992). The upper
watershed of the Medellin River has a long history
°l human disturbance due to the influence of
'mall urban settlements and conversion of forest
pastures for cattle ranching and for forest
plantations. The current landscape is dominated
hv second growth, pastures with isolated trees,
semi-open areas at different stages of succession,
and Eucalyptus and pine (Pinas panda) planta¬
ins. Patches of native montane forest remain in
'he upper hills and the Alto San Miguel Nature
Reserve. Red-bellied Grackles have been ob¬
served nesting at this location since at least
'999 (AMC, pers. obs.). We describe the nests
and behaviors of seven groups observed along the
river.
We followed individuals along a 2-km transect
tr°m January through July 2006—2009 along the
Medellin River that exhibited nesting or parental
behavior and searched for nests and nesting
groups following Martin and Geupel (1993). We
recorded nest stage (under construction, incuba-
hon. nestling, or inactive), the species of tree or
shrub, and height for each nest. We measured
nests whenever possible (inner and external
diameters, depth, and height) after nestlings
Hedged or nests were depredated, and eggs
(length, width, fresh mass at day 0); we weighed
eggs every 2 days for one nest to estimate mass
loss rate during incubation. We measured nest¬
lings' body mass every day until they fledged, and
estimated nestling growth rate following Martin
et al. (2011) using the logistic growth curve based
on the equation: W (t) = A/( 1 + e 1 K<" w'here
W(i) denotes body mass of a nestling at time /. A is
the asymptotic mass that nestlings approach, f, is
the inflection point of the curve, and K is a
constant scaling rale of growth (Ricklefs 1967.
Ricklefs 1968. Rentes and Martin 2002). All
measurements were taken on site w ith an accuracy
of 0.05 g (FlipScale F2 ) for mass and 0.1 mm for
external measurements with a caliper.
We monitored nests every 1 to 3 days during
incubation, or until the last egg in the clutch
hatched, and during the nestling period from
clutch hatching until nestlings fledged. Every
monitored nest was observed for 1 hr in the
mornings within the 0900-1100 hrs period, and
from distances > 1 5 m. We recorded brooding
behavior, nest attentiveness (proportion of time
adults were on the nest over total time of
observation), provisioning rate (food deliveries/
hr), and type of food items (c.g., arthropods, fruits
and flower parts, and small vertebrates) given to
nestlings by direct observation. We estimated the
proportion of eggs that hatched (hatching success)
and the proportion of young that fledged (fledg¬
ling success) based on observations of 21 nests.
We calculated daily survival rate and nesting
success using the Mayfield estimator (Mayfield
1961), but used exposure days in incubation and
nestling periods combined because we did not
have information on the exact hatching day for a
number of clutches. We assumed nestlings
Hedged successfully when nests were empty and
Hedglings remained in the group territory'. We
observed the first and subsequent hatchings of the
clutch of two nests allowing us to ascertain if all
eggs of the clutch hatched synchronously (within
a 24-hr period).
Size. age. and gender (M/Ft composition of
each breeding group was based on counts of the
number of adult and immature individuals. Adults
were recognized by their scarlet bellies and shiny
black plumage, and their bicolored irides (pale
yellow with a bright red outer margin). First-year
birds were recognized by their pale red belly, dull
540
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124. No. 3. September 2012
brownish-black plumage, and dark brown to
grayish-yellow irides. Adults were classified as
males or females in the field from behavioral
differences and the larger size of males (135 vs.
97 g in body mass; AMC, unpubl. data); (~30 vs.
27 cm total length) (Hilty and Brown 1986).
However, gender of first-year birds could not be
identified in the field. We marked captured birds
with two plastic color bands to identify individ¬
uals, one colored band to recognize breeding
group and the other, individuals in the group. All
fledglings front five nests were banded to examine
if first-year birds act as helpers in the next
breeding season and if they remain in natal
groups. We used a general linear mixed model
(GLMM) to examine the variation in clutch size
as a function of group size where we specified
group identity as a random -effect variable. We
had 18 observations from six groups. We used the
glmmPQL function implemented in the R package
MASS to lit the GLMM (Venables and Ripley
2002). This function used pseudo- and penalized
quasi-likelihood to estimate the parameters of the
model (Bolker et al. 2009), Values are presented
as means ± SD.
RESULTS
Most breeding events occurred from March to
June (it = 35). All seven breeding groups located
every year exhibited a cooperative breeding
system. Groups varied in size from three to seven
individuals in each breeding event (5 ± 1.3, // =
27), not including nestlings, and also varied by
gender and age class composition (e.g.. 1-2 adult
males. 1-3 adult females, and 1—3 first-year birds
or subadults). We observed two adult males (by
size) in one breeding event; one was much more
active vocalizing from a high perch and delivering
vocalizations that have solely been observed for
dominant males, suggesting primary and second¬
ary males in that group. Individual colored bands
placed on 13 nestlings in live nests indicated
breeding groups raise the helpers of the following
years, and that groups have high fidelity to
breeding territories across years. Nine of 13
marked fledglings remained in their group and
spatial territory for at least 2 consecutive years.
We did not re-encounter the remaining four
fledglings and they may have been depredated
or dispersed to another area.
Nests. We found 38 nests attended by seven
groups. Nests averaged 4.6 ± 2. 1 m above ground
(it - 34). but four were at a height of 15 m. Most
were on bifurcations of lateral branches of a
variety of trees or tall shrubs of 1 1 species in
Clusiaceae, Melastomataceae. Monimiaccac, Ru-
taeeae. Solanaceae, and Tiliaceae. Introduced
trees including Eucalyptus camaldulesis (Mynu-
ceae). Finns pa tula (Pinaceae). and Cupresm
lusitanica (Cuprcssaceae) were also used for
nesting. Nests were in trees and tall shrubs at
the edge of forest fragments (;i = 16), or in
isolated trees in pastures at a mean distance of
12.5 m (range = 5-81 m, n = 22) from the nearest
forest edge. The mean distance of nests to the
river edge was 13.8 m (range = 0-66 m. n = 3U
Nests of Red-bellied Gracklcs were ovoid
open-cup structures of two layers of sticks and
roots that had different diameters (internal layer -
0.5 t 0.2 mm. n - 85 items; external layer: 1.0 1
0.3 mm. n = 75 items; n = 3 nests), Nests went
lined with dry leaves. There appeared to be little
variation in materials used, although one group
added an extra external layer of an epiphyte
( Tillaiidsia usneoides , Brotneliaceae). Mean mea¬
surements were based on a subset of eight nests:
inside cup depth = 77 ± 14 mm, outside cup
depth = 155 ± 22 mm. inside opening = 103 ± 1
X 1 12 ± 8 mm, outside opening = 152 ± 15 8
182 ± 24 mm. We observed construction of only
one nest, and this nest was completed between 4
and 8 days; we only observed one adult female
building it. Nest materials were collected in the
surrounding area (<100 nr) by the female and
other members of the group, which also supplied
her with food. We did not quantify the rate of
delivery of nest materials or food items to the
female. The male did not participate actively in
construction of this nest.
Eggs ami Clutch Size. — Eggs were elliptical in
shape and light blue in color with purplish brown
spots and stripes that w'ere denser towards the
w ider end (Fig. 2). Fresh egg mass averaged 7J)
± 0.3 g (n = 12, from 4 nests), and their external
measurements averaged 28.8 ± 1.0 mm X 21.0 -
0.4 mm (/? = 35. from 1 1 nests ). Females laid one
egg per day. and clutch size averaged 3.1 - O '
(range - 2-4. from 2 1 nests). Breeding group size
and clutch size were positively correlated (slope
= 0.25 ± 0.09 (SE). P = 0.03).
Incubation Period. — Incubation periods lasted
16 ± 1 days (15. 15, 17 days, respectively; n = 31-
Eggs lost up to 1 1 .9% of their weight during this
period at a rate of 0.07 ± 0.0 1 g per day (R:
0.92. n = 4; Fig. 3). Nest attentiveness averaged
69 ± 18% during incubation of the total
Ocampo et al. • BREEDING BIOLOGY OF HYPOPYRRHUS
541
FIG. 2. Nest, eggs, and hatchling of Red-bellied Grackles at Alto San Miguel. Photograph by M. Camila Estrada-F.
FIG. 3. Egg mass loss during the incubation period for four eggs in one nest of the Red-bellied Grackle. Lines connect
to'y weight loss values for each individual egg.
542
THE WILSON JOURNAL OF ORNITHOLOGY • Vo/. 124, No. 3. September 2012
2 4 6 8 10 12 14 16 18
Nestlings age (days)
FIG. 4. Mean ± SD body mass of Red-bellied Grackle nestlings during development at the nest (« = 1 1 . from 4 nests),
the gray line shows the logistie growth curve (R2 = 0.98) based on the equation W(r) = A/(l + e
observation time tor the three nests monitored
from egg laying to hatching (37 hrs). The indi¬
vidual incubating the eggs was a female, which
was fed an average of 1.9 ± 1. 1 times/hr (n = 3
nests) by other members of the group during 41 hrs
of observations (data from 12 of the 14 days of
the incubation period). The incubating duties on
the nest were alternated between females (/? = 3
events), and were followed by a provisioning
event. We directly observed all eggs hatch at two
nests, both with a clutch si/e of four eggs and. in
all cases, the entire clutch hatched within 24 hrs.
Adult males did not participate in brooding but
remained perched in the surrounding trees, often
vocalizing.
Nestlings. The nestling period was 17.3 ±
1.3 days (n = 5). Nestlings weighed 5.2 ± 0.7 g (/;
= 5, from 2 nests) at hatching. Nestlings had light
orange skin, black downy feathers, while claws, a
whitish bill with a darker lip. and a bright yellow
gape (Fig. 2). Nestling growth rate (AT was 0.304
0? = 1 1 from 4 nests; Fig. 4). These 12 nestlings
opened their eyes on the sixth or seventh day. The
eyes were dark brown, and the bill was black at this
point. Nestlings were covered hy a dull black
plumage by day 1 5 except in the naked area around
the eyes, and on the lower breast and belly where
the feathers were reddish orange. Nestlings were
active at that age and able to exercise their wings
and perch by themselves. Nestlings fledged when
16 to 18 days ot age with a mean mass of 76.3 ±
10.1 g (n - 4 from 2 nests), Their flight ability was
limited, the tail was <50% of full length, and flight
feathers were still growing. Fledglings continued to
be led by members of the group.
Eight fledglings were still fed by the group
2 weeks after leaving nests, their tails were sail
growing, and their overall plumage was brownish
black with orange or dull red bellies. Ten fledg¬
lings —6 wrecks of age u'ere able to forage more nr
less independently along with the group and were
clearly distinguishable from older birds. Six
juveniles still had dull plumages after 12 months
but they had dark-yellow irides. were similar in
size to subadults and females, and started to
participate as helpers in the group (observations
from 4 breeding groups). Individuals (n = 4) at
22 months of age, and probably after completing a
second molt, had bicolored irides and reached the
plumage brightness and coloration of adults, and
continued to serve as helpers in their group.
The brooding adult remained the first 5 days of
the nestling period at the nest (n = 3: Fig. 5) ano
was ted by helpers, during which time the
provisioning rate of the nestlings averaged I5-S
visits/hr (55 hrs of observation: Fig. 5). Sonic
food was delivered by regurgitation (n = 4 -
groups) but, after the fifth day, it was progres¬
sively passed from helpers to nestlings as parts
whole items. Helpers occasionally passed looti
items to the brooding individual at the nest that n
turn delivered food to nestlings. Provisioning
young decreased gradually within the last
days of the nestling period (Fig. 5). We identified
450 prey items during 95 hrs of observations at
three nests. The nestlings’ diet consisted mainly o(
arthropods (72%. n = 353), fruits and flower parts
of melastome ( Tibouchina lepidota, 9.4%. ”
44). and small vertebrates (3 unidentified frogs-
and 4 An olis maria rum lizards). Provisioning
Ocampo el al • BREEDING BIOLOGY OF HYPOPYRRHUS
543
45
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16
Time (days)
FIG. 5. Nest attentiveness of helpers during the nestling period of the Red-bellied Crackle depicted as the hourly
provisioning frequency to nestlings (gray) and to brooding frequency (black i. Data are from two breeding events.
mostly by immature helpers and females (94%)
and less by adult males (6%). based on 627 visits
at three nests.
Fledgling Survival. —The daily survival rate
was 0.97 and nesting success was 0.39 in = 24
nests), hatching success was 92%, and 86% of
'hesc nests were depredated during the nestling
period. The cumulative fledgling survival over
tour breeding seasons (2006-2009) was 29%.
corresponding to 19 fledglings (from X nests) from
^ eggs laid (21 total nests) that ultimately
integrated into their family groups. Nests were
also lost to harsh environmental events such as
heavy rainstorms or to unknown factors. All
groups that lost their nest reinitiated breeding
during the same season, and there were three
double-brooding events in 2010 (unpubl. data).
DISCUSSION
Red-bellied Graekles exhibited a cooperative
breeding system with juveniles staying in natal
territories and assisting with subsequent breeding
df°rts of their family group. Nest construction,
brooding, and nestling care was mostly by females
and young helpers, while adult males remained in
'he territory often vocalizing, which we interpret
as involved in social cohesion and defense.
Cooperative breeding at Alto San Miguel is
consistent with previous casual encounters with
nesting groups of Red-bellied Crackles not only at
this study site, but elsewhere across its disjunct,
restricted range where nests were also attended by
three or more individuals (Ochoa and Cuervo
1998, Cuervo 2002; J. J. Leon and S. Vargas
Troncoso, pers. comm,). We demonstrated by
color-banding juveniles, that they become helpers
at the nest (Skuteh 1935) of their own family
group in subsequent years. However, behavioral
and genetic studies are needed to understand
juvenile dispersal and kin structure in this
population. Family groups in the disturbed
landscape of Alto San Miguel were cohesive
throughout the year, but this may not be the case
in populations from less disturbed habitats where
large flocks arc observed outside the breeding
season (AMC. pers. obs.). Unknown social
interactions and the ecological conditions ot
undisturbed habitats could be involved in fusion
and division of groups during non-breeding and
breeding seasons, respectively.
The breeding activity of Red-bellied Graekles
in our study area was concentrated between
March and June, which agrees with previous
anecdotal information of breeding in this species
(Hilty and Brown 1986. Ochoa and Cuervo 1998.
Jaramillo and Burke 1999), We did not detect any
indication of breeding during four visits to the
same transect from August to December.
The nests and eggs of the Red-bellied Gracklc
described here match the illustrations and
544
THE WILSON JOURNAL OF ORNITHOLOGY • Voi 124. No. 3. September 2012
descriptions by Sclater and Salvin (1879) and
Ochoa and Cuervo ( 1998), although we found one
group that consistently built its nests with an outer
layer of an epiphyte. The closest relatives of the
Red-bellied Grackle are the Oriole Blackbird
(Gymnomystax mexicanus) and the Velvet-fronted
Grackle ( Lamp r ops a r ranagrinus) (Cadena
et al. 2004, Eaton 2006). The bulky cup nest of
the Red-bellied Grackle is more similar to the
nest of the Oriole Blackbird (Jaramillo and Burke
1999) but not to the hanging basket nest of the
Velvet-fronted Grackle (Maillard and Herrera
2007). Egg coloration (but not size) is similar
among (he three species, all having pale blue or
greenish eggs with dark brown or purplish spots
(Skutch 1967. Maillard and Herrera 2007).
Cooperative breeding likely evolved indepen¬
dently in the Icteridae. but is most pervasive in
South American species of g cackles (Orians el al.
1977, Jaramillo and Burke 1999. Fraga 2008). The
Oriole Blackbird, among Red-bellied Grackle
relatives, is a solitary breeder (Jaramillo and
Burke 1999) and the Velvet -fronted Grackle has
apparently been observed breeding cooperatively
(J. A. Tobias cited by Fraga 2008), but published
information is inconclusive (Jaramillo and Burke
1999, Maillard and Herrera 2007). The scarcity of
breeding ecology data and missing taxa in the
phylogenv of the Icteridae make unclear if
occurrence of cooperative breeding in the Red-
bellied Grackle is phylogenetieally or ecologically
constrained. Observation of solitary breeding
individuals of Red-bellied Grackles (Hilly and
Brown 1986) reported prior to our study, if true,
would imply either plasticity or temporal or
geographic variation in breeding strategies. We
suspect those reports resulted from incomplete
observations. Recently, helpers attending a nest of
Red-bellied Grackles have been observed in Huila
in the southern part of its range (J. J. Leon and S.
Vargas Troncoso. pers. comm.).
Nest attentiveness across the incubation period
was variable, similar to that reported for other
neotropical montane birds (Martin et al. 2007).
The weight loss of eggs during incubation
(11.9%) is surprisingly small in comparison to
the —18% loss documented for 475 species (Rahn
and Ar 1974) or the known estimates for other
neotropical birds iut
personal funds. We thank Idea Wild, Optics for the Tropics,
and G. J. Colorado for providing field equipment. Plant
material was identified by F. J. Roldan (Herbarium
Universidad de Aniioquiu. Medellin. Colombia). "c
appreciate the effort of all the people that helped us a*
Ocampo et al. • BREEDING BIOLOGY OF HYPO PYRRHUS
545
Geld assistants especially T. Hinestroza Koppel and D.
Sanchez Duque. J. L Parra. A. D. Perez, and G. J. Colorado
kindly provided advice on analyses. We thank CORAN-
TIOQL'IA. Reserva Alto San Miguel. C. F. Londono. and
especially, the La Clara community for allowing us to work
in the area. W. H. Weber for access to his library, and J. J.
Leon and S. Vargas Troncoso for shitting their observa¬
tions. C. D. Cadena. R. M. Fraga. T. E. Martin, J, V.
Rcmscn. Gary Ritchison. R. S. ferrill. C. L. Braun, and four
anonymous reviewers provided insightful comments that
improved our manuscript.
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The Wilson Journal of Ornithology 1 24( 3 ): 547—557 , 2012
NESTING BIOLOGY OF THE YELLOW-OLIVE FLATBILL
(TYRANNIDAE. ELANINAE) IN ATLANTIC FOREST FRAGMENTS
IN BRAZIL
MARINA ANCIAES,' 43 THAIS MAYA AGUILAR,' LEMUEL OL1VIO LEITE,2,3 RENATA
DORNELAS ANDRADE,1 AND MIGUEL ANGELO MARINE
ABSTRACT. — The Yellow-olive Fiatbill (Tolmomyias sulphurescens) is a small insectivorous passerine inhabiting
Ncoiropic forests. Us breeding biology is poorly know n despite its abundance and conspicuousness. We describe the nesting
biology of Yellow-olive Flatbills from Atlantic Forest fragments in Belo liori/ontc County. Minas Gerais State,
southeastern Brazil. Eighty nests were monitored every 2-5 days from August to January between 1995 and 2000. Active
nests were found front mid-September through late December with a peak from mid October through late November. First
dutches were usually laid during the first rains, but prior to the main peak in annual rainfall- The Yellow-olive Fiatbill
builds closed, pencile nests oil tree branches along streams or rouds. principally of dark fungal ( Marastnius sp.) fibers.
Clutch size ranged from two to four white eggs. Incubation was irregular and hatching was asynchronous. Incubation and
nestling periods were 20 and 23 days, respeem cly . Nesting success across all 5 y ears w as 29- r ( i nean among years — 31%,
Cl 25-37%). and nest predation was the main cause of nest failure (49% I. Mayfield estimates of nest survival were low
i mean = 26%. Cl = 17-36%). and the probability ol an egg to produce a fledgling was only 10%. Fledging success was
0.8 fledglings per breeding pair, and chicks fledged at 107% (Cl = 106-108%) of mean adult body mass. Our results do not
'upport the purported pattern of long breeding seasons for tropical birds. The Yellow-olive Fiatbill laid unusually large
clutches, had lower nest survival, and greater fledgling productivity compared with other tropical passerines. Received 26
April 2009. Accepted 23 March 2012.
Studies of avian nesting biology are crucial for
understanding many concepts in population biol¬
ogy. are relevant to evolutionary theory, and have
many applications in conservation biology (Reed
ei al. 1998, Duca et ul. 2009). Most studies of
avian reproduction focus on temperate species
(Stutchbury and Morton 2001). and studies on the
reproductive ecology of tropical passerines are
fewer (but see Marini 1992; Marini et al. 1997;
Aguilar et al. 1999, 2000; Almeida and Macedo
-901; Marini and Duraes 2001; Aguilar and
Marini 2007; Duca and Marini 2004. 2005; Marini
al. 2007). Nest architecture, brood size, and
incubation time are all life history baits that
impact individual fitness, and are subject to
''election from environmental conditions such as
Curso de Pos-Graduayiio cm Ecologia. Conservayao e
Manejo da Vida Silvestre, t'FMG. Belo Horizonte, MG
30161-970 Brasil.
Departinento de Zoologia. 1CB, L'niversidadc de
Brasilia. Brasilia. DF 70910-900 Brasil.
Centro de Cicncias bioldgicas e da Saude. I niversidade
Federal dc Montes Glares, Montes Cluros. MG 39401-089
Brasil
; Current address: Coordenayao de Biodiversidade e
Programa de Coleyoes c Aeervos Cientificos. Instituto
National dc Pesquisas da Ama/6nia-!NPA. Avenida Andre
Araujo. 2936. Aleixo. Manaus. AM 69011-970 CP 478
Brasil.
'Corresponding author;
e-mai I : marina. anciaes @ gmai 1 .com
food availability and predation (Mason 1985).
Accumulating results on the breeding biology of
tropical birds is crucial for testing hypotheses
about the evolution of breeding strategies and the
selective forces acting on populations nesting in
different environments. For example, breeding
cycles are influenced by changes in light levels
and precipitation (Hau ct al. 2008, Wikelski el al.
2008). Furthermore, few studies provide detailed
information about the breeding biology of species
based on large sample sizes, and frequently lack
sufficient evidence for hypothesis testing (re¬
viewed by Ricklefs 2000).
The Yellow-olive Fiatbill (Tolmomyias sul-
plntrescem) is a common suboscine inhabiting
neotropical forests throughout Central and South
America (Ridgely and Tudor 1994). Virtually no
information is available on its breeding biology,
despite being relatively ubiquitous. The few data
reported in the literature indicate the species lays
an utypicallv large clutch for tropical passerines
(3-4 eggs) (Sick 1997). Yom-Tov et al. (1994)
reported an average clutch size of 2.7 for tyrant
flycatchers in the tropics, and most species of
tropical passerines lay only two eggs in contrast to
the larger clutches of temperate species (Ricklefs
1969. Stutchbury and Morton 2001 ). The Yellow-
olive Fiatbill offers an exceptional opportunity for
testing theories about evolution ol life history
traits in tropical systems.
547
548
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 3. Sept ember 2012
The Yellow-olive Flatbill in Brazil occupies,
but is not restricted to. threatened habitats such as
Atlantic Forest fragments and gallery forests of
the Cerrado, both within highly disturbed biomes.
Forest fragmentation may affect breeding success
through increased brood parasitism and nest
predation, reducing bird numbers in fragmented
landscapes (Wilcove 1985. Temple and Cary
1988. Robinson 1989. Marini 1997, Tewksbury
et al. 2006). The "V ellow-olive Flatbill represents a
model lor studies addressing the effects of habitat
fragmentation on nesting success and. ultimately,
population viability in these fragmented systems
(e.g.. Duca et al. 2009).
We describe the nesting biology of the Yellow-
olive Matbill in Atlantic Forest fragments in
Minas Gerais. Braz.il. We report morphometric
measurements ot eggs, nestlings, and nests; nest¬
ing seasonality, and duration of breeding cycles
between 1996 and 2000; and estimated egg fail¬
ure, fledgling productivity, and overall survival
rates for the study period.
METHODS
Study Area. This study was conducted in the
protected areas of the Barreiro and Mutuca
reserves, owned by Minas Gerais Water Company
(COPASA MG). The reserve system is in the
municipalities of Nova Lima and Belo Horizonte
Minas Gerais State. Brazil (20 02'-20 00' S. 42
59'-44 00' W). We searched for and monitored
nests in one 50-ha and one 200-ha forest fragment
at Barreiro Reserve each year from 1996 to 2000
during July through January. We searched for and
monitored nests in 1996 in a 300-ha forest frag¬
ment at Mutuca Reserve. Both reserves contain a
combination ol dry, semi -deciduous, and gallery
forests which are secondary growth with succes-
sional stages varying between 90 and 150 years
(CETEC 199.3). These three forest fragments
represent the only forest habitat available in the
reserves, and they were included in the study.
Trails within the reserves were chosen randomly
and we also searched for and monitored nests
along the main river courses within the forests.
This region is subject to warm, rainy summers and
cool, dry' winters with most precipitation between
November and March. Annual precipitation varied
studv Th ( ^ IO mm (,997) durin£ °ur
; u'T""" teniPera,ure recorded was 9 C
and 1 9 )7) and the maximum was 37 C ( 1 997)
(Mutuca and Fechos climatic stations, managed by
MBR-Minerafocs Brasileiras Reunidas and CO¬
PASA MG, respectively).
/Vest Monitoring. Nest searches began in Juh
and were conducted systematically every 3-5 daw
along rivers, roadbeds, and in the forest interior.
We marked locations of nests with pink plastic
Hugging 5-10 m from the nest and checked nest
status every 3-5 days. We counted eggs and/or
nestlings during each visit, weighed them with a
0.1 or ().2-g spring dynamometer, and measured
them with 0.05-mm precision calipers. We
measured nests with calipers after nests were
considered inactive.
We considered a nest successful when at least
one nestling left the nest. Monitored nests found
empty alter the maximum known age for nestlings
to Hedge, and did not have signs of structural
damage caused by predation were considered
successlul. These nests were successful at the
prior visit and lacked common evidence of pre¬
dation (leathers, partial nest destruction), and wc
assumed they produced fledglings. Nests found
empty prior to predicted fledge dates, as well as
those with evidence of predation such as feathers
or damage to the nest structure, were considered
depredated. Nests w'ere considered abandoned
when eggs remained intact in the nest for longer
than the incubation period. Nests with dead
nestlings without any signs of aggression were
also considered abandoned. Nests abandoned
belore eggs were laid were not considered in
analyses of reproductive success.
Nestling Growth and Productivity. — Growth
curves lor nestlings were plotted using logistic
regression (Ricklefs 1976. Zullingeret al. 1984):
M(t) — A(e-k " " + l)~f, where A = asymptote
(mass. wing, tail, tarsus or bill), t = age (days), k
= growth rate constant (days-1), and / = age al
the inflection poim (days). We calculated egg
volumes using Hoyt's (1979) equation: volume =
0.51 X (length) X (breadth)-. We divided the total
number of nestlings by the total number of egg>
laid to calculate hatching rate. Morphological
parameters ot eggs and fledglings are presented as
means t. SB. We estimated productivity from the
ratio between total number of fledglings and total
number of broods.
Statistical Analyses. — We followed Mayfield
(1961. 1975) and Manolis et al. (2000). Alterna¬
tive nest survivorship estimation methods have
recently been proposed, but we used the Mayfield
method because it has proven as useful as other
indices when sample siz.es are large (n > 25) and
Anciaes et al • NESTING OF YELLOW-OLIVE FLATBILLS
549
TABLE 1 Nesting parameters of monitored nests of Yellow-olive Flatbills during .lie incubation and nestling phases
and over the entire nesting period. Survival probability was estimated by .he Mayfield method. Values tor datly survival
plabTmy of aurvival through phase (PSP,, and standard deviu.ions are used ,o compare
survivorship between phases.
Nest pture or comem
Momiored nests
or cement
Exposure men. eggs,
nesilings-davs)
Duration (days)
Lost nests
or content
DSP ± SD
PSP = SD
Incubation
Nestlings
Totals
Eggs
Nestlings
Totals
63
53
80
267
121
388
939
735
1.444
2.720
1,189
3.909
20.09 ± 0.43
23.43 ± 0.68
43.29 ± 1.08
20.09 :± 0.43
23.43 ± 0.68
43.29 ± 1 .08
29
23
52
95
79
174
0.97 ± 0.01
0.97 ± 0.01
0.98
0.96 ± 0.01
0.93 ± 0.01
0.95 ± 0.02
0.53 ± 0.32
0.49 ±0.17
0.26 ± 0.21
0.49 ±0.15
0.20 ±0.12
0.13 ± 0.07
the interval between visits is small (Jehle et al.
2004. Nur et al. 2004). We estimated confidence
intervals for survival probabilities tollowing
Hensler and Nichols (1981) and Mason (1985)
lo compare nest success between egg and nestling
periods: these values were compared to a normal
distribution. We calculated the absolute (naive)
survival of monitored nests as the percentage ol
successful nests through each nest period ( 1 minus
the proportion of lost nests during each nest
period X 100).
RESULTS
Nests.— We found 103 nests and monitored 73;
13 were inactive nests from previous breeding
seasons and 17 were active, but >7 m in height,
making them too high to be monitored. We were
unable to ascertain the final fate of 10 ol the 73
nests monitored, and these were excluded from
the analyses. Seventeen nests were reused within
the same breeding cycle, resulting in 80 active
nests monitored when reuse was considered, and
63 unique nests (Table 1 ). Nests were similar in
structure and material composition. All were
closed, hanging nests with a short (4-7 cm. n =
2> tunnel entrance, constructed predominately
trom dark fibrous fungi of the genus Marasmius
'Fig. 1). Nests were suspended from thin tree
branches usually hanging over streams (n — 59.
94%); nests were also found hanging over diit
roads (n = 4). in the forest interior (n = 1 ) or on a
ravine of the main river in the study area (n — 1 )•
Mean ± SE nest height was 3.1 — 0.1 m (n = 67).
External nest dimensions were: 18.4 — 2.6 cm (n —
9) in height and 9.8 ± 0.5 cm in = 9) in width. Nest
entrances were 5.3 ± 0.2 cm wide (n = 4), and egg
balls were 9.5 and 12.5 cm (n = 2) deep.
Breeding Phenology.— The reproductive season
of the Yellow-olive Flatbill began with the start of
the rainy season. We found active nests from mid
September through late December with a peak
between mid October and late November coin¬
ciding with the first rains, and another peak before
the start of the heavy rains in late December. Nest
activity also coincided with a subtle increase in
photoperiod (Fig. 2). First clutches were laid just
FIG. 1 . Nest of the Yellow-olive Flatbill hanging from
a tree branch over the main stream on the Barreiro Reserve.
Photograph by Paulo Cordeiro. 23 December 1996.
550
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124. No. 3. September 2012
>
V)
m
u
o
o
#
TJ
O
k_
01
CL
O
S
SZ
CL
■D
C
ro
.C
V)
*->
V)
01
C
a
'o
oj
Month
FIG. 2. Nesting activity ot Yellow-olive Fluthills, and average monthly precipitation and
1995 and January 2000 in the Barreiro Reserve, Belo Horizonte, Brazil.
photoperiod between July
after the first rains in 4 of the 5 years but, first
clutches in 1997 coincided with the onset of the
seasonal rains. Dry seasons varied in length from
2 to 3.5 months, but this variation did not seem to
aflect the start of reproduction. Reproduction in
2 years (1996 and 1997) was more synchronous
among individuals (Fig. 3).
Clutches and Eggs.— The Yellow-olive Flatbill
laid three (« - 27. 47%) or four (/? = 28. 48%)
eggs, more rarely two (n = 3. 5%) (mean ± SE =
3.4 ± 0.1. n = 58). Eggs were apparently laid
every other day. as laying of a four-egg clutch
took 7-8 days. Most eggs were immaculate, but
one clutch of three had brown spots on the larger
end. Eggs weighed 2.57 ± 0.05 g (n = 28 j and
were 21.9 ± 0.4 mm [n = 30) long by 15.2 ±
0.2 mm (// = 30) wide with a mean volume of
2.57 ± 0.06 cm’ (n = 30).
Incubation Period. — Incubation presented ir¬
regular rhythm delay, starling before ihe clutch
was complete, and hatching was asynchronous.
We observed only one individual incubating the
eggs. The attending adult would leave the nest
when we approached and perch silently at least
10 m from the nest. Incubation lasted 20.1 ±
0.4 days (n =11) and ihe hatching rale was 0.81.
Both parents cared for the nestlings.
Brood Size and Nestling Growth. — Most suc¬
cessful nests produced two fledglings (17 of 29
nests that produced fledglings) with total fledgling
productivity of 0.8 fledglings per nest (consider¬
ing all breeding attempts by a breeding pair) and
one fledgling per breeding pair (considering only
successful attempts). Nestlings reached 50% of
their Hedging size in -5 days (tarsus) and 14 days
(tail ); chicks Hedged at an average of 107% (Cl =
106-108%) of mean adult body mass (Table 2.
Fig- 4).
Nestling Period. — The nestling phase was 23.4
— 0.7 days (n = 7). We observed one adult during
nest monitoring performing alarm calls while
perched 30 m from an active nest in the nestling
phase. This individual flew into the nest carry ing
an insect larva and. shortly thereafter, two adult
individuals left the nest.
Reproductive Success. — Overall raw nest suc¬
cess for the 5 years was 29% (mean among years =
31%. Cl - 25-37%). Nest predation was the main
cause of nest failure (49%). 7% of the nests were
abandoned, and 15% failed due to other causes.
Antilles el al • NESTING OF YELLOW-OLIVE FLATBILLS
551
Eggs laid
Precipitation
400
350
300
250
200
150
100
50
0
400 -p-
350 £
300
250 O
200 §
150 '9-
o
100 0)
50 °-
0
Month
FIG. 3. Frequency of eggs of Yellow-olive Flatbills laid and total monthly precipitation for 1995-2000 (A-E) in the
Barreiro Reserve. Belo Horizonte. Brazil.
such as storms, which would break tree branches
or cause small trees to fall. Estimated Mayfield
survival probability was 26% (Cl = 17-36%) and
'he probability of survival during incubation (53%)
was similar to that during the nestling period (49%)
(Z = 0.4. P = 0.29). The probability of an egg
producing a fledgling was 10%. There was a 49%
probability for partial egg loss during incubation
and 20% for partial nestling loss; these differences
were not significant (2 = I .8, IJ = 0.21; Table I >
based on 95% confidence intervals. Most causes of
nestling loss were not evaluated, as nestlings would
disappear before expected Hedging dates without
evidence of predators or signs of nestling or nest
destruction. Known causes of nestling losses were
nest falling and nest destruction due to rainfall or
other unknown factors. Yellow -olive Flatbills
apparently use old nests as cues for selecting nest
sites, and frequently built nests close to inactive
nests from previous years, which led to a small
increase in nest survival (MAM, unpubl. data).
DISCUSSION
The Yellow-olive Flatbill has a short breeding
season, similar to other passerines in southeastern
Brazil (Marini et al. 2007). The incubation period
552
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124. No. 3. September 2012
TABLE 2. Growth parameters for Yellow-olive Flatbill
fledglings based on the logistic equation: A = mean final
value. / = inflexion point or stabilizing age at 50% of final
value, and % Adult = percentage of A in relation to mean
adult size.
A
/ (days)
% Adult
Body mass (g)
17.1
8
107
Wing (mm)
47.1
12
Tail (mm)
26.7
14
Tarsus (mm)
19.0
5
Nostril (mm)
4.8
5
supports the relevance of annual precipitation
peaks in inducing nesting activity (Cody 1985,
Hau el al. 2008). Precipitation may affect insect
abundance (Tanaka and Tanaka 1982), and food
abundance has been shown to affect breeding
cycles in other tropical regions (Young 1994. Best
et al. 1996, Woodworth 1997: reviewed by
Stutchbury and Morton 2001).
The nests of the Yellow-olive Flatbill resemble
those of other species in the genus Tolniomni ;
from Suriname with the exceptions that eggs were
smaller, lighter in color, and usually lacked the
spotted pattern described for congeners (Ha-
was irregular in rhythm delay (terminology
reviewed in Wang and Beissinger 2011) and
hatching was asynchronous, Clutch size was
unusually large and survival rates were relatively
low for tyranninds or tropical passerines in
general (e.g.. Aguilar et al, 1999. 2000; Robinson
et al. 2000: Aguilar 2001; reviewed by Yom-Tov
et al. 1994). Our observed clutch sizes agree with
previous descriptions for the species in Brazil
(Sick 1997) and in southwestern Ecuador (H. F.
Greeney. pers. comm.), although other breeding
accounts for the species indicate clutch sizes are
usually only 2-3 eggs (reviewed by Jetz et al.
2008). A higher initial investment could represent
an opportunity lor increased reproductive success
in favorable seasons (Forbes 1991, Stienen and
Brenninkmeijer 2006). It is important to focus
further studies on sampling the temporal variation
in resource availability and abiotic conditions,
including precipitation and effects on survival
rates.
The hypothesis that breeding cycles are asea-
sonal in the tropics has been recently refuted, as
more climatic and reproductive data became
available (Hau et al. 2008). The common
association between breeding and annual precip¬
itation cycles may apply to tropical birds in
strongly seasonal environments, such as our study
population of Yellow-olive Flatbills. The marked
breeding seasonality of the Yellow-olive Flatbill
is similar to that observed for all tyrannids studied
in the sanie reserve system (Aguilar et al.
1999, 2000; Aguilar and Marini 2007). and is in
agreement with findings for other passerines in
southeast Brazil (Cavalcanti and Pimentel
988, Mann, 1992, Belton 1994. Picltorim et al.
QOO 2aSCOnCdos ami Lombardi 1996. Sick
997, Marini and Duraes 2001). The association
between nesting and precipitation observed
were more similar to those described for ihis
species Irom Colombia (Hilly and Brown 1986).
Eggs were laid at irregular intervals (i.e.. more
than 24 hrs apart j in the majority of nests in =
47), and were incubated for longer periods than in
regular egg-laying tyrannids, including Leptopo-
Ron omaurncephalus (Simon 1997. Aguilar and
Marini 2007). Pyrrhomyias citmwmmeus ( Collins
and Ryan 1995), Lathrotriccus euleri (Aguilar
el al. 1999), and Mionectes rufiventris (Aguilar
et al. 2000).
Hatching success (i.e., the probability of an egg
to produce a nestling) was higher than for several
passerine species reported in Ricklefs (1969). and
lor tyrannids studied by Aguilar ct al. (1999.
2000). Aguilar (2001). and Aguilar and Marini
(2007 1 in the same study areas. Eggs may fail if
hatch due to infertility (Davis 1958) or embryonic
death (Clemmons and Buchholz 1997. Yerkes 1998).
Other causes of egg loss may include infections,
nutritional deficit, and water loss (Jamieson el al.
1999). Causes of egg failure were not systemati¬
cally investigated in our study, although some
un hatched eggs did not have embryos, possibly a
sign of inbreeding due to low dispersal in thes
fragmented landscape. Other indicators of distur¬
bance caused by restricted gene flow in the area are
mutant phenotypes from other species (Anciaes
et al. 2005) and higher developmental instability in
forest fragments in the same region of the study
area (Anciaes and Marini 2000).
The present data suggests the high investment
in egg production is not related to low hatching
success in the species, but may reflect an
opportunity to increase fitness under favorable
abiotic (e.g.. rain) and biotic (e.g., food) condi¬
tions. Limits to the number of eggs laid seem to be
more affected by the capacity of parents to raise a
brood than energetic requirements to lay more
Anciaes et al. • NESTING OF YELLOW-OLIVE FLATBILLS
553
B
E
Age (days)
FIG. 4. Growth curves derived using the logistic model. (A) body mass. (B) wing. (C) tarsus. (D) tail, and (E) bill for
nestling Yellow-olive Flatbills.
eggs (Martin 1987). Alternative hypotheses for
large clutch sizes include increased adult mortal¬
ity and reduced predation risk associated with
short incubation periods, typical of northern
latitudes (Martin 1995. 2002). These hypotheses,
however, are directed at explaining breeding
differences between temperate and tropical re¬
gions in response to selective forces operating at a
554
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 3. September 2012
coarser scale than observed within one region.
The extended incubation and high nest predation
rates observed for Yellow-olive Flatbills suggests
predation risk per se is unlikely to explain the
observed large clutch size. There is also no
obvious reason to expect adult mortality to be
higher for this tropical species, which could
explain investment in larger clutches.
The nestling period of Yellow-olive Flatbills was
longer than for tyrunnids with synchronous nesting
cycles such as Lathrotriccus euleri (Aguilar et al.
1999), Mionectes rufiveniris (Aguilar et al. 2000).
or Leptopogon amaurocephalus (Aguilar 2001) in
the same area as die present study. Breeding pairs
of Yellow-olive Flatbills had more fledglings than
other tyrannids in our study area (Aguilar et al.
1999, 2000; Aguilar and Marini 2007). Fledglings
had similar body masses, but were heavier relative
to adult body mass than other synchronous breed¬
ing tyrannids (e.g., Pyrrhomxias cimamomeus,
Collins and Ryan 1995; L cimaurocephalus .
Aguilar 2001). Heavier body masses of Yellow-
olive Flatbills fledglings may reflect asynchronous
hatching in combination with the more synchro¬
nous fledgling events, which indicates older
fledglings remain longer in nests, being fed by
adults, at a low energy cost and accumulating body
mass. Broods with irregular laying and asynchro¬
nous hatching are usually larger and produce
smaller nestlings, as competition for food sets
the balance between brood and fledgling sizes
( Ragusa-Netto 1996. Stenning 1996). Our findings,
however, suggest food resources are likely not a
limiting factor for nestling growth in our study
area.
We observed nest provisioning only once, but it
was not possible to confirm if it was food transfer
to nestlings or mate feeding. Considering the nest
was in the nestling phase, and that two adults Hew
from the nest, it was possibly feeding nestlings, as
both parents usually provision nestlings in tyrannids
(Skutch 1960, 1967). However, the second adult
attending the nest may also receive and eat the
provisioned food instead of transferring it to the
nestlings (Hannelly and Greeney 2008).
Predation was the main cause of Yellow-olive
Flatbill nest failure and was equally likely during
incubation (53%) and nestling (49%) periods.
Similar predation rates were observed across 19
passerine species with closed nests (Oniki 1979,
Martin 1995) and, in Empidona.x oberholseri. nest
loss was as high as 72% of which 96% was due to
predation (Liebczeit and George 2002). The
species studied by Aguilar et al. (2000) and
Aguilar and Marini (2007) experienced higher
rates of nest predation during the nestling phase
than during incubation, possibly due to increased
parental activity at the nest site, which increased
attraction of predators during this phase (Rodri¬
gues and Crick 1997. Conway and Martin 2000.
Galhambor and Martin 2000).
The higher nest predation rates observed for
Yellow-olive Flatbills in comparison to other
tyrannids with closed nests likely resulted from
longer exposure of a larger and asynchronous
clutch, and higher activity levels at the nest site
caused by more nestlings. Evolutionary theory
would predict higher predation rates would act
to reduce exposure and broods (Martin 1993).
However, when opportunities to increase fitness
are used, leading to production of more chicks on
average, it may also increase predation probabil¬
ity. Increased clutch size and longer incubation
periods of Yellow-olive Flatbills suggest the cost
of increased exposure is overcome by fledgling
productivity in the studied population.
The overall survival of Yellow-olive Flatbill
nests was lower than reported for passerines in
temperate zones (Mayfield 1961, Sargent et al.
1997) in agreement with the well documented
pattern of higher predation rates in the tropics
(reviewed by Robinson et al. 2000; but see Martin
1996). This species also has the lowest nest
survival rate among studied tyrannids from the
study area. This observation is valid for spe¬
cies that build open nests ( Lathrotriccus euleri.
Aguilar et al. 1999) or closed nests (Mionectes
rufiveniris. Aguilar et al. 2000 and Leptopogon
cimaurocephalus, Aguilar and Marini 200'1).
Yellow-olive Flatbill nest survival probabilities
w ere similar to estimates of passerines common to
open areas ( Pyrocephalus rubious and Zonoiri-
chiti capensis. Mason 1985; Elaetiia chiriquensis
albi vertex, Medeiros and Marini 2007; Suiriri
affinis. Lopes and Marini 2005: Elaenia cristata
Marini et al. 2009), suggesting a possible effect ot
high exposure from nesting in sites relatively clear
of vegetation, such as rivers, streams, and dirt
roads, where Yellow-olive Flatbills nest. Nest site
selection is an important adaptive behavior as it
may influence individual fecundity, survivorship,
and breeding success as dense vegetation provides
better concealment from predators (Martin 1993,
1995; Howleu and Stutchbury 1996). Yellow-
olive Flatbills apparently use old nests as cues tor
Aticiaes el al. • NESTING OF YELLOW-OLIVE FLATBILLS
555
selecting nest sites, and frequently build nests
dose to inactive nests from previous years.
More research is required to understand which
mechanism, or failure of mechanisms, contributes
to the low nest survival we observed. The
increased fledgling productivity suggests a bal¬
ance between high predation rates and enlarged
clutch size in this species.
ACKNOWLEDGMENTS
We thank the National Council tor Scientific and
Technological Development iCNPq) for fellowships to the
authors. CNPq and FAPEMIG provided financial support
through grants to MAM. We are grateful to COPASA-MG
for authorization to study on their properties and to Charles
Duca. Fabiane Sebato. Juliana Gonqalvcs, Andrcssa
Bomfim. Paulo Cordeiro. and Marcos Maldonado-C'ocllio
for nest-monitoring efforts. Paulo Cordeiro kindly provided
the nest photograph. Catherine Bechtoldt. two anonymous
referees, and the editor provided valuable suggestions that
greatly improved the manuscript.
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The Wilson Journal of Ornithology 1 24(3):558-57 1 . 2012
SPECIES, FUNCTIONAL GROUPS, AND HABITAT PREFERENCES OF
BIRDS IN FIVE AGROFORESTRY CLASSES IN TABASCO, MEXICO
HANS VAN DER WAL, 1,3,5 BEATRIZ PENA-ALVAREZ,'
STEFAN L. ARRIAGA-WEISS,1 2 * * 5 AND SALVADOR HERNANDEZ-DAUMASj
ABSTRACT. — We studied species, functional groups, and habitat preferences of birds in live classes of agroforestry
systems: agroforests, animal agroforestry, linear agroforcsiry. sequential agroforeslry. and crops under tree cover in
Tabasco, Mexico. Sampling sites were >2 km from natural forest fragments. Observations were made at 38 sites using
30-min point and transect counts in the morning and afternoon in the rainy season, season ol northern winds, and dry season
Irom June 2(108 to May 2009. We observed 3,551 birds, which were assigned to 102 species: 72 were resident and 30 were
migratory species. Overall efficiency of sampling was 82.4% and varied from 68.7% in linear agroforestry to 81.5% in
animal agroforestry. Total species richness varied from 43 in sequential agroforestry to 64 in animal agroforestry Species
richness and Shannon diversity indices revealed no differences among agroforestry classes. Bird communities in animal
agroforestry, linear agroforcsiry. and sequential agroforestry had similar species compositions, as did agroforcsls and crops
under tree cover. Birds in all agroforestry classes were mainly forest generalists, although specialists of open areas were
common, particularly in animal and sequential agroforestry. Only one individual of a forest specialist species was observed
during sampling. Migrant species were mostly forest generalists, but some open area specialists occurred in animal
■igrolorestry. Resident birds were distributed over all foraging guilds in all agroforestry classes, whereas migrants were
mainly foliage-gleaning insecti votes, foraging guilds had different relative abundances among agroforestry classes.
Structural diversity ol agrolorestry classes did not seem to influence bird species richness, forest specialist species were
virtually absent in agroforestry classes, but the avifauna in agroforestry is diverse and valuable in itself. Received 9 Julv
2010. Accepted 7 March 2012.
Deforestation and biodiversity loss in recent
decades (FAO 2006) have increased attenlion
on the contribution of agroforestry systems to
conservation (Reitsma et al. 2001. Harvey et al.
2006. Harvey and Gonzalez- Villalobos 2007.
Bhagwat et al. 2008, Scales and Marsden 2008,
Najera and Simonetti 2010). Agroforestry systems
are primarily production oriented and combine
tree components with crops or animals (Nair
1985, Sinclair 1999. Torquebiau 2000). They
contribute to conservation by the inherent diver¬
sity of their components (trees, shrubs, crops, and
tended animals) and by hosting associated species
ol birds, invertebrates, reptiles, and mammals. The
inherent diversity of agroforestry systems is fre¬
quently limited to a few species (Lamb et al. 2005).
although home gardens (Kumar and Nair 2004.
Scales and Marsden 2008). shifting cultivation Helds
1 El Colegio de la Fronteru Stir. Dcpartamcnto de
Agroecologfa. Carretera Villahermasa-Ref'orma Km 15.5
sin ntimero. Ranchena Guineo 2“ Section. CYidigo Postal:
86283, Municipio Centro, Tabasco, Mexico,
* Universidad Juarez Autonoma de Tabasco, Avcnida
Universidad sin numero, Cddigo Postal: 86040. Municipio
Centro, Tabasco, Mexico.
’Forest and Nature Conservation Policy Group. Wagen-
ingen University and Research, Drocvendaalsesteeg 3. 6708
PB Wageningen, The Netherlands,
Deceased.
5 Corresponding author; e-mail: hvanderwal@ecosur.mx
(Romero- Romero et al. 2000), and plantations of
coffee ( Coffea arahicu and C. robusta) (Soto-Pinlu
et al. 2000), cacao ( Theobroma cacao) (Oke and
Odebiyi 2007), and chamaedorea palms (Cluunae-
darea spp.) (Granados el al. 2004) maintain plan!
biodiversity.
Associated biodiversity has been studied in
several agroforestry systems (Harvey et al. 2006.
Beukema et al. 2007, Gordon et al. 2007).
Diversity of land cover in the landscape favors
species richness, as the composition of bird
communities varies among cover types. Species
richness of birds had a positive correlation with
species richness of tree cover in a study in
Nicaragua (Harvey et al. 2006). However, Lawton
et al. (1998) and Beukema et al. (2007) recom¬
mend caution in supposing species richness of one
taxon shows positive correlation with species
richness in other taxa. A larger number of tree
species in agroforestry systems does not neces¬
sarily imply larger species numbers of birds,
invertebrates, or other groups.
Structural diversity of agroforestry systems is
frequently considered a biodiversity catalyst.
Gordon cl al. (2007) found a positive correlation
between height of the canopy, cover by shade
trees, and percentage of epiphyte- bearing trees in
coffee plantations and species richness of birds
with a preference for forest habitats (generalists
and specialists). However, the variables studied
558
yonder Wal et al. • AVIFAUNA IN AGROFORESTRY IN TABASCO, MEXICO
559
may be associated with distance to forests as
indicated by the authors. Najera and Simonelli
1 2010) experimentally showed that higher struc¬
tural diversity in plantations of African oil palm
l Elaeh guineensis), obtained by integrating a
herbaceous and a shrub stratum, increased species
richness and abundance of the associated avifau¬
na However, there were no forest specialists
among the observed species. Reitsma et al. (2001 )
found a weak correlation between number of tree
species and trees in the canopy of cacao groves in
Costa Rica, and the abundance of forest specialists
and generalists. These parameters together ex¬
plained only 24ct of the variation. Indications ol a
positive correlation between system structural
complexity and bird species richness have been
found, but results are too few, and not sufficiently
robust to be conclusive.
Bird communities in agroforestry systems were
as abundant and species rich as in forests in
TaJamanca, Costa Rica. However, fewer forest
specialist species and more open area specialist
species occurred in agroforestry systems ( Harvey
and Gonzalez-Villalobos 2007). No differences
among agroforestry systems were found in
abundance, species richness, and habitat preler-
ence. Cacao groves in the same region had tower
forest specialists than forests (Reitsma et al.
2001). Rubber (Hevea brasitknsis) agroforests
in Sumatra, Indonesia had fewer forest specialist
species and more forest generalist species com¬
pared to native forests (Bcukemu ct al. 2007).
file avifauna in a landscape of pasture lands near
forest fragments in Tabasco, Mexico consisted
mainly of forest generalists and open area
specialists, whereas forest specialists were scarce
•Arriaga-Weiss el al, 2008). The number of
specialist bird species of the forest understory
species was small in comparison w ith forests in
coffee crops under shade trees in Mexico ( Tejeda-
Cruz and Sutherland 2004). cacao interplanted in
'orest in Brazil (Faria et al. 2006), and •mate’ tea
' Hex paraguayensis) under tree cover in Paraguay
(Cockle et al. 2005). This is also one of the
findings of Bhagwat ct al. (2008) in their review
o! research on birds near forest reserves.
Studies that compare avifauna between agro¬
forestry classes are scarce. 1 hesc studies are par¬
ticularly of interest where the original vegetation
cover has been replaced almost completely, as is
the case in the tropical lowlands o! Tabasco,
Mexico (Arriaga-Weiss ct al. 2008). Ditterences in
avian diversity and abundance among agroforestry
classes would suggest which classes and which
structural assets should be stimulated most through
policies to obtain maximum conservation benefits
of associated biodiversity.
We compared avifauna among live classes of
agroforestry systems distinguished by Torquebiau
(2000). which varied in structural complexity.
Agroforests resemble forests as they are composed
of plants of different species and different growth
forms without a fixed arrangement (e.g.. home
gardens). Agroforests have the highest structural
complexity (Torquebiau 2000. Kumar and Nair
2004). Crops under tree cover are defined by a
tree upperstory that shades a crop (e.g.. cacao and
coffee). This class has lower structural complexity
than agroforests, as the height of trees is
homogeneous in the upper and lower stratum,
and trees are generally at fixed distances. Trees
and crops appear side by side in agrofarestry in a
linear arrangement. Structural complexity is low,
as high and low components are separated and
regularly spaced. Trees and crops in sequential
agrofarestry do not simultaneously occupy a
field; cropped and recently abandoned fields are
structurally simple, relatively open areas. Tree
species in animal agrofarestry are used to teed
ruminants. Tree cover is sparse in open fields and
structural complexity is low. Our objectives were
to investigate if: (I) species abundance and
richness of bird communities vary among agro-
lorcstry classes in the three climatic seasons in
Tabasco, and (2) (he abundance and species
richness of foraging guilds and habitat preferences
vary among agroforestry classes.
METHODS
Study Area. — The State of Tabasco in south¬
eastern Mexico borders the Gull of Mexico
between the states of Veracruz and Campeche. It
is bordered on the south by Chiapas and to the east
by Guatemala. Its territory consists mainly ot
tropical lowlands, deposited in the Holocene by
the Grijalva and Usumacinta rivers (West et al.
1985). Extensive wetlands occur, roughly paral¬
leling the east-west coast line. Alluvial plains are
succeeded by hills of weathered Pleistocene
fluvial deposits to the south, and Tertiary
mountains of sedimentary and volcanic rocks.
Rainfall is 1.500 mm per year near the coast and
up to 5.000 mm in the mountains. Three seasons
are distinguished. The wet season from June to
November is followed by a season of northern
winds from December to March, which brings
560
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124. No. 3. September 2012
TABLE 1. Distribution of fields, observation points, and observation time over five agroforestry systems in Tabasco.
Mexico in 2008 and 2009. AA = animal agroforestry; AF = agroforest: LA = linear agroforestry; SA = sequential
agroforestry: CT = crops under tree cover; min = minutes; * = transect count; all others - point counts.
Rainy season
Northern winds
Dry season
AD
n fields
n points
Time (min)
n fields
n points
Time (min)
n fields
n points
Time Imin)
Time (rain
AA
7
9
528
7
9
540
7
9
500
1,600
AF
8
8
480
8
8
480
8
8
470
1,462
LA
4
4*
325
5
5*
311
5
5*
338
984
SA
4
4
238
4
4
244
4
4
240
738
CT
7
II
666
8
12
724
7
11
658
2.086
All
30
36
2,237
32
38
2,299
31
37
2.206
6.870
substantial rains. The dry season
lasts from April
with a fixed radius of 30
m in all <
classes of
- - - - - UWIIUMI IVIII|/VIUUIIV. 1.1
(West et al. 1985).
Tabasco had wide scale colonization and
deforestation programs, and immigration in the
second hall ot the 20th century. Farmers in
deforested areas have established new agroforest¬
ry systems, which complement the traditional
home gardens, cacao groves, and shifting cultiva¬
tion fields. Animal agroforestry is currently the
most widely extended class of agroforestry
systems. Agroforests, particularly home gardens,
cover a small total area, but are the most frequent
system and occur throughout the slate. Cacao
groves, in the class of crops under tree cover, are
irequent in selected areas. Shifting cultivation
fields occur in the southern hills and mountains
(Sanchez-Munguia 2000).
Selection of Bird Monitoring Sites.— Selection
of study sites was conducted in two stages. We
traveled over primary and secondary roads in
Tabasco, recorded the main characteristics of 500
agroforestry fields selected at random, and
assigned them to classes following Torquebiau
(2000). We selected 32 fields, considering logis¬
tics, in which we placed 38 sampling points and
transects, distributed over the agroforestry classes
with the largest numbers of f ields and points in the
most frequent classes, and smaller numbers in the
sequential and linear classes (Table I). Spatial
clustering of fields could not be avoided altogeth¬
er, but distance between fields was >2 km. and
between points in the same field was >|00 m.
Bird Monitoring and Groupings. — Bird counts
were conducted in all three seasons: rainy season
between 22 August and 27 October 2008, season
of northern winds between 20 January and 24
Feb.uaiy _009, and dry season between 30 March
and 2 June 2009. We used the point-count method
agroforestry systems, except for linear agroforest¬
ry systems where we used the linear transect
method with a width of 30 m. We recorded all
birds that used the system (foraging, perching
etc.) during 30 min in the early morning and in 'he
afternoon al each point. We listed birds recorded
by family and species, and assigned them to
foraging guilds, habitat preferences, and migrato¬
ry status following Howell and Webb ( 1995)
and Hughes et al. (2002). We distinguished 13
foraging guilds: scavengers, arboreal frugivores,
granivores. bark -gleaning insectivores. foliage
gleaning insectivores. arboreal insectivores/frugi-
vores. terrestrial insectivores, sallying/sweeping
insectivores, nectarivores/insectivores, omnivores,
aquatics, piscivores, and raptors. Habitat prefer¬
ence categories were forest specialists, forest
generalists (recorded most commonly in forest'
and uncommonly in open areas and secoitdar)
vegetation) following Howell and Webb (N^)
and Hughes et al. (2002), open area specialists,
and species occurring near water bodies. Migra¬
tory or resident status of species was also assign-’'
based on the scientific literature.
Data Treatment and Analysis.— We estimated
Jacknife I total species richness using Estimate
software (Colwell and Coddington 1994, Colv-eil
2006) and calculated the efficiency of sampling
by dividing die number of observed species b>
estimated total species richness. We calculated
dominance indices (Simpson), Shannon doers1:
indices (H), Buzas and Gibson's evenness, and
cqui lability (Shannon diversity divided by in-
logarithm of the number of taxa) for each point in
each class of agroforestry systems in all sea*1 t
using PAST software (Hammer et al. 2001). Wo
used ANOVA and Tukey’s HSD-tests when data
were normally distributed (Shapiro-Wilks: tests'
vander Wal el al .AVIFAUNA IN AGROFORESTRY IN TABASCO. MEXICO
561
TABLE 2. Number ol bird species and individuals observed in eonnls in 32 fields of five agroforestry classes in
Tabasco. Mexico in the rainy season. 2008 and the northern winds and dry season. 2009. AC = agroforestry class; nso =
number of species observed in all points; ni = number of individuals in all points; as - average number ol species per
point: pi = average number of individuals per point: ens estimated number of species; SI: sampling efficiency, A A —
animal agroforestry; AF = agroforest; FA = linear agroforestry; SA = sequential agroforestry: C’T = crops under
iree cover.
Rainy season Season of northern winds
AC
a*»
ni
as
ai
nso
ui
as
ai
nso
AA
40
432
11.7
48.0
41
329
10.1
36.6
46
AF
27
237
8.4
29.6
31
337
11.6
42.1
40
LA
27
99
8.5
24.8
26
103
9,2
20.6
40
SA
28
168
11.0
42.0
23
98
10.5
24.5
24
a
25
288
7.9
28.8
40
400
10.4
33.3
46
All
64
1.224
9.4
34.0
66
1.267
10.4
33.3
76
Dry season All seasons
ni
as
ai
nso
ni
as
ai
ens
se %
286
12.5
31.7
64
1.047
11. 2
38.8
81.3
78.7
280
13.6
35.0
53
854
11.4
35.6
67.7
78.6
108
11.6
21.6
59
310
9.6
22.1
85.9
68.7
77
8.8
19.3
43
343
10. 1
28.6
55.8
77.1
309
12.0
28.1
60
997
10.2
29.3
73.6
81.5
.060
12.1
28.6
102
3.55 1
10.6
32.0
123.8
82.4
and non-parametric Kruskal-Wallis and Mann-
Whitney (7- tests in SPSS Version 17 to evaluate
differences in richness and abundance, diversity,
dominance, evenness, and cquitability among
classes in all seasons. We used the raw data for
comparing species richness among agrolorestry
classes, and repeated the analysis with estimated
richness for each agroforestry class in each
season. We calculated the number of shared
species and Chao-Jaccard abundance based sim¬
ilarity indices following Chao et al. (2000. 2005).
We used Principal Component Analysis (PCA).
and Analysis of Similarity (ANOSIM) and
Similarity Percentage Analysis (SIMPER) in
PAST (Hammer et al. 2001) to examine if
agroforestry classes had different species compo¬
st lion and which species contributed most to
observed differences. We also used ANOSIM and
SIMPER to examine if agrolorestry classes had
different abundance of feeding guilds.
RESULTS
The observation time per agroforestry class in
each season varied from 4 to 12 hrs with a total
observation time of 1 14 hrs (Table I). Sampling
efficiency was >65% in all agroforestry classes
and near 80% in all seasons. Overall sampling
efficiency was 82.4%/ (Table 2), We observed
3,551 individuals in the three seasons that
belonged to 102 species (Appendix). Sixty-four
species were observed in the rainy season. 66 in
the season of northern winds, and 76 in the dry
season.
Analysis of raw data of all sampling points and
transects (all seasons and all systems) indicated
species richness did not vary among agroforestry
classes (Kruskal-Wallis test. P = 0.527). Analysis
of data of Jackknife I estimated species richness
for all agroforestry classes revealed no differences
(ANOVA. F = 1.374. P = 0.310). but abundance
varied among classes (Kruskal-Wallis test. P =
0.003). There were more birds at sampling points
in animal agroforestry (Mann- Whitney (7-test. P
- 0.002) and agroforests (Mann- Whitney (7-test,
P = 0.001 ) than in linear agroforestry. There were
no significant differences in abundance among
animal agroforestry, agroforests, crops under tree
cover, and sequential agrolorestry. The average
species richness and abundance in the rainy
season was not significantly different among
agroforestry classes (Kruskal-Wallis lest, P =
0.106 and P = 0.207). Species richness did not
vary among classes in the season of northern
winds and dry season (Kruskal-Wallis test, P =
0.311 and P — 0.152), hut abundance varied
(Kruskal-Wallis lest, P = 0.025). There were
more birds in agroforests than in linear agrofor¬
estry in the season of northern winds (Mann-
Whitney U- test. P — 0.007) and in the dry season
there were more birds in agroforests than in linear
and sequential agroforestry (Mann- Whitney
(7-test. P = 0.040 and P = 0.006). The number
of observed species differed among seasons
(Kruskal-Wallis test. P = 0.001) and w'as higher
in the dry season than in the rainy season and
season of northern winds (Mann- Whitney (7-test.
P = 0.001 and P = 0,020).
Dominance. Shannon diversity index, and
cquitability of the bird community, considering
all sampling points and transects in all seasons,
did not reveal differences among agroforestry
classes (Kruskal-Wallis test. P — 0.829, 0.927,
and 0.083), whereas some differences were
observed in evenness (Kruskal-Wallis test. P =
562
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 3. September 2012
TABLE 3. Indices of dominance. Shannon diversity, evenness, and equilability. Numbers are averages for each
agroforestry class obtained from the abundance data of all point and transect counts in three sampling seasons. D =
dominance; H = Shannon diversity index; E = evenness; E-J = equitability: AA = animal agroforestry: AF = agroforest:
LA = linear agroforestry: SA = sequential agroforestry; C'T = crops under tree cover.
Season
index
Rainy season
Northern winds
D
H
E
E-J
D
H
E
E-J
AA
0.20
2.00
0.69
0.84
0.19
1.96
0.74
0.86
AF
0.17
2.00
0.74
0.86
0.13
2.25
0.83
0.92
LA
0.18
1.90
0.83
0.91
0.16
2.02
0.84
0.92
SA
0.17
2.04
0.74
0.87
0.15
2.14
0.82
0.91
CT
0.22
1.77
0.79
0.88
0.17
2.02
0.74
0.87
Average
0.19
1.92
0.75
0.87
0.16
2.07
0.78
0.89
Season
Dry season
All seasons
index
D
H
E
E-.I
15
H
E
E-J
AA
0.14
2.21
0.77
0.89
0.18
2.06
0.73
0.86
AF
0.13
2.34
0.78
0.90
0.16
2.11
0.78
0.89
LA
0.12
2.29
0.88
0.95
0.15
2.08
0.85
0.93
SA
0.18
1.92
0.80
0.89
0.17
2.03
0.79
0.89
CT
0.13
2.27
0.81
0.91
0.17
2.02
0.78
0.89
Average
0.14
2.24
0.80
0.91
0.17
2.06
0.78
0.89
0.033) (Table 3). Evenness was less in animal
agroforestry and crops under tree cover than in
linear agroforestry (Mann-Whitney U-test, P <
0.001 and P = 0.023). No significant differences
among classes were observed (Kruskal-Wallis
tests, P all >0.096) when analyzing the indices
separately for the three seasons. H-diversily
indices varied among seasons and were higher in
the dry season than in the rainy season and the
season of northern winds (ANOVA, F = 10.51,
P < 0.001; Tukey’s HSD-test, P = 0.01 and P =
0.034). Dominance indices varied among seasons
(Kruskal-Wallis test. P < 0.001) and were higher
in the rainy season than in the season of northern
winds and dry season (Mann-Whitney (/-test, P =
0.033 and P < 0.001), and higher in the season
of northern winds than in the dry season (Mann-
Whitney U- test, P = 0.027). Great-tailed Grackle
(■ Quiscalus mexicamts), Golden-fronted Wood¬
pecker ( Melanerpes aurifrons), American Red¬
start {Seiophaga rit tic ilia), and Brown Jay
(Psilorhinus mono) were the most abundant
species (Appendix). Each included >6% of the
total number of observed birds. The Great-tailed
Grackle was the most abundant species in
agroforests and animal agroforestry, American
Redstart in linear agroforestry, Melodious Black¬
bird (Dives dives) in sequential agroforestry, and
Golden-fronted Woodpecker in crops under tree
cover.
Bird communities in the agroforestry system
classes had from 56.3 to 83.7% of the observed
species in common, when considering all sam¬
pling seasons (Table 4). Chao-Jaccard indices of
estimated similarity ranged from 0.71 to 0.98.
Agroforests and sequential agroforestry were least
similar, and agroforest and animal agroforestry
had comparatively low similarity. Chao-Jaccard
estimates of similarity were not different among
seasons (ANOVA. F = 2.595. P = 0.093). The
average number of observed species in com¬
mon was significantly different among seasons
(ANOVA, = 8.706. P = 0.001), and was higher
in the dry season (23.0 species) than in the rainy
season (15.4 species) (Tukey HSD-test. P =
0.001). This was related to the total number of
species in most classes in the dry season
(Table 2); the proportions of shared species of
those observed were not different among seasons
(ANOVA. F = 1.592, P = 0.222 and F = 0.735.
P = 0.489). The fraction of the number of
sampling points where the 25 most abundant
species were observed did not vary among classes
in the rainy and dry seasons (Kruskal-Wallis test.
P = 0.986 and P - 0.282), and when considering
all sample points of all seasons. The relative
frequency of abundant species was significantly
different in the season of northern winds (Kruskal-
Wallis test, P = 0.001). Abundant species had
higher relative frequencies in agroforests than in
render l Veil el al • AVIFAUNA IN AGROFORESTRY IN TABASCO, MEXICO
563
TABLE 4. Similarity of bird communities in five agroforestry classes in Tabasco, Mexico in 2008-2009. AF -
agroforest; AA = animal agroforestry; LA = linear agroforestry; SA = sequential agroforestry; CT = crops under tree
cover, S = sample; nso = number of species observed; sso = shared species observed; C-J = ( hao-Jaccard estimated
similarity index.
s s
• 1 12
Rainy season
Northern winds
Dry season
All seasons
nso
#1
nso
#2
SSO
C-J
nso
a |
nso
1 2
SSO
C-J
nso
ft i
nso
ft 2
SSO
C-J
nso
# 1
nso
#2
SSO
C-J
AF .AA
27
40
18
0.90
31
41
21
0.71
40
46
23
0.72
53
64
38
0.76
AF AL
27
27
10
0.34
31
26
15
0.51
40
40
22
1.00
53
59
35
0.79
AF AS
27
28
17
0.54
31
23
14
0.59
40
24
16
0.55
53
43
33
0.75
AF CT
27
25
14
0.79
31
40
22
0.79
40
46
28
0.84
53
60
39
0.85
AA AL
40
27
20
0.67
41
26
17
0.47
46
40
25
0.68
64
59
44
0.89
AA AS
40
28
21
0.79
41
23
20
0.76
46
24
19
0.63
64
43
36
0.87
AA a
40
25
16
0.62
41
40
26
0.64
46
46
28
0.71
64
60
43
0.81
LA SA
27
28
13
0.50
26
23
13
0.48
40
24
19
0.65
59
43
36
0.98
LA CT
27
25
12
0.44
26
40
19
0.62
40
46
30
1.00
59
60
40
0.85
SA CT
28
25
13
0.51
23
40
18
0.72
24
46
20
0.71
43
60
34
0.81
animal agroforestry (Mann- Whitney U- test, P =
0.002 ) and crops under tree cover (Mann-Whitney
6-test. P = 0.017).
Only one of the 102 species recorded was a
forest specialist. The Common Black-Hawk
{Ruteogallus anthmcimis) (I individual) was
observed in crops under tree cover. Seven
individuals of four species with habitat preference
for water bodies were observed. MosI species (75)
were forest generalists; 22 species were specialist
°f open areas. The richness of open area
specialists varied among agroforestry classes
'ANOVA, F = 5.060. P = 0.003) and was larger
1(1 :in'mal agroforestry than in agroforests, linear
ngroforestry. and crops under tree cover (Tukey’s
HSO-tests, P < 0.01 in all cases). The abundance
"• specialists of open areas also varied among
agroforestry classes (ANOVA. F = 5.685, P =
^*1 '• and was larger in animal agroforestry than
ln linear agroforestry and crops under tree cover
(Tukey' s HSD-tests, P = 0.001 and 0,039). and in
^quential agroforestry than in linear agroforestry
l|p ~ 0.048). It was also larger in agroforests than
m linear agroforestry i P = 0.034). No significant
diflerences were observed in the rainy season
'Kruskal- Wallis tests. P - 0.163 for richness and
p = 0.483 for abundance) when comparing
r'diness and abundance of forest generalists in
£ach season and in the season of northern winds
'Kruskal-Wallis tests, P = 0.165 for richness and
^ = 0.167 for abundance). Richness did not vary
‘imong classes (Kruskal-Wullis test, P — 0.06) in
dry season, but abundance varied ( Kruskal-
'Vallis test, P = 0.014). Specialists of open areas
were more abundant in agroforests, animal
agroforestry, and sequential agroforestry than in
linear agroforestry and crops under tree cover
(Mann-Whitney U- tests, P < 0.05).
The richness and abundance of forest general¬
ists did not vary among agroforestry classes in the
rainy season (Kruskal-Wallis test. P = 0.098 and
P = 0.737). Richness did not vary among
agroforestry classes in the season of northern
winds (ANOVA, F = 1,054, P = 0.395). The F
statistic indicated difference in abundance among
classes, but Tukey’s HSD-test did not indicate
significant differences between particular pairs of
agrolorestry classes. Average abundance in this
season was the same in agroforests and crops
under tree cover (29.3). It was lowest in sequential
agroforestry (15.8), and had an intermediate value
in animal agroforestry (21.0). The pattern was
similar in the dry season; there were no significant
differences in richness and abundance between
pairs of agroforestry classes. The highest average
abundance was observed in agroforesLs, and the
lowest in sequential agroforestry. Richness and
abundance of forest generalists also did not vary
among the agroforestry classes (ANOVA, F =
2.651. P = 0.051) when data were summed over
all seasons. Forest generalists were equally
abundant in animal agroforestry and the other
classes. Abundance of forest generalists in all
agroforestry system classes, including animal
agroforestry, was higher than abundance of open
area specialists (Fig. 1). Differences between the
number of forest generalists and open area
specialists were largest in agroforests, linear
564
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 3. September 2012
(A)
FIG. I . Resident (A) and migrant (B) birds by habitat preference in live agroforestry system classes in Tabasco. Mexico
in 2008 and 2009. WB = water bodies; FS = forest specialists; FG = forest generalists; OAS = open area specialists
AF = agroforest; AA = animal agroforestry; LA = linear agroforestry; SA = sequential agroforestry; CT = crops under
tree cover. Scale on Y-axis in (B) is adapted.
agroforestry, and crops tinder tree cover. From 5 1 .7
to 75.1% of resident birds were forest generalists
(Fig. 1A) depending on agroforestry class; >93%
of migrant birds were forest generalists in all
agroforestry classes (Fig. IB).
Principal components analysis explained 4S.8%
ot variation in species composition among agro¬
forestry classes on the first three axes. A NOS I M
with Bray-Curtis' distance measure indicated
significant differences in community composil
among agroforestry system classes (R = 0.32 ;
P = 0.001). Comparisons between pairs of syst
classes with sequential Bonferroni correc
^-values indicated significant differences
agroforests and crops under tree cover with anil
agroforestry, linear agroforestry, and sequen
agroforestry (all 1> < 0.005). SIMPER indica
Great-tailed Crackle. Clay-colored Thrush (Tun
gray,) and Ob ve-throated Parakeet (A rat in
nana) contributed most to differences bet we
agroforests and crops under tree cover with animal
agroforestry. Great-tailed Grackle and Clay-
colored Thrush contributed most to the dissimilar¬
ity between agroforests and linear agrotoresm
Clay -colored Thrush and Golden-fronted VorxI-
pecker contributed most to differences betwee
crops under tree cover and linear agroton’M
Melodious Blackbird. Great-tailed Grackle. u* ■
Clay-colored Thrush contributed most to ihc di
ference between communities in agrolore sis-
sequential agroforestry. Melodious Blacker.
Clay-colored Thrush, and Golden-fronted WooJ
pecker contributed most to the difference betwee
crops under tree cover and sequential agrofonNP
AN OS I M with abundance data for toracing
guilds (P-values with sequential Bonferroni sig¬
nificance) indicated significant differences
agroforestry classes ( R = 0.19. P - ll(HL
Linear agroforestry was different from agrc,,lir'
esis. sequential agroforestry, and crops under t ^
van der Wale l al. • AVIFAUNA IN AGROFORESTRY IN TABASCO. MEXICO
565
100
P
e
r
c
e
n
t
90
80
70
60
50
40
30
20
10
0
E3TI
□ SI
QR
ONI
□ FI
HAQ
□ AIF
FIG. 2. Distribution of resident (A) and migrant (B) birds by foraging guilds in five agroforestry classes in Tabasco.
Mexico. SC = scavenger; AF = arboreal frugivore; GR = granivore; B1 = bark-gleaning insectivore; FI - foliage-
gleaning insectivore; AIF = arboreal insectivores/frugivores; T1 = terrestrial insectivore; SI - sallying/swecping
insectivore; N1 = nectarivore/inseclivorc; O = omnivore; AQ = aquatic; P = piscivore; R = raptor, AA - animal
agroforestry; AF = agroforest; LA - linear agrofnrestry; SA = sequential agroforcstry; CT - crops under tree cover.
cover (Fig. 2). Animal agroforestry was different
trom crops under tree cover, and the latter was
different from sequential agroforestry (all P <
0-05). SIMPER showed that differences between
linear agroforestry and agroforests were due to
higher abundance of terrestrial inseetivores, arbo¬
real insectivores/frugivores, and omnivores in
agroforests. Differences between linear and se¬
quential agroforestry were mainly due to higher
abundance of arboreal insectivores/frugivores in
sequential agroforestry and of foliage-gleaning
inseetivores in linear agroforestry. Foliage-gleaning
inseetivores were more abundant in linear agroior-
estry than in crops under tree cover, whereas bark-
gleaning inseetivores and arboreal inseetivores/
frugivores were more abundant in the latter.
Arboreal frugivores. terrestrial inseetivores, and
sallying/sweeping inseetivores were more abundant
in animal agroforestry than in crops under tree
cover. Arboreal insectivores/frugivores were more
abundant in sequential agroforestry than in crops
under tree cover, whereas foliage-gleaning insecti-
vores were more abundant in the latter. Large
differences in bird distribution over guilds were
566
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124. No. .?, September 2012
observed between resident (Fig. 2A) and migrant
birds (Fig. 2B). Migrant birds were mostly-leaf
gleaning insectivores and arboreal insectivores/
frugivores. Resident birds were distributed over
all foraging guilds.
DISCUSSION
We observed 102 species of birds in the
sampled agroforestry fields. —19% of the 539
species documented for Tabasco (Winker et al.
1999). This number included Keel-billed Toucan
(Ramp host os sulfit rains ) . which is on the Mexican
list of threatened species, and Olive-throated
Parakeet and Montezuma Oropendola (Psaroco-
liits montezuma), which are on the list of protected
species (SEMARNAT 2002). Thus, agroforestry
systems support important avifauna as reported by
several authors (Hughes et al. 2002, Cardenas cl al.
2003, Harvey et al. 2006, Bhagwat el al. 200K).
The average number of species in the three
counts of each agrotorcstry class corresponding lo
the three seasons in each field in our study varied
from 9.6 to 11.4, and the number of individuals
from 22.1 to 38.8 (Table 2). Reitsma et al. (2001)
observed in two 10-min point counts in crops
under tree cover an average of 8.6 and 8.5
individuals and 5.2 and 5.9 species in abandoned
and managed cacao in Talamanca, Costa Rica.
Arriaga- Weiss (2008) observed 15.4 species and
54.3 individuals in three 10-min counts in the
matrix of pasture lands within a distance of 500 m
from forest fragments. Our numbers are within the
range of those reported in other studies. However,
the community we observed is more depauperate
than that observed by Arriaga- Weiss (2008) in
pasture lands near forest fragments, indicating
the importance of these fragments for conserving
avifauna.
We found no significant differences in the
number of species between pairs of agroforestry
classes. This confirms findings of Cardenas et al.
(2003) in Costa Rica, who observed 45 species in
sequential and animal agroforestry, and 42 species
in live fences (linear agroforestry). Species
richness in both animal and linear agroforestry
in our study was higher than found by Cardenas
et al. (2003). and equal in sequential agroforestry.
This may be due to an overall low forest cover
in Tabasco resulting in birds seeking trees in
the agroforestry systems as there are no others
available. Life zone differences may also have a
role, tropical dry forest in Costa Rica versus
tiopica! moist and wei forest in Tabasco.
Shannon diversity, equitability, and dominance
indices of pooled data and of data for each season
were similar in all agroforestry classes (Table 3).
Cdrdenas et al. (2003) also found similar Shannon
diversity indices in animal, sequential, and linear
agroforestry. Only evenness showed difference'
among agroforestry classes and was larger in
linear agroforestry than in animal agroforestry and
crops under tree cover (Table 3).
Abundance ot birds was higher in animal
agroforestry and agrolorests than in linear agro-
forestry. whereas no significant differences were
observed in abundance among animal agrofor¬
estry. agroforests, crops under tree cover, and
sequential agroforestry. Cardenas et al. (2003)
also found higher abundance of birds in animal
agroforestry than in linear and sequential agro-
forestry. This indicates there is no direct relation¬
ship between bird diversity and structural com¬
plexity. and tree diversity of agroforestry systems.
We would have found higher diversity and
abundance ol birds in agrolorests and in crops
under tree cover if there was a relationship. The
absence ol differences may be due to movement
of birds between systems.
We found mostly common species in all
agroforestry classes, as few' rare species were
observed. Seventy-five percent of the species we
observed also occurred in the matrix of pasture
lands near forest fragments (Arriaga- Weiss cl al.
2008). Nineteen of the 23 species reported by
Najera and Simonetti (2010) in oil palm planta¬
tions in Guatemala were also present in the
agroforestry systems in Tabasco. The prevalence
of common and low frequency of rare species
is not a reason to disregard the contribution of
agroforestry systems, as these conserve biodiver¬
sity in otherwise open landscapes, enhance
species movements between habitat remnants,
reduce human pressure on remaining forests, and
complement conservation in protected areas
(Bhagwat et al. 2008).
Most observed species were forest generalise-
and specialists of open areas as few forest
specialist species occurred in agroforestry fields.
Only 1% of species and 0.03% of individuals
were forest specialists in our total sample. Most
open area specialist species ( 18 vs. 1 1-13 in the
other system classes) were in animal agroforestry
fields, which are the most open agroforestry
systems (Fig. I). Habitat preferences of the bird
communities in agroforestry classes were quite
distinct from those observed in forest fragments
xander Wal el al. • AVIFAUNA IN AGROFORESTRY IN TABASC O. MEXICO
567
where 25% of resident species were forest
specialists (Arriaga-Weiss 2008). Seven percent
of species and individuals in the matrix of pasture
lands near forest fragments were forest specialists.
Our study confmns die shift from forest specialist
species in forests and fragmented landscapes to
generalist species in agroforestry systems as
documented by several authors (Reitsma et al.
2001, Hughes et ai. 2002, Cardenas et al. 2003.
Beukema el al. 2007, Harvey and Gonzalez-
Villalobos 2007).
We did not find a relationship between
structural complexity of agroforestry systems
and bird species richness. Agroforests had similar
species richness and abundance as crops under
tree cover, and forest specialist species were levs
in both classes. Noise, presence of humans, and
fowl and other domesticated animals, as well as
the intense management of the agroforest floor
resulted in the absence of forest understory
specialists. Understory specialists were also
absent in cacao in thinned forest in Brazil (Faria
et al. 2006) and mate tea plantations under natural
shade in Paraguay (Cockle et al. 2005). farm
management has been shown to strongly influence
avian diversity (Lang el al. 2003, Najera and
Simonetti 2010). Species richness was not lower
in animal agroforestry than in agroforests and
crops under tree cover.
Our results confirm those of Naidoo el al.
(2004), which indicated that agroforestry pro¬
grams would not increase tree densities to levels
that would support conservation of forest special¬
ists. This is also true for agroforestry systems with
high tree cover, such as agroforests and crops
under tree cover. Agroforestry systems would
only benefit conservation of forest specialists il
they are close to existing forests (Naidoo 2004).
Keitsma et al. (2001 ) found the number of forest
•'pecialists in cacao groves was negatively corre¬
lated with distance to forests, and concluded
cacao groves cannot substitute lor lorest in the
conservation of avifauna, although they provide
habitat for many species that depend on lorests.
Our results generalize this finding to all agrotor-
es|ry classes in Tabasco.
The distribution of species over foraging guilds
indicates the wide ecological functionality ot all
ugroforcstry classes (Fig. 2) and the value ol these
systems for the conservation ot common and (lew )
care species. The distribution of birds over guilds in
lorest fragments was. however, quite dilterent Irom
those in forest fragments (Arriaga- Weiss et al.
2008). Arboreal frugivores and arboreal insecti-
vores/frugivores were more abundant in loiest
fragments than in agroforestry systems (this study),
whereas granivorcs were absent in lorest tiag-
ments. Agroforestry system classes had several
differences in abundance and species richness of
foraging guilds. Omnivores were most abundant in
animal agroforestry and agrotorests. Bark-gleaning
insectivores were most abundant in crops under
tree cover. Most raptor species were in crops under
tree cover, and most leaf-gleaning insectivore
species were in linear agroforestry and crops under
tree cover. Most species in animal agroforestry
were sweeping and sallying insectivores. leal-
gleaning insectivores. arboreal insectivores, and
tree frugivores. This differs Iron) Cardenas et al.
(2003), who found mainly carnivores, granivores,
and omnivores in animal agroforestry. These
differences may be due to the abundance of insects
in the wet climate of Tabasco, distinct species
composition of trees in both study areas, and
differences in tolerance of foraging guilds to
fragmented landscapes (Tscharotke et al. 2008).
The ecological functionality of the bird com¬
munity in agroforestry systems, indicated by the
distribution "of birds over all foraging guilds in
all systems, as well as diversity, can be further
strengthened through management (Lang et al.
2003). Policies regarding bird conservation in
agroforestry systems should enhance properties
that attract bird taxa of interest (Bcrges et al.
2010). Thus, management of the forest tloor in
agroforestry systems should be further studied, as
well as the effect ol' including shrubs in live
fences ( Bernier- Leduc et al. 2009), and epiphytes
( Beukema cl al. 2007. Gordon el al. 2007) in trees.
Trees of complementary phenology could be
integrated into agroforestry systems to assure
availability of food for frugivores throughout the
year. Experiments should be conducted on how to
increase (he contribution from different agrofor¬
estry systems to conservation ot avitauna.
ACKNOWLEDGMENTS
We thunk farmers for letting ns conduct bird censuses on
their lands. This research was financed by the National
Council of Science and Technology and the Tabasco State
Government through grant TAB-2006-C08-43S67 for the
project -Eeophysiology and productivity ot agrolorestry
systems in Tabasco*. Elvia Jimenez gave valuable com¬
ments on earlier versions. Gilberto Villanueva Lope/
participated in field work and Juan Carlos Jimenez provided
logistic support. We thank R. K. Colwell and K. A. Babb
Stanley for constructive comments on an earlier dralt ol the
568
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 3. September 2012
manuscript. This article is dedicated to the memory of
Salvador Hemandez-Daumas.
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570
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124. No. 3. September 2012
APPENDIX. Foraging guilds, habitat preference, and status of bird species in five agroforestry classes in Tabasco
Mexico m 2008 and 2009. Guilds: SC = scavenger; AF - arboreal fnigivore; C.R = granivore; BI = bark-gleaning
insect! vore; FI - foliage-gleaning insectivores: All- - arboreal insectivores/frugivorcs: TI = terrestrial inseaivur SI =
sallying/sweeping msectivore: Nl = nectarivore/insect.vore; O = omnivore: AQ = aquatic organisms: P - pis mm R
raptor Habitat preferences: WB = water bodies; FS = forest specialists: FG forest generalists; OAS = open «ca
specialists. Status: M migratory: A' - resident. Agroforestry classes: AA = animal agroforestry; AF = agroforest; LA =
linear agrolorestry; SA = sequential agroforestry; CT = crops under tree cover.
Species
Ortalis vetulu
Egretta thula
E. caerulea
Bubulcus ibis
PI egad is chilli
Coragyps atratus
Cathartes aura
Elanus leucurus
Buteogallus anthracinus
Buteo magnirostris
Caracara cheriway
Herpetotheres cachinnans
Columba livia
Patagioenas Jlavirostris
Zenaida asiatica
Columbina inca
C. minuta
C. talpacoti
Leptotila verreauxi
L. plumbeiceps
Aratinga nana
Amazona albifrons
A. autumnalis
Coccyzus americanus
Crotophaga sulcirostris
Glaucidium brasilianum
Phaethomis striigularis
Amazilia Candida
A. tzacatl
Archilochus colubris
Momotus momota
Megaceryle torquuta
Pteroglossus torquatus
Ramphastos sulfiuratus
M elanerpes formic i vorus
M. aurifrons
Colaptes rubiginosus
Dryocopus lineatus
Contopus cinereus
Empidonax flaviventris
E. traillii
E. albigularis
E. minimus
Pyrocephalus rubious
Myiarchus tuberculifer
M. tyrannulus
Pitangus sulphuratus
M egarynchus pi tang ua
Myiozetetes similis
Myiodynastes maculatus
Tyrannus melancholicus
Guild
Preference
Slums
t
AF
FG
R
AQ
WB
R
AQ
WB
R
TI
OAS
R
AQ
WB
M
SC
OAS
R
SC
OAS
R
R
OAS
M
R
FS
R
R
OAS
R
1
R
FG
R
R
FG
R
GR
OAS
R
AF
FG
R
GR
OAS
R
1
GR
FG
R
GR
OAS
R
GR
OAS
R
5i
AF
FG
R
AF
FG
R
i
AF
FG
R
1.
AF
FG
R
l:
AF
FG
R
t
FI
FG
R
(
TI
OAS
R
5:
R
FG
R
(
NI
FG
R
c
NI
FG
R
i
NI
FG
R
1C
NI
FG
M
0
AIF
FG
R
0
P
WB
R
0
AIF
FG
R
1
AF
FG
R
5
BI
FG
R
11
BI
FG
R
49
BI
FG
R
0
BI
FG
R
1
SI
FG
R
4
FI
FG
M
0
FI
FG
M
0
FI
FG
M
0
FI
FG
M
I
SI
OAS
R
41
SI
FG
R
1
SI
FG
R
3
SI
FG
R
35
SI
FG
R
11
SI
FG
R
15
SI
SI
FG
FG
R
R
0
12
AA
AF
LA
SA
3
1
0
51
0
19
II
0
0
18
3
0
0
2
3
2
0
6
4
0
0
0
0
2
3
0
0
2
0
7
20
12
15
0
1
5
2
2
II
0
0
0
44
2
0
7
17
0
4
0
0
0
0
85
I
I
0
0
0
0
0
0
0
1
58
4
3
0
0
0
0
3
1
0
1
2
0
0
5
0
1
0
9
0
1
0
3
2
0
2
7
3
1
10
0
0
3
7
0
0
I
0
1
0
12
0
0
5
1
0
1
3
0
0
5
13
5
9
1
2
0
0
0
23
0
1
2
0
0
6
0
0
0
1
4
0
0
2
2
0
10
8
0
0
13
0
0
5
17
2
0
0
0
0
0
16
4
3
0
7
2
0
0
0
0
0
7
I
5
1
0
a
l
0
o
0
I
5
7
I
1
24
1
2
18
17
2
0
0
3
2
0
46
34
0
0
34
4
2
17
55
0
0
0
0
3
0
133
0
2
2
0
0
0
10
0
2
0
39
2
3
1
5
ran der Wale, al • AVIFAUNA IN AGROFORESTRY IN TABASCO. MEXICO
571
APPENDIX. Continued.
Species
Guild
Preference
Status
T. forhcatus
SI
OAS
M
T. savana
SI
OAS
M
Tnyra semifascia, a
SI
FG
R
T. inquisitor
SI
FG
R
1 Ireo sriseus
FI
FG
M
Vi flaxifrons
FI
FG
M
Psilorhimis morio
AIF
FG
R
Cranocorax xucatanicus
AIF
FG
R
Tachvcineta bicolor
SI
OAS
M
Stelgidoptem serripennis
SI
OAS
R
Hirundo rnrica
SI
OAS
M
Campylorhynchus zonatus
FI
FG
R
Cistoi horns platensis
FI
FG
R
Polioptila cacrulea
FI
FG
R
P ■ plumbea
FI
FG
R
Hylocickla muslelina
TI
FG
M
Turdus graxi
Tl
FG
R
Dmelella carolinensis
FI
FG
M
Mimus gilvus
FI
FG
R
Parkesia noveboracensis
AIF
FG
M
Mniotilia varia
AIF
FG
M
Geoihlypis trichas
FI
FG
M
Selophaga citrina
FI
FG
M
S. ruticilla
FI
FG
M
S. magnolia
FI
FG
M
S. fiisca
FI
FG
M
S. petechia
FI
FG
M
S. virens
FI
FG
M
Basileutenis rufifrons
FI
FG
R
Cardellina canadensis
FI
FG
M
C. pusilla
FI
FG
M
Ramphocelus sanguinolentus
AIF
FG
R
Thraupis episcopus
AIF
FG
R
T. abbas
AIF
FG
R
Salta, or coerulescens
AIF
FG
R
S. atriceps
AIF
FG
R
Volatinia jacarina
GR
OAS
R
Sporophila americana
GR
OAS
R
!>• lorqueola
GR
OAS
R
Gryzoborus funereus
GR
OAS
R
■\rremonops chloronolus
AIF
FG
R
Piranga rubra
FI
FG
M
Pheucticus ludovicianus
AIF
FG
M
Dives dives
AIF
OAS
R
Quiscalus mexicanus
0
OAS
R
Icterus dominicensis
AIF
FG
R
1 spurius
AIF
FG
M
1- gularis
AIF
FG
R
1 '• galbula
AIF
FG
M
Psarocolius montezuma
AIF
FG
R
n
Euphonic i hirundinacea
AF
FG
K
AA
AF
LA
SA
i
0
0
0
i
1
0
0
10
0
6
7
0
0
2
0
0
3
0
0
0
0
2
0
62
56
16
27
0
0
0
0
12
0
0
0
1
10
0
0
0
0
0
0
0
22
0
0
0
0
2
0
16
7
13
6
0
0
0
0
1
0
0
0
18
90
1
1
5
1
1
0
16
0
0
0
0
2
1
0
5
2
5
1
26
22
11
7
23
12
7
6
77
38
34
15
6
18
13
1
0
0
0
0
27
8
9
7
3
0
0
0
0
0
8
0
0
2
0
0
0
0
6
0
0
0
4
0
0
4
1
0
8
0
0
0
0
3
0
1
2
14
1
6
2
2
3
3
0
2
1
16
107
0
0
1
24
31
5
0
0
2
0
0
1
0
62
119
1
1
35
2
0
0
1
1
1
0
0
7
0
4
18
0
0
1
8
6
0
19
0
9
0
1
1
0
48
15
0
0
4
0
19
0
CT
0
0
11
0
0
0
65
4
0
0
o
10
0
4
4
2
64
2
0
29
7
26
32
83
9
14
19
0
0
0
2
0
0
0
0
0
0
0
5
0
0
1
0
43
46
2
1
24
0
3
4
The Wilson Journal of Ornithology 1 24(3 ):572- 580. 2012
THE COMPOSITION OF MIXED-SPECIES BIRD FLOCKS IN
ALTO QUINDIO, COLOMBIA
ENRIQUE ARBELAEZ-CORTES1-’ AND OSCAR H. MARIN-GOMEZ'
ABSTRACT.— Mixed-species bird nocks are a prevalent characteristic of Andean avian communities. We describe the
species composition of mixed-species bird flocks observed in a high mountain zone (3.000 to 3.450 m) of Quindio. central
Andes Colombia. The total number of species observed in mixed-spccies Hocks was 42. and the mean number of species
anc me ividuals per flock were 5.1 and I 1.5. respectively. Flock species composition was similar along the elevation
gradient studied. Our observations suggest that five species (Margaromis sc/uamiger. Iridisomis rufivertex. Coniwstrm
S'"',/- Stictopterus. and Difossa cyanca) could be nuclear species in the flocks. Received II August
201 1. Accepted 7 February 2012.
Mixed-species bird flocks are heterospecific
groups of individuals traveling and feeding togeth¬
er, and represent a prevalent characteristic of
practically every terrestrial habitat in the tropics
(Moynihan 1962, Powell 1985). The cohesion
within any flock seems to result front attractions
among their participants and not from the presence
of clumped food resources (Moynihan 1962, Morse
1977, Powell 1985). There are two general
hypotheses to explain why birds may benefit from
multispecies flocking. One is related to enhanced
foraging and the other with reduction in predation
pressure (Morse 1977. Jullien and Clobert 20(X),
Sridhar et al. 2009). Species that participate in
mixed-species bird flocks have been divided as
nuclear or leaders in flocks and satellites or
followers according to their role in cohesion of
flocks and their relative position within them
(Moynihan 1979, Powell 1985). Species with
cohesive roles in mixed-species bird flocks could
be niche constructors that are creating a complex
social environment that shape their own ecology
and that of other species (Harrison and Whitehouse
2011).
The Andes is a region with some of the most
diverse and threatened bird faunas worldwide
(Fjeldsa and Krabbe 1990), and mixed-species bird
flocks represent a biologically important feature of
their avian communities. These Andean flocks
have large numbers of participating taxa. a high
1 Programa de Lieenciaiura en Biologia y Kducacibi
Ambiental, Facultad de Edueacion, Universidad del Quin
dio. Armenia, Quindio. Carrera 15. Calle 12 N. Colombia
Cun-en. address: Museo de Zoolog, a. Dcpartamcn.o d,
Biologia Evolutiva, Faculiad de Ciencias and Posgrado ei
Ciencias Biologicas, Universidad Nacional Autdnoma di
Mexico. Mexico DC. Ciudad Universitaria 04510. Mexico
Corresponding author;
e-mail; enriquearbelaez@gmail.com
frequency of occurrence, and usually contain
Managers that seem to be involved in their overall
cohesion (Moynihan 1979. Remsen 1985. Poulsen
1996, Bohorquez 2003. Arbelaez-Cortes et al.
201 la). I he bird species richness of the Andes is
associated with many species occupying onh a
narrow elevation band, promoting a dense vertical
segregation of different species on their mountain¬
sides (Newton 2003). The patterns of bird com¬
munity changes along elevation gradients in the
Andes have been studied (e.g., Terborgh 1 977 ). but
it has not been tested whether there are also
changes in composition of mixed-species bird
flocks. Switches in species with cohesive roles in
mixed-species bird flocks at different elevations
have been documented in New Guinea (Diamond
1987). Our objectives are to: (I) describe the
composition of mixed-species bird flocks in a high
mountain zone of the central Andes of Colombia.
(2) compare species composition along an eleva¬
tion gradient (3,000 to 3.450 m). and (3) focus on
identifying species that could have the role of
nuclear species important in cohesion of flocks.
METHODS
Study Area. — The area studied was in the Alto
Quindio zone (Paynter 1997) in Salento municipality.
Quindio Department, on the western slope of the
central Andes of Colombia. The observations were
made along an elevation gradient (04 37' 40” N. 75
27' 04" W to 04 37' 13" N. 75 25' 19” W; 3,000-
3,450 m: Fig. I) including both cloud forest and
paramo vegetation (Arbelaez-Cortes et al. 201 lb).
We visited the zone four times during September-
October 2005 and April 2007 when conducting
observations (82 hrs) above Estrella de Agua. The
Paramo de Frontino and El Mirador-Estrella de Agua
were explored by OHM-G in January 2006 (10 hrs)
and April 2007 (29 hrs), respectively.
572
Arbelaez-Cortes and Marin- Gomez • MIXED-SPECIES BIRD FLOCKS
573
FIG. 1 . Study area. El Mirador-Pdramo de Frontino section (3.000-3,450 m) in the Alto Quindio. Salento municipality,
Quindio. central Andes of Colombia, where mixed bird nocks were surveyed between 2005 and 2007. Inset map shows
location of Quindio in Colombia.
We conducted observations Irom 0600-0630
(COT) to 1500-1800 hrs while walking along a
path (Fig. 1). We studied mixed-species bird
flocks by observations through binoculars when
there was extreme multi-species bird activity. A
mixed-species bird flock was defined as a
heterospecific group of individuals actively mov¬
ing and showing evidence of cohesion (e.g..
574
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 3. September 2012
constant calling and individuals moving in the
same direction) without the presence of clumped
food resources such as fruiting plants. Differen¬
tiation of mixed-species bird flocks from other
bird groups, such as frugivorous birds foraging in
trees, was straightforward due to the conspicu¬
ousness of mixed-species bird flocks enhanced by
their constant movement (Moynihan 1962, Morse
1977). We noted all times each species was
observed during our fieldwork in 2005 to obtain
information about species tendencies to partici¬
pate in mixed-species bird flocks (Arbeldez-
Cortes el al. 201 lb) and considered if they were
within Hocks or apart from them. We recorded the
time of day. species composition, number of
individuals per species, and the relative position
of the mixed-species bird Hocks in the vegetation
once a mixed-species bird flock was located. Data
about foraging maneuvers, following behavior
among species, and vocalizations were noted
when possible. We checked the direction of
movement of each mixed-species bird flock and
compared it with the next mixed-species bird
flock detected to assure it was coming from a
different direction to avoid repeatedly recording
data from the same mixed-species bird flocks.
Statistical Analyses. — We used cluster analyses
in PAST 3 (Hammer et al. 2001) and the Jaccard
index to examine if composition of mixed-species
bird flocks differed among three elevation hands
of 150 m each. This also provided information if
mixed-species bird flocks encountered consecu¬
tively were similar. We conducted multiple Chi-
square and Fisher’s exact tests for species
observed in >10% of the mixed-species bird
flocks to identify which species pairs co-occurred
more than expected by chance (Cole 1945). We
designated a species as a potential nuclear species
following Powell (1979) if its’ presence was
correlated with the presence of at least two other
species by Chi-square and Fisher's exact tests. We
also considered qualitative trails that seem to
be related with a cohesive role including: (I)
contrasting or conspicuous plumages. (2) high
occurrence, (3) large intraspecific groups, (4)
conspicuous maneuvers. (5) regular calls, and
(6) a tendency to be followed more than they
followed others (Moynihan 1979, Powell 1985.
Hutto 1994. Sridhar et al. 2009. Goodale and
omTCuimP 201 °’ Harrison and Whitehouse
201 1). We calculated the proportion of occurrence
m mixed-species bird flocks on each elevation
hand for those species considered as potential
nuclear species. Taxonomy and nomenclature
follows Gill and Donsker (2012).
RESULTS
We recorded 42 species (Table 1 ) in 64 mixed-
species bird flocks during 121 hr.s of fieldwork.
Forty percent of all species observ ed participated
regularly (>10% of all events) in mixed-species
bird flocks (Table I ) highlighting the significance
of this behavior in this avian community. Main
other species observed in flocks were occasional
participants; 14 species (22%) were observed only
in one mixed-species bird flock (Tabic 1).
Tanagers (Thraupidae) were represented by die
highest number of species (17) with the Scarlet-
bellied Mountain-Tanager ( Anisognathns igniwn-
tris) being most frequent (recorded in 35 ntixed-
speeies bird flocks). This species was common in
(he area blit was observed more times alone than
in mixed-species bird flocks. In contrast, nine
species were more often in mixed-species bud
flocks than apart from them (Table I). The
number of species and individuals per mixed-
species bird flock ranged from two to 19 (mean -
5.1) and from three to 66 (mean = 1 1.5),
respectively. Some species were observed in
groups of up to seven individuals but most were
recorded in pairs or small groups (Table 1).
Number of species and individuals per mixed-
species bird flock were correlated i r = 0.91).
Mixed-species bird flocks did not cluster by
dittereni elevation bands (Fig. 2), and only a few
flocks in the same elevation band had some
similarity (Jaccard index >0.6). Cluster analysis
also indicated the more similar mixed-species bird
flocks were not observed consecutively, support¬
ing the observation that we did not repeatedly
record the same flock. Mixed-species bird flock*
were more frequent in the morning during 070%
0800 hrs (17% of the mixed-species bird flocks).
We observed mixed-species bird flocks moving
principally in the sub-canopy and the understory
I lie analysis of co-occurrence of species pair*
( Table 2) indicated 15 species pair comparisons
were significant (all P < 0.05) with 10 positive
and five negative. Six co-occurrences could be
deemed significant (y = 0.05) only by chance
because of the multiple comparisons conducted
Five species were observed in two or more
positive co-occurrences (Table 2) and exhibited
several attributes related to nuclear roles in flocks
( Table 3). Those species considered as potential
nuclear species were: Pearled Treenmner {Mar-
Arbelaez-Cortes and Marin-Gomez • MIXED-SPECIES BIRD FLOCKS
575
TABLE 1. Bird species observed participating in mixed-species bird flocks in a high montane zone ol Qumdio, central
.Andes of Colombia. The right column depicts results only from 2005 observations. _
Family/Species
Number of mixed-
species bird Hocks
Number of individuals/ More common wilhin mixed-species
mixed-species bird flock (mean) bird Hocks lhan apart from ihcm
Trogonidae
Trogon personatus
Picidae
Colaptes rivolii
Furnariidae
Sywllaxis unirufa
Margaromis squamiger
Pseudocolaptes boissonneautii
Tyrannidae
Phyllomyias nigrocapillus
Mecocerculus stictopterus
M. leucophrys
Pieitdotriccus ruficeps
Myiotheretes fumigatus
OMoeca nifipectoralis
0. cinnammeivenlris
Hemilriccus granadensis
Cotingidae
Ampelion rubrocristatus
Tityridae
Pachyramphus versicolor
Corvidae
Cyanolyca armilluta
Troglodytidae
Troglodytes solstilialis
Tliraupidac
Cnemoscopus rubrirostris
Henuspingus atmpileus
H. supercUiaris
d. venicalis
Buthraupis montana
B. eximia
B. wetmorei
Anisognathus lacrvmosus
A. igniventris
dubusia taeniata
Iridosomis rufivertex
Tongara vassorii
Coni rostrum si iticolor
Oiglossa cyanea
0. lafresnayii
0 albilatera
Crothraupis stolz/naiwi
Emberuidae
Arremon torquatus
Atlapetes pallidinucha
A. schistaceus
3
1-2 (1.3)
1
3
25
1-7 (1.9)
9
1-5 (1.7)
4
1-2 (1.3)
10
1-3 (1.9)
21
1-7 (3.2)
2
1-2 (1.5)
2
1-2 (1.5)
1
1
1
1
1
1
1
1
1 I
13
1
1-3 (1.7)
2
2
3-5 (4.0)
11
1-4 (1.9)
10
1-7 (2.9)
12
1-5 (2.7)
15
1-4 (2.1)
2
1-3 (2.0)
20
1-4 (1.9)
35
1-5 (1.8)
1
3
19
1-5 (3.3)
19
1-5 (2.3)
20
1-5 (2.4)
8
1-4 (2.5)
6
1-2 (1.8)
1
2
7
2-5 (3.6)
1
1
4
1-5 (3.0)
5
1-5 (2.2)
576
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124, No. 3, September 2012
TABLE 1. Continued.
Family/Species
Number of mixed-
species bird flocks
Number of individuals/ More common within raixeil-species
mixed-species bird flock (mean) bird flocks than apart from them
Parulidae
Setophaga fusca
1
I
Myioborus ornatus
21
1-4 (2.4)
Myiotlilypis luteoviridis
1
3
Icteridae
Cacicus chrysonoim
2
2-5 (3.5)
Fringillidae
Chlorophonia pvrrhophrys
2
2 (2.0)
garornis squamiger). Golden-crowned Tanager
(I rid iso mis ru/ivertex). Blue-backed Conebill
(Coni rostrum silt i color). White-handed Tyrannu-
let (Mercocerculus stictopterus), and Masked
Flowerpiercer ( Diglossa cyanea). We observed
at least one of these species in 43 of the 64 flocks,
and we once observed all five in a single flock.
We cannot be sure whether one of these potential
nuclear species was present unobserved in the
other 21 flocks, or whether some other species
then had that role. Some of the potential nuclear
species varied in their proportion of occurrence in
mixed-species bird flocks along the elevation
gradient (Table 3). For example, the Golden-
crowned Tanager was more common in mixed-
species bird flocks in the higher elevation hand
(3,300-3,450 m). while the Masked Flowerpiercer
was more common in flocks of the lower
elevation band (3.000-3. 1 50 m).
Other species, besides the five potential nuclear
species, that occurred only in one positive co¬
occurrence also had some qualitative traits that
seem to be related with a cohesive role. For
example, the Black-headed Hcmispingus ( Hemi -
s ping us vertical is) and Black-backed Bush Tana¬
ger (Urothruupis stolzjnanni ) were followed by
other species on several occasions, contrasting
with the Golden-crowned Tanager and the Blue-
backed Conebill that seem to be followers, while
the Pearled Treerunner was observed both fol¬
lowing and being followed. The White-throated
Tyrannulet {Mecocerculus leucophrys). Golden-
crowned Tanager, and Blue-backed Conebill in
some mixed-species bird flocks often gave contact
calls while foraging. The Golden-fronted White-
start (Myiohortts omaius). White-handed Tyran-
nulel. Blue-backed Conebill, and Pearled Tree-
runner foraged more often with conspicuous
maneuvers such as sally and hang. The negative
association among the White-throated Tyrannulet
and other species is suggestive of competitive
interaction but we cannot rule out these negative
associations are due to chance based on the
available data. Wc consider it important that the
Masked Mountain Tanager (Buthraupis wet-
morei), a vulnerable and rare species (Arbelaez-
Cortes and Baena-Tovar 2006). was observed in
the paramo within two mixed-species bird Docks
accompanied by tanagers and finches while
foraging in branches at mid-level vegetation,
apparently following the Black-backed Bush
Tanager.
DISCUSSION
The number of species participating in mixed-
species bird flocks in our study area is within the
range reported for other Andean sites ( 10— 75
species) (Poulsen 1996. Herzog et al. 2002.
Bohdrquez 2003. Rodriguez 2003, Arbelaez-
Cortes et al. 2011a), and represent 38% of the
total species known from this area (Arbclaez-
Cortes et al. 2011b: EA-C and OHM-G. pcTS.
obs.j. Our documented species participation ts
below that for other Andean forests iRemsen
1985. Poulsen 1996. Arbelaez-Cortes et al.
201 la). Twenty-one species observed by a- also
have been recorded in mixed-species bird flock'-
in another site at high elevation (3,200-3,800 m)
in this Andean region (Rodriguez 2003). Grib
nine species were shared with mixed-species bird
flocks from mid-elevations (2,200-2.600 nn 11,1
the same mountain slope (Arbelaez-Cortes cl
201 la). These differences are related to species
composition among communities and indicate
mixed-species bird flocks reflect the species :”u'i
of one locality (Hutto 1994. Peron and Crochet
2009). However, four species: Pearled Treerun-
ner. Masked Flowerpiercer, Slaty Brush f |[,L’1
Arbelaez-Cortes and Marin-Gomez • MIXED-SPECIES BIRD I LOCKS
577
C_Flock10
C Flock30
FIG. 2. Cluster analysis, based on the Jaccard index, of mixed-species bird flocks in a high zone of Quindto.
central Andes of Colombia. The named terminals represent flocks and elevation bands are. ■ ’
3.150—3.300 m. and C = 3.300-3,450 m. Shaded names depict those mixed species bird flocks with similarity values -0.6.
578
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 3. September 2012
TABLE 2. Matrix of interspecific associations of species observed in >10% of the mixed-species bird flocks in a mon
tane zone of Salerno. Quindio, central Andes of Colombia. The number of co-ocurrences and P value (among brackets) is
indicated for each species pair. Significant associations {P < 0.05) are in bold type.
M. squarniger M. leucophrys \l ornatus
A. lacrynutsus
C siltieolor
1 rufivertex
T. vassori
II eximia
T. uSitihatU
A. igniventris
16 (0.346) 13 (0.587) 2 (0,993)
7 (0.063)
7 (0.002)
3 (0.246)
2 (0.542)
1 (0.17)
6 (0.703)
M. squarniger
9(0.871) 6 (0.352)
6 (0.468)
13 (0.009)
1 1 (0.084)
5 (0.281)
8 (0.321)
5 (0.788)
M. leucophrys
7 (0.824)
5 (0.541)
9 (0.265)
6 (0.876)
I (0.002)
4 (0.403)
1 (0.027)
M. ornatus
7 (0.971 )
7 (0.971)
4 (0.156)
6 (0.876)
6 (0.716)
7(0.139)
A. 1 aery mo sits
5 (0.662)
3 (0.072)
7 (0.739)
3 (0.228)
5 (0.769)
C. sitticolor
6 (0.796)
6 (0.797)
7 (0.248)
3 (0.362)
1. rufivertex
0 (0.0)
5 (0.97)
5 (0.663)
T. vassori
5 (0.975)
5 (0.663)
B. eximia
5 (0.286)
T. solstitialis
B.. niontana
H. superciliaris
H. verticalis
M. stictopterus
P. boissoneauti
D. cyanea
( Atlapetes schistaceus ). and Golden-fronted
Whitestart, participated in mixed-species bird
flocks at different elevations suggesting this
behavior is important in their biology as well as
for the nine species observed more often within
mixed-species bird Hocks than apart from them
(Table 1). Most of these species are known to be
usually present in mixed-species bird flocks along
the Andes (Hilly and Brown 1986. Fjeldsa and
Krabbe 1990).
Several tanager species participated in mixed-
species bird flocks in our study zone. A similar
pattern has been documented for other sites along
the Andes where tanagers seem to be involved in
cohesion of mixed-species bird Hocks (Moynihan
1979. Bohorquez 2003. Arbelaez-Cortes et al.
20 1 la). Three of the five potential nuclear species
belong to the Thraupidae. Species contributing
significantly to cohesion of mixed-species bird
Hocks share attributes including: contrasting or
conspicuous plumages, high occurrence, large
intraspecific groups, conspicuous maneuvers,
regular calls, and a tendency to be followed more
than they follow others (Moynihan 1979. Powell
1985. Hutto 1994. Sridhar et al. 2009, Goodale
and Beauchamp 2010, Harrison and Whitehouse
201 1 ). Some of these attributes could be used as
signals by other species that follow them or could
be related to enhancing the sensitivity of those
species to predators. The five potential nuclear
species in the Alto Quindio (Table 3) exhibit
some of these attributes, but only share one ot
TABLE 3. Potential nuclear species of mixed-species bird flocks in a high montane zone of Quindio. central Andes of
Colombia. Their proportions of occurrence in the three elevation bands evaluated are indicated. Five attributes related with
cohesive roles in mixed-species bird flocks arc depicted for each species (X = present).
Occurrence in mixed-species bird flocks Attributes related with a nuclear role in mixed-species bird flocks
Elevation Elevation Elevation
_ . band A band B band C
Speoes (3,000-3. 150 m) (3,150-3.300 ml (3.300-3.450
M squarniger
14.3%
37.5%
45.5%
1. rufivertex
0.0%
8.3%
5 1 .5%
C. sitticolor
0.0%
33.3%
36.4%
M. stictopterus
14.3%
16.7%
15.2%
D. cyanea
57.1%
4.2%
9.1%
Large
intraspecific
groups
Conspicuous
maneuvers
Regular
calls
Contrasting
or conspicuous
plumages
Tendency w be
followed by other
species
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
Arbelaez-Cortes and Marin-Gomez • MIXED-SPECIES BIRD I- LOCKS
579
TABLE 2. Extended.
B. monuma
6 (0.967)
2(0.151)
1 (0.041)
6 (0.286)
3 (0.442)
5 (0.604)
2 (0.233)
6(0.174)
4(0.291)
3 (0.459)
H. superciliaris
7 (0.747)
8 (0.015)
0 (0.007)
2 (0.221)
4 (0.47)
5 (0.447)
5 (0.37)
4 (0.42)
3 (0.504)
1 (0.287)
2 (0.66)
H. venicalis
7 (0.475)
7 (0.034)
2 (0.291)
3 (0.574)
5 (0.307)
5 (0.307)
5 (0.248)
4 (0.334)
3 (0.429)
2 (0.673)
3 (0.276)
4 (0.059)
M. slicmpterus
7 (0.476)
7 (0.034)
3 (0.574)
5 (0.371)
2 (0.332)
7 (0.008)
1 (0.132)
4 (0.335)
6 (0.008)
2 (0.674)
3 (0.277)
2 (0.549)
2 (0.49)
P. boissoneauti
5 (0.621)
4 (0.49)
4 (0.328)
3 (0.623)
5 (0.098)
4 (0.288)
3 (0.537)
1 (0.18)
2 (0.64)
2 (0.588)
1 (0.461)
2 (0.485)
3 (0.139)
1 (0.57)
I). cyanea
2 (0.077)
4 (0.378)
2 (0.474)
5 (0.068)
2 (0.516)
3 (0.483)
2 (0.048)
1 (0.243)
2 (0.606)
2 (0.516)
3 (0.163)
2 (0.416)
1 (0.635)
4 (0.016)
1 (0.687)
U. slolznianni
5 (0.3)
3 (0.565)
4 (0.152)
0 (0.052)
0 (0.062)
2 (0.621)
5 (0.020)
0 (0.073)
0 (0.138)
0 (0.186)
1 (0.608)
0 (0.248)
0 (0.285)
0 (0.285)
0 (0.326)
0 (0.373)
them: large intraspecific groups (mean number ol
individuals per flock = 1.9 to 3.3). However,
these attributes were not exclusive ol these five
species. Thus, other species could also be nuclear
in the study zone because we did not observe
these five potential nuclear species in all flocks.
This nuclear role is based mainly on qualitative
data and a precise definition needs turlher
quantitative or experimental approaches (e.g.,
Goodale and Kotagama 2005). We did not find
differences in the composition of mixed-species
bird flocks along the elevation gradient, but some
of the potential nuclear species dittered between
elevations bands. For example, the Golden-
crowned Tanager was mainly observed in the
higher elevation band while the Masked Flower-
piercer was recorded principally in the lower
band. These differences are related with changes
in elevation and habitat where the species occur
(Fjeldsa and Krabbe 1990). as has been docu¬
mented for mixed-species bird flocks in New
Guinea (Diamond 1987). However, switches in
those species with cohesive roles in mixed-species
bird flocks along an elevational gradient deserve
further attention.
ACKNOWLEDGMENTS
Universidad del Quindio (Viccrrectoria de Investigaciones i
provided financial support for held work in ihe tirst slage ol
this project. We especially acknowledge Oscar Baena-Tovar
and J. C. Ospina-Gonzalez for help during some field tnps. A.
G. Navarro-SigUenza. C. E. Braun, and two anonymous
referees made valuable comments that improved this
manuscript. EAC thanks CONACyT-Mexico for a graduate
studies scholarship (# 210543) during writing of this paper.
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Neotropics. Ornithological Monographs 36:713-732
Remsi N, J. V. 1985. Community organization and ecology
of hiuls of high elevation humid forest of the Bolivian
Andes. Ornithological Monographs 36:733-756.
Rodrigue/. (,). 2003. Estudio dc la comunidad avinria fit
la Rcserva Natural Semillas de Agua Paramo de lo>
Valles. Cajamarca. Tolima. Aleteo 9:1-15.
Sridhar, H.. G. Beauchamp, and k. Shanklr. 2009. Why
do birds participate in mixed-species foraging flocks? A
large-scale synthesis. Animal Behaviour 78:337-347.
I ERbORGH. J. 1977. Bird species diversity on an Andean
elevational gradient. Ecology 58:1007-1019.
The Wilson Journal of Ornithology 1 24( 3):58 1 -588, 2012
BIOLOGY OF INVASIVE MONK PARAKEETS IN SOUTH FLORIDA
MICHAEL L. AVERY.14 ERIC A. TILLMAN.1 KANDY L. KEACHER.'
JOHN E. ARNETT.23 AND KELLI J. LUNDY'
ABSTRACT. — Monk Parakeets ( Mxiop&itta monachus) have been m Honda lor -40 >rs ha\ ong ^ been
thousands for the pet trade. This conspicuous, charismatic spec.es ■> now Widely and
about its population biology outside South ‘ body sue and aspects of reproductive
collections by uultty company personnel in 2003/2004 and J«>6/ -00 t tQ the mortachus
biology and primary molt. Body measurements confirm Monk nf females exceeded that of males
-ubspectes. Adult males averaged 15 to 3.5% larger than females, but the
dunng March-May, the period of egg development. The M4u» 5.6 for
spnng with fledglings first appearing in the second week o Arnett c ^ f ^eJamined KJK replacing primary
multiple-entry nests compared to 4.9 for single-entry nests. Over 94 * ot the ad ulto we exam n R ^ ^ jn
others during June-August. The extent and timing of breeding and molt in south _ ; - characteristic of
South America, although offset by -6 months. Monk Parakeets ,n south Honda e arn a Received ,
the ancestral population, bu, their flexible behavior enables them to adapt and thnve in new envrronments.
Savember 201 1. Accepted 3 March 2012.
The Monk Parakeet (. Myiopsilta monachus) is
native to South America, occurring from central
Bolivia and southern Brazil south to central
Argentina (Forshaw 1989). The species has become
established in the mainland United States. Puerto
Rico, Bahamas. West Indies. England. Belgium,
Italy, Spain. Israel, and elsewhere through acciden¬
tal and purposeful introductions (Spreycr and
Bucher 1998). The species first became established
in the United Stales during the 1960s. The Monk
Parakeet in Florida was first recorded breeding in
Miami in 1969 and has been firmly established
since the early 1970s (Owre 1974).
The U.S. Fish and Wildlife Service initiated a
naiionwide control and removal program in the
early 1970s based on the species' reputation as an
agricultural pest in South America. This program
ended in 1975 and reduced the existing population
by approximately one half (Neidermyer and
Hickey 1977). The Monk Parakeet has thrived
since 1975. however, in the USA and has become
an urban/suburban species with no obvious factor
limiting population growth. Monk Parakeets ate
unique among psitlacines as they use sticks and
twigs to construct bulky nests which house from
'U.S. Department of Agriculture. Wildlife Services.
National Wildlife Research Center, Florida Field Station.
2820 East University Avenue. Gainesville. FL 32641. 1 SA.
'Department of Wildlife Ecology and Conservation.
University of Florida, Gainesville. FL 32611. USA.
5 Current address: 56th Range Management Office. Luke
Air Force Base. AZ 85309. USA.
4 Corresponding author; e-mail:
michael.l.avery@aphis.usda.gov
one to many individual nesting chambers (Spreyet
and Bucher 1998). Parakeets in south Florida
build nests principally on man-made structures
such as stadium light poles, cell towers, and
electric utility facilities (Newman et al. 2008).
They exploit backyard bird feeders and non-native
ornamental plants for food. Adverse effects of
predation, diseases, and parasites to Monk Para¬
keets have not been documented in the USA.
Aspects of Monk Parakeet natural history have
been well-documented in its native range (c.g.,
Navarro and Bucher 1990. Navarro et al. 1992a.
Martin and Bucher 1993. Eberhard 1998). Nest-
site selection (Burger and Gochfeld 2000. Pranty
9009) food habits (Hyman and Pruett-Jones 1995.
South and Pruett-Jones 2000). population growth
(Van Bael and Pruett-Jones 1996). nestling
growth and development (Caccamise 1980). and
population genetics < Russello et al. 2008. Gon¬
salves da Silva et al. 2010) have been studied m
the USA. but other basic life history characteris¬
tics have not been quantified. We examined Monk
Parakeets from south Florida to document their
size, reproductive biology, and primary molt. Wc
assessed variation between males and females and
among seasons in these characteristics; the first
•analysis of a Monk Parakeet population outside its
native range.
METHODS
Sources of Birds.— We obtained birds at two
different times. Personnel with Florida Power and
Light Company removed 335 nests from distri¬
bution poles in Miami-Dade and Broward coun-
581
582
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 3. September 20/2
ties during January-October in 2003 and 2004 to
help prevent power outages (Tillman el al. 2004).
Utility company personnel trapped parakeets
during nest removals by adapting a method
developed in Argentina (MarteHa et al. 1987).
Utility crews approached parakeet nest structures
after dark, covered one or two nest entrances
using long-handled nets, and then captured birds
as they flew from the nest (Avery et al. 2006). The
netted birds were euthanized with carbon dioxide
as were any nestlings remaining inside the nest.
All birds from a given nest structure were bagged
together with a record sheet detailing location and
characteristics of the nest structure. The number
of entrances was recorded w hen a nest structure
was removed, but the number of nest chambers
within the nest structure was not ascertained.
Thus, we used the number of entrances as a
minimum estimate of the number of nest cham¬
bers. All contents from a single nest structure
were comingled during the removal process.
Thus, w'c could not assign contents to individual
nest chambers for multi-chamber structures. The
carcasses were frozen and shipped overnight to
the Florida Field Station of the USDA’s National
Wildlife Research Center, Gainesville, Florida for
necropsy. We tagged each carcass with a unique
number and stored the necropsied carcasses in
freezers. Most of the carcasses were discarded in
2010 when they spoiled following failure of one
of the freezers.
We conducted field evaluations of diazaeon, a
candidate contraceptive for Monk Parakeets in
electric utility substations in 2006 and 2007
(Aver) et al. 2008). Utility workers removed 50
nests during April and May as part of the diazaeon
study at four substations which served as
untreated control study sites. There was no effort
to trap adults, but we documented the contents of
the 50 nests.
Body Measurements and Primary Molt.— 'We
measured body mass of each bird on a digital
scale. We measured wing chord, flattened wing,
tail length, tarsus, and exposed cut men (from the
anterior edge of the cere ) for adults and fledglings
(Baldwin et al. 1931), We examined the primary
feathers of each wing anil scored molt following
Ginn and Melville (1983): 0 - old; I - missing or
completely in pm; 2 - just emerging from sheath
up to 1/3 grown; 3 - new feather 1/3 lo 2/3 grown;
new feather >2/3 grown with waxy sheath
remaining; 5 - Ju/ly grown new feather. The
maximum score for each wing was 50. signifying
all fully grown, new feathers. We combined the
molt scores for both wings (maximum score =
100) and summarized the results by month of
collection. We distinguished fledglings from older
birds during June-September by the fresh, unworn
condition of their recently molted plumage
(Navarro et al. 1992b). We also noted that
juveniles had more green on crown and facial
feathers and less yellow on the breast and belly
compared to adults at this time of year.
We dissected each adult and fledgling to
identify males and females, and we measured
the diameter of the largest ovum or follicle in
adult females. We assumed the ova and follicles
were spherical and converted the linear measure¬
ment to volume. Wc also noted the presence or
absence of an incubation patch (Mammal 1974:.
We measured the length and width of both testes
ol adult males. We calculated total testicular
volume (Mollcr 1991). summarized the results by
month, and evaluated population level changes
throughout the year, Few adults were collected in
September, and we combined that month with
October in all analyses. We used one-way
analyses of variance for statistical testing unless
otherwise stated.
RESULTS
Nesting Biology. — Monk Parakeets in south
Florida are seasonal breeders. Testes volume
peaked in March-April and steadily decreased
thereafter (Fig. I A). Females had the same
temporal pattern as mean size of the largest
follicle or ovum increased almost a thousand-fold
Irom February to March and rapidly diminished
after May (Fig. IB). Nests with eggs occurred
from 22 March through the first week of July
(Fig. 2). The nestling period extended from 21
April to 21 July, except for one nest with two
nestlings removed in late August. Total contents
(eggs plus nestlings) of nest structures ranged
from one to 12. Average (± SE) contents of
multiple-entry nests on distribution poles (5.6 ±
0.5; a = 36) exceeded (F , 74 = 5.57; P = 0.021 1
those of single-entry structures (4.4 ± 0.2; n =
40; Table I ).
We recorded incubation patches for 52 of 66
(78%) females during April-July. Eight of 104
(7.7%) females examined in other months had
incubation patches. Females having incubation
patches (// = 52, mean ± SE = 117.8 ± 1.1 g)
during April-July were heavier ( P < 0.001: Fu w
= 17.47) than those without (// = 14. mean ± SE
Avery et al • MONK PARAKEETS IN SOUTH FLORIDA
583
10000 -i
E
£
00
00
cu
o
_o;
o
dUl, “ ^
Monk Parakeets collected in south Florida. 2003-2004. Capped vertical bars denote 1 SE.
100
80
S 60 3
c
0.251 between males and females in each age elass Male measurements exceeded
female measurements for all other characters IP < UJ»5), except for fledgling wmg chonl If - 0.0631. _
Adult
Fledgliny
Male Female
Character
n
Mean
± SE
n
Mean ± SE
Body mass (g)
255
113.7
± 0.5
280
1 1 1.6 ± 0.6
Wing chord (mm)
255
150.2
± 0.2
280
147.9 ± 0.2
Wing flat (mm)
255
155.3
± 0.2
280
153.0 ± 0.2
Tail (mm)
249
138.3
± 1.1
273
138.3 ± 0.8
Tarsus (mm)
64
18.2
± 0.1
66
17.8 ± 0.1
Culmen (mm)
253
20.4
± 0.1
278
19.7 ± 0.1
Male
n Mean - SE
51 105.8 ±1.2
51 149.3 ± 0.7
51 152.6 ± 0.7
51 145.0 ± 1.5
39 18.2 ± 0.1
51 19.6 ± 0.1
Female
ii Mean ± SE
69 100.5 ±1.1
69 147.5 ± 0.7
69 150.1 ± 0.7
69 142.3 ±1.9
65 17.9 ±0.1
69 19.2 ± 0.1
586
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124, No. 3. September 2012
CO
to
03
E
>
TD
o
CD
FIG. 5. Body mass ol adult female Monk Parakeets exceeded that of males only during March-May, which
corresponded to the period of egg-laying.
competition and lack of divergent size or second¬
ary sexual characteristics (Collar 1997, Masello
and Quillfeldt 2003).
We noted incubation patches only among
females, consistent with field observations that
female parakeets, not males, incubate (Eberhard
1998). Nestling Monk Parakeets in south Florida
apparently undergo considerable recession of body
mass prior to fledging (Fig. 4), consistent with
findings from Argentina (Navarro and Bucher
1990). This phenomenon has been documented in
other Psittaciformes (e.g.. Burrowing Panot [Cya-
noliseus patagonus], Masello and Quillfeldt 2002)
as well as in seabirds and swallows (Ricklefs 1968.
Ydenberg et al. 1995). and is believed to result
from interactions between parental provisioning
and nestling departure decisions (Morbev et al.
1999).
Successful invasive species possess behavioral
attributes that enable them to adapt and exploit
key resources in the non-native range (Wright
et al. 2010). Monk Parakeet populations in the
100
pos^ibiemol^ro^isTootdf^ m3'e ^ Pdrakeets (dark bars> ^h[|y lagged that of females (open bars). Maximum
a ing complete replacement of primaries on both wings. Capped vertical bars denote I SE.
Avery et al. • MONK PARAKEETS IN SOUTH FLORIDA
587
TABLE 3. Tinting of biological attributes of Monk
Parakeets in south Florida and Argentina.
Attribute
Florida
Argentina’
Testes enlargement begins
Feb
Aug
Female body mass > male
Mar-May
Sep-Dec
Clutch initiation
mid-Mar
Oct
Peak period of remige molt
Jun-Aug
Fcb-Mar
wiad Bucher 1998.
USA are essentially urbanized (South and Pruett-
Jones 2000.1 in contrast to their native range where
the species is mostly rural. The Monk Parakeet's
ahihty to thrive in human-altered environments
often creates conflicts and the need for aggressive
management (Neidermyer and Hickey 1977.
Avery et al. 2008). Flexible nest-building behav-
'er. which contributes to the Monk Parakeet's
success, is exactly what has created conflict. The
•species is a valued, charismatic component of
'ocal avifauna in many communities, but the
propensity of these birds to select man-made
-Luctures as nesting substrates is increasingly at
odds with safe, efficient operation of electric
u'ilitv facilities (Newman et al. 2008). It would
nnI be surprising if additional conflicts arise as
Monk Parakeets colonize new environments (Sol
e'nl, 1997), given their dietary flexibility (South
jnd Pruett-Jones 2000) and dispersal ability
(Gonsalves da Silva et al. 2010).
ACKNOWLEDGMENTS
binding was provided by the National Wildlife Research
remer and Florida Power and Light (FPL) Company
hrougj] a cooperative research agreement with Pandion
^tems Inc. (J. R. Newman, president). We appreciate the
flc,d avsi&iance and support provided by J. R. Lindsay,
buddy Merchant. Donald HofFmeier. and Joseph Wright of
lp[- during the project. J. R. Eherhard provided helpful
aliments on an earlier version of the manuscript.
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The Wilson Journal of Ornithology 124(3): 589-596, 2012
VARIATION IN THE DIET OF WESTERN BARN OWLS (TYTO ALBA )
ALONG AN URBAN-RURAL GRADIENT
PABLO TETA,1 3 CARINA HERCOLINI,2 AND GERARDO CUETO-
ABSTRACT. — We studied geographic variation in the diet of Western Barn Owls ( Tyto alba ) along a urban-rural
gradient in central-eastern Argentina and identified 5.231 prey items. Mammals were present in all samples, whereas birds
and amphibians were present in 79.1 and 50.09r of the samples, respectively. There were significant ditterences in
vertebrate assemblages consumed by Barn Owls at the opposite extremes ol the gradient. Native sigmodontine rodents
comprised 85. 8^ of the total prey items, especially towards periurban and rural areas. Exotic murid rodents were the main
prey item in urban sites, while birds increased in frequency in urban and periurban areas. Food niche breadth and
standardized food niche breadth values were higher at intermediate levels of urbanization (= periurban). This periurban
peak' in species diversity is a relativ ely well-known pattern, previously reported for taxa such as birds, lizards, bumblebees,
and butterflies among others. The trophic habits of Barn Owls along this gradient were mostly similar to those reported in
other studies in southern South America, where the main prey items were native rodents and tood niche breadth values
'measured at the level of Orders) were low . Western Bam Owls in our study maintained specialization as a micromammal
predator. Received 13 October 2011. Accepted lb April 2012.
The Western Barn Owl (Tyto alba ) is one of the
most common and best-studied raptors in Ihe
world (Marks et al. 1999). Its food habits have
been widely documented throughout its distubu-
lional range, demonstrating this species has a
marked preference for mieromammalian prey
(Taylor 2004). Despite the abundant information
about its food habits in southern South America
(e.g., Bellocq 2000, Bo et al. 2007), its trophic
ecology in temperate latitudes is strongly biased
towards studies in agricultural or relatively
undisturbed grassland areas (e.g., Faverin 1987,
Bellocq 1998. Leveau et al. 2006, Gonzalcz-
bischer et al. 2011). The diet of urban and
periurban-dwelling Barn Owls in this same area
ls poorly known with a few exceptions (e.g..
Massoia 1988, 1989). Literature about dietary
responses at regional scales, especially along
abrupt environmental gradients, is also scarce
le-g-. Travaini et al. 1997, Leveau et al. 2006,
Trejo and Lambertucei 2007).
Bam Owls commonly breed in urban areas that
provide suitable nest sites (e.g.. Salvati et al.
-002), hut the trophic ecology of the species in
Oiese habitats is poorly known. Vargas et al.
(|9S4) indicated birds and reptiles accounted lor
‘Unidad de lnvestigacidn Dfvcrsidad, Sistematica y
Evnluciiin. Centro Nacional Patagfinico. CC 128. 9120
Puerto Madryn. Chubut. Argentina.
Departamento de Ecologia. Genet ica y Evolueion,
Eaculiad de Ciencias Exactas y Naturalcs, Umversidad de
Buenos Aires. Avenida Intendente Giiiraldos 216, Ciudad
Tnivcrsitaria. Pabellfin II, 4 Piso. (C1428EHA). Buenos
Aires. Argentina.
’Corresponding author; e-mail: antheca@yahoo.com.ar
>50Cr of the prey items at urban locations in
southern Spain, suggesting that small mammals
were secondary resources in urban habitats. Use
of alternative prey in urban environments was also
recorded for central Argentina, where bats were
seasonally dominant in the diet of this ow l. Salvati
et al. (2002) and Charter et al. (2007), in contrast,
found high rodent consumption in urbanized
neighborhoods of central Italy and Israel. Under¬
standing food preferences of this species of
special concern in relation to other parameters
(e.g., breeding success, habitat use) may provide
useful information Tor a variety of habitats,
including urban and rural areas (Salvati et al.
2002). The objective of our study was to provide
new information on the trophic ecology of
Western Barn Owls along a urban to rural gradient
in central-eastern Argentina.
METHODS
Study Area. — The area studied is between 34
00 to 34 50’ S and 57 59 to 59^ 11' W, Province
of Buenos Aires, central-eastern Argentina
(Fig. 1), including the City of Buenos Aires and
its influence area or lGran Buenos Aires’. The
area was originally covered by grasslands, patches
of xerophylous forests, wetlands, and subtropical
riverside forests (Cabrera 1968). This landscape
has been gradually modified by agriculture and
human settlement since formation of the city of
Buenos Aires in the 16* century (Morello et al.
2000). Today, this area is one of the most
populated in southern South America with —13
million people (Instituto Nacional de Estadisticas
y Censos; http://www.indec.gov.ar/). The matrix
589
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THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 3. September 2012
FIG. I. Study area, northeastern Buenos Aires Province, central-eastern Argentina; shaded areas represent the surface
on which buildings, paved roads, or other construction replaced the natural substrate (= ‘built habitat’). Sites are arranged
from north to south. Numbers correspond to those in Table 1.
of Buenos Aires is formed by buildings and paved
streets with patches of parks and open green areas
(Morello et al. 2000, Cavia et al. 2009). Towards
the north, west, and south, urbanization is
gradually replaced by pastures and cultivated
fields, where grasses occupy small relicts along
field borders and roads (Soriano et al. 1991). The
landscape in some littoral areas is still composed
of small, highly fragmented, fringes of humid
grasslands intermixed with reduced patches of
riparian thickets and xerophylous forests (Mat-
teucci et al. 1999). The climate is characterized by
mean annual precipitation of 1.014 mm and mean
temperatures of 23 C in January (summer) and
10 C in July (winter) (Murphy 2008).
Data Collection. — Fresh pellets were collected
mostly between 2005 and 2006 at nest and roosting
sites from 24 localities (Fig. 1 ). One to six collections
were made at each site. All results from each roost
were combined, and each site provided only one
sample. Pooling data was necessary to minimize the
effects of possible seasonal and annual biases, given
there were insufficient data to use in the analysis
(Clark and Bunck 1991, Love et al. 2000). Analyses
were performed only with samples from sites with
>1(X) prey items. Studied sites were ordered along a
urban to rural gradient (Table I) considering build¬
ings. paved roads, or other construction that replaced
the natural substrate or the percentage of tree and
herbaceous cover, among others (Table 1; Hercolini
2007). We follow Morello et al. (2000) in delining
‘urban’, ‘periurban’, and ‘rural’. We used the area
covered by human constructions (‘built habitat’.
sens u Whitney 1985) as an approximate measure of
urbanization for statistical procedures (Hercolini
2007. Cavia et al. 2009; Table I). Landscape
variables, including ‘built habitat', were recorded
for each site in an area of 2.5-km radius using die
continuous land classification of Hansen et al. (2002)
and data from MODIS (Moderate Resolution
Imaging Specirorudiometer). We used a 2 5-ktn
radius coinciding with the mean home range of Bam
Ow ls (Hercolini 2007).
Vertebrate prey items were identified to species
level by comparisons with reference collections
housed at die Museo Argentino de Ciencias Natural^
‘Bernardino Rivadavia’ (Buenos Aires. Argentina).
We computed die food niche breadth for each sample
(FNB = 1/(Y pi:) where pi is the proportion ot each
class i in the diet (Orders = class) and the
standardized food niche breadth iFNBst = FNB
I )/(;? — 1 ) where n is the total number of prey classes
(Marti 1987). A Principal Component Analyst
(PC A) was performed using software Infostat Di
Rienzo et al. 2010) to detect and describe changes in
the composition and abundance of prey categories;
i.c.. Orders Anura, Columbiformes. Passerifom*”'-
Didelphimorphia. Chiroptera. Rodcntia (native anJ
exotic species were considered separately following
Clark and Bunck 1991), and Lagomorpha.
Teta et al • VARIATION IN WESTERN BARN OWL DIETS
591
RESULTS
We identified 5,152 prey items, mostly native
sigmodontine and exotic murid rodents (Table I ).
Mammals were present at all sites, whereas birds
and amphibians were present at 79.1 and 50. (Ur ot
the sites, respectively (Table I ). We identified
4.815 mammals of which 4,729 (98.2%) were of
species with mass <250 g. Larger mammals
(>500 2) occurred in low frequencies and
nduded young lagomorphs ( Lepus europaeiis),
caviomorphs ( Cavia aperea ), and marsupials
(Didelphis albiventris).
The native sigmodontine rodents Akocloit
azarae, Calomys spp. (including C. laucha and C.
nmculinus), and Oligoryzomys flavescens com¬
posed 85.8% of the total prey items (Table I ).
These species were prominent toward periurban
{ Akodon azarae, Oligoryzomys flavescens) and
rural ureas (Calomys spp. ). and were replaced bv
exotic murid rodents, such as Mus musculus and
Rottus spp. in urban settlements (Table 1. fig. 2).
Birds, especially passerines, were present in low to
moderate proportions (0.4-40.0%) in most sam¬
ples. increasing in frequency al urban and periur¬
ban areas (Table 1, Fig. 2).
FNB varied between LOO and 2.92. while FNBsl
varied between 0 and 0.48; both parameters
increased in values at intermediate levels oi built
Habitat, decreasing towards the extremes ol the
gradient and describing second order polynomial
functions (R: = 0.655 and R: - 0.468, respectively).
The two first axes generated by PCA analysis
accounted for 99.3% of the variance in the diet
'Fig, 2). Representation of sites and prey categories
i.e.. Orders Anura. Columbiformes, Passeriformes.
Didelphimorphia. Chiroptera. Rodentia [exotic].
Rodemia [native], and Lagomorpha) defined by
'he two first factors segregated urban from periurban
and rural samples. Prey in urban sites included
mostly exotic murid rodents, while in periurban and
rural areas the most common prey were native
sigmodontine rodents (Fig. 2. Table I). Birds were
more abundant at urban and periurban areas.
DISCUSSION
Bam Owls feed primarily on micromammalian
prey with weights between 10 and 150 g (Taylor
2004). Stenophagy and specialization, which are
characteristics of these owls, decrease when the
diversity and abundance of its main prey decreas¬
es (Taylor 2004). Birds, amphibians, arthropods,
and bats have been reported as prey of Barn Owls
when preferred micromammalian prey species
declined (Vargas ct al. 1984. Bose and Guidali
2001 ). such as in urban areas (Charter et al. 2007).
However, our study documented that small
mammals represented the main prey items, and
were only partially replaced by other taxa at some
sites (e.g.. by birds in some urban and periurban
areas [e.g., sites 12. 13, 16; Fig. 1 1 or amphibians
near wetlands or water courses |e.g.. sites 4. 15:
Fig. I|). Barn Owls in our study, unlike other
birds of prey that switch their diet from small
mammals in rural areas to birds in cities (e.g..
Yalden 1980. Pikula et al. 1984. Kubler et al.
2005). maintained their selectivity as micromam¬
mal predators. Dominance of small mammals in
the diet at all sites explained the low values tor
FNB and FNBst. Overall, our results are in
agreement with those ot Bellocq (1998). Leveau
ct al. (2006), and Gonzalez-Fischer et al. (201 1)
who studied food habits ot Barn Owls at similar
latitudes in central-eastern Argentina: they also
found high predation on micromammalian picy
and low values of food niche breadth (at the level
of Order) for this species.
Urban development produces some of the
greatest extinction rates and frequently eliminates
the large majority of native species (McKinney
2002 and references therein). This is certainly true
in the case of native sigmodontine rodents, which
were almost completely replaced by exotic rats and
mice in urban areas of central-eastern Argentina
(e.g.. Massoia and Forties 1967, Cavia et al. 2009).
Hercolini (2007) described in detail the micro-
mammal communities along the same gradient that
we studied and suggested that exotic rodents, such
as Rati us spp. and Mus musculus prevail at the
urbanized extreme, while mice of the genus
Calomys spp. were the most frequent species in
rural areas. High proportions of some native
species (e.g.. Akodon azarae , Oligoryzomys Jlaves¬
cens) occur at middle portions ot the gradient in
periurban areas surrounded by large patches of
parklands and spontaneous vegetation (Hercolini
2007: Tabic 1). This ‘periurban peak' in species
diversity is a relatively well-known pattern,
previously reported for taxa such as birds, lizards,
bumblebees, and butterflies (Racey and Euler
1982. Pawlikow ski and Pokomiecka 1990. Blair
2001. Germaine and Wakeling 2001 ). 1 he increase
of FNB and FNBst values at intermediate urban¬
ization levels in our study agrees with this pattern.
It is usually accepted that Bam Owls may
capture commensal rodents in low frequencies.
TABLE 1. Relative frequency (%) of prey items in Western Barn Owl pellets sampled along an urban to rural gradient in northeastern Buenos Aires province, central-eastern
Argentina (see Hercolini 2007 for more detail about the site arrangement along the gradient ). Numbers correspond to those in Fig. I . Abbreviations: FNB = food niche breadth, FNBst
= standardized food niche breadth.
592
THE WILSON JOURNAL OF ORNITHOLOGY • Vul. 124. No. 3. September 2012
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Teta et al. • VARIATION IN WESTERN BARN OWL DIETS
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594
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 3. September 2012
Passenformes
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FIG. 2. Representation of sites (black dots) and Western Barn Owl prey categories (open circles) on the plane defined
by axes I and II ot a principal component analysis. Numbers for urban settlements correspond to those in Table 1.
even in anthropically modified areas (e.g., Clark
and Bunck 1991, Magrini and Facure 2008).
However, we found high consumption rates of
exotic rats and mice at the urbanized extreme of
our gradient, demonstrating the opportunistic behav¬
ior of Bam Owls under certain environmental
conditions (Taylor 2004). Commensal rodents arc
mainly associated with human activities, and an
increase in their abundance in Bam Ow l diets can be
used as an indicator of environmental degradation
(Clark and Bunck 1991). Moderate to high frequen¬
cies of exotic murid rodents were also repotted in the
diet of this owl at other periurban localities of
southern South America (e.g., Nores and Gutierrez
1990. Gonzalez Acuna et al. 2004).
The dominant prey species along the study
gradient of the entire sample was Oligvryzomys
flavescens, the main hantavirus reservoir in
central-eastern Argentina (Enria and Levis
2004). Hantaviruses are infectious agents dissem¬
inated by rodents in several parts of the world
(Enria and Levis 2004); they cause Hantavirus
Pulmonary Syndrome (HRS) with a lethality that
reaches 50%, which is transmitted to humans
through inhalation of particles in excretions of wild
rodents. The expansion of urban areas is a reality in
the present world (e.g., McKinney 2002) and
political actions are needed to preserve minimum
spaces o 1 natural habitats that ensure maintenance
°f Predator-prey relationships. Barn Owls may
have an important role in control of O. flavescens.
especially at periurban places of central-eastern
Argentina, where ~ 1 3 million people live and HPS
is an endemic disease (Busch et al. 2004).
ACKNOWLEDGMENTS
Emiliano Muschetto and Martin Zamero participated in
collection and disaggregation of owl pellets. U, F. J
Pardinas provided some of the samples and literature, and
made valuable comments on an earlier version of diis
manuscript.
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Clipperton Island: Life History Consequences and Insight into Etiology
Robert L. Pitman,13 Lisa T. Ballance,1 and Charles A. Bost-
ABSTRACT,— ‘Angel wing’ is a developmental
wing deformity among birds that can cause flightless¬
ness: it is mostly known from domestic birds, especially
waterfowl, and has only rarely been reported among
wild bird populations. We estimated ihat 508 (4.9%)
Masked Booby (Sula ( lucivlatra ) chicks on Clipperton
Island (10 18' N. 109 13' W) in the eastern tropical
Pacific Ocean exhibited angel wing during March 2005.
Both hatching-year birds and after- hatching-year birds
exhibited the condition; the latter included seven
flightless birds in adult plumage (i.e.. minimum 2 yrs
of age) which were still being fed by their presumed
parents. The angel wing outbreak coincided in time with
high nestling mortality, apparently related to food
shortage, and we speculate on causal linkages. Received
8 December 201 1 . Accepted 10 March 2012.
’Angel wing’ is a musculoskeletal disorder that
can result in permanent wing delormity and
flightlessness in birds (Rear 1973). The proximate
cause is a deformity of the distal end ot the
carpometacarpus, which at times causes the
primary flight feathers to droop when the wing
is folded next to the body, or it can result in a
dorsolateral rotation of the primaries, causing
them to twist and project outward (Rear 1973,
Zsivanovits et al. 2006). The resulting appearance
gives rise to the 20 or more common names tor
this condition, depending upon whether the
primaries twist (e.g., flip. tilt, airplane, or angel
wing), or droop (e.g.. slipped, dropped, or drooped
wing). Symptoms begin during the chick stage,
apparently as primary feather growth exceeds
the development of the supporting tissue ot the
carpus. The condition can occur unilaterally or.
less commonly, bilaterally; unilaterally, it occurs
much more commonly on the leli than the right
wing, and more commonly among males than
females. It can be successfully treated in captive
'Protected Resources Division. Southwest Fisheries
Science Center. National Marine Fisheries Service. NOAA.
La Jolla Shores Drive. La Jolla. CA 92037, USA.
J Centre d' Etudes Biologiqucs de Chizc. CNRS. 79360
Villiers en Bois. France.
3 Corresponding author; e-mail: robert.pitman@noaa.gov
birds (Zsivanovits et al. 2006). but is probably
mostly fatal among birds in the wild due to the
consequences of flightlessness.
Angel wing has been reported far more
commonly among domesticated birds or wild
birds raised in captivity than among birds in the
wild. The vast majority of reported cases have
been of waterfowl, but it has also occurred among
psittacines, raptors, bustards, herons, and cranes
(Rear 1973, Serufin 1982. Naldo et al. 1998.
Thompson et al. 2006. Zsivanovits et al. 2006).
Other wild waterbirds diagnosed with angel wing
have included Double-crested Cormorants (Pha-
lacrocorax cturitus ) nesting in Canada (Ruiken
et al, 1999) and American White Pelicans
(P elec anus erythrorhynchos ) nesting in Minne¬
sota (Drew and Rreeger 1986). To our knowledge,
angel wing has not been reported among wild
populations of any marine birds. We document a
high incidence of angel wing among Masked
Boobies (Sula dacytylatra) at Clipperton Island
in the eastern Pacific Ocean, comment on its
etiology, and discuss some lite history conse¬
quences of its occurrence.
METHODS
Study Area. — Clipperton Island (10 18' N,
109 13’ W) is an isolated, uninhabited, French-
owned atoll in the middle of the eastern tropical
Pacific Ocean. -1,280 km w'est of the coast of
Mexico (Fig. 1 ). It is ~4 km long and 3 km wide
with a large central lagoon: it is tiny (1.7 km2 of
total exposed surface area), but is home to the
largest Masked Booby colony in the world
(Pitman et al. 2005).
Procedures— We participated in a private
French scientific expedition to Clipperton Island
(Charpy 2009) where we studied the diet of
Masked Boobies nesting there during 3-27 March
2005. Five w'eeks prior to our visit (3-28 Jan), and
as part of the same expedition. H. Weimerskirch
and M. Le Corre also conducted booby research
on the island (Weimerskirch et al. 2008. 2009).
597
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THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124. No. 3. September 20/2
OBSERVATIONS
One ot us (RLP), during eight previous visits to
the island (from 1985 to 2003), had occasionally
noticed Masked Booby chicks with deformed
wings, but during March 2005 the number was
much larger. This condition prevents affected
chicks from ever flying or leaving the island.
We surveyed the entire atoll during 11-12
March 2005 and counted 10.375 individual
Masked Booby chicks. Clipperton is a low, flat
atoll with almost no vegetation and the entire
population was counted easily. We subsampled
the chick population on 11-12 March to ascertain
the percentage of individuals with deformed
wings. We used a stretched, 22-m length of poly¬
propylene line and made a series of strip transects
between pre-determined landmarks, zigzagging
between the lagoon side and the ocean side
around the entire island. We had one person
olding each end ot the line and one person in the
middle, which allowed us to count every chick
wuhm the transect, dead or alive, and note those
w.th deformed wings. We sampled 1,019 live
chicks using this method, corresponding to 9.8%
of ‘he total chick population; of those. 50 (4.9%)
individuals had deformed wings, including 45
(4.4%) hatching-year (HY) and five (0.5%) after¬
hatching-year (AMY) individuals. We extrapolat¬
ed to the total population and estimated that
508 chicks on the island at the time had wing
deformities, including 456 HYs and 52 AHYs.
DISCUSSION
Birds with deformed wings exhibited three
modal plumages and. because Masked Boobies
breed synchronously at Clipperton Island (Wei-
merskirch et al. 2008; RLP. pers. obs.). we
inferred these modes represented at least three
separate year classes (plumage descriptions in
Nelson 2005). HY had dark backs, heads, and
necks r Fig. 2A), often with some downs plumage.
Many HYs were flying around the colony during
the daytime by the end of our stay (27 Mar), but
still returning in the afternoon or evening to be fed
by the parents. Some AHYs had white heads,
necks, and upper backs, but still had residual dark
flecking on the rump, lower back, and on the
greater coverts of the upper wing (Fig. 2B); these
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599
„ —
* — - "»— = — ati" phwosraph was
taken the chick was fed.
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THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124. No. 3. September 2012
were 1-2 year old birds. Flying birds in this
plumage are normally rare at Clipperton because
most fledglings begin a nomadic phase and do not
return to the colony until they are full adults
(Kepler 1969. Nelson 2005). The third plumage
was the lull adult stage: all white except for black
flight feathers and tail (Fig. 2C); birds in this
Plumage were in their third year or older.
The degree of wing deformity varied among
birds, from relatively slight in one wing (Fig. 2C),
to major deformities in both wings (Fig. 2B). The
majority of affected birds had only one deformed
wing; relatively few had both. The outward
appearance ot the deformity was also variable.
Some birds had the classic outward rotation of the
primaries when the wing was folded against the
body, presenting the angel wing appearance
(Fig. 2B), while others (the majority) displayed
only drooping primaries; the so-called slipped or
dropped wing condition (Fig. 2A).
We saw at least seven Masked Boobies in adult
plumage during our stay that, because of wing
deformities, were flightless and still being fed by
their presumed parents (Fig. 2C). This is. to our
knowledge, the longest period of time (min -
2 yrs) that parents ot any bird species have been
recorded feeding dependent young. The only
remotely comparable situation of which we are
aware involves another seabird, the Great Frigate-
bird ( Fregata minor), which has a fledging period
of up to 169 days with post-fledging feeding by
the parents for up to an additional 428 days (total
587 days; Schreiber and Burger 2002:670). Our
observations also suggest the time and age at
which Masked Boobies terminate parental care is,
at least in some cases, affected by the chick and
not by the adults.
The etiology of angel wing is unknown but
some of the suggested causes have included
vitamin or nutrient deficiency or imbalance
(Zsivanovits et al. 2006). elevated protein con¬
centration in the diet (Kear 1973), elevated levels
of contaminants (polychlorinated biphenyls, poly¬
chlorinated dibenzo-p-dioxins. and polychlori¬
nated dibenzofurans; Thompson et al. 2006), or
a genetic effect, perhaps due to inbreeding after a
bottleneck event (Kreeger and Walser 1984. Drew
and Kreeger 1986). Some specifics about the
outbreak at Clipperton shed some light on these
role in the occurrence of the observed angel wing.
Under normal conditions during the chick-feeding
stage, foraging adults depart the island in the
morning, feed and return to the nest by dusk; on
average they range only 103 km off the island
with a maximum of 242 km (Weimerskirch et al.
2008). Thus, it seems unlikely that chicks raised at
Clipperton were exposed to any significant
sources of anthropogenic contamination.
A direct genetic effect is a possibility but also
seems unlikely (Kear 1973), at least in part
because none of the afflicted individuals would
ever successfully breed. Kreeger and Water
( 1984) documented nine cases of angel wing in
a population of Giant Canada Geese \Branm
canadensis maxima) breeding in and around
Minncapolis-St. Paul, Minnesota. That subspecies
was once thought to be extinct and. because
current stocks were derived from very small
populations (as few as 1 pair in some casest.
Kreeger and Walser (1984) suggested the angel
wing condition may have been a genetic disorder
resulting from inbreeding. Masked Boobies at
(. lipperton Island also experienced a bottleneck
event, although perhaps not as extreme as in the
case ol Giant Canada Geese. Pigs were introduced
on Clipperton in 1917 and by 1958 the once
massive Masked Booby population had collapsed
to an estimated 150 individuals (Stager 1964). The
pigs were eliminated, and by 2003 the population
had rebounded to >100.000 individuals (Pitman
et al. 2005). The prevalence of angel wing at
Clipperton based on our visits to the island seems
to vary considerably from year to year, which
suggests it is more likely linked to some factors)
other than genetics. Wc also saw at least one
Brown Booby (S. leucogaster ) chick with this
condition in 2005, perhaps further evidence the
condition is not inherited.
Excess protein in the diet has often been cited
as a possible cause of angel wing (Kear 1973.
Serafin 1982, Zsivanovits et al. 2006. Meredith
and Keehle 201 1). However, Masked Boobies at
Clipperton normally feed on a high protein diet
comprised almost exclusively of flyingfish ( Exo-
coetidae), and smaller amounts of ommastrephid
squid ( Ommastrephidae ) and other fish (Wei¬
merskirch et al. 2008: R. L. Pitman and L. T.
Ballance in prep.). Angel wing has also been
The sheer isolation (Fig. 1) and lack of
inhabitants at Clipperton almost certainl
dudes the possibility of contaminants ha:
reported in wild populations of Double-crested
Cormorant and White Pelicans (Drewr and Kree¬
ger 1986. Kuiken et al. 1999), two species that
also feed almost exclusively on fish. The only
SHORT COMMUNICATIONS
601
dietary changes that could possibly have contrib¬
uted to the development of this condition at
Clipperton would have been either a change in the
ratio of fish and squid consumed, or an overall
food shortage.
Another possible cause of angel wing could he
adult boobies acting aggressively toward other
chicks. For example, non-breeding adult Nazca
Boobies (A grant! ) have been documented to
attack nestlings of Blue-footed (5. nebonxii). Red-
footed (S. sula). and other, nonfumilial Nazca
boobies, resulting in lacerations on the chicks
bodies, broken wings at times, and occasionally
death (Nelson 1978. Townsend el al. 2002.
Anderson et al, 2004, Muller ei al. 201 1 ). These
interactions have purportedly resulted in twisted
wings' among the chicks, hut for three reasons, we
do not believe such aggression is the cause ol angel
wing. First, nearly all documented cases ol angel
wing have involved domesticated waterfowl and
the explanations that have been offered for its
occurrence have not included aggression towards
nestlings by adults, which should be fairly evident
among birds raised in captivity. Second, angel
wing has also been documented among hand-
reared birds in a variety of species, more evidence
that it is not aggression-induced. Third, we have
seen no evidence of other damage (e.g... lacerations
to the head and body) to chicks, including those
with angel wing, which is commonly evident when
adult Nazca Boobies attack chicks (Anderson et al.
2004). We conclude adult aggression is not the
cause of angel wing on Clipperton, although we
cannot rule it out entirely.
Evidence .suggests there was a food shortage at
Clipperton, which resulted in a major chick die-olt.
and this clearly coincided with and may have
contributed to the high incidence ol angel wing.
We counted 167 dead chicks during our strip
transect survey. These birds appeared to have died
fairly recently < we estimated within the prev ious 3-
4 wks) and were from the current cohort ol chicks
still alive on the island. We divided the number ot
dead chicks by the total number of live plus dead
chicks on our transects, minus the AHA chicks
(167/1.019 + 167 - 5) to estimate the number of
chicks that had died recently. We extrapolated the
resulting 14.1% mortality rate to the entire island
and estimated a minimum of 1.703 Masked Booby
chicks had died during the recent event.
This was apparently part of an even greater die¬
off. Weimerskirch et al. (2009) counted 19.686
active Masked Booby nests (36% with eggs, 64%
with chicks) on the island in January 2005; thus,
the 10,375 chicks we counted 2 months later
represenled a loss ol 9,31 1 nests, a 47.3%
reduction. The die-off occurred mainly during
February because Weimerskirch et al. (2009)
reported ' normal’ feeding during January and,
when we were there in March, adult Masked
Boobies were bringing heavy loads to lecd chicks.
We infer the die-off was due to a food shortage
because prc-fledging mortality among chick
boobies is usually due to starvation ( Anderson
1993). All previous large-scale nesting failures
and chick die-offs documented at booby colonies
have also been attributed to food shortages (e.g..
Dorward 1962. Schreihcr and Schreiber 1984.
Anderson 1989). We know of no records of
epizootic disease causing large scale mortalities in
any sulid species (Nelson 2005:1 15).
There are at least two reasons why boobies
might have experienced reduced foraging success
at Clipperton in early 2005. Masked Boobies, like
many other seabirds in the eastern tropical Pacific
(FTP), depend heavily on feeding schools of
yellowTin tuna ( Thuwms alhacares ) to drive prey
to the surface and make it available ( Au and Pitman
1986, Ballance et al. 1997). Catch rates for
yellowfin tuna in the FTP in 2005 were lower
than average, and fish caught were of smaller size
(1ATTC 2006); this alone could have resulted in
reduced feeding opportunities at Clipperton. In
addition, commercial fishermen in the ETP not
only target the same tuna schools that boobies rely
on. but often use feeding bird flocks to help them
locate tuna schools (Perrin 1969, Au and Pitman
1986). It may be significant that Weimerskirch et al.
(2009) reported (hat up to seven luna purse seiners
were present al Clipperton Island during their visit
in January 2005. That a Beet of tuna purse seiners
was operating in the waters around the island just
prior to the time when the colony suffered a major,
probably food-related, chick die-off. further em¬
phasizes the possible negative impact that tuna
fishing can have on seabird foraging in the ETP
(Ballance et al. 1997. Ballance and Pitman 1999,
Weimerskirch et al. 2008). Further research at
Clipperton Island could provide not only key
information on the etiology of angel wing among
bird populations, but could also shed some light on
the possible impact of industrial -sc ale tuna fishing
on a globally important tropical seabird population
(Weimerskirch et al. 2008).
Prepared skeletons of tw o Masked Boobies and
the one Brown Booby with angel wing from
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THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124, No. 3. September 2012
Clipperton in 2005. along with radiographs of all
three specimens, are housed at the San Diego
Museum of Natural History (SDNMH 51044.
51046. and 51045, respectively).
ACKNOWLEDGMENTS
We gratefully acknowledge J.-L. Etienne for organizing
the 2005 Clipperton scientific expedition and supporting
our participation. A. E. Henry. D. J. Anderson (and
students), and an anonymous referee provided useful
comments on an earlier draft of this paper.
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The Wilson Journal of Ornithology 124(3):603-607, 2012
Fledgling Peruvian Pelicans (. Pelecanus thagus) Attack and Consume Younger
Unrelated Conspecifics
Maximiliano Daigre,1 Paulina Arce,' and Alejandro Simeone1 2
ABSTRACT. — Aggression between chicks and fledg-
lings. at limes ending in siblicide and cannibalism, has
been mostly studied among nest mates. It is Frequent
among colonial-nesting birds and is usually related to
competition for limiting resources (e.g.. food and space)
and competitive disparities between siblings, among
other factors. We report three observations of fully-
grown Peruvian Pelican l Pelecanus thagus t fledglings
attacking unrelated eonspecitlc nestlings at a breeding
colony in central Chile. One case ended in cannibalism.
Five elements were common in all three cases: ( I )
nestlings that were attacked were left unattended by their
parents in the nest. (2) nestlings that were attacked were
newlv hatched (up to 5 days of age). (3) aggressors were
fully-grown fledglings (60-75 days of age). (4) aggres¬
sive fledglings always attacked nestlings in groups, and
(5) all cases were observed late in the breeding season.
We suggest aggression toward and cannibalism of
nestlings by fledglings arc opportunistic behaviors, based
on the opportunity of finding unattended nests and arc
triggered by food deprivation, although hormonal
mechanisms may also be involved. Our observations
constitute the first report of aggression and cannibalism
hy Peruvian Pelican fledglings. Received 20 January
2012. Accepted IS April 2012.
Aggression in chicks and fledglings has been
typically studied in the context of sibling rivalry
'Gill 2007 ). Aggression may positively relate to
food limitation; nest mates compete for food and
aggressive interactions may end in siblicide
(Mock 1984. Mock and Parker 1997) and even
cannibalism (Stanback and Koenig 1992). Mock
cl al. (2009) suggested besides competition for
food, the way in which food is provisioned to
chicks, weaponry, competitive disparities between
siblings, and spatial confinement are also impor¬
tant factors driving siblicide. These conflicts are
most frequent in dense breeding colonies, where
there is competition lor limited resources such as
food and nesting space (Mock 1984. Stanback and
Koenig 1992).
1 Departamento de Ecologia y Biodiversidad, Facultad de
Ecolugia y Recursos Naturales. IJniversidad Andres Bello.
Republica 470. Santiago. Chile.
Corresponding author; e-mail; asimeone@unab.cl
Aggressive acts among seabirds and between
siblings involving siblicide (Drummond 1987;
Anderson 1990a. b) and cannibalism (Stanback
and Koenig 1992), have been well documented in
Pclccani formes, particularly boobies (Sit la spp.) and
pelicans (Pelecanus spp.). Sachs and Jodice (2009)
observed aggression among sibling Brown Pelicans
(P. occidentalism and Nelson (2005) reported
siblicide as consequence of fights for food by this
species. Smith and Munro (2008) observed canni¬
balism by Australian Pelicans (P. conspicillatus ) of
small chicks hy young from the same season. We
report the first observations of aggression and
cannibalism among unrelated Peruvian Pelican (P .
tlutgus) chicks at a breeding site in central Chile.
METHODS
We conducted observations at Pajaro Nino
Island (33 21' S; 71 41 1 W ) in Algarrobo, central
Chile. Pajaro Nino is a 3-ha island that was joined
to the mainland in 1977 lo build a marina. The site
regularly supports colonies of Humboldt Penguins
(Spheniscus luunholdti). Neotropic Cormorants,
(Phalacrocorax hrasilianus). Kelp Gulls (Lams
dominicanus), ancl Peruvian Pelicans (Simeone
and Bernal 2000, Simeone et al. 2003). Peruvian
Pelicans in the area breed asynchronously, laying
from mid-December throughout mid-April with the
last chicks fledging in June. Breeding numbers
ranged from 4.000 pairs in 2009/2010 to 7,000
pairs in 2010/201 1 (pers. obs.).
Two observers visited and observed the pelican
colony every' 15 days from December to June (each
time from 1200 lo 1600 hrs) during the 2009/2010
and 2010/2011 breeding seasons using 10 X 42
binoculars. Canon SX10 IS and Canon SX20 IS
digital cameras were used to collect photographic
data. We documented at each aggression event:
number and age of birds involved, duration of the
event, and outcome ot the aggression (attacked bird
injured, survived and left alone, killed, or bird
predated). The ages of involved chicks followed
the description of Schreiber (1976) for Brown
Pelicans and our own observations.
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THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 3. September 2012
FIG. I. Sequence of Peruvian Pelican fledglings attacking a conspecific nestling. Algarrobo. central Chile. 27 March
2010. Photographs by M. Daigre.
RESULTS
A group of five fully-grown pelican fledglings
(ranging in age from 60 to 75 days) approached
an unattended nest on 27 March 2010 containing a
5-day old chick (Fig. I A). One of the fledglings
seized the small chick by the neck (Fig. IB) and
moved it 2-3 m from the nest by means of pecks.
This action continued for 20 min and all
aggressors participated simultaneously by pecking
the small chick in different body parts. An adult
Kelp Gull approached the group (Fig. 1C) and
attempted to steal the small chick. Three pelican
fledglings persisted in the aggression along with
the gull (Fig. ID). Finally, the gull took over the
small chick, killed and subsequently consumed it
(Fig. IE).
A group of four fully-grown fledglings (75 days
of age) approached an unattended pelican nest on
10 April 2010 containing three chicks, ranging in
age from 5 to 10 days. The aggressors unsuccess¬
fully attempted to grab the smallest chick and pull
it Irom the nest and subsequently aborted ihe
aggression. No photographic records are available
for this event.
A group of five fully-grown pelican fledglings
(age 60 days) on 19 April 201 1 approached an
unattended pelican nest which contained a single
5-day old chick. One of the fledglings seized the
small chick by the head (Fig. 2A) and moved it a
few meters front the nest (Fig. 2B). Subsequently,
three more fledglings (age 75 days) joined the
group along with a Kelp Gull: the latter attempted
to steal the chick (Fig. 20. but the fledglings
chased the gull from the group (Fig. 2D). Shortly
after, a 60-day of age pelican grabbed the chick
and placed it into its gular pouch (Fig. 2E) and
SHORT COMMUNICATIONS
605
FIG. 2. Sequence of Peruvian Pelican fledglings attacking and consuming a conspecific nestling. Algarrobo, central
Chile. 19 April 2011. Photographs by M. Daigre.
606
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 3. September 20/2
attempted several times to swallow it. In one of
these attempts, the small chick fell to the ground
and was rapidly captured by another pelican
fledgling (75 days of age). This last bird moved
from the other pelicans with the chick in its heak
and subsequently placed it into its gular pouch
(Fig. 2F. G). This fledgling started to swallow the
small chick with repeated head and neck move¬
ments until it was completely ingested (Fig. 2H).
The pelican then returned to the group of
aggressors. The cannibalism event was nearly
45 min.
DISCUSSION
Aggression between chicks of the same species
has been widely reported in the literature, partic¬
ularly among nest mates (at limes resulting in
siblicide and sibling cannibalism) of herons, gulls,
hawks, and owls (Sianhack and Koenig 1992). Our
observations report groups of fully grown Peruvian
Pelican fledglings (60-75 days of age) attacking
and consuming smaller (5 days of age) pelican
chicks within neighboring nests. Guerra and
Cikutovic (1985) observed fully-grown Peruvian
Pelican fledglings (similar in age to the agressors
observed in this study) approaching unattended
conspecific nests and pulling nest material out
of the nest, but no aggression or canibalism to
nestlings was evident.
Harassment and consumption of conspecific
chicks by fledglings is an unusual behavior,
different from typical siblicide. Siblicide occurs
among nest mates and is directed to reduce com¬
petition for food delivered by parents (Mock
1984, Mock and Parker 1997). but aggression to
and consumption of unrelated conspecil'ies seems
to be primarily motivated by the nutritional value
of cannibalism anti has been reported in colonial -
nesting species, including American White Ibis
( Eudocimus albus ) (Herring et al. 2005), Austra¬
lian Pelican and Australian White Ibis (Thres-
kiornis molueeus) (Smith and Munro 2008), and
Black-crowned Night Heron {Nycticorux nyai-
corcix) (Riehl 2006). Young/fledglings in all
cases, attacked and consumed small chicks from
unguarded nests or nestlings on the ground that
had fallen from nests.
We identified five common elements in all
three observed cases of aggression. (I) All
attacked nestlings were unattended by their
parents in the nest which allowed aggressors to
avoid confrontation with guarding adults. This
suggests aggression and cannibalism of nestlings
by fledglings were opportunistic behaviors, ex¬
hibited only when an unattended nest with chicks
was discovered. (2) All attacked nestlings ranged
in age from newly hatched to 5 days of age
The small nestlings that served as a prey item for
the aggressors were defenseless and easy
to swallow. (3) All aggressors were fully-grown
fledglings, typically 60 days or older. (4) Ag
gressive fledglings always attacked nestlings in
groups of 4 to 8 individuals, never alone. (5) All
cases were observed late in the breeding season
(Mar-Apr). All victims were from late breeding
parents and aggressors were from the first-hatched
birds in the colony. Thus, occurrence of aggres¬
sion and cannibalism needs a certain asynchrony
within the colony and is restricted to short periods
during the breeding season, mainly when fully-
grown fledglings coexist with newly hatched
chicks.
One explanation for the observed behaviors
could be related to food deprivation of fledglings.
Adults of colonial nesting seabirds normally
leave fledglings unattended and feed them at
irregular intervals thus exposing them to periods
of fasting (Stanback and Koenig 1992. Shealer
2002. Smith and Munro 2008). This situation is
consistent with our observations; 7,000 pelican
fledglings wandered across the colony in mid
April 201 1. out of sight of their parents which
were probably foraging at sea. Fledglings during
this period are not able to forage for themselves
and completely rely on their parents for food
(young Peruvian Pelicans probably do not forage
for themselves until they are 1 00— 1 20 days of
age. pers. obs.). We have observed fledglings
begging for food from unrelated conspecific
adults, most likely in an attempt to obtain food
!i is thus conceivable that some fledglings were
seeking food sources and opportunistically took
advantage of unguarded nests with newly hatched
chicks and depredated them. Local food shortage
can also induce cannibalism as fledglings are
forced to seek alternative food resources t Riehl
2006). However, we w'ere unable to find any
evidence of a shortage in the area, nor did vve
observe any signs of starvation. Cannibalism may
be also regarded as a feeding opportunity and not
necessarily a response to food deprivation (Mock
1984).
Several authors have suggested there is hor¬
monal regulation of aggression in chicks (e.g..
Ros et al. 2002, Anderson et al. 2004. Muller et al.
2008). Chicks exposed very early in their
SHORT COMMUNICATIONS
607
development to androgen levels develop more
aggressive behaviors towards conspecific chicks
and adults. This has been demonstrated in the
N'azca Booby (Sul a grant i) (Anderson et al. 2004.
Muller et al. 2008) and the Black-headed Gull
I Chroicocephalus ridibundus ) (Ros el al. 2002),
both colonially-nesting seabird species.
There are many reports in the literature ol
egression and cannibalism by adults consuming
eggs, chicks or body parts of other individuals
fStanback and Koenig 1992). but little is known
about the occurrence of these behaviors by
fledglings and young birds. To our knowledge,
our observations constitute the first report of
aggression and cannibalism in Peruvian Pelican
fledglings.
ACKNOWLEDGMENTS
We thunk D. W. Mock and M. T. Stanback for help with
literature. Funding was provided by research grant DI-4S-
10 from the Vicerrectoria de Investigacion y Doetorado.
Universidud Andres Bello (Chile), The Milwaukee County
Zoo. and the Zoological Society of Milwaukee (USA). We
are also grateful toConsejo de Monumentos Naeionalcs and
Cofradia Nautica del Paeifico (especially to F Carlicr) for
granting access to the island. R. S, Wallace kindly corrected
early versions of the manuscript. We thank Christina Riehl
and an anonymous reviewer for their comments on the
manuscript.
LITERATURE CITED
Anderson. D. J. 1990a. Evolution of obligate siblicide in
boobies. I. A lest of the insurance-egg hypothesis,
American Naturalist 135:334-350.
Anderson, D. .1. 1990b. Evolution of obligate siblicide in
boobies. 2. Food limitation anil parent-offspring
conflict. Evolution 44:2069-2082.
Anderson. D. j.. E. T. Porter, and E, D. Fkrree. 2004.
Non-breeding Nazcu Boobies (Stria grant i) show
social and sexual interest in chicks: behavioural and
ecological aspects. Behaviour 141:959-977.
Drummond. H. 1987. A review of parent-offspring conflict
and brood reduction in the Pelccaniformes. Colonial
Waterbirds 10:1-15.
Gill. F. b 2007. Ornithology. Third Edition. W. H.
Freeman and Company. New York. USA.
Guerra. C. G. and M. A. Cikutovic. 1985. Algunos
aspectos de la nidificacidn y el crecimiento de
Peleccuius occidentalis thagus Molina, I7S2 en el
none de Chile. Pages 33-48 in Proceedings 1 Simposio
de Omitologia Neotropical (F. G. Styles and P. G.
Aguilar. Editors). Arcquipa. Peru.
Herring, G., M. D. Johnston, and E. M. Cal. 2005.
Intraspccific predation in juvenile White Ibis. Water-
birds 28:531-532.
Mock. I). W. 1984. Infanticide, siblicide and avian nesting
mortality. Pages 3 30 in Infanticide: comparative and
evolutionary perspectives (G. Ilausfater and S. B. Hrdy,
Editors). Aldinc Publishing Company. New York. USA.
Mock. D. W. and G. A. Parker 1997. The evolution of
sibling rivalry. Oxford Series in Ecology and Evolu¬
tion. Oxford University Press. New York. USA.
Mock. D. \v„ H. Drummond and C. h. Stinson. 2009.
Avian siblicide. Pages 236-247 in Exploring animal
behavior: readings from American Scientist (P. W.
Sherman and J. Alcock. Editors). Sinauer Associates,
Sunderland. Massachusetts. USA.
Mi H-er. M. S.. J. F. Brennecke. E. T. Porter. M. A.
OrriNGKR. and D. J Anderson. 2008. Perinatal
androgens and adult behavior vary w ith nesiling social
system in siblicidal boobies. Flos One 3:1-6. e2460.
Nelson. J. B 2005. Pelicans, cormorants, and their rela¬
tives. The Pelccaniformes. Oxford University Press.
New York. USA.
Kir lit.. C. 2006. Widespread cannibalism b> fledglings in a
nesting colony of Black-crowned Night-Herons. Wil¬
son Journal of Ornithology 1 18:101-104.
Ros, A. F. 11.. S. J. DielemAn. and T. G. G, Groothuis.
2002. Social stimuli, testosterone, and aggression in
gull chicks: support for the challenge hypothesis.
Hormones and Behavior 41:334-342.
Sachs. E. B. and P. G. R. Jodice. 2009. Behavior of parent
and nestling Brown Pelicans during early brood
rearing. Waterbirds 32:276-281.
ScHRl-antU. R. W. 1976. Growth and development of
nestling Brown Pelicans. Bird-Banding 47:19-39.
SHEALER. D. A. 2002. Foraging behavior and food of
seabirds. Pages 137 177 in Biology of marine birds
(E. A. Sehreibcr and J. Burger. Editors). CRC Press.
Boca Raton, Florida, USA.
SlMI-ONE, A. AND M. Bkrnai . 2000. Effects of habitat
modification on breeding seabirds: a case study in
central Chile. Waterbirds 23:449—456.
SlMEONE. A.. G. Luna-Jorquera. M. Bernal. S. Garthe,
F. Sepulveda. R. Villablanca. U. Ellenberg, M.
CONTRERAS, J. MUNOZ, and T Ponce. 2003. Breeding
distribution and abundance of seabirds on islands off
north-central Chile. Revisia Chilenu de Historia
Natural 76:323-333.
Smith. A. C. and U. Mlnro. 2008. Cannibalism in the
Australian Pelican [Pclrumnx consph-illatus) and
Australian White Ibis ( Thmktornis niahtcca). Water-
birds 31:632-635.
STANBACK, M. T. and W. D. Koenig. 1992. Cannibalism in
birds. Pages 277-298 in Cannibalism: ecology and
evolution among diverse taxa (M. A. Elgar and B. J.
Crespi. Editors). Oxford University Press. New York, USA.
608 THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 3. September 2012
The Wilson Journal of Ornithology 1 24(3 ):608— 6 1 1. 2012
Malicious Motherhood: Instance of Infanticide by a Female Barn Swallow
Joanna K. Hubbard1 : and Audrey L. Tobin1
ABSTRACT. — Infanticide, the killing of dependent
offspring, often provides direct or indirect fitness
benefits to the perpetrator. Infanticide in socially
monogamous systems, like that in many passerine
birds, is typically performed by males in an attempt to
gain access to potential mates. We observed infanticide
by a female Barn Swallow ( Hirmulo nistica ) in North
America and. to the best of our knowledge, this is the
first documentation of this behavior. A female pecked
and threw out nestlings belonging to a neighboring pair
of swallows. There were no obvious fitness benefits
gained by this female, thus established evolutionary
explanations arc not applicable. Further investigations
into the frequency of female infanticide, easily mistaken
for predation, should be pursued to better assess the
selective pressures driving this behavior. Received 17
January 2012. Accepted IS April 2012.
Infanticide occurs in many animal laxa, and
many hypotheses attempt to explain this behavior.
These include: (1) sexual selection. (2) resource
competition. (3) exploitation of the infant, and (4)
parental manipulation (Hrdy 1979, Sherman 1981.
Ebensperger 1998: Table 1). Unmated males, or
males new to a social group, are typically (he
culprits in sexually-selected infanticide; by killing
a female's dependent offspring, a male increases
their chance of mating w ith that female and siring
offspring (Trivets 1972. Hrdy 1979). Infanticide is
also commonly the result of resource competition
when resources are limited. A parent will kill
unrelated offspring in the area to increase the
available resources and the chances of survival for
its own offspring (Hrdy 1979. Sherman 1981.
Ebensperger 1998). Infanticide can also be a form
of exploitation or parental manipulation. Infanti¬
cide is considered direct exploitation when an
individual directly gains from the act. for
example, by cannibalizing the infant (Fox 1975)
or “play mothering' or “aunting to death' (Lan¬
caster 1971, Hrdy 1979, Quiatl 1979). Alterna¬
tively, an individual may increase its own survival
Department of Ecology and Evolutionary Biology, Uni¬
versity of Colorado at Boulder. Boulder, CO 80309, USA.
' Corresponding author:
e-mail: Joanna.Hubbard@colorado.edu
or the survival of healthier offspring by killing
unhealthy or debilitated infants (Low 1978). The
parent manipulates the situation to increase its
fitness directly or indirectly by increasing the
resources available to viable offspring.
Barn Swallows (Hirmulo nistica) are a socially
monogamous passerine with a Holarctic distribu¬
tion (Moller 1994). They breed semi-colonial!}
with North American groups typically ranging in
size from nine to 35 pairs (Safran 2004). Sexually-
selected infanticide by Barn Swallow males to
gain access to a female has been observed (Crook
and Shields 1985; Mpller 1988. 2004). Mollcr
(2004) proposed that infanticide by males is more
common in benign years that allow individuals of
lower condition to survive spring migration, The
number of unmated males increases in these years,
and the average condition of mated pairs is lower,
thus reducing their ability to defend nests and
prevent infanticide, Moller (2004) directly ob¬
served infanticide by males in European popula¬
tions and estimated the rate to be —25$; this
behavior has also been documented in North
American swallows at low frequency (Crook and
Shields 1985). Infanticide was not directly
observed until 2011 in our study population in
Colorado, USA, which has been under intensive
observation since 2008. We report infanticide
performed by a paired female Barn Swallow: to
the best of our knowledge, this is the first
observation of female infanticide in Bam Swal¬
lows and suggests a need for future studies to
explore the prevalence of this behavior.
OBSERVATIONS
Our study population breeds in bams and
culverts in Boulder. Weld, and Jefferson counties.
Colorado, USA. Autumn Hill, the site where
infanticide was observed, is a large equestrian
center in Boulder County (40 08' N. 105 lb VV|-
the barn houses —30 horses with a large indoor
arena in (lie center. There is a relatively high
amount of human activity; although, the swal¬
lows do not appear disturbed. The site has T1
breeding pairs, —40 of which we are able to
monitor; nests in the arena are too high to access.
SHORT COMMUNICATIONS
609
TABLE 1. Hypotheses and predictions commonly used lo explain why an
adult would perform infanticide.
Hjpothcsis
Prediction
Citation
Sexual selection
Increases mating opportunity and
allows one to raise own offspring
drivers 1972. Hrdy 1979)
Resource competition
Increases one's own offspring survival
in time of limited resources
(Hrdy 1979. Sherman 1981.
Ebenspcrger 1998)
Exploitation
Increases fitness directly via exploiting the
infant (i.e.. cannibalism or play mothering)
(Lancaster 1971. Fox 1975.
Hrdy 1979. Quiatt 1979)
Parental manipulation
Increases survival of healthy offspring
by killing unhealthy offspring
(Low 1978)
We observed 12 and 13 day-old nestlings on IK
and 19 July 201 1 being pecked and pushed out ot a
nest (# 106) by the female at a nearby nest (# 37).
Nest # 106 had four nestlings and nest # 37 had
recently (within 3 days) Hedged three young; the
two nests were ~2 in apart. The barn manager saw
three nestlings full from nest # 106 onto the
concrete below on the evening of IS July 201 1.
Upon seeing the first nestling fall, she watched as
an adult pushed out the other two. All three
survived the fall, hut two died shortly after. The
third was kept overnight and taken to an animal
rehabilitation center the next morning. We watched
as the female from nest # 37 pecked and pushed out
the fourth nestling at —0900 hrs on 19 July 2011. It
appeared the nestling was dead prior to the fall,
likely due to a large puncture wound on its body.
We expected the female from nest U 37 to mate
with the male from nest # 106, or alternatively,
that the pair from nest # 37 would take over nest
# 106 for their second brood. 1 lowever. no activity
was seen for I week; 8 days after the nestlings
were killed, the pair from nest # 37 initiated a
clutch in a newly built nest within 30 cm of their
original nest, and Hedged four young. A new pair
laid eggs in nest # 106. but later abandoned the
clutch; the original pair from nest # 106 was not
seen for the remainder of the breeding season.
DISCUSSION
Infanticide is typically a behavior that increases
an individual's fitness, either directly through
increased access to mates, or indirectly through
increased resources for offspring (Hrdy 1979).
Thus, infanticide without apparent fitness benefits
is much more difficult to explain. Any titness
benefits gained by the female, direct or indirect, in
our observations arc difficult to ascertain ( Table 2).
Evidence for sexually-selected infanticide has been
documented for male Barn Swallows, but this
behavior has not been observ ed for females. Female
infanticide has been documented in other passer¬
ines. particularly in species where male mates are
limited (Veiga 1990, Chek and Robertson 1991,
Hansson et al. 1996. Veiga 2004). It is possible the
female from nest # 37 killed the nestlings from nest
# 106 in an attempt to usurp the male from that nest
for a future breeding attempt, but it seems unlikely
given the pair from nest # 37 remained intact lor a
second nesting attempt. However, the pair from nest
# 106 was not observed for the remainder of the
season and. while completely speculative, perhaps
the female’s intention of usurping the male was not
realized due to his disappearance.
The architecture of the particular barn made it
difficult to monitor active nests in the indoor
arena and we do not know whether birds captured
but not associated with a nest were truly floaters
(males and females), or nesting in the arena. We
observed 43 females and 50 males in the barn-
captured in mist nets or detected as unhanded
adults attending nests. This ratio suggests a
surplus of males, which further contradicts the
hypothesis of sexually-selected infanticide by
females as reported for other socially monoga¬
mous passerines with biparental care (Veiga 1990,
Chek and Robertson 1991, Veiga 2004).
Alternative explanations could involve limited
resources, either nests or food.. Limited availabil¬
ity of nest sites is unlikely given the number of
available potential sites in the barn. There were
two other active nests in close proximity to nest
# 37 that remained undisturbed, and the pair
renested within 30 cm of their original nest (# 37)
where they continued to tolerate these neighbors.
The pairs at these undisturbed nests may have
been better nest guarders (Moller 1988). but we
did not observe any differences in nest attendance
(JKH and ALT, pers. obs.). Limited availability of
food resources is also unlikely. We have seen high
nestling mortality and predation resulting in low
reproductive success in past years. However, the
610
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 3. September 2012
TABLE 2. Why the reported incident of infanticide does not appear to support established evolutionary hypotheses.
Hypoihesis
Predict urn
Citation
Sexual selection
Female from nest # 37 did not mate with
male from nest # 106
(Trivers 1972. Hrdy 1979)
Resource competition
Nest # 37 and # 106 were not synchronous:
resource availability was not dramatically
different at time of event
(Hrdy 1979. Sherman 1981.
Ebensperger 1998)
Exploitation
Female from nest ft 37 did not eat or further
manipulate nestlings from nest # 106
(Lancaster 1971. Fox 1975. Hrdy
1979. Quiatt 1979)
Parental manipulation
Nestlings did not belong to female from
nest # 37: there were no size or mass
differences among the nestlings and no
nestlings were left unharmed
(Low 1978)
2011 season was a particularly productive year
(JKH. pers. obs.) suggesting food resources were
plentiful and environmental stressors were rela¬
tively mild. Moreover, there was no significant
change in local climate conditions (temperature
and rainfall) that may have affected food
resources leading to this event.
This particular case of infanticide is difficult
to explain, and is perhaps an example of a
pathological behavior, but it does raise the
question of how often infanticide is mistaken for
predation. Missing eggs and nestlings, as well as
nestlings that are found dead in nests, are typically
attributed to predators such as domestic cats (Pel is
cat us) or Black-billed Magpies (Pica hudsouia) or
competitors for space such as House Sparrows
(Passer domes ticus). However, in light of this
observation, as well as relatively high rates of
infanticide in European populations of Barn
Swallows (Moller 2004), it seems probable a
portion of these instances could actually be
cases ot infanticide. Furthermore, if infanticide
is performed to gain access to mates, we are
overestimating the strength of natural selection
imposed by predation and underestimating the
strength of sexual selection. Dark coloration is
sexually-selected in the North American subspe¬
cies (H. r. erythrogaster) (Safran et al. 2005) and
in our population, darker males are more likely to
have their nests depredated (A. J. Flynn, unp'ubl.
data). This event poses an alternative hypothesis:
darker males arc more likely to experience
sexually-selected infanticide by potential female
mates. We have only witnessed one case of
infanticide in our population, and future work-
should attempt to differentiate between infanticide
and predation to better understand the selective
pressures imposed on traits related to fitness.
ACKNOWLEDGMENTS
Wc thank J. A. Barringer-Richers, Greenwood Wildlife
Rehabilitation Center. Autumn Hill Equestrian Center, and
the Safran Laboratory. Wc thank W. M. Shields and an
anonymous reviewer for helpful comments on a previous
draft of this manuscript. This work was funded b\ a
National Science Foundation Grant (10S-0707421) to R J.
Sal ran. Bioscience Undergraduate Research Skills and
Training award to A. L. Tobin, and a Graduate Student
Research Grant from the University of Colorado Ecology
and Evolutionary Biology Department to J. K. Hubbard
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The Wilson Journal of Ornithology 124(3):61 1-614, 2012
Intraspecific Brood Parasitism of the Pale-breasted Thrush (Tardus leucomelcis )
Paulo V. Davamjo,1 Livia M. S. Souza,1
Leonardo S. de Oliveira,1 and Mercival R. Francisco1’2
ABSTRACT.— We report the first evidence for
intraspecific brood parasitism (IBP) of the opcn-cup
nesting Pale- breasted Thrush ( Tardus leucomelus) in
southeast Brazil. Four of 15 nests followed from
building stage onwards had evidence of IBP <27Tf). as
detected from laying of two eggs in the same day in a
nest (/) = 2). laying of an additional egg after onset of
incubation in = I). and egg laying before the end ol
nest construction (n = I ). Only a few cases of IBP have
been reported for neotropical songbirds but it is likely
more will be reported as they become belter studied. We
believe limited territory availability or nest loss during
laying were potential causes of IBP in our study
population. Received 23 August 2111 1 . Accepted I May
2012.
The study of avian brood parasitism has
focused mainly on obligate interspecific parasites
(Lyon and Eadie 2008). A grow ing body of work,
however, documents facultative intraspecific
brood parasitism (IBP) (Yom-lov and Gellen
2006. Shaw and Hauher 2009). This reproductive
1 Universidade Federal de S jo Carlos. Campus de Soro-
caba. Departumento de Ciencias Ambientais, Rodovia Joao
Lcme dos Santos, Km I 10- Sorocuba. SP. CEP 18052-780.
Brazil.
2 Corresponding author; e-mail: mercival@ufscar.br
strategy is more than twice as common as
interspecific parasitism (Yom-Tov 2001. Schiel-
zeth and Behind 2010), but has received less
attention probably because it is more difficult to
detect (Lyon and Eadie 2008, Eadie ei al. 2010).
Females using this strategy lay their eggs in nests
of conspecifics without providing any additional
parental investment (Yom-Tov 1980, Lyon and
Eadie 2008. Griffith et al. 2009). Records of IBP
have been observed disproportionately more in
precocial species (46% of Anseri formes vs. 1% of
Passeriformes; reviewed by Yom-Tov 2001).
Precocial birds may exlubit this behavior more
because they lay more eggs and have a longer
laying period, leaving more time for conspecific
parasitism to occur. In addition, parasitic eggs and
young for precocial species may tax host-parent
resources less than for altricia! birds, providing less
incentive for hosts to develop behaviors to
counteract parasitism (Yom-Tov 1980, Sorenson
1992, Yom-Tov el al. 2000). Despite the altricial
versus precocial duality. 57.5% of the known cases
of IBP are from colonial breeders: among the
Passeriformes it reaches —70% (Yom-Tov 2001 ).
Researchers have looked tor IBP dispropor¬
tionately more in Anseri formes than in any other
avian group (Yom-Tov et al. 2000, Yom-fov
612
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124, No. 3, September 2012
2001): thus the low rate of IBP in altricial species
may reflect researcher bias rather than an actual
biological pattern. It is possible rates of IBP are
underestimated since they are higher in areas
where most ornithologists work (Yoin-Tov 2001 ).
Only a few cases of IBP have been reported in the
Neotropics. (Dyrcz 1983, Langen 1996, Carvalho
et al. 2006. Rios-Chelen et ai. 2008). probably due
to the lack of detailed nesting behavior studies in
this region (Auer et al. 2007).
We report the first evidence for IBP in a
neotropical songbird species, the Pale-breasted
Thrush ( Turdus leucomelas ), in southeast Brazil.
METHODS
We examined nests of the Pale-breasted Thrush
during a breeding behavior study on the campus
of Sorocaba's Engineering University, Sao Paulo
State, in southeastern Brazil (23 28' S, 47 25' W).
and in an adjacent urban park. The campus totals
1 0.5 ha and has extensive lawns and gardens where
exotic trees (predominantly Pinus sp„ Eucalyptus
sp.. Mangifera sp„ and Grevilleu robusta) are
interspersed with native species typical of the
Cerrado habitat. Buildings and streets are widely
spaced and cover -30% of the campus. The
adjacent park is a 2-ha sensu strictu Cerrado
habitat. These locations are traversed by two
streams and form a patch of partially' open
vegetation isolated within a densely urbanized
area.
We systematically searched for nests during
three breeding seasons (2006-2007, 2007-2008,
2008-2009), by covering the entire area two to
three times a week (0700-1000 hrs) from August
to May. We located nests by following adults
while they were carrying materials for nest
construction or delivering food to nestlings.
Nests were bulky open cups made of rootlets,
mosses, and dead leaves compacted with mud. We
checked nest contents daily during late nest con¬
struction and during the laying stage to document
clutch initiation dates and onset of incubation.
Pale-breasted Thrushes lay their eggs between
0600 and 0730 hrs (PVD, unpubl. data), and we
checked nests 4 hrs after sunrise (0900-1000 hrs)
to avoid counting eggs before additional eggs
could have been laid in the same day. We report
observations ol nests as evidence for IBP in which
(1) more than one egg was laid in the same day,
. ®gg.s Were la,tl - or more days after onset of
incubation, and (3) eggs were laid 2 or more days
before nest construction ended (Yom-Tov 1980.
Pieman and Belles-Isles 1988, Latif et al. 2006
Peer 2010).
RESULTS
We monitored 15 nests of Pale-breasted Thrush
from building through hatching and observed
evidence for intraspecific brood parasitism in four
nests (27%). One nest was found on 8 October
2008 in the early construction stage. The first egg
was laid on 16 October and. on the following day.
three eggs were observed in the nest, suggesting
that one egg had been laid by a parasitic female.
Incubation was initiated on 17 October and one
egg hatched on 28 October and another on 30
October. One of the eggs w as inf ertile. One of the
nestlings disappeared a few days later and the
other fledged on 15 November.
A second nest was found on 21 October 2008 in
the middle of the construction stage. The first egg
was laid on 25 October and the nest contained three
eggs the following day. Incubation started on 27
October, and eggs hatched on 7 (n = 2) and 8
November (n = I ). All young fledged successfully
on 22 November.
A third nest was found on 2 September 2007 in
the middle of the construction stage, but already
contained one egg. The female continued carrying
and arranging nest materials until 5 September.
Two additional eggs were laid between 6 and 9
September, and incubation started on 10 Septem¬
ber. Only one egg hatched on 21 September and.
on 26 September, the young and the remaining
infertile eggs were depredated.
A fourth nest was found on 3 November 2008
in late construction stage. The first egg was laid
on 8 November, and a second egg was laid on 10
November when incubation started. A third egg
was laid 6 days after onset of incubation. The first
two eggs hatched on 23 November and the third
egg hatched on 29 November. All young fledged
on 8 December with the younger individual flying
weakly due to poorly developed feathers.
DISCUSSION
Proposed explanations for intraspecific brood
parasitism in precocial species and colonial
nesters are not regularly applicable to territorial
passerines (reviewed by Yom-Tov 2001). Several
alternative hypotheses have been proposed to
explain IBP in songbirds, such as a scarcity ol
suitable nesting sites, nest loss during the laying
stage, and a high proportion of unmated females
or floaters in the breeding population (Yom-Tov
SHORT COMMUNICATIONS
613
1980. Rothstein 1993. Shaw and Hauber 2009,
Schielzeth and Bolund 2010). The first hypoth¬
esis is less capable of explaining IBP in our study
population as the Pale-breasted Thrush is plastic
in types of sites they use for nesting; they are
capable of nesting in human-built structures, such
as on rafters and pillars, as well as in natural
sites, such as trees in Cerrado areas or forest
borders. Thirty-three (69%) of 48 nests that we
monitored on the study area were in trees or
bushes. 14 (29%) were in man-made structures
(eaves, rafters or on the top of pillars), and one
was in a niche in a bank. Thus, unlike cavity
nesters that may exhibit IBP due to limited nest
site availability (Yom-Tov 1980, Rohwer and
Freeman 1989), this parameter is unlikely to
shape Pale-breasted Thrush reproductive strate¬
gics. The other hypotheses are plausible lor
explaining IBP in this species. Overall nesting
success estimated using the Mayfield (1961 1
method was among the highest ever documented
for thrushes (57%; 748 nest days, n = 37 nests)
(PVD. unpubl. data), but many nests are depre¬
dated. Our study area is an isolated patch ot
habitat in which a high number ot fledglings are
produced each season, and territory availability
may be limited, potentially resulting in a high
number of unpaired and/or floater lemales.
Testing these hypotheses would be worthwhile
for future research.
The IBP rate apparent from our data must be
viewed with caution. The first and second obser¬
vations arc more reliable than the third and fourth,
because it seems physiologically possible lor a
female to lay an egg early or late but not to lay tw o
eggs in 1 day (Yom-Tov 1980). We arbitrarily
assumed in the third and fourth observations that an
egg being laid 2 or more days betore nest com¬
pletion or 2 or more days after onset of incubation
onset could be evidence for IBP. Females did not
lay eggs more than 1 day alter beginning ot
incubation except for the fourth nest, in which an
egg was laid 6 days alter onset ot incubation. 1 bus.
6 days is a large deviation from the norm lLatii
et al. 2006). We observed other cases of potential
IBP in addition to the records we considered as
evidence for IBP. We observed a 1-day gap be¬
tween the first and second egg in another nest, and
there was a 1 -day gap between the second and third
egg in two additional nests.
Our observational methods could not identify
parasitic eggs laid the day after clutch completion
or the day before clutch initiation, as well as eggs
that could have been ejected (Latif et al. 2006).
The IBP rate of the Pale-breastcd Thrush might be
higher, if our estimate is low, than that lound lor
the neotropical Blue-black Grassquit (Volatinia
jacarina) (27.3%) (Carvalho et al. 2006). Both are
remarkably higher compared with cavity or open
nesting songbirds from temperate regions: 0-
7.1% for European Pied Flycatchers ( Ficedula
hxpoletiea). 4.6-5% for Cave Swallows (Petru-
chelidon fulva), and 10.7-11.9% for American
Cliff Swallows (P. pyrrlumota) (Yom-Tov 2000.
Weaver and Brown 2004).
Onr data document a potential case where
limited territory availability or nest loss duiing
laying periods' may be inducing IBP. Further
researeh is needed to test these and other potential
explanations for IBP in our study population.
Only a few cases of IBP have been reported for
neotropical songbirds, they include representa¬
tives of different families: White-throated Mag-
pic-Jav ( Calocitia formosa) (Corvidae) (Langen
1996)! Vermilion Flycatcher (Pyrocephalus ntbi-
nus) (Tyrannidae) (Rfos-Chelen et al. 2008),
Clay-colored Robin ( Turd" s grayi) (Muscicapi-
dae) (Dyrcz 1983), and Blue-black Grassquit
(Emberizidae) (Carvalho et al. 2006), supporting
the evidence this strategy can be more widespread
than previously thought (Yom-Tov 2001). Our
study provides new evidences for IBP among
neotropical thrushes.
ACKNOWLEDGMENTS
We are grateful to Faculdade de Engenharia de Sorocaba
(FACF.NS) for authorizing field work in die campus. PVD
was supported by Universidade Federal de Sao Carlos
(PIADRD fellowship programe), and LSO received a
fellowship from Conselho Nacional de Desenvolvimento
CicnuTico e Tecnologico (PIBIC/CNPq). We especially
lhank A. J. Piratelli. M. N. Schilindwein, A. V. Christiamm.
and two anonymous referees for important comments on
previous versions of this manuscript.
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The Wilson Journal of Ornithology 1 24( 3 ):6 14-620. 2012
Estimation of Female Home-range Size During the Nestling Period of
Dark-eyed Juncos
Dustin G. Reichard' 2 and Ellen D. Ketterson1
ABS TRACT. — Studies of spatial activity of songbirds
during the nesting cycle have largely focused on male
activity and neglected female space use. particularly
outside the fertile period. We estimated the home-range
size of seven female Dark-eyed Juncos Uunco hyemalis )
3 days after their nestlings had hatched. We used
radiotelemetry to track female movements for 2 hrs on
ihe afternoon of day 3 of nestling life, and 2 hrs on both
the morning and afternoon of days 4 and 5. Female
location and beha\ ior were recorded every 10 min for the
1 Department of Biology and Center for the Integrative
IN47405Au'™A BChaVi°r’ ,ndiani' Univcrsil>'' Bloomington,
2 Corresponding author; e-mail: dgreicha@indiana.edu
duration of tracking. Females exhibited a mean home-
range size of 0.833 ha (range = 0.156-2.450 ha). Our
estimate ot home-range si/e during the nestling period
was significantly smaller than a previous estimate of
female home-range size during the fertile period in the
same junco population. Home-range size varied greatly
between individuals, and the observed differences may
be attributable to variation in resource availability.
Received 2 November 201 1 . Accepted 25 February 2012.
The home-range size of temperate songbirds
(Passeriformes) during the breeding season can
have profound effects on access to resources and
SHORT COMMUNICATIONS
615
reproductive success of both males and females
(Zack and Stutchbury 1992. Both and Visser
2000. Rolando 2002). Males defend territories
with song and active monitoring, presumably to
protect resources for their offspring and to guard
against extra-pair fertilizations (EPFs), while also
moving outside of their defended territory to
potentially seek their own EPFs or other resources
(Moller 1987. 1991). Males of most socially
monogamous species also contribute to care of
young, but females often perform a larger portion
of parental care including incubation, brooding,
and provisioning (Trivers 1972. Bennett and
Owens 2002). Male spatial activity and home-
range size, despite differing in territorial and
parental behavior from females, have received
much more attention than female home-range
size, particularly during incubation and nestling
provisioning (Whitaker and Warkcntin 2010).
Female songbirds encounter a variety of chal¬
lenges during the nesting cycle. Females are not
limited in use of space by incubation or nestling
care during their fertile period and should have
their largest home ranges at that time (Moller 1987,
1990). Females of many species are known to
undertake 'forays' outside of their mate’s territory
in addition to foraging and nest building during the
fertile period, potentially resulting in EPFs as well
as female home ranges that are much larger than
territories defended by their social males (Neudort
et al. 1997, Pedersen et al. 2006. Stapleton and
Robertson 2006, Evans cl al. 2008; but see Akc^iy
et al. 2011).
Female home-range size is predicted to de¬
crease as incubation begins as females no longer
seek copulations and make shorter movements oft
the nest to forage and engage in nest defense.
However, the abundance and proximity of re¬
sources to the nest can alfect home-range size,
and females may maintain larger home ranges
depending on food availability (Moller 1990). Hie
subsequent transition from eggs to nestlings marks
a period of increased effort as females begin to
forage for nestlings in addition to themselves and
may continue to devote a large amount ol time to
brooding. This increase in time spent toraging
during the early nestling period predicts an
increase in female activity but presents contrast¬
ing predictions about home-range size. Females
may forage close to the nest and maintain smallei
home ranges than during the fertile period to
minimize energy expenditure and maximize lime
spent regulating nest temperature through blood¬
ing. which can impact nestling fitness (Dawson
et al. 2005. Butler et al. 2009). Conversely, fe¬
males may increase their home-range size to use a
variety of foraging locations or to gather higher
quality food items (Zach and Falls 1979. Grundel
1992, Garcia-Navas and Sanz 2010).
We quantified female home-range size during
the nestling period for Dark-eyed Juncos (Junco
hyemalis) to examine if female home-range size
declines between the fertile and nestling periods.
We compared our home-range estimate to previ¬
ously published data from Neudorf et al. (2002),
collected from the same junco population, which
estimated female home-range size during the
fertile period.
METHODS
Study System and Site.—' This research was
conducted at Mountain Lake Biological Station
(MLBS) and adjacent grounds of Mountain Lake
Hotel in Pembroke. Virginia (Giles County;
37 22' N, 80 32' W). USA between 29 April
and 24 July 2007. Vegetation on the study site was
largely mixed deciduous and coniferous forest that
supports an abundant population ot Dark-eyed
Juncos (J. li. ccirotinensis) (Chandler et al. 1994).
All juncos cm the study site received unique color
bands and the population has been continuously
monitored since 1983.
Dark-eyed Juncos are socially monogamous
(28% of 187 offspring sampled in our study
population were sired by an extra-pair father.
Ketterson ct al. 1998) and only females incubate
and brood while both sexes contribute to provi¬
sioning of nestlings (Nolan et al. 2002). Juncos
spend the majority of the breeding season near the
ground as they are a ground-nesting species and
forage for seeds and insects in the leaf litter as well
as in the understory vegetation (Nolan et al. 2002).
Radiotelemetry. — Radiotelemetry has been used
in previous studies to monitor activity of both male
and female juncos (Chandler et al. 1994. 1997;
Snntlders et al. 2000; Neudorf et al. 2002). We
used a modified leg-loop harness (Rappole and
Tipton 1991 ) to attach BD2A transmitters (Holohil
Systems Ltd., Woodlavvn, ON. Canada) to seven
female juncos in the morning (0500-1000 hrs EST)
when their nestlings were 3 days post-hatch. The
average ( ± SE) combined w eight of the transmitter
and harness was 0.9 ± 0.005 g and average female
mass was 21.5 ± 0.38 g. We tracked females
opportunistically to maximize our sample and all
616
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124, No. 3. September 2012
TABLE I. Home-range size of female Dark-eyed Juncos and metrics of tracking effort and female characteristics.
Mountain Lake Biological Station. Pembroke, Virginia. USA. The effect of implant type was tested using a Kruskal-Wallis
test (x;). All other relationships were tested using a Spearman's Rho Correlation (r).
Home-range size thal
No. of locations
Tracking time (hrs)
Julian date
Age
Nesting attempt
Implant
0.156
53
8.17
202
2
4
Control
0.350
65
10.00
149
1
1
Control
0.390
62
9.84
197
1
3
Control
0.613
65
10.00
188
1
3
Testosterone
0.657
59
9.00
150
1
1
Testosterone
1.215
65
10.00
175
4
2
Control
2.450
65
10.00
189
1
1
None
r or ■/;
0.493
0.493
-0.214
-0.045
-0.543
2.89
P
0.261
0.261
0.645
0.924
0.208
0.235
females receiving transmitters had a brood size of
three.
We used a TRX 1000-S receiver with a three-
element Yagi antenna (Wildlife Materials Inc..
Carbondale. IL, USA) to track each female via
homing tor 10 hrs, 2 hrs on the afternoon of day 3
of nestling life (1300-1800 hrs EST) and 2 hrs on
the morning (0800-1200 hrs EST) and afternoon
(1300-1800 hrs EST) of days 4 and 5 of nestling
life. We did not track during periods of heavy rain
and collected <10 hrs of data for three females
(mean = 9.56 hrs, range = 8.17-10.0 hrs). Trans¬
mitters were removed on the morning of day 6 of
nestling lite, We chose to track during the early-to-
mid nestling period (nestling juncos typically
fledge at 11—12 days post-hatch) as opposed to
the mid-to-late nestling period in an effort to
maximize our sample as nests are frequently
depredated even after reaching the nestling stage.
We only sampled females for 3 days to limit the
amount of time that each female carried the
transmitter and to ensure the transmitters could
be removed without Hedging the nestlings early.
DGR recorded female location and behavior
every 10 min for the duration of tracking. We
marked location points with flagging tape after the
female had moved at least 15 m distant to avoid
affecting the female’s movements. The 10-min
interval between observation points was chosen
to ensure our total number of observation points
(n = 65) per female was similar to the mean
number ol points per female reported by Neudorf
et al. (2002; 71.5 points/female) to facilitate a
meaningful comparison of home-range size be¬
tween our studies.
Six of the seven females received a subcutane¬
ous implant on the left flank, consisting of a 7-mm
(1.47 mm internal diam, 1.96 mm outside diam)
Silastic® tube (Dow Corning Corp.. Midland. MI,
USA) filled with 5 mm (~ 0.1 mg) of crystalline
testosterone (Sigma-Aldrich Inc., St. Louis. MO,
USA) or an empty tube filled with air as part of a
separate study investigating the impact of elevated
plasma testosterone on female reproductive be¬
havior (O'Neal et al. 2008). Implants were in¬
serted at least 2 weeks prior to attachment of a
transmitter to allow females to recover and adjust
physiologically to the implant. Female juncos
receiving implants in this study and previous
stuilies had full mobility immediately alter
implantation and remained active breeders for
the duration of the breeding season, suggesting the
implantation process had limited effects on the
activity of our subjects (Clotfelter et al. 2004.
O’Neal et al. 2008). Previous studies of the effect
of elevated testosterone on male spatial activity
successfully implanted males with larger testos¬
terone implants than those used in our study and
attached transmitters of a similar size without any
noticeable adverse effects on male body mass,
activity, or survival (Chandler et al. 1994. 1997:
Smulders cl al. 2000). All methods used were
reviewed and approved by the Indiana University.
Bloomington. Institutional Animal Care and Use
Committee (BIACUC Protocol # 06-242) prior to
data collection.
Estimating Home-range Size. — We attempted to
obtain 65 observation points for each female
(Table I), which were translated into coordinates
using a Trimble Pathfinder Pro XRS Global
Positioning System (GPS) unit (Trimble Naviga¬
tion Limited, Sunnyvale. CA, USA) with an
accuracy of <1 m. GPS positions were differen¬
tially corrected using GPS Pathfinder Office 2.90
( Trimble Navigation Limited. Sunnyvale. CA.
USA) with correction data from the Blacksburg.
SHORT COMMUNICATIONS
617
2.5
.§ 1.5
0.5
0
Fertile period Nestling period
FIG. 1. Female Dark-eyed Junco home -range size during the fertile and nestling periods. There was a significant
difference in female home-range size between periods (P = 0.01 1: fertile period, n = 8: nestling penod. n - 7). Error
represent ±1 SE. Fertile period data from Neudorf ct al. (2002).
Virginia base station (37 12' N. 80 25' W). The
corrected coordinates were projected in shapefile
format into Universal Transverse Mercator (UTM)
zone 17. NAD 83. using the Geographic Informa¬
tion System (CIS) Program ArcGIS 9.2 (ESR1
2007). A home-range area (in ha) lor each female
was estimated using minimum convex polygons
(MCP) in Hawths Tools 3.26 (Beyer 2004).
The MCP method (Harris et al. 1990 provides a
comparison of common methods of home-range
estimation) was chosen to allow lor an equivalent
comparison with previously published data on
female home-range si/e during the. lertile period
(Neudorf et al. 2002). We used a nonparametric
Mann-Whitney LMest to compare home-range
sizes, and a Spearman’s Rho Correlation to test
tor relationships between home-range size and
methodological effects. A Kruskal-Wallis test was
used to examine differences between implant types.
All tests were performed in SPSS 1 1 .5 ( SPSS 2002).
RESULTS
We had an average of 62 (range = 53-65)
observation points per female, and the total
number of observation points did not correlate
with home-range size (r — 0.493. P - 0.261;
Table 1). We found substantial variation (mean ±
SDi in female home-range size during the nestling
period with females maintaining a mean home
range of 0.833 ± 0.788 ha (Table 1). Home-range
size was not significantly correlated with duration
of tracking (r = 0.493. P = 0.261). Julian date
(r = -0.214. P = 0.645). female age (r -
-0.045, P = 0.924). or nesting attempt (r =
-O.543' P = 0.208) (Table l).We were unable to
make strong statistical comparisons about the
effect of elevated testosterone on female home-
range size due to our small sample size (testos¬
terone-implant - 2, control -implant = 4) and a
low effect size (Observed Effect Size [hi from
Retrospective Power Analysis - 0 050). The two
females that received testosterone implants had
intermediate size home ranges, and did not ditfei
detectably from females receiving control im¬
plants (Table 1; = 2.89. P = 0.235).
DISCUSSION
Female home range was significantly smaller
during the nestling period than during the fertile
period when comparing our data to Neudorf et
al.’s (2002) fertile period home-range estimate
collected at the same study site from different
individuals (Fig. 1; Z = 0.008; P = 0.011). We
collected a mean of 62 (range = 53-65)
observation points per female, similar to the
number collected by Neudorf et al. (2002) (mean
= 71.5 points/individual, range = 54-77) during
the fertile period. Thus, variation in the number of
observation points between studies likely had
minimal impact on our comparison.
The difference in home-range size between the
fertile and nestling periods may also be confounded
618
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124. No. 3. September 2012
by between-year variation in types of females
sampled, population density, and other aspects of
resource abundance and predation pressure
(McLoughlin and Ferguson 2000). We cannot rule
out these possible effects, but the density of the
study population as measured by the total number
of nests found (1998 = 154: 1999 = 163; 2007 =
120) and number of breeding pairs (1998 = 75:
1999 = 78; 2007 = 72) was slightly higher during
the fertile period study (1998, 1999) than during
the nestling period study (2007). We predicted
decreased density to cause larger home ranges due
to decreased competition for space (Hooper et ul.
1982, Anich cl al. 2010), but females still had
significantly smaller home ranges during the
nestling period despite lower densities.
The decline in female home-range si/c between
the fertile and nestling stages can potentially be
attributed to a transition from nest building and
seeking copulations during the fertile period,
which often causes females to leave their social
mate's territory (Stapleton and Robertson 2006,
Whitaker and Warkcntin 2010), to focus on
parental care and nest defense during the nestling
period. We quantified female movements from
days 3 to 5 of nestling life, likely before nestlings
could thermoregulate independently (Dawson
et al. 2005) and females were still frequently
brooding. The junco nestling period lasts 1 I to
12 days before fledging, and females are known to
decrease their time spent brooding by as much as
75% between days 4 through 7 and days 8 through
10 of nestling life (Wolf et al. 1990). Female
home-range size may expand during the second
half of the nestling period as females spend less
time brooding and potentially take advantage of
more distant resources.
Previous estimates of male Dark-eyed Junco
home-range size in our study population indicated
that males do not differ delectably in home-range
size across the nesting cycle (Chandler et al. 1994,
1997), which contrasts with our result for females.
Male home-range size (mean ± SD.i during the
nestling period (1.31 ± 0.525 ha: Chandler et al.
1994) was larger than our estimate of female
home range during the nestling period (0.833 ±
0.788 ha), but this difference was not statistically
significant (Two-sample Kolmogorov-Smimov
Test; Z = 1.220; P = 0.102). Male and female
juncos pertorm approximately an equal amount
ot provisioning throughout the nestling period
(Ketterson et al. 1992), which may contribute to
the similarity in home-range size. Female juncos
maintained a slightly larger (mean ± SD) home-
range size during the fertile period (2.44 =
0.992 ha: Ncudorf et al. 2002) than males (2.11
— 0.539 ha; Chandler et al. 1997). which may
explain why females have a significant decline in
home-range size between the fertile and nestling
stages while males do not.
Female juncos exhibited substantial individual
variation in home-range size during the nestling
period suggesting not all females were minimiz¬
ing distance traveled from the nest, despite the
increased energetic costs and potential spatial
constraints associated with nestling care The
observed variation could be a product of among
home-range variation in resource availability
(Moller 1990, Rolando 2002). The largest and
smallest home ranges in our study were in the
same general area of the study site (~ 350 in
apart) and no large-scale differences (e.g.. hole!
property vs. mature forest) in habitat characteris¬
tics were observed betw-ecn these two territories.
There may be finer scale differences in habitat
quality contributing to these large differences in
home-range size. For example, juncos are known
to roost exclusively in coniferous trees (Chandler
et al. 1995) and, in our study, females appeared to
preferentially forage in and around hemlock
( Tsuga spp.) (DGR. pers. obs.). One explanation
lor the large differences in home-range size over a
relatively small spatial scale may relate to
differences in distribution of hemlock. Thus,
identifying the relative importance and distribu¬
tion of limited resources within a home range,
such as hemlock trees, is an important topic for
future studies of avian spatial activity. Future
studies should also compare the spatial activity ot
individual females across the nesting cycle to
control for individual variation between females
and years.
ACKNOWLEDGMENTS
We thank S. E. Schrock. D. M. O’Neal. N. M. Gerlach.
K. L. Gray son. Jcrrah Jackson. Christina Jenkins, J. J. Pnce.
and Erin Spcvak for assistance in the field. E. A. Snajdf and
E. M. Schultz also provided Held assistance and summa¬
rized nesting and pairing data, V. A. Formica, E. S. Nagy
and R. Ci. Thurau provided crucial technical support with
the (iPS equipment and GIS software. Four anonymous
reviewers provided comments that improved the manu¬
script. We also thank the director at Mountain Lake
Biological Station. E. D. Brodie lit, the Mountain Like
Motel, and the Uolinger Family for allowing us to work on
their property. This study was funded by a National Science
Foundation Grant to EDK (IOB-05-1921 1).
SHORT COMMUNICATIONS
619
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The Wilson Journal of Ornithology 124(3): 620-625. 2012
Movement and Cover-type Selection by Fledgling Ovenbirds
(Seiiirus aurocapilla) after Independence from Adult Care
Henry M. Streby1-2-3 and David E. Andersen2
ABSTRACT. — We used radiotelemetry to monitor
movements and cover-type selection by independent
lledgling Ovenbirds ( Seiurits aurocapilla) at two
managed-forest sites differing in mature-forest matrix:
open-understory deciduous lores! and dense-uiulerstory
mixed-deciduous-conifer forest. Ovenbirds at each site
made one to three single-day long-distance movements:
those movements were of similar distance at the
deciduous site Cv = 849 ± 159 m) and the mixed-
deciduous-conifer site (v = 1,133 2 228 m). They also
moved similar mean daily distances within stands at the
deciduous site (x = 101 ± 12 m) and ihe mixed-
deciduous-conifer site (a- = 105 r 1 1 m). and used
areas ol similar local vegetation density, but
denser than that ol' their nesling habitat. Fledg¬
lings in the deciduous study area selected sapling-
dominated clearcuts and forested wetlands over
mature forest and shrub-dominated clearcuts.
Fledglings in the mixed-deciduous-conifer study
area generally used cover types in accordance
with availability, and tended not to use shrub-
dominated clearcuts. Our results suggest regener¬
ating clearcuts may be important areas for
independent fledgling Ovenbirds in landscapes
Department ol Fisheries. Wildlife, and Conservation Biol¬
ogy, University of Minnesota, 200 Hudson Hall. St. Paul
MN 55108, USA.
U.S. Geological Survey, Minnesota Cooperative Fish and
Wildlife Research Unit. 200 Hudson I fall. St. Paul, MN 55108.
uoA.
'Corresponding author; e-mail: streb006@umn.edu
that consist ol otherwise contiguous open-under-
story mature forest, but not until saplings establish
in those clearcuts, and not necessarily in forests
where dense understory and naturally dense areas
such as forested wetlands are common. Received 3
January 2012. Accepted 26 April 2012.
Many bird species that nest in mature forest use
other cover types during the time between nesting
and tall migration, or the post-fledging period
(Anders et al. 1998; Pagen et al. 2000; Marshall
et al. 2003; Vega Rivera et al. 2003; Vitz and
Rodewald 2006; White and Faaborg 2008; Strebv
ct al. 2011a, b). The posi-fledging use of
regenerating clearcuts and forested wetlands by
mature-forest species (species that breed and nest
primarily in mature forest) has been linked to
denser vegetation and greater food availability in
those cover types (Vitz and Rodewald 200T
McDermott and Wood 2010, Streby et al. 201 la).
Survival of fledgling Ovenbirds (Seiurits auroca¬
pilla) is positively associated with use of dense
understory vegetation and woody debris (King
et al. 2006, Streby 2010. Vitz and Rodewald
2010), Ovenbirds from nests near sapling-domi¬
nated clearcuts use those stands within days of
Hedging and experience increased survival com¬
pared to fledglings from nests near shrub-
dominated clearcuts or in core mature forest
SHORT COMMUNICATIONS
621
(Streby and Andersen 2011). Fledgling songbird
survival is usually lowest during the First few days
after fledging ( Anders et al. 1997. Berkeley el al.
2007, Rush and Stutehbury 2008, Moore et al.
2010) and variation in fledgling survival can
influence population growth as much or more than
nest productivity (Streby and Andersen 2011).
However, telemetry and banding studies demon¬
strate use of non-nesting cover types by fledgling
mature-forest birds occurs primarily utter birds
reach independence from adult care (Anders et al.
1998. Vitz and Rodewald 2010. Streby et al.
2011b). a period of relatively high fledgling
survival (King et al. 2006. Streby and Andersen
2011) .
Most studies describing non-nesting cover type
use by mature-forest songbirds have used mist
nets to capture birds in regenerating clearcuts and/
or forested wetlands (Pagen et al. 2000; Marshall
et al. 2003; Vitz and Rodewald 2007; McDermott
and Wood 2010; Streby et al. 2011a, b), and
relatively few have used radiotelemetry to track
movements of individual birds (Anders et al.
1998. Mitchell et al. 2010, Vitz and Rodewald
2010), However, capture data are limited in their
utility for estimating the proportion of fledglings
that move from mature forest to other cover types,
how far birds move to access those stands, how
long birds spend in those stands, and whether
birds are selecting other cover types over mature
forest (i.e., use them disproportionately relative to
availability). We used radiotelemetry to monitor
movements and cover-type selection by fledgling
Ovenhirds after independence from adult care in
managed forests of northern Minnesota. Our
objectives were to: (1) assess how many fledg¬
lings used forested wetlands and regenerating
clearcuts of different serai stages (shrub-dominat¬
ed and sapling-dominated). (2) leant how far birds
moved to access those stands, and (3) whether use
was in accordance w ith availability ot cover types
on the landscape. We conducted this study at two
sites similar in landscape cover-type composition,
but differing considerably in mature-forest under¬
story density, and assessed whether availability o!
dense understory vegetation alfected use ol
clearcuts and forested wetlands.
METHODS
Study Am/.— We studied Ovenbirds in 2007
and 2008 at two sites in the Chippewa National
Forest in north-central Minnesota. Both sites
consisted of forested wetlands, lakes, and legen-
erating clearcuts of different ages interspersed
within a matrix of mature forest >50 years of age.
The two sites were separated by 25 km. and
mature forest stands differed considerably in
structure and species composition between the
sites: one site was deciduous and the other was
mixed-deciduous-eonifcr forest. Mature forest at
our deciduous site was primarily open-understory
deciduous forest dominated by sugar maple (Acer
sacchartnn ). American basswood (Tilia america-
nti), paper birch ( Betula papyrifera), quaking
aspen ( Populus tremuloules). big-tooth aspen (P.
grcindidentata), and red maple (A. rubrum).
Mature forest at our mixed-deciduous-conifer site
ranged from stands dominated by red pine (Pious
resinoxa) to stands of mixed red pine and
deciduous trees. The mature-forest understory at
the mixed-deciduous-conifer site was: (1) domi¬
nated by dense sugar maple and hazel ( Corylus
spp. ). (2) denser than the open understory of the
deciduous site, and (3) similar in density to
forested wetlands and sapling-dominated clearcuts
at both sites (Fig. 1).
Field Procedures.— We attached radio trans¬
mitters to nestling Ovenbirds in mature-forest
stands at each site and tracked fledglings through¬
out the post-fledging period. We monitored nests
in randomly selected 10-ha nest-search plots, and
attached transmitters to 1-2 nestlings in each
brood that survived to within 2 days of its
expected fledge date. Wc attached transmitters
using a figure-eight harness design for songbirds
modified front Rappole and Tipton (1991).
Transmitters were 4.3— 4.9% ol nestling mass at
time of attachment, and as low as 3.0% of
fledgling mass before fledglings reached indepen¬
dence from adult care. Detailed nest-monitoring,
transmitter-attachment, and ground-based teleme¬
try methods are provided in Streby and Andersen
(2011). We continued to monitor all fledglings
that survived beyond independence from adult
care until either the birds were depredated or their
transmitters failed. We assumed all birds were
independent from adult core 25 days after fledging
(Streby and Andersen 201 1 ). A few birds (n = 3)
were accompanied by adults 26-28 days after
fledging but we did not observe them being fed by
those adults. The 23 fledglings we monitored were
from 23 separate broods, and we assumed their
movements were independent ot each other. We
monitored each fledgling daily (i.e.. one location
per day) using ground-based telemetry methods.
We located birds that moved beyond the range of
622
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124, No. 3. Sep, ember 2012
80
75
g 70
& 65
co
g 60
x>
55
o
ot 50
-o 45
c
=> 40
35
30
Used
Mature Mature mix. Forested Sapling Shrub
deciduous conifer wetland clearcut clearcut
wetlands santa d'ZnT,8?'^ *"***"»** *>•«■"<* ''»«<• malure mixed-decid„ouS-conifcr tom toml
Z p 'dencJ l emr SSW™nUttd “»• '«*»"> used bv Ovenbird Dedpngs after
boarS a, TO random Z '",u T M,nncsn,a' 'P™ -f board obscured) was measured using a profile
mean SE aZSZci es„Z v T T ml 58 "“W* '“‘“i""8' Diamonds, boxes, and whisker nrpresem
mean, Sb, and 95 h Cl, respectrvely. Letters represent significantly diflbnm groups at a = 0 05
our ground-based telemetry capabilities using
fixed-wing aircraft following standard aerie
telemetry methods (Meeh 1983). We located biro
from the air and communicated those locations vi
cellular lext message (upon landing) to a groun
crew, which continued tracking the bird on fool
We ceased monitoring each fledgling when th
fledgling died, the transmitter fell off, or tin
signal was lost and could not be found for 3 day
from the ground and after one telemetry flight
We assumed transmitter signals lost during Thi:
period were due to transmitter expiration because
they were near expected battery expiration dates
we were usually able to recover transmitters aftei
predation events (Streby and Andersen 201 1 ).
We recorded cover type at each fledgling daily
location and recorded the location with a hand-held
global positioning system (GPS) unit (100 points
averaged to improve accuracy). Ovenbird post-
fledging habitat use and survival have been
associated with use of areas with denser understory
vegetation than that of their nesting locations (King
et al. 2006), and the fledglings we monitored were
within 2-m of the ground during nearly all
observations. We used a profile-board method
modified from MacAnhur and MacArthur (1961)
to estimate understory vegetation density at tledg-
hng locations every fourth day (based on logistical
constraints) and at random locations within each
used, cover type. We used a 2 X 0.25-m board
d.v,ded into eight. 0.25 X 0.25-m squares. One
investigator held the boani vertically (ground to 2 n,
above ground) while a second investigator stood
° a ™dom direction (azimuths chosen
consecutively from an electronically produced list of
random numbers between I and 360) and estimated
the percent of each square obscured by vegetation.
We turned the board 90 degrees and repealed the
process. We used the mean of 16 estimates (8 from
each direction) us a single estimate of understory
vegetation density at each location.
We measured straight-line distances between
subsequent daily fledgling locations using global
information system (GIS) software. We used
aerial photographs and cover-type layers (U S.
Forest Service, Chippewa National Forest) in GIS
software to measure the proportional availability
of cover types within a 5-km radius from the
center of each study site. Space available to
individual animals is difficult to accurately assess
for wild populations (Acbischer et al. 1993).
However, increasing or decreasing the radius ol
our study areas by 1 km. and moving the center of
each study area 1 km in each cardinal direction,
had little effect (< 2% change for all cover types)
on cover-type composition. This method assumes
all locations within the study area are available to
each individual on all days of the study. Some
birds monitored moved -3 km within 2 days of
independence from adult care, and all cover types
were present <1 km from any location in our
study area, suggesting all cover types were
similarly accessible by all birds on all days of
the study.
Data Analysis. — We reclassified cover types
delineated in U.S. Forest Service cover-type
layers into five categories: (1) mature forest. (2>
forested wetlands, (3) sapling-dominated clearcuts
SHORT COMMUNICATIONS
623
TABLE 1 Availability and use of cover types by fledgling Ovenbirds alter independence from adult care in sites
dominated by open-understory deciduous forest and dense-understory mixed-dec.duous-comler foiest in
northern Minnesota.
Cover type
Mature forest
Forested wetland
Sapling-dominated clearcut
Shrub-dominated clearcut
Deciduous
Available (%)
Used (500 m
several times and each time the signal slopped
moving we caught up with the perched hawk). We
could not identify the locations of those fledglings
when they were initially captured by hawks, but
both were observed in mature forest with open
understory the day before they were depredated.
DISCUSSION
Independent fledgling Ovenbirds we tracked
used non-mature-forest stands as in previous
studies (Pagen et al. 2000. Marshall et al. 2003,
Vitz and Rodewald 2006). Fledgling Ovenbirds
moved long distances 6.1 km) between areas
used during the independent post-fledging period
(after independence from adult care but before
migration), likely explaining why nestlings banded
in mature forest adjacent to clearcuts are rarely
among the fledglings captured in those clearcuts
(Streby et al. 2011b). Our results are consistent
with those of Vitz (2008) who reported that
independent fledgling Ovenbirds in Ohio did not
use clearcuts more than expected based on
availability, but rather used riparian areas, treefail
gaps, and mature-forest with dense understory
vegetation. Similarly, independent fledgling Black-
poll Warblers (Setup/mga striata) and Yellow-
rumped Warblers (S. coronata) moved through
riparian areas ol river valleys in landscapes where
legenerating clearcuts were available (Mitchell
et al. 2010). Vitz (2008) suggested regenerating
clearcuts may be more heavily used by fledgling
Ovenbirds in areas with even-age open -understorv
mature forest. Fledglings we tracked in deciduous
forest with relatively open understory selected
sapling-dominated clearcuts and forested wetlands
substantially more than mature forest. Birds at our
deciduous sites spent several days in and made
considerable I -day movements (s 6.1 km) be¬
tween sapling-dominated clearcuts and/or forested
wetlands, apparently moving through mature
forest. Birds at the mixed -deciduous-conifer site,
where mature-forest understory was relatively
dense, made movements of similar distance to
those at the deciduous site, but used cover types in
accordance with their availability on the landscape
with the exception of under using shrub-dominated
clearcuts. This suggests resources available in
forested wetlands and sapling-dominated clearcuts
also are available in mature forests with a dense
understory. We observed only one independent
fledgling Ovenbird in a recently harvested, shrub-
dominated clearcut. consistent with low mist-net
capture rates in those stands, which may be related
to low food availability despite very dense
vegetation (Streby et al. 201 la).
It is important to consider that selection of any
cover type over another only suggests relative
importance, and information about survival and
food availability in those cover types is necessary
to make conclusions about their relative value to
birds that use them, Survival and food availability
in our investigation of habitat use and survival of
fledgling Ovenbirds still dependent on adult care
were highest in sapling-dominated clearcuts and
forested wetlands (Streby 2010). Survival of
independent fledglings was too high to compare
rales among cover types with our sample size,
although the only tw'o mortalities we recorded
apparently occurred in mature forest. Regenerating
clearcuts can be important areas for fledgling
Ovenbirds during the independent post-fledging
period, but not until saplings establish, and not
necessarily in landscapes in which dense mature-
forest understory or forested wetlands are common.
ACKNOWLEDGMENTS
I hose data were collected during a project funded by the
U.S. Fish and Wildlife Service and the U.S. Geological
Survey through Research Work Order 73 at the Minnesota
Cooperative Fish and Wildlife Research Unit with in-kind
support trom the U.S. Forest Service. We handled, banded,
and attached radio transmitters to Ovenbirds following
Protocol #0806A3576I. approved by the University ol
Minnesota Institutional Animal Care and Use Committee.
We thank D, L). Dcssecker, A. C. Edmond. J. L. Hammers,
SHORT COMMUNICATIONS
625
K. J. Iknayan, M. C. Loven, T. L. McAllister, E. S. Michel.
A. P. Monroe, S. M. Peterson, and J. M. Refsnidcr for
assistance in field data collection, and J. P. Loegering anil
two anonymous reviewers for constructive comments on
the manuscript.
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cover and food resource variation on post-breeding
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626
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 3. September 2012
I he Wilson Journal of Ornithology 124(3):626-629. 2012
Asymmetries in Mobbing Behavior Among Nuclear Flockmates
Jason R. Coulter1 *•
ABSTRACT. — Tufted Titmice (Baeolophus bicolor )
and Carolina Chickadees ( Poecile carolinensis) often
occur together in mixed species flocks during the non¬
breeding season and. as nuclear species, often initiate
mobbing bouts. We compared the mobbing behavior of
Tufted Titmice and Carolina Chickadees and. specifi¬
cally, their tendency to approach five potential preda¬
tors. We exposed flocks of chickadees and titmice to
study skins of live species of raptors in 2008; raptors
were categorized as either low-threat (rarely preying on
chickadees or titmice) or high-threat (more likely to
prey on chickadees or titmice). We noted the distance of
closest approach by titmice and chickadees during trials,
and whether a chickadee or titmouse spent more lime
within 5 m of the raptor, Titmice were more likely to
remain within 5 m of both low (P = 0.0008) and high-
threat [P = 0.0015) raptors. Titmice approached low-
threat raptors closer than chickadees ( P 0.01 4). There
was no difference in the mean distance of closest
approach by chickadees and titmice during high-threat
trials {P = 0.34). Titmice generally approached and
remained closer to raptors during mobbing bouts than
chickadees, possibly because larger titmice (~ 21 g) are
more likely targets of aerial predators than smaller
chickadees (— 1 1 g). Titmice may be willing to take
greater risks because the potential benefits (reduced risk
of predation) are greater if mobbing causes potential
predators to leave an area. Received 30 September 201 1.
Accepted 14 April 2012.
Mixed-species flocks during the non-breeding
season in the southeastern United States are often
composed of nuclear species including Tufted
Titmice ( Bcteoiophus bicolor) and Black-capped
(■ Poecile atricupillus ) or Carolina (P. carolinensis )
chickadees and attendant species (Moynihan
1962). Nuclear species direct group movements
toward food, maintain flock cohesion, and are
typically the first to approach potential predators
and initiate mobbing bouts (Dolby and Grubb
1999, Templeton et al. 2005, Bartmess-LeVasseur
et al. 2010).
1 Department of Biological Sciences. Eastern Kentucky
University. Richmond. KY 40475. USA.
C urrent address: School of Agricultural, Forest, and
Environmental Sciences. CIcmson University. Clemson SC
29634, USA.
'Corresponding author; e-mail: jcourte@demson.edu
and Gary Ritchison1
Mobbing can be beneficial, causing a predator
to leave an area, but such behavior can also be
costly, including the risk of being injured or killed
lor birds that closely approach a predator (e.g..
Denson 1979, Sordahl 1990). The costs and
benefits of mobbing may vary among species
depending on the identity of the predator. For
example, because larger predators tend to take
larger prey (Vezina 1985), larger raptors may
represent more of a threat to larger species in
mixed-species flocks. Roth and Lima (2007)
lound that Cooper's Hawks ( Accipiter cooperii)
generally prefer larger avian prey, while Roth
cl al. (2006) found that Sharp-shinned Hawks (A.
st rial us) typically do not target prey species
weighing <20 g. Thus, the potential benefits of
mobbing larger raptors may be lower for smaller
species in mixed-species flocks (e.g.. Carolina
Chickadees: ~ 1 1 g; Mostrom et al. 2002) Ilian
for larger species (e.g.. Tufted Titmice: — 21 g;
Grubb and Pravasudov 1994).
Both Tufted Titmice and Carolina Chickadees
utter 'chiek-a-dce* alarm calls when mobbing
perched aerial predators. Carolina Chickadees vary
the number of ‘dee* notes per call to potentially
convey information to conspecillcs about the threat
posed by different predators (Soard and Ritchison
2009). Tufted Titmice vary the rale at which ’dee'
notes are uttered which may convey information
about predator threat; this variation in call rate may
also deter predators by causing them to overesti¬
mate the number of titmice present (Courier and
Ritchison 2010). Thus, the alarm calls of Tufted
Titmice may differ functionally from those of
chickadees, conveying information to conspecillcs
and 'misinformation' to predators. These species
also differ in size and other aspects of their
mobbing behavior may also differ. Our objective
was to compare the mobbing behavior of Tufted
Titmice and Carolina Chickadees responding to
different species of raptors. We examined their
spatial relationships relative to potential predators
because proximity to predators, i.e.. approach
distances and time spent near potential predators,
may be related to risk (Krams et al. 2010) or
willingness to accept greater potential costs.
SHORT COMMUNICATIONS
627
METHODS
Study Area. — Free-ranging flocks of Carolina
Chickadees and Tufted Titmice were studied at
eight locations in Madison County. Kentucky
(37 4i' 58" N. 84° 16' 20" W) from 5 January to
27 February 2008. Study sites included private-
residences in = 7) and a public campground (// -
li and were separated by a minimum distance of
1.5 km. A feeding station, if not already present at
a site, consisting of a 1-nr section ot plywood was
placed 1 m above ground at each site in December
2007. All feeding stations were regularly stocked
with black-oil sunflower seeds.
Predator Presentations. — We used study skins
of five raptors in our experiment that differed in
potential threat they posed to parids (Templeton
et al. 2005. Soard and Ritchison 2009. Courier and
Ritchison 2010). Common predators of parids
(Gaddis 1980. Grubb 1998. Roth and Lima 2007).
including Eastern Screech-Owl (Megascops asio),
Sharp-shinned Hawk, and Cooper’s Hawk were
considered high-threat predators (Templeton et al.
2005). Great Homed Owls (Bubo virginianus) and
Red-tailed Hawks ( Buteo janiaicensis ), species
that rarely, if ever, prey on parids, were
considered low-threat predators ( lempleton et al.
2005, Nocera and Ratliffe 2010). An empty
platform (Baker and Becker 2002. lempleton
et al. 2005) and a study skin of a Ruffed Grouse
( Bonasa umbel Ins: a non-predutory bird) were
used as control presentations.
Trials were conducted at each location from 5
January to 27 February 2008 during 0900 to 1400
hrs EST with at least 48 hrs between successive
trials. Each trial was conducted by JRC and began
by placing a randomly-selected raptor (or control)
in a life-like position on a platform I m above
ground and I m from a feeding station. Specimens
were initially covered with a white sheet during a
5-min pre-presentation period while the observer
sat 5 m away. The pre-presentation period was
intended to acclimate birds to the observer s
presence and ensure chickadees and titmice would
remain near a feeding station sufficiently long for
an experiment to be completed. The observer then
walked to the feeder, removed the sheet to expose
the raptor or control, and returned to the
observation site to monitor the behavior of
chickadees and titmice for the 5-min trial period.
The observer noted during each trial: (1) the
number of chickadees and titmice present, (2) the
distance of closest approach by a titmouse and
chickadee, and whether a chickadee or a titmouse
(3) first approached within 5 m ol the raptor or
control, and (4) spent more time within 5 m of the
predator. Mean approach distances were estimated
( ± 0.5 m) using the width of the predator platform
( 1 m). distance of platform to feeding station
(I m). and the distance between the observer and
the feeding station as references.
Statistical Analyses. — W e calculated a mean
distance of closest approach for chickadees and
titmice in each of the eight flocks during the two
control trials, the two low-threat predator trials,
and the three high-threat predator trials. We
ascertained the percentage of control, low-threat,
and high-threat trials where titmice and chicka¬
dees in each flock were first to approach within
5 m and remained within 5 m ol controls oi
predators the longest. We compared the mean
distance of closest approach by chickadees and
titmice, and the percentage ol trials where each
species was first to approach and remain within
5 m of controls and predators using Wilcoxon
tests for paired samples. All tests were two-tailed.
We used Kruskul- Wallis tests to examine possible
differences in flock si/.e during control, low-
threat. and high-threat predator trials. We used the
Statistical Analysis System for all analyses (SAS
Institute 2004). Values are presented as means ±
SE.
RESULTS
The mean ± SE number of chickadees present
during trials was 3.2 ± 0.2 (range = 1-6) and the
mean number of titmice present was 2.6 ± 0. 1
(range = 1-5). Mean numbers of chickadees
(Kruskal-Wallis '/ji = 0.1 . P = 0.93) and titmice
(Kruskal- Wallis ti = 0,5, P = 0.80) present
during control, low-threat, and high-threat trials
did not differ. Chickadees and titmice were
equally likely to he first to approach within 5 m
of controls or predators in response to control (Z
= 1.4. p = 0.08), low-threat (Z = 0.2, P = 0.41),
and high-threat (Z = O L P = 0.50) treatments.
Titmice and chickadees did not differ in tendency
to remain within 5 m ot controls (Z = 0.1, P —
0.50). However, titmice were more likely to
remain within 5 m during trials with both low-
threat (Z = 3.2. P = 0.0008) and high-threat (Z =
3.0, P = 0.0015) predators. Titmice in the eight
flocks tested spent more time within 5 m than
chickadees during an average of 81.2 ± 9.0% ot
all trials with low-threat predators and 79.4 ±
9.1% of high-threat trials.
628
THE WILSON JOURNAL OF ORNITHOLOGY • VoL 124. No. September 2012
We found no difference in the mean distance of
closest approach by chickadees and titmice during
either control (Z = 0.1, P = 0.50) or high-threat
trials (Z = 0.4, P = 0.34). However, titmice
approached predators closer than chickadees
during low-threat trials (Z = 2.2, P = 0.014).
The mean distance of closest approach during
low-threat trials was 1.4 ± 0.3 m for titmice and
3.2 ± 0.6 m for chickadees, whereas (lie mean
closest approach distance during high-threat trials
was 1.7 ± 0.2 m for titmice and 2.4 ± 0.5 m for
chickadees.
DISCUSSION
Titmice in our study generally approached and
remained closer to predators than chickadees.
One possible explanation is that larger titmice
are dominant to smaller chickadees (Waite and
Grubb 1988) and, as a result, chickadees may
remain some distance from titmice to avoid
possible aggression. Another possible explana¬
tion. however, is that larger titmice may be more
likely targets of aerial predators than smaller
chickadees and, it so, titmice may mob with
greater intensity because those predators repre¬
sent a greater threat to titmice than chickadees.
Gehlbach (1994), in support of this hypothesis,
examined the behavior of 17 species of song¬
birds that mobbed Eastern Screech-Owls In
Texas and found a significant positive correla¬
tion between how often a species mobbed
screech-owls and how often screech-owls preyed
upon those species. Previous studies have re¬
vealed that Cooper's Hawks, for example,
generally prefer larger avian prey (Roth and
Lima 2007), and Sharp-shinned Hawks typically
do not target prey species weighing <20 g (Roth
et al. 2006). Larger titmice may also be less
maneuverable than smaller chickadees (Dial et al.
2008), possibly increasing their vulnerability to
aerial predators and providing additional incen¬
tive for titmice to aggressively mob predators
(Cresswell 1994a, b; Flasskamp 1994; Courier
and Ritchison 2010). Nocedal and Ficken (1998)
reported that Bridled I ittniee ( Baeolophus wolt-
weberi) in similar mixed-flock contexts in the
American southwest aggressively mobbed North
ern Pygmy-Owls ( Glaucidium gnoma), some¬
times approaching the owls as close as 30 cm.
Intense bouts ol mobbing behavior that include
close approaches to predators are adaptive
strategies that deter predators (Petti for 1990)
and cause raptors to change their roost locations
(move-on hypothesis; Sunde et al. 2003, Hen-
drichsen et al. 2006).
Titmice generally approached closer to preda¬
tors and remained closer for longer periods than
chickadees, but the difference in approach dis¬
tance by these two species with high-threat
predators was not significant. Small raptors such
as Sharp-shinned Hawks and Eastern Screech-
Owls are unlikely to prey on birds as small as
chickadees, but they almost certainly represent a
greater potential threat to chickadees than large
raptors including Red-tailed Hawks and Great
Horned Owls. Thus, for chickadees, the benefit of
more vigorous mobbing behavior (i.e., small
raptors leaving an area in response to vigorous
mobbing) may outweigh the potential costs (i.e..
risk ol predation by closely approaching a
potential predator).
Nolen and Lucas (2009) examined the mob¬
bing behavior of Tufted Titmice. Carolina
Chickadees, and White-breasted Nuthatches
{Sinn carol ineuxis) and found that chickadees
and nuthatches mobbed an Eastern Screech-Owl
model with greater frequency and intensity, and
typically approached the model closer than
titmice. We examined the combined responses
ol chickadee and titmice to three high-threat
predators; titmice in our study exhibited a
stronger response to Eastern Screech-Owl. spend¬
ing more time within 5 m than chickadees during
seven ol eight trials and, on average, approaching
closer (mean approach distances = 0.7 m for
titmice and 1.6 m for chickadees). One possible
explanation for this apparent difference in
responses of titmice and chickadees is that we
used study skins to elicit mobbing behavior,
whereas Nolen and Lucas (2009) presented a
model combined with playback of the screech-
owl monotonic trill. Nolen and Lucas (2009) and
others (Lind et al. 2005) noted a predator's
behavior may influence mobbing behavior. A
calling screech-owl likely represents less of a
threat than a silent owl that may be actively
hunting and titmice may respond less aggres¬
sively to the former than the latter.
ACKNOWLEDGMENTS
We lhank the Kentucky Ornithological Society for
linancial support. C. M. Soard for assistance in developing
our methods, L. A. Courter for help with field work, and N.
Santangelo. C. E. Braun, and an anonymous reviewer for
helpful comments.
SHORT COMMUNICATIONS
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Allometry of alarm calls: Black-capped Chickadees
encode information about predator size. Science
308:1934-1937.
Vf.zina. A. F. 1985. Empirical relationships between
predator and prey size among terrestrial predators.
Oeeologia 67:555-565.
Waite. T. A. and T. C. Grubb Jr. 1988. Copying of
foraeing locations in mixed-species flocks ol temper¬
ate-deciduous woodland birds: an experimental study.
Condor 90:132-140.
630
THE WILSON JOURNAL OF ORNITHOLOGY • Voi 124. No. 3. September 2012
The Wilson Journal of Ornithology 124(3):630-633, 2012
Eastern Screech-Owl Responses to Suburban Sprawl, Warmer Climate, and
Additional Avian Food in Central Texas
Frederick R. Gehlbach1
ABS I RACT. — Effects of suburban development
(sprawl), concurrent climate and increasing avian food
on a population of Eastern Screech-Owls (Megascops
asio) were studied for three decades using nest boxes and
natural tree-cavity nests in residential yards and adjoin¬
ing natural lores! in central Texas. The suburban climate
was warmer by 5.7 C associated with suburbia's heat-
island effect by the last decade of study. Nesting started
earlier by an average of 4.5 days annually and fledgling
productivity increased by 31,4%. Avian prey increased
and contributed to 93% successful annual nests in a more
stable population. Bird feeders and bird baths were likely
enhancing factors at residences, where owls obtained
prey and used bird-bath water for drinking and bathing.
Received 13 September 2011. Accepted 6 March 2012.
Suburban-nesting Eastern Screech-Owls (Mega-
scops asio ) differ from rural populations in central
Texas by living in a warmer climate, nesting earlier,
and producing more fledglings (Gehlbach 2008).
The effects of warming city climates have not been
widely considered for raptors nesting in cities and
suburbs of the United States until quite recently
(e.g., Meyburg and Chancellor 1994. Bird el aL
1996. Marzluff 2001, Bildstein 2008. Dunn and
Winkler 2010). I evaluated the likely ‘heat-island*
(Landsberg 1981) of increasing suburban develop¬
ment and its effects on Eastern Screech-Owls and
their avian prey in residential and remaining natural
habitat (cf Marzluff et al. 1998, Gehlbach 2005).
METHODS
Study Site. — Data were recorded annually
during 1980-2009 in a 270-ha study plot at
180-184 m elevation in Woodway, a suburb of
Waco, McLennan County. Texas (Gehlbach 1988.
2008). Suburban housing, other buildings, and
road development replaced all but 48 ha (18%) of
natural forest habitat during this study. Wooded
residential yards with 6-15 mature deciduous
and evergreen trees, open-canopy woodland, and
closed-canopy riparian forest were used for
nesting and toraging by screech-owls.
7 '^rnt c,rBiolo&y- fUylor University, Waco. TX
76798, USA: e-mail: Fred Gehlbach@Baylor.edu
Data Collection and Analyses. — Twenty wood
nest boxes were scattered randomly in the plot:
L5- 1 7 annually in wooded front and back yards
and the rest in natural riparian forest. Boxes were
7-12 m from the nearest house and street, and 3 m
high on tree trunks with diameters equal to or
greater than the 2 1 -cm box width. Annually, (i to
19 yard nests did not differ from 0 to 3 similar
natural, tree-cavity nests (Gehlbach 1994). Used
and potential nest sites were checked weekly or
more often during the March-May nesting season,
and all adult and feathered nestling occupants
were marked with l ISGS leg bands.
Suburban sprawl was measured as the cumula¬
tive number ol annual, city-issued building permiLs
ol all types in the study plot and adjoining area
within I km. Air temperature and precipitation were
recorded weekly in a wooded yard adjoining a 6-ha
private riparian forest preserve centrally located in
the study plot. Nesting birds were counted weekly
in residential yards and the preserve for data on
avifauna! size, composition, possible competition,
and potential food for screech-owls (Gehlbach
2005). Use of avian prey was based on stored
bodies and their remains in screech-owls' nests.
Annual data were assembled by single and
multiple decades for comparisons using factorial
analyses of variance (F). while 30-year population
and environmental relationships were evaluated with
best- fit linear, second-, or third-order polynomial
regressions. Comparative stability was considered
with coefficients of variation (CVs). A Principal
Components (PC) Analysis with orthogonal trans-
iormalions and varimax solution identified signifi¬
cant population and environmental factors ranked by
their individual sum of PC values. Numerical data
are given only for significant (P < 0.05) values and
summarized by means ± standard errors.
RESULTS
Population. —Most (71%) of the study's 367
screech-owl nests were in wooded residential
yards, and 48% of the 23 natural cavity nests were
in yards. All sites were within 104 m of riparian
SHORT COMMUNICATIONS
631
forest. Number of nests averaged 13.1 ± 1.0
(CV = 29.9) per year in the 1980s. decreased
insignificantly during the 1990s and stabilized
(CV = 12.6) at 10.7 ± 0.2 per year in the 2000s
(2n r = -0.66. P = 0.0005). The closest contem¬
poraneous screech-owl nests in residential yards
and forest were >46 in apart.
First eggs were laid in March and increasingly
earlier annually (r = —0.49. P = 0.005). Dales
averaged 21.3 ± 1.4 March in the 1980s and
advanced to 16.8 ±1.1 March in the 2000s • =
5.3, P = 0.005). Dates per year and decade were
unrelated to distance from the nearest building,
street, screech-owl or other raptor nest Screech-
owl nests were >30 m from the nearest yard¬
nesting Cooper's Hawks (Accipiwr cooperif) and
Mississippi Kites ( Iciiniu mississippiensis). and
the exclusively forest nesting Broad-winged
Hawks (Buteo plaryptems ) and Barred Owls
{Si rix varia).
Productivity, measured as fledglings per egg,
increased (2° r = 0.45, P = 0.03) from 50.3 ±
5.9% in the 1980s to 81.7 ± 5.7% in the 2000s
(F = 15,5, p = 0.0001) and was related to
increasing mean age of repeat-nesting females (2"
r = 0.54, P = 0.02). Female screech-owls s2 yrs
old laid larger clutches than yearlings (4.1 1 0.7
vs. 3.6 ± 0.8 eggs; F = 28.3, P = 0.0001) and
were more productive (3.2 ± 1.5 vs. 2.6 ± 1.4%;
F = 9.8. P = 0.002). Brood size increased from
2.3 ± 0.2 to 3.6 ± 0.1 (F = 42.9. P = 0.001 ) with
increasing female age (experience) as did percent
of successful nests defined as 2rl fledglings: 55.5
± 4.1 to 81.4 ± 2.2% ( F = 15.7, P = 0.0001).
Environmental Change and Relationships.
Suburban sprawl advanced by 2 to 8 buildings
annually in the first two decades (CV = 22.9) and
stabilized (CV = 1.8) in the third decade (2°
= 0.97, p = 0.0001 ). Number of screech-owl
nests tracked sprawl (r 0.85. P - 0.0001) as did
number of experienced nesting lemales (r = 0.59.
P = 0.009), population productivity (r = 0.82,
P = 0.0001), and percent of successful nests (r =
0.71, P = 0.0002) which peaked at 93% during
2000-2009.
Mean annual air temperature increased from
16.7 to 20.4 C during the first two decades {r -
0.75, P = 0.0001) but only 2.0 C afterward.
Earlier mean annual first-egg dales followed
increasingly warmer mean January-February
(pre-nesting) temperatures (r - -0.62. P =
0.0009). Percent successful nests and their
productivity tracked earlier first eggs (/
-0.39, P > 0.02) and, separately, an increas¬
ingly warmer March-Aprii nestling-fledgling
period (3" r 2= 0.58, P < 0.04). There were no
trends or relationships in precipitation and the
owl population.
Cached carcasses and identifiable remains in
owl nests represented 13 permanent and two
summer resident avian species, each of which
increased and stabilized with sprawl (2 r > 0.69,
P < 0.001). Screech-owl fledgling productivity
and nesting density were correlated annually with
the total number of potential avian prey (r ^ 0.61,
P < 0.001 ; r > 0.46. P < 0.03), whereas neither
measure related to numbers of other raptor nests
by species or collectively.
Ten significant population and environmental
factors that explained the suburban ecosystem
included five of each type (Table 1 ). Earlier eggs
laid by older, more productive females were the
principal population factors, while potential avian
food and warmer pre-nesting and nestling-fledg¬
ling period temperatures were the leading envi¬
ronmental factors. The added warmth of suburban
sprawl was the fundamental environmental factor
followed by increased avian prey.
DISCUSSION
Increasing thermal and resulting biological
effects on pre-nesting screech-owls in January-
February may include earlier available ectothermic
prey such as insects, crustaceans, and reptiles.
Warmer Apri 1-May periods may also promote food
and nest productivity, as food demand is highest for
foraging adults, growing nestlings, and dependent
fledglings at this time (Gehlbach 2008). Feathered
nestlings were weighed when banded within a
week of Hedging and showed no significant
changes in mass over the 30-year period.
Known ectothermic prey were active earlier in
the year and more continuously with the earlier
warmer temperatures (Gehlbach 2008). This prey
was more abundant in suburban yards than
concurrently in adjacent riparian forest (Gehlbach
2010). Suburban residences also focused avail¬
ability of known endothermic prey at bird feeders,
bird baths, and artificial ponds (Gehlbach 1996,
2005, 2008). Fifty-six percent of the screech-
owls' nest sites in yards had nearby feeders that
attracted prey noted in owl nests, and hall ot those
yards had bird baths and/or artificial ponds used
by the owls and other birds.
Increasing temperatures were also associated with
increasing tropical species such as White-winged
632
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 2. September 2012
TABLE I. Significant population and environmental factors affecting Eastern Screech-Owls nesting in suburban
central Texas based on annual data during 1980-2009 evaluated by Principal Components (PC) analysis. Factors are listed
in order of their highest (top) to lowest sums of PC scores regardless of sign. The proportion of each PC's explained
variance is in parentheses (total 11%).
Factor*
PC 1 (39%)
PC It H7%)
PC III (12%)
PC IV (9% i
Number of nests
0.49
-0.36
0.55
0.33
Mean first egg date
-0.05
0.23
0.62
-0.26
Females > 2 years of age
0.14
-0.03
-0.05
0.81
Pairs of nesting birds (food)
-0.11
0.37
0.17
0.18
Mean Jan-Feb temperature"
0.32
-0.19
-0.15
-0.12
Fledglings/eggs (productivity i
-0.17
0.41
0.07
—0.1 1
Mean annual temperature
0.38
-0.05
0.11
0.03
Mean Apr-May temperature1'
0.07
0.03
0.03
0.32
Suburban growth (sprawl)
0.06
0.18
-0.06
-0.08
Percent successful nests
-0.04
0.29
-0.02
0.07
“ Pre-nesting period.
' Nestling-fledgling period.
Doves (Zenoitla asiatica) first eaten in 1981 by
nesting owls and Cooper’s Hawks in yards.
Suburban Eastern Screech-Owls capture more 10-
150-g birds than mammals (Marzluff et al. 1998),
and birds in this size range such as doves. Northern
Cardinals {Cardinal is cardinal is), and House Finch¬
es ( Carpodacus mexicanus) visited feeders at dusk
when nesting adult screech-owls begin hunting
(Gehlbach 2008). Remains of these three species
were among others in owl nests.
Earlier nesting is also advantageous because of
the longer nocturnal owl-activity period, when
disturbance is less likely because of reduced or no
residential yard and garden maintenance, outdoor
play, and construction (pers. obs.). Moreover, there
is potentially less competitive impact front relum¬
ing migratory hawks until April (pers. obs.). Nests
are more likely to be disturbed, as human use of
yards increases later in the season, but begging
nestlings and fledglings in April-May were not
abandoned in contrast to eggs (Gehlbach 2008).
The decrease in nest density in early years,
coincident with increasing sprawl, probably
resulted from lost natural forest and more
disturbance from building and street construction,
The remaining forest was not fully protected until
the last decade of study, when abundance of the
plot s nesting birds stabilized together with sprawl
(Gehlbach 2005). Leg bands of screech-owls
banded as fledglings on the plot and returned
from outside areas up to 144 km distant,
numbered 0.2 per year before 2000 in contrast
to 0.7/year afterward, possibly reflected the last
decade of highest nest productivity.
ACKNOWLEDGMENTS
Baylor University supported this study. The Sugar Creek
Homeowners' Association allowed use of its private nature
preserve ol ravine-slope woodland and riparian forest.
Several ol my college students helped with field work, My
biologist wife, Nancy, was the principle help at nests during
handing. She read the manuscript with five decades of
practical experience and made suggestions throughout.
W. E. Stout and James Ward also read the manuscript
LITERATURE CITED
Bn. ostein, K. L 2008. A brief history of raptor
conservation in North America. Pages 5-36 in Stale
of North American birds ol prey (K. L. Bildstein. J. P.
Smith, h. R. Inzun/a. and R. R. Veit. Editors). Nuttall
Ornithological Club and American Ornithologists’
Union, Washington. D.C.. USA.
Bird. D M.. d. e. Varland. and J. J. Negro. 1996.
Raptors in human landscapes: adaptations to built and
cultivated environments. Academic Press. San Diego.
California. USA.
Dunn, P. O. and D W. Winker. 2010. Effects of climate
change on timing of breeding and reproductive success
in birds. Pages I 13-128 in Effects of climate change
on birds (A. P. Moller. W. Fiedler, and P. Berthold,
Editors). Oxford University Press. New York, USA.
Gl-Hl-BACH. F. R. 1988. Population and environmental
features that promote adaptation to urban ecosystems
the case of Eastern Screech-Owls (Of us asio) in Texas.
Proceedings of the International Ornithological Con¬
gress 19:1809-1813.
Gehlbach, F R. 1994. Nest-box versus natural cavity nests
of the Eastern Screech-Owl; an exploratory study
Journal of Raptor Research 28:154-157.
Gehlbach. F. R. 1996. Eastern Screech Owls in suburbia a
model of raptor urbanization. Pages 69-74 in Raptor-,
in human landscapes: adaptations to built and
cultivated environments (D. M. Bird. D. E. Varland.
SHORT COMMUNICATIONS
633
and J. J. Negro, Editors). Academic Press, San Diego,
California, USA.
GEHLBACH, F. R. 2005. Native Texas avifauna altered by
suburban entrapment and a method for assessing
natural avifauna! value. Bulletin of the Texas Orni¬
thological Society 38:35-47.
GEHLBACH, F. R. 2008. The Eastern Screech Owl: life
history, ecology, and behavior in the suburbs and
countryside. Second Edition. Texas A & M University
Press. College Station. USA.
Gehlbach. F. R. 2010. Suburbanization of a central Texas
herpetofauna. International Reptile Conservation
Foundation. Reptiles and Amphibians 17:87-03.
Landsberg, H. E. 1981. The urban climate. Academic
Press. London. United Kingdom.
Marzluff. J. M. 2001. Worldwide urbanization and its
effects on birds. Pages 19 47 in Avian ecology and
conservation in an urbanizing world (J. M. Marzluff,
R. Bowman, and K. Donnelly, Editors). Kluwer
Academic Publishers. Boston, Massachusetts, USA.
Marzluff. J. M.. F. K. Gehlbach, and D. A. Manuwal.
1998. Urban environments: influences on avifaunas
and challenges for the avian conservationist. Pages
28.3-299 in Avian conservation: research and man¬
agement (J. M. Marzluff anil R. SaJIabanks, Editors).
Island Press. Washington. D C.. USA.
Meyburg, B. U. and R. D. Chancellor (Editors). 1994.
Raptor conservation today. World Working Group on
Birds of Prey and Owls. Helm Information Ltd.. East
Sussex. United Kingdom.
The Wilson Journal of Ornithology 124(3):633-635, 2012
Diurnal Activity of the Austral Pygmy Owl ( Glaucidium liana) in
Southern Chile
Heraldo V. Norambuena1 *-3 and Andres Munoz-Pedreros:
ABSTRACT.— The Austral Pygmy Owl ( Glaucidium
naiia ) is usually recorded us actively calling and
foraging during daylight. We studied the diurnal activity
of the Austral Pygmy Owl over I year in Cerro Nielol
Natural Monument in southern Chile totaling 339 Ins ot
observation. The most intense activity was recorded at
mid-morning between 0900 to 1200 hrs when conspic¬
uous perching and foraging attempts were observed.
Vocalizations showed a pattern associated with the
reproductive season. The contact pair call was most
used throughout the year (5491). slightly more than the
territorial call ( 46%). Received 20 July 201 1 - Accepted
14 April 2012.
The Austral Pygmy Ow l ( Glaucidium tutna ) is
widely distributed in almost all environments in
Chile from Atacama (24 S) to Tierra del Fucgo
(53 S) (Jaramillo 2003). This species has been
described by numerous authors as having diurnal
activity (i.e.. Mousse 1945. Barms 1949. Goodall
et al. 1951. Venegas and Jory 1979. Narosky and
1 Raptor Conservation Program and Biological Control.
Centro de Estudios Agrarios y Ambientales, Casilla 164.
Valdivia. Chile.
:Nucleo de Investigation en Estudios Ambientales NEA.
Facultad de Recursos Naturales. Universidad Cutbhca de
Temuco. Casilla 15-D. Temuco, Chile.
3 Corresponding author; e-mail: buteonis@gmail.com
Yzurieta 1987). often calling during daylight
(Housse 1945. Banos 1949) and foraging on
diurnal birds, mammals, and reptiles (e.g.. Plain-
mantled Tit-Spinetail [Leptasthmirv aegitha-
l aides]. While-crested Elaenia [Elaeniu albiceps],
degu rat 1 Octodon degu\. and lizards \Liolaemus
spp.]; Jimenez and Jaksic 1989, 1993). However,
to the best of our knowledge, records on diurnal
activity arc mostly anecdotal and have not been
systematically described. Our objective was to
collect new data on the diurnal activity of the
Austral Pygmy Owl to support the observation
that it is primarily a diurnal bird of prey.
METHODS
The study was conducted in Cerro Nielol
Natural Monument (CNNM) (1 14 ha) (38 43 S,
72 35' W), a public protected wildlife area in
the central lowland of the Araucama Region in
southern Chile. Most of CNNM (76%) is covered
by temperate forest, dominated by associations of
boldo-roble (Peanuts boldus-Nolhojugus obliqua ),
peumo-boldo ( Cryptocarya (dha-Peumus ho Id us),
and olivillo ( Aextoxicon punchitumY, less repre¬
sented (24%) are the open shrublands dominated
by maqui (Aristoteiia chilensis), retamilla (Teline
monsppesulana), blackberry (Rubus ultnifolius), and
colonial bentgrass (Agmstis capillaris) (Hauenstein
et al. 1988).
634
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 3. September 2012
The diurnal activity of the Austral Pygmy Owl
was recorded by ( I) visual observations with 7 X
50 binoculars and a 20-60X telescope, and (2)
records of spontaneous calls (without playback,
Martinez and Zuberogoitia 2002). We identified
vocalizations following Banos (1949) and Good-
all et al. (1951): discriminating between the
contact pair call as a whistle with 6 to 7 notes/
sec described as huj-huj-huj-huj-huj-huj (Jimenez
and Jaksic 1989) and a territorial call (incorrectly
described as a hunting call by Goodall cl al. 1 95 1 )
as a sharp trill described as truie-lruie-yi-yi.
Observations were conducted from 6 March
2009 (austral autumn) to 26 February 2010
(austral summer), once a week from as early as
0700 through 1900 hrs (mean ± SD daily
observation time was 9.97 ± 0.32 hrs, n = 34)
for 339 hrs of observation (112 in summer. 35 in
autumn. 98 in winter, and 93 in spring) during 34
field trips.
OBSERVATIONS
We obtained 31 records of daytime activity of
the Austral Pygmy Owl of which 84% (n = 26)
were acoustic and 1 6% (n = 5) were visual records.
Acoustic Records. — Vocal activity was more
frequent al mid-morning between 0900 and 1200
hrs with a marked decline between 1300 and 1600
hrs and a gradual increase toward the crepuscular
hours (big. |). Daytime vocalizations were re¬
corded throughout the entire year of study with
the contact pair call being the most commonly
heard (54% of the records), slightly more than the
territorial call (46%). The contact pair call was
mTJlqri i75%) comParctJ to the territorial
call (25 7c) in early spring (1 Aug to 20 Sep) and
during the austral spring (Oct to Dec; 100%)
when the territorial call was not recorded. The
territorial call was heard more frequently in the
austral summer (Jan to Mar: 75%) and austral
autumn (Apr to Jun: 100%), when the contact pair
call was not recorded.
Visual Records. — Visual observations occurred
in all seasons of the year (2 in winter, and I in
each ot the other seasons), all between 0800 and
1400 hrs. Individual Austral Pygmy Owls were
observed perched and scanning in four of these
records. We recorded an individual Austral
Pygmy Owl stalking and attacking a White-
crested Elaenia, which was ~3 m distant perched
on a roble beech (Nothofagus obliqua) (height 15-
20 m) only once (7 Mar 2009 at 1 1 10 hrs); the owl
was unsuccessful and returned to its original
perch. I wo Tufted Tit-Tyrants ( Anairetes paru-
hts) and one Striped Woodpecker ( Veniliomis
lignarius ) approached the owl from the rear at
1121 hrs which continued watching them. The
Striped Woodpecker flushed, uttering alert vocal¬
izations when the ow l approached to within ~2 m.
chasing it and the two Tufted Tit-Tyrants. Thb
owl flushed at 1125 hrs and perched on the edge
of a road with human traffic,
DISCUSSION
Our results suggest the diurnal activity of the
Austral Pygmy Owl varies during the day, similar to
that reported for other raptors in the Strigidae (Negro
et al. 1990, Sovern et al. 1994, Sun and Wang 1997).
However, the owl's activity does not reach its
maximum immediately after sunrise or before
sunset, but during the mid-morning when most
passerine birds are still active (Ralph et al. 1996).
SHORT COMMUNICATIONS
635
Our records of contact pair calls coincided with the
period of pair formation (Aug) and laying (Sep-Nov)
iBairos 1949. Goodal let al. 1951, Marks et al. 1999),
while territorial calls were more common during the
juvenile dependence period (Feb-Mar). possibly to
stimulate juvenile dispersal from the natal territory
HVN and AM, unpubl. data).
The high proportion of crepuscular/diurnal prey
m the diet of the Austral Pvgmy Owl (Jimenez and
Jaksic 1989. 1993) and occasional observations of
daytime foraging and calling ( Housse 1 945. Ban os
1949. Goodal 1 et al. 1951. this study ) indicates this
owl is largely a crepuscular/diurnal species with a
peak of activity in the mid-morning and after
sunrise, similar to the Northern Pygmy-Owl (G.
gnorna ), a primarily diurnal species that is most
active between dawn and dusk (Ciiese and Forsman
2003, Saler el al. 2006, Deshler 201 1 ). However,
more studies are needed to know more precisely
about the nocturnal/diurnal activity and other
biological aspects about the little known Austral
Pygmy Owl.
ACKNOWLEDGMENTS
We express thanks to V. A. Raimillu lor cooperation in
the field and comments on the manuscript, and to t liile s
National Forest Service (CONAF) for the logistical support.
C. E. Braun, E. D. Forsman, J. E. Jimenez, and an
anonymous reviewer provided comments that greatly
improved the manuscript. We also thank the Direction
General de Investigaeibn y Postgrado of the Univcrsidad
Cutblica de Tenmco, Project DGIPUCT N C'D 2010-01
and Project Mecesup UCT 0804.
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Sovern. S. G„ E. D. Forsman. B. I . Biswe.ee, D. N.
Roi pii. and M. TayloR. 1994. Diurnal behaviour of
the Spotted Owl in Washington. Condor 96:200-202.
Sun. Y. H. AND Y. Wang. 1997. Tawny Fish Owl activity
pattern. Wilson Bulletin 109:737-741.
Venegas. C. and J. Jory. 1979. Guta dc campo para las
aves de Magallanes. Publicaciones Instituto de la
Patagonia, Serie Monograffas 1 1 . Puma Arenas. Chile.
636
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 3. September 2012
The Wilson Journal of Ornithology 124(3):636-640. 2012
Raptor Migration at Concepcion, Bolivia
Matias A. Juhant1-2
ABSTRACT. — I conducted the second austral au¬
tumn raptor count at Concepcion Watch Site in the
eastern Bolivian lowlands to document species compo¬
sition. liming, and abundance of migrating raptors
between 10 Match and 6 April 2009. I counted migrants
for 26 days (134.5 Ill's) recording 6,979 migrating
raptors of 1 6 species. Mississippi Kites Uctinia tnissis-
sippienm ) comprised 80% (n 5.571). Black Vultures
1 1% (Cnragyps atrottiy n 747). and Snail Kites 5%
( Rostrhatuus sociahi/is , n - 396). The remaining 4%
(n = 263) included 13 species and other unidentified
raptors, I also recorded lion-raptor species on migration
from the lookout, including 36 Maguari Storks ( Cieonia
maguuri), a flock of I I Anhinga ( Anhinga anhinga),
and thousands u! Barn Swallows (77 irunda rustica). My
observations confirm previous records suggesting a
significant raptor migration occurs at the Concepcion
Watch Site in the austral autumn. Raptor monitoring
should continue at Concepcion annually and the site
used to promote raptor conservation and awareness in
Bolivia. Received 12 December 2011. Accepted 10
April 2012.
Raptor migration in South America is largely
undescribed with lew published papers using
standardized migration monitoring protocols. This
topic is understudied, but of international concern
(Juhant 201 1 ). Thirty-five raptor migration watch
sites have been recognized in South America of
which eight are in Bolivia (Juhant 2011). Con¬
cepcion Watch Site in the eastern Bolivia low¬
lands was previously identified for conducting
long-term studies of raptor migration in both
austral spring and autumn (Davis 1989; Zalles and
Bildstein 2000; Olivo 2001, 2005. 2007a. b).
The first studies of raptor migration at Con¬
cepcion Watch Site began in the mid 1980s when
several thousand Mississippi and Plumbeous kites
(Ictinia tnississippiemis. I. phtmbea ) were count¬
ed in two consecutive austral springs (Davis
1989). Olivo (2001) conducted the first systematic
raptor migration count at Concepcion Watch Site
in 2000 counting >40.000 raptors during late
Faculty of Natural Sciences and Mathematics, Univer¬
sity of Maribor. Slovenia.
2 Current address Guriceljska 16 LjuMjana-Seiitvid 1000.
Slovenia; e-mail: maliasJuhantePyaJuio.com.ur
October. These included >37.000 Mississippi
Kites (Olivo 2001). Subsequent austral spring
counts in 2001 and 2003 recorded >120,000 and
>150.000 raptors, respectively, between late-
September and late-November (Olivo 2005.
2007a. b). The Mississippi Kite was the most
common species in both seasons with >115.000
and >145.000 kites recorded (Olivo 201)4.
2007b). The first and only study of raptor migra¬
tion during austral autumn was conducted in
March 2003 and recorded 5.000 raptors (Olivo
2007a, b). These included —4.000 Mississippi
Kites (Olivo 2007b). These studies reveal a large
number ol soaring raptors have been recorded at
Concepcion, but migration patterns at the site are
not well understood (Olivo 2004).
I documented species composition, timing, and
abundance of migrating raptors at Concepcion
Watch Site, Bolivia during austral autumn 2009
using standardized migration monitoring techniques.
METHODS
Study Area. — Concepcion town (16 08' S.
62 02' W ). Nuflo de Chavez Province. Santa Cruz
Department. Bolivia is 270 km (by road) northeast
ol Santa Cruz de la Sierra. Concepcion Watch Site
is 2 km southwest of the town center in the gated
community. Guantdtiatno. The lookout is on a pier
at the loot of Sapocd Lake created by a dam and
has a view of 360 degrees. Floristically. the
vegetation of the area contains elements of
evergreen tropical rainforest of the Amazon Basin
and subtropical thorn-scrub of the Gran Chaco
(Davis 1993). The region has dry (May-Ocl) and
wet seasons (Nov-Apr) with rainfall exceeding
1 ,100 mm, and an average temperature of 24.5 C
(Davis 1993).
Sampling. — I counted migrating raptors at the
Concepcion Watch Site during austral autumn
2009. The count was conducted over 26 days
1 134.5 hrs) in March and April: 21 days in March
( 10-12. 14-31; 1 13 hrs) and 5 days in April (2-6;
21.5 hrs). I counted 6 hrs per day (0900-1500
lies). The count was during the wet season, and
66% (88 hrs) of the count days were overcast.
26%' (35 hrs) were sunny, and 8% ( 1 1.5 hrs) were
SHORT COMMUNICATIONS
637
TABLE 1. Raptor counts by species at Concepcion Watch Site, Bolivia during austral autumn 2009 (10 Mai 6 Api).
Species
Migralion peak
Largest flock
Total
Counl
Dale
Size
Dale
Black Vulture Cora g\ps atratwf
747
104
14 Mar
40
14
Mar
Turkey Vulture Cathartes ultra'
26
6
17 Mar
4
Apr
king Vulture Sarcoramphus papa''
30
13
17 Mar
12
1 /
Mar
Western Osprey Pandion haliaetu s"
5
2
17 Mar
Hook-billed Kite Chondrohierax uncinatus b
2
2
25 Mar
80
20
Mar
Snail Kite Roslrliamus sociabilis c
396
130
23 Mar
Rufous-thighed Kite Harpagus diodon1'
12
6
2 Apr
2.000
29
Mar
Mississippi Kite Iclinui mississippiensis'
5.571
2,507
29 Mar
Lone -winged Harrier Circus bujfonf
1
1
19 Mar
Rufous-thighed Hawk Accipiter erythroncmiu.C
12
7
15 Mar
Great Black Hawk Buleogallus urubitinga'
2
1
14 Mar
Savanna Hawk B. meridionatis'
1
1
27 Mar
Swuinson's Hawk Buteo swainsoni"
4
2
29 Mar
White-tailed Hawk B. albicaudatus'
1
1
29 Mar
Yellow -headed Caracara Milvago chimachima'
2
1
1 1 Mar
Southern Crested Caracara Caracara plancus '
14
5
28 Mar
Unidentified
153
Totals
6,979
" Nearciic-Neoiropie migrant.
Neotropic-Intra-tropical migrant.
' Unknown migrant.
rainy, I identified all migrating raptors at the
count site using Swarovski 10 x 50 binoculars.
I scanned the southern sky in a 180 degrees arc,
from east to west, to locate migrants. Raptors
were considered migrating if they appeared on the
horizon and flew north past the watch site using
powered or soaring flight. Black Vulture ( Cora -
gyps at rains), Turkey Vulture (Cathartes aura).
and Snail Kites (Rostrluamis sociabilis) arc
common in the study area, and 1 identified these
species as migrants only if they passed the lookout
from the south using unidirectional I light and
Hying high. Data were collected hourly using the
standardized daily report protocol of Hawk Migra¬
tion Association of North America (Dunne et al.
1986). I selected days with consistent high numbers
of birds counted to document migration timing.
Wind speed and ambient temperature were record¬
ed using a Kestrel 20(H) Pocket Weather Station
(Nielsen Kellerman, Chester. PA. USA).
Raptor Identification. The following field
marks were used to identify species of raptors:
underwing and upperwing color patterns, flight
silhouette, and position of the wings in different
Hying modes. I consulted raptor Held guides
(Clark and Wheeler 2001, Ferguson-Lees and
Christie 2001) as needed.
RESULTS
Raptor Counts.—) counted 6,979 migrating
raptors of 16 species at Concepcidn Watch Site
(Table 1). The Mississippi Kite was the most
common species representing 80% Of = 5,571) of
the individuals counted, followed by Black
Vulture with 1 1% Of = 747). and Snail Kite with
5% Of = 396). Unidentified raptors accounted for
2% Of = 153). The remaining 2% (ft =112) were:
Turkey Vulture Of = 26). King Vulture ( Sarcor -
amphus papa, n = 30), Western Osprey (Pandion
Imliaetus, n = 5), Hook-billed Kite ( Chondro -
hi eras uncinatus, n =2). Rufous-thighed Kite
(Harpagus dindon. n = 12), Long-winged Harrier
(Circus buffoni. n = 1). Rufous-thighed Hawk
( Accipiter erythronemius, n = 12), Great Black
Haw'k ( Btileogallns urubitinga, n = 2), Savanna
Hawk (B. meridionatis, n = I ), Swainson’s Hawk
( Buteo swainsoni, /i = 4). White-tailed Hawk ( B .
albicaudatus, n = 1), Yellow-headed Caracara
(Mileage chimachima, n — 2), and Southern
Crested Caracara (Caracara plancus, n = 14)
(Table I ). I also recorded migrating non-raptor
species from the lookout, including 36 Maguari
Storks (Ciconia maguari), and u flock of 1 1
Anhinga (Anhinga anhinga). I also recorded
thousands of Bam Swallows ( Hirundo rustica)
638
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124. No. 3. September 2012
(A)
i Black Vulture □ Snail Kite □ Mississippi Kite
0900
1000
1100
1200
1300
1400
Time of day
RnMv h 1 percentage of Black Vultures. Snail Kites, and Mississippi Kites counted at Concepcion Watch Site,
milrtrnn .h^ Apr’' 'B' Pallern of Black Vulture, Snail Kite. andMississippi Kite
Mar 6 Apn * °f observcd/hr> Concepcion Watch Site. Bolivia dunng austral autumn 2009 (10
which peaked during the last week of March with
only a few passing in early April.
Raptors were observed flying mostly in two
directions in migration. 47% (n = 3,300) of
individuals migrated on the south-to-north axis.
43% (n = 3.010) on the southcast-to-northwest
axis with only a small fraction 10% (n 699)
Hying in other directions. Count days exceeded
500 raptors on 14. IX. and 29 March; the counts
were 665, 1,527, and 2.575 raptors, respectively.
Migration Timing. — Black Vulture (// = 747)
migration exhibited two peaks in passage one
between 14 and IS March when 47% of migrants
(» - 349) were observed, and another between 29
March and 4 April when 31% (n = 232) were
observed (Fig. 1 A). Most Black Vultures (56%.
n = 418) migrated past between 0900 and 1200
hrs (Fig. I B).
Flic Snail Kite (// = 396) migration peaked
between 15 and 25 March when 92% (n = 364 1 of
the individuals were counted (Fig. I A). Most
Snail Kites (90%, n — 356) migrated past between
0900 and 1200 hrs (Fig. IB)/
The Mississippi Kite (n = 5.571) migration
exhibited two peaks in passage rate, one on IS
March when 23% of migrants (n = 1.296) were
observed, and another on 29 March when 45% (n
= 2,507) were observed (Fig. I A). Mississippi
SHORT COMMUNICATIONS
639
Kites had a bi-modal distribution in time of
passage with 31% (n = 1,747) flying by between
0900 and 1000 hrs and 37% (n = 2,080) between
1400 and 1500 hrs (Fig. 1B>.
DISCUSSION
My observations, together with those of Olivo
(2001. 2004. 2005, 2007a, b). demonstrate that
significant movements of soaring raptors occur at
Concepcion, where 23 migratory species converge
during both austral autumn and spring. These
studies show a continentally important migration
site exists, but migration timing and number of
migrants recorded at Concepcion are not well
understood, especially during autumn. Concepcion
ranks as one of the lop areas to study seasonal
timing and abundance of migrating raptors in the
southern cone of South America (Juhant 201 1 ).
The three species of vultures recorded at
Concepcion are considered sedentary in the
southern part of their distribution (Ferguson -Fees
and Christie 200 1 ). However, these species were
previously counted on migration at the site by
Olivo (2001, 2005. 2007a). The Black Vulture is
the most common vulture recorded with an
average of 810 birds counted in autumn (Olivo
2007a, this study), and 895 birds in spring (Olivo
2005, 2007a). Satellite data of breeding Black
Vultures from the Argentine Pampas reveals they
migrate short-distances within the country (www.
vulturemovements.org/hms/hms_tv.htm). 1 he
number of Black Vultures, together with the low'
number of King Vultures, may indicate local
migration movements within the lowlands ot
Bolivia. Breeding Turkey Vultures I mm the
Argentine Pampas migrate northward east cl the
Andean foothills of Bolivia anti Brazil to
overwinter (www.vulturemovements.org/hms/hms_
tv.htm). Thus, vultures counted at Concepcion
could originate from southern latitudes.
The migration route of Snail Kites throughout
its range is largely unknown, but the species has
been recorded at many watch sites in South
America (Juhant 2011). The migration time of
Snail Kite in the lowlands of Bolivia is between
mid-February and carly-April (Zallcs and Bild-
stein 2000, Dobbs and Huizinga 2005, Olivo
2007a. this study), and between late-September
and late-November (Zalles and Bildstein 2000,
Olivo 2001. 2005, 2007a). It is not known if kites
recorded at Concepcion belong to the Austral-
Neotropic and Neotropic-1 ntra-tropical migration
systems or both. Study of migration of Snail Kites
in the Neotropics remains a fertile ground for
future research.
Mississippi Kites comprised nearly 80% of the
migrating raptors. The high numbers of kites
recorded in this study coincide with previous
counts at the site during austral autumn and spring
(Olivo 2001. 2004, 2007a). The average number
of kites counted in autumn is 4.710 (Olivo 2007b,
this study), whereas the average number of kites
counted in spring is 132,080 birds (Olivo 2004.
2007b). The difference in kite numbers recorded
between seasons may be caused by seasonal
factors. First, kites may migrate northward pri¬
marily in late Austral summer. A single flock of
1 0,000 kites was outlined on 20 February, 1 .000 km
south of Concepcion Watch Site migrating north¬
ward in Fuerte Esporanza town (25 1 1' S. 61 55' W)
in the Chaco lowlands of Argentina (Areta and
Seipke 2006). Second, kites may fly very high to
avoid storms or fly within the clouds in the autumn
(wet season), making it difficult to detect them
from the ground on migration (Smith 1985).
Finally, they may have an elliptical northward
migration route or may fly north in a more
dispersed (broader) front, avoiding this site. The
migration time of Mississippi Kites at Concepcion
is through March (Olivo 2007b, this study) and
between late-Scptember and late-November (Olivo
2004, 2007b).
The migration route and wintering distribution
of Mississippi Kites throughout South America is
largely unknown (M. A. Juhant and J. I. Areta,
unpubl. data), and the species has been recorded
on migration principally at Concepcion, which is
the only bottleneck area known for the species
south of the Panamanian isthmus (Juhant 2011).
Mississippi Kites have been reported in several
countries of South America but. despite the
growing number ot reports, it is considered
scarce, rare or transient in every country where
it is found during the boreal winter.
More research is needed to completely describe
timing of the raptor migration in the austral autumn
at Concepcion. An annual season-long count
by experienced observers from mid-February to
niid-Mav (northbound migration) and from
mid-September to late-November (southbound
migration) is recommended to gain a better under¬
standing of migration timing and composition at
this important site. A full-time annual count could
potentially provide critical long-term monitoring
data for several species of Nearctic and Neotropic
raptors, as done at many North American sites
640
THE WILSON JOURNAL OF ORNITHOLOGY • Vo l 124. No. 3. September 2012
(Goodrich and Smith 2008). It would be fruitful to
involve and train local residents in the phenome¬
non of observing long-distance migrating raptors
as Concepcion altords an exceptional opportunity
to study and appreciate raptor migration in South
America.
ACKNOWLEDGMENTS
I am grateful to Cristian Olivo for help with logistics of this
work. I thank the Herzog family. Sebastian. Carol, and Nanuq
lor hosting me at their home and also for looking after me
when I was sick. I also thank Ramona Hoffman, Elizabet and
Toto for hosting tnc at their house during the study. J learned
the techniques to study raptor migration as an International
Intern at Hawk Mountain Sanctuary. Travis Rosenberry from
the Peregrine Fund Library sent me multiple papers about
raptor migration. Also, it mi fomilia par apoyanne en exie
proyecto. I thank Laurie J. Goodrich and Juan I. (Naeho)
Arcta for many helpful comments on an early draft of this
manuscript. I thank Clait E. Braun, Mark Martel], and an
anonymous referee for their reviews and valuable comments
on the manuscript. 1 his is Hawk Mountain Sanctuary
contribution to conservation science number 215.
LITERATURE CITED
Areta. J. I. AND s. H. Sejpke. 2006. A 10,000 Mississippi
Kite flock observed in Fuerte Espcranza, Argentina.
Omitologia Neotropical 17:433-437.
Clark, w. S. and B. K. Wheeler. 2001. A field guide to
hawks of North America. Houghton Mifflin. Boston,
Massachusetts. USA.
Davis, S. E. 1989. Migration of Mississippi Kite Ictinia
missis '.ippiensis in Bolivia, with comments on /.
plumbea. Bulletin of the British Ornithologists’ Club
109:149-152.
Davis. S. E. 1993. Seasonal status, relative abundance, and
behavior ot the birds ol Concepcion. Departamcnto
Santa Cruz. Bolivia. Fteldiana Zoology 71:1-33.
Dobbs. R. C. and M. Huizinga. 2005. Noteworthy records
of migrating birds in the Bolivian Chaco. Cotinga
23:82-83.
Dunne, P., D. Keller, and R. Kochenberger. 1986.
Hawk Watch: a guide for beginners. Cape May Bird
Ohservalory/New Jersey Audubon Society. Cape May,
New Jersey. USA.
Ferguson- Lf.es, J. and D. a. Christie. 2001. Raptors of
the world. Houghton Mifflin, New York. USA.
Goodrich, L . J. andJ. P. SMITH. 2008. Raptor migration in
North America. Pages 37 149 in Status of North
America's birds of prey (K. L. Bildstein. J. P. Smith.
I. E. Ruelas, and R. K. Veit, Editors) Series in
Ornithology 3. Nutiall Ornithological Club. Cam¬
bridge. Massachusetts, and American Ornithologists'
Union. Washington. D.C.. USA.
J CHANT, M. A. 201 I. Where to watch raptor migration in
South America. Neotropical Birding 9:8-16.
OLIVO, C. 200l Bolivia Studying: migrating raptors at four
watchsites in Bolivia. Hawk Migration Studies 26:
32-38.
Ol.ivo, C. 2004. Migration patterns of Mississippi Kite
(falnta missisxippieitsis ) in the eastern lowlands of
Bolivia. Omitologia Neotropical 15( Supplement):
261 266.
Olivo. C. 2005. Cold fronts and raptor migration in
Bolivia. Omitologia Neotropical 16:109-115.
Olivo, ( , 2007a. Black Vulture movements in the eastern
lowlands ot Bolivia. Pages 73- 77 in Neotropical
raptors (K. L. Bildstein. D. R. Barber, and A.
Zimmerman. Editors). Hawk Mountain Sanctuary,
Orwigsburg. Pennsylvania, USA.
Ol-t VO. C. 2007b. Kite migration in eastern lowlands of
Bolivia. Pages 63-72 in Neotropical raptors tK. L.
Bildstein, D. R. Barber, and A. Zimmerman, Editors).
Hawk Mountain Sanctuary. Orwigsburg. Pennsylva¬
nia, USA.
SMITH. N. (I. 1985. Dynamics of trans-isthmian migration
ol raptors between Central and South America. Pages
271-290 in Conservation studies on raptors (I Newton
and R. C. Chancellor, Editors), Technical Publication
5. International Council for Bird Preservation. Cam
bridge, United Kingdom.
Zalles. J. L. and K. L. Bildstein. 2000. Raptor watch: a
global directory of raptor migration sites. BirdLife
International, Cambridge, United Kingdom.
The Wilson Journal of Ornithology 1 24(3): 640-643, 2012
Simultaneous Multiple Nests ot Calliope Hummingbird and
Rufous Hummingbird
Ned Batchelder,1 Gigi Batchelder,1 Dale A. Livezey,2 and Jeffrey S. Marks3'4
' 193 South 330 West, Ivins, UT 84738, USA.
1 2707 Street East. Helena. MT 59601, USA.
'4241 SE Licbc Street, Portland. OR 97206, USA.
‘Corresponding author; e-mail: jeffl7_marks@ni.sn.com
ABSTRACT. — We report the first cases of simulta¬
neous double brooding known for Calliope Humming¬
bird ( Stellula calliope) and Rufous Hummingbird
(Selasphorus rufus) from observations of two females
SHORT COMMUNICATIONS
641
in Montana. Each female laid two eggs and started
incubating while feeding large young in a nearby nest,
and each successfully Hedged young from both nesting
attempts. Simultaneous multiple nests base been
documented for five other hummingbird species that
breed north of Mexico, suggesting the behavior is
widespread in the family outside the tropics, factors
that might allow rapid renesting in temperate species
include young that begin to feed themselves within a
week after Hedging, and longer day length that allows
more time for females to forage than would be' available
in the tropics. Received 5 February 2012 Accepted 2
April 2012.
Reports of female hummingbirds simulta¬
neously caring for eggs and young from
successive nesting attempts date to the mid-
1930s when Skutch ( 1935:258) watched a female
White-eared Hummingbird (Hylnchuris leucotis)
feed a fledgling between bouts of incubation at
what he assumed was her second nest ol the
season. Rapid multiple brooding has since been
documented or strongly suspected for tit least
nine other species, the successive attempts
beginning soon after young from an earlier
attempt have Hedged (Blue-throated Humming¬
bird | Lampontis clemenciae], Williamson 2000;
Lucifer Hummingbird | Calothorax lucifer \.
Scott 1994; Anna’s Hummingbird | Calypte
cmim], Maender et al. 19%; Allen’s Humming¬
bird [Selasphorus sasin |, Pitelka 1951). oi
overlapping when a female lays eggs and begins
incubation while feeding large young at another
nest (Broad-billed Hummingbird | Cynantlvis
latirostris], Baltosser 1989; Ruby-throated Hum¬
mingbird Archilochus coluhri. s|, Nickcll 1948,
Black-chinned Hummingbird \A. alexanclri\.
Cogswell 1949; Costa’s Hummingbird I Calypte
costae], Baltosser and Scott 1996; Broad-tailed
Hummingbird [Selasphorus platycercm 1. Bailey
1974). Females of some species in the first group
may build a second nest while Iceding nestlings
but have not been documented laying eggs until
after the first brood has fledged (e.g.. Anna s
Hummingbird, Scarfe and Finlay 2001; Allen s
Hummingbird. Legg and Pitelka 1956). We
provide the first report of overlap nesting in
two other species, the Calliope Hummingbiid
(Stella la calliope ) and Rufous Hummingbird
{Selasphorus ru/us). The female laid a second
clutch in each case and began incubating while
provisioning large young in a nearby nest. We
also consider the factors that enable some
hummingbirds to initiate breeding attempts in
rapid succession despite the challenges of
uniparental care of altricial young.
OBSERVATIONS
On 3 July 2001, NB, GB, and John Vanderpoel
were shown two Calliope Hummingbird nests in
a rural backyard near Red Lodge. Montana. Each
nest was in a quaking aspen ( Populus tremu-
U tides) ~ 2.7 m above ground; the nest trees were
14 m apart. One nest contained two eggs and the
other had two large nestlings that were ~1 week
from fledging. They watched the nests for 4 hrs
on 3 and 4 July and witnessed several instances
in which the female incubated for -15 min at
one nest and then disappeared from view tor 5-
10 min before returning to feed the young in the
other nest. The female at times flew directly to
the nest with esgs and incubated after feeding
young at the other nest, verifying she was the
same parent that attended each nest. The home-
owners later reported that two young fledged
from each nest.
On 27 June 2008, DAL found a Rufous
Hummingbird nest with two eggs -1 m above
ground in a Douglas-fir (Pseudotsuga menziesii)
sapling near Seeley Lake, Montana. He later
watched the female leave (he first nest and fly to a
second nest -6 m above ground in a larger
Douglas-fir 20 m from the first nest. The second
nest contained one large nestling that was within
1 week of Hedging. On 2 July. DAL. NB, and Bob
Martinka watched and photographed the female as
she fed the nestling at the high nest and then Hew
directly to the low nest and incubated. The single
young from the high nest disappeared (presum¬
ably fledged) a day or two later, and the two
young that hatched at the low nest fledged in early
August.
DISCUSSION
Successful multiple nesting attempts in rapid
succession have been documented for at least 12
species of hummingbirds whose breeding ranges
occur wholly or partly north of the tropics. Two
nests can be occupied simultaneously for seven of
these species, one with large young, and the other
with recently laid eggs. Overlap nesting probably
occurs regularly in species tor which it has been
observed and likely will be documented in other
temperate hummingbird species. At least six
species of strictly tropical hummingbirds are
known to raise more than one brood per year
(Schuchmann 1999). but overlap nesting has not
642
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124. No. 3. September 2012
been reported (Haverschmidt 1958:143, Skutch
1973:81, Schuehmann 1999:514). Presumably, the
mild climate experienced by resident humming¬
birds in the tropics allows females to nest multiple
times without constraints of weather and migra¬
tion that cause some double-brooded females of
temperate species to renest so quickly that nest
construction, laying, and start of incubation must
occur before young from a previous attempt have
Hedged.
Hummingbirds are unusual among species with
altricial young because parental care is performed
solely by the female. Female hummingbirds may
seem poorly suited for attending two nests
simultaneously because they receive no assistance
from their males or from nest helpers (cooperative
breeding is unknown in trochilids). Female-only
care by birds with altricial young is confined to
species that eat fruit or nectar (Cockburn 2006).
Perhaps the energy-rich diet of nectar, rapid
absorption of nutrients (Schuehmann 1999),
ability to enter torpor during energy shortages
(Calder 2002), and longer day length at higher
latitudes allow females of temperate species to
maintain a positive energy balance while simul¬
taneously producing a second clutch of eggs and
provisioning large nestlings.
Rapid renesting appears to be a viable repro¬
ductive strategy for temperate-breeding hum¬
mingbirds in terms of tledgling production, but
nothing is known about survival of fledglings
from single-brooded versus multi-brooded fe¬
males. Young from first broods must be able to
care for themselves shortly after fledging for the
strategy to be evolutionary successful.
Little has been published on the postfledging
biology of wild hummingbirds, but the period of
parental dependency is thought to be short, from
a few days to a few weeks (Stiles 1973.
Baltosser and Scott 1996, Robinson et al.
1996. Russell 1996. Baltosser and Russell
2000). Young Broad-billed, Anna’s, and Costa's
hummingbirds raised in outdoor aviaries can
start feeding themselves 7 days after fledging,
although they are provisioned for longer periods
if their mothers do not attempt to renest (Karen
Krebbs. pers, comm.). Incubation constancy
normally ranges from 60 to 85% in humming¬
birds (Skutch 1962, Baltosser 1996. Calder
2002). rhus, it is not unusual for hummingbird
eggs to be left unattended for brief periods, as
would be necessary when females overlapped
two nesting attempts.
ACKNOWLEDGMENTS
Wc thank John Vanderpoel and Boh Maninka for
assisting with observations: William Baltosser. Karen
Krebbs. Karl -Ludwig Schuehmann. Peter Scott, and Sheri
Williamson for helpful discussions and manuscript reviews:
and the Kujala and Lamb families for allowing us to
observe hummingbirds on their respective properties.
LITERATURE CITED
BaILEY. A. M. 1974. Second nesting of Broad-tailed
Hummingbirds. Condor 76:350.
BALTOSSER. W. II. 1989. Nectar availability and habitat
selection by hummingbirds in Guadalupe Canyon.
Wilson Bulletin 101:559-578.
Baltosser, W. II. 1996. Nest attentiveness in humming¬
birds. Wilson Bulletin 108:228-245.
Baltosser, W. 1 1, AND s. M. RUSSEI.L. 2000. Black-
chinnetl Hummingbird ( Archilochus alexandri). The
birds of North America. Number 495.
Bal rosSER, W. H. AND P. E. Scon. 19%. Costa's
Hummingbird ( Calypte costae). The birds of North
America. Number 251.
Calder III, W. A, 2002. Characteristics and constraints of
incubation in hummingbirds. Pages 207-222 in Avian
incubation (D. C. Deeming. Editor). Oxford University
Press. Oxford. United Kingdom.
C OCKI1URN, A. 2006, Prevalence of different modes of
parental care in birds. Proceedings of the Royal
Society of London. Scries B 273:1375-1383.
COOSWLI.L. II. L. 1949, Alternate care of two nesls in the
Black-chinned Hummingbird. Condor 51:176-178.
Haverscmmidt. E. 1958. Nesting notes on Amaulia
fimhriota in Surinam. Ardea 46:138-144.
Lego, K. and I- A. Pitelka. 1956. Ecologic overlap of
Mien and Anna hummingbirds nesting at Santa Cm/.
California. Condor 58:393-405.
Mafnukr. G. .1.. K. L. Hurrr. and S. J. Bailey. 1996.
Nesting Anna's Hummingbirds in urban Tucson.
Arizona. Western Birds 27:78-80.
Nickli i , W. P. 1 948. Alternate care of two nests by a Rubv-
ihroated Hummingbird. Wilson Bulletin 60:242-243.
PlTELKA, P. A. 1951. Breeding seasons of humming¬
birds near Santa Barbara. California. Condor 53:198-
201.
Robinson, T. r.. r. r. Sargent, and M. B. Sargent.
1996. Ruby -throated Hummingbird (Archilochus colu-
bris). The htrd.s of North America. Number 204.
Ri-sst.i t_ S M. 1996. Anna's Hummingbird (Calypte
uitmt). The birds of Norrh America. Number 226.
Scarfe, A xnd J. C. Finlay. 2001. Rapid second nesting
by Anna’s Hummingbird near its northern breeding
limits. Western Birds 32:131-133.
SCH UCHM ANN. K. L. 1999. Family Trochilidae ihummmg-
hirds). Pages 468-535 in Handbook of the birds of the
world. Volume 5. Barn-owls to hummingbirds (J. del
Hoyo, A. Elliott, and J. Sargatal. Editors). Lynx
Edicions. Barcelona, Spain.
Scott, P. E. 1994. Lucifer Hummingbird ( Calothorax
lucifer). The birds of North America. Number 134.
SHORT COMMUNICATIONS
643
SKUTCH, a. F. 1935. Helpers at the nest. Auk 52:257-
273.
Skltch. A. F. 1962. The constancy of incubation. Wilson
Bulletin 74:1 15-152.
Skitch, A. F. 1973. The life of the hummingbird. Crown
Publishers. New York, USA.
The Wilson Journal of Ornithology 124(3):643. 2012
Stiles, F. G. 1973. Food supply and the annual cycle of the
Anna Hummingbird. University of California Publica¬
tions in Zoology. Number 97.
Williamson, S. L. 2000. Blue-throated Hummingbird
( Lainpomis clemenciae). The birds of North America.
Number 531.
Editorial News
On 1 July 2012. Mary Bomberger Brown and
Melissa Panella assumed the roles of Editor and
Associate Editor, respectively, of the Wilson Journal
of Ornithology. All new manuscripts and correspon¬
dence should he addressed to them at w jo ft?1 unl.edu.
The Wilson Journal of Ornithology and its
predecessor, the Wilson Bulletin, have a strong
tradition of emphasizing field studies of birds. We
will continue to welcome high quality research on
breeding biology, life history, behavior, popula¬
tion and community ecology, migration, distribu¬
tion, systematic^, conservation, and field based
physiology. WJO and Wli have traditionally
encouraged studies by ornithologists and field
biologists from all disciplines including those not
professionally trained in ornithology; this group
has made many significant contributions to
ornithology. We welcome submissions Irom
professionals, serious observers, and students at
any point in their careers. Our primary hope is that
authors of any paper based on high-quality, dnta-
eentered. field-related ornithological science will
consider WJO as an outlet for their work.
Beginning in March 2013 (Volume 125. Issue 1)
we will include searchable key words with every
paper. This addition will make the results being
reported more easily accessible to readers. We
have made a few' other changes to the Guidelines
for Authors (available on the Wilson Ornithologi¬
cal Society web page; http://wilsonsociety.org).
Authors should consult the Guidelines as they
prepare their manuscripts for submission to
WJO.
We will continue the tradition of including a
color frontispiece illustrating the lead article w'ith
every issue. The frontispiece artwork is supported
by the George M. Sutton Fund. We would like to
feature the artwork of up-and-coming bird artists
and encourage authors of lead papers to identify
suitable artwork.
WJO will soon reveal a new web page to the
world. We are working w ith Allen Press to design
a full service site where current and archived
issues of the journal w ill be available, along with
Guidelines for Authors, and information about the
Wilson Ornithological Society.
Finally, we thank Clait and Nancy Braun for
their years of dedicated service to the Wilson
Journal of Ornithology. For the past 6 years they
have tirelessly worked to make every issue of the
WJO the best il could possibly be. They skillfully
guided new authors through the maze of publish¬
ing in a professional journal and helped them
develop their manuscripts into fine papers. During
their tenure, the WJO has become a journal of
which w'e can all be proud, and we arc grateful loi
everything they have done tor WJO and WOS.
The editorial staff and WOS welcome com¬
ments about all aspects of the journal’s editorial
process, and we are always receptive to sugges¬
tions for improvement. — Maty Bomberger Brown
(wjo@unl.edu)
The Wilson Journal of Ornithology 124(3):644 648, 2012
Ornithological Literature
Margaret A. Voss, Book Review Editor
AVIAN ARCHITECTURE. HOW BIRDS
DESIGN. ENGINEER, AND BUILD. By Peter
Goodfellow. Princeton University Press. Prince¬
ton. New Jersey. USA. 2011: 160 pages. 300 full
color photographs, 12 architectural blueprints,
numerous color illustrations. ISBN: 978-0-691-
14849-6. S27.95 (hardcover). — I have a passion
lor animal architecture. Termite mounds, anthills,
beaver lodges, and especially the Taj Mahals of
the animal world— bird nests. Over the years
many books have focused on different aspects of
avian nest structure. At one end of the spectrum
are field guides; some are bare bones, complete
with questionable photography, while others arc
richly detailed with elegant full color plates and
illustrations. At the opposite end of the spectrum
are books written from either the perspective of
the behavioral ecologist attempting to understand
why birds build complex structures, or from the
viewpoint of the physiologist trying to understand
how nest structures augment the process o|
incubation. All ol these books, from field guides
to studies of behavior and function, tend to be
rather utilitarian. They are either useful in the
field or are text heavy and extremely academic in
nature. Some have become classics ( Karl von
Frisch's Animal Architecture comes to mind),
while others are largely forgettable. Peter Good-
fellow’s book is quite different from all that have
come before it. It is a beautifully illustrated
architectural digest of avian structure.
The book begins with a Forward by Mike
Hansell, who is probably the world’s leading
authority on animal architecture. In just a few
brief paragraphs. Professor Hansell succinctly
places the subject of this book within its proper
historical and biological framework. To some
extent, this frees the author to focus on the
intricacy and beauty of the structures he describes
and the complexity of nest building behaviors.
The book is organized thematically; each chapter
explores variations on the theme of a particular
nest structure (e.g., scrape nests, cup nests,
bowers, etc.). The introduction familiarizes the
reader with the book's organization, pointing out
that beyond a common nest structure - many
species share little in the way of breeding ecology.
To illustrate this and to put the function of the
structure into species-specific perspective, each
chapter ends with a series of case studies illu¬
strating how common structure can be adapted for
specific habitats and physiological requirements.
The resulting layout is visually beautiful, highly
functional, and easy to reference.
A unique aspect of this book is the use of
architectural blueprints' to describe general nest
structures. In this case, a picture is quite literally
worth a thousand words. The clean graphic
presentation packs a lot of information into each
description. One of my older books requires 1 1
pages of text to describe the design of a generic
bower. I he bower blueprint in this book covers
the general structure and function of a bower,
illustrates the three primary types, and includes
representative physical dimensions and some
species-specific information in two we 1 1 -designed
pages. In all chapters, the blueprints logically lead
into the species-specific case studies. Each case
study (35 in all) includes a brief species descrip¬
tion. a summary of its classification, details for the
physical dimensions of the nest structure and nest
materials, and descriptions and beautiful illustra¬
tions ol nesl building behavior. Most chapters
include multiple examples of species from around
the world, The Iasi chapter of the book covers
edible nests and food stores — as in nests humans
consume and the places birds store their own
comestibles. This chapter is brief, but filled with
interesting anecdotal and historical tidbits, and
some beautiful photography. I found this to be the
least detailed but most interesting chapter and
would have liked to have seen a more in depth case
history of one of the swiftlets that produce such
amazing nests from salivary secretions. The book
concludes with a glossary of terms and a
reasonably well researched list of resources and
web sites that would be useful to explore the study
of avian nest structure in more detail. Although
well done, these aspects of the book are probably
most useful for the casual reader: both professional
and experienced amateur ornithologists would
likely find them too basic for their purposes.
In the end, I found the book to be detailed,
scientifically accurate, well written, and visually
644
ORNITHOLOGICAL LITERATURE
645
beautiful. I would recommend it to both the casual
reader of ornithological literature and the profes¬
sional. The author has done a wonderful job of
melding what can become a dry and technical
topic (the study of nest structure.) into the format
of a so-called coffee table book. Unlike many
books primarily designed to be beautiful, this text
has solid scientific credentials and the ability to
inform even those with academic interest in nest
structure. Instead of displaying the book on a
coffee table only to become unintended support
tor lounging legs. I suggest a prominent place on
an office desk. The pictures are likely to draw in
anyone who casually thumbs through the book —
while the well written, detailed text will surely
inform even the most reticent reader. 1 plan to try
this little experiment in guerilla education on
some unsuspecting undergraduates in the near
future.— MARGARET A. VOSS. Associate Pro¬
fessor. The Pennsylvania State University at
Erie. Behrend College. 4205 College Drive. Eric,
PA 14063. USA: e-mail: mavll@psu.edu
avian coloration and vision requires them to go
back to the basics and try to learn, or relearn,
about the fundamental nature of light. The
problem is that cutting-edge physical and chem¬
ical research is way too specialized, and that a
typical physics or chemistry curriculum does not
include the specific topics that are relevant to bio¬
logy. The process is bard, and the result is
mistakes are made. I know from personal
experience!
The Optics of Life by Sonke Johnsen, of the
Department of Biology at Duke University, seeks
to till this intellectual need with an introductory
but serious book on all aspects of light that are
relevant to biology. Johnsen works mostly on
marine invertebrates, and has made especially
interesting contributions on the transparency in
marine environments. Johnsen's research com¬
bines a real fascination with organisms and their
functions, serious field work, and hard core phy¬
sics. His background makes him an excellent
person to try to bridge the fields of organismal
biology and optics.
Johnsen's book takes a broad approach, and
THE OPTICS OF LIFE: A BIOLOGISTS
GUIDE TO LIGHT IN NATURE. By Sonke
Johnsen. Princeton University Press. Princeton,
New Jersey. USA. 2012: 336. ISBN; 978-0-691-
13990-6. $99.50 (hardcover), ISBN: 978-0-691-
13991-3. $45.00 (paper).— An exciting develop¬
ment in ornithology over the last 20 or 30 years
has been a breadth of new research that takes light
-seriously. It took a few decades lor the discovery
of the four color cone visual system and
ultraviolet visual sensitivity of birds to move out
of physiology laboratories and into the conscious¬
ness of ornithologists working on communication.
This was catalyzed by the production of the first
affordable, broad spectrum liber optic spectro¬
photometers in the 1990s. Over the subsequent
years, the science ol avian color and color vision
has expanded tremendously. 1 he richness ol avian
color vision and color communication insures
these Helds will remain important, and that many
more phenomena remain to be discovered and
investigated.
Research programs in this area must Irequently
span i he fields of ethology, behavioral ecology,
physiology, chemistry, and physics. There are
even conservation issues if you consider migrat¬
ing birds killed by colliding with buildings,
towers, or wind turbines they have failed to see.
Many ornithologists have found their research in
incorporates all the optical phenomena that are
actually occurring in biological systems and those
that occur in the abiotic environment that influ¬
ence the functions of biological systems. The
chapters cover the typical topics in optics
emission, absorption, scattering, scattering with
interference, fluorescence, and polarization— with
special chapters on units ol light and the mea¬
surement of light... But the book is not like a
traditional text in optics.
Johnsen's treatment is both inviting and sophi¬
sticated. He introduces every idea with a carefully
worded and straight- forward description, often
with analogies to other real world experiences or
ideas. He treats the mathematical details on a
'need to know' basis, and usually goes no further
than some simple algebra. Blit Johnsen has picked
the details he does present carefully, and the sim¬
ple principles have profoundly important impacts
on biological optics and how we study it. For
example, Johnsen presents an equation to describe
the optics of vision that is the product of four
terms, but he then spends four full pages describ¬
ing the equation and unfolding what this relation¬
ship means.
The Optics of Life is also quirky and funny.
Johnsen introduces the discussion ol optical
absorption with a story about how, when he was
a child, different parts of the family's Dodge Dart
646
THE WILSON JOURNAL OF ORNITHOLOGY • Voi 124. No. 3. September 2012
would resonate at different speeds. He recom¬
mends lhal we loo look at Froot Loops under
blacklight and watch the chewing Wint-o-Green
LifeSavers in the dark, hut then describes how
these things should be relevant to life. (The inci¬
dental fluorescence of Froot Loops is particularly
relevant to why the fluorescence of some parrot
pigments remains a functional mystery.) The book
does have a few limitations, which are necessary
for a book of this scope. For example, it includes
no details on the physiology or neurobiology of
vision. Rut the chapter on measuring light will be
especially helpful to those getting into work on
plumage coloration.
Ornithologists will find that this book was not
written especially for them. This is no surprise
given the great breadth of the topic. Consequently,
the main topics of current research interest in birds
are not high-lighted above others merely because
they are popular. From my own perspective, 1 wish
Johnsen had focused more attention on some recent
discoveries from birds that have broad application
for all of life — e.g., the production of structural
coloration through interference from ‘quasi-or¬
dered’ nanostructures. Thus, ornithologists may
not consider Optics of Life to be required reading.
However, what Johnsen knows and communi¬
cates clearly is fundamental and important to life.
It seems to me that ornithologists who read this
book and master this material will be well poised
to make the next generation of discoveries about
the Optics of Ornithology. — RICHARD O. PRUM.
William Robertson Coe Professor of Omitholo-
gy.Yale University, Peabody Museum of Natural
History, P. O. Box 20815. New Haven. Connecti¬
cut, USA; e-mail: richard.pmm@yale.edu
TROPHIC INTERACTIONS: PREDATORS.
PREY AND THE CHANGING DYNAMICS OF
NATURE. Edited by John Terborgh. and James
A. Estes. Island Press, Washington. D.C., USA.
2010: 464 pages. ISBN: 978- 1-56726-487 $47.50
(paper). — Top-down or bottom-up? What is the
strongest driver of ecological processes in nature?
John Terborgh and James Estes tackle this 50-year
old question in their four-part book. Leading experts
in aquatic systems, terrestrial systems, predator- prey
dynamics, and food webs provide evidence that
strong relationships exist between predators and the
entire ecosystem in which they reside, supporting
the green hypothesis posed by Hairston. Smith
Slobodkin (HSS; 1960) that predators have an
important role in ecosystem functions and specifi¬
cally ecosystem producers. Each chapter and section
contributes to the mounting evidence from expen-
mental, observational, and opportunistic studies that
suggest cascading impacts from predators have a
key role in ecosystem processes.
Chapter one provides the foundation that top-
down and boltom-up driving forces are not
mutually exclusive, and this oversimplification
ol ecological processes has distracted ecologists
from close examination of complex food webs
and the role predators have in ecosystem function.
Trophic cascades, identified as the process bv
which predators can influence other species
beyond their prey, are introduced as the ‘holy
grail' to understanding how ecosystems function
and to predict their responses to system perturba¬
tions. This chapter sets the stage for evidence
presented from aquatic, terrestrial, and general
predation studies to shift paradigms to focus on
the strong relationships within food webs that
stabilize ecosystems and maintain diversity,
largely tied to the function predators have in
these systems. A major emphasis is placed on
three-level trophic interactions, typically predator,
prey, and producer, but with the recognition the
chains within cascades may be two or potentially
larger than three levels.
Part one focuses on case studies in aquatic
systems that provide supporting evidence of top
predators affecting producers. The strongest
forces of top predators are observed in whole-
lake systems, and intertidal and benthic marine
environments. Evidence for effects from top
predators does exist for pelagic systems, but there
is a general lack of studies focusing attention on
top-dow n el lects of predators in oceanic systems
relative to other aquatic ecosystems. Sea otters
( Enhydra lutris ) influence sea urchins (Stronglyo-
centrotus purpuratus) and kelp forests, -as well as
the role of star fish ( Pisaster ochraceiis) on
species composition on rocky shores are examples
of strong interactions where top-down forces
influence the producer trophic level. Direct
interactions of changes in population size were
only one impact of top predators, but a secondary
theme of indirect influences such as behavioral
changes begins to emerge as an influence of
higher trophic levels on their prey.
Part two delves into case studies demonstrating
the role of top predators on terrestrial ecosystems
with a focus on impacts of herbivore-plant inter¬
actions, as well as influences of top predators
ORNITHOLOGICAL LITERATURE
647
which have been lost from most terrestrial
systems and how their impacts on herbivores
have resulted in dramatic shifts in plant commu¬
nity composition and. ultimately, the management
necessary in these systems. A large emphasis is
placed on the role of mega-herbivores which, like
apex predators, have largely disappeared from
many ecosystems. These mega-herbi\ ores are key
drivers in plant structure and composition; the
need for fire as a conservation tool is likely more
important with decreased numbers of mega¬
herbivores providing grazing pressure and periodic,
potentially intense, disturbances to ecosystems.
Some general guidelines for strong interactions
begin to emerge relative to ecosystem complexity
and links with the theory of island biogeography,
and strength of relationships across trophic levels
can be generalized. For example, strong cascades
can he observed when species diversity is low on
smaller or more remote islands and when there is
kw functional redundancy (i.c.. simple ecosystems
with few species that can be removed and their role
compensated by other members of the community).
Part three addresses the process of predation
and the results of shifts in predator composition
on lower trophic level predators (o.g.. mesopre-
dalors) and behavioral responses of prey. Remov¬
al of lop predators and increased role of human
influences on the landscape have resulted in
altered ecosystem composition where mesopreda-
tors thrive in the absence of top-down forces and
with subsidized food and habitat conducive for
them to nourish. Furthermore, mesopredator and
herbivore behavior is altered in systems devoid of
apex predators. Comparisons of ungulate behavior
demonstrate fear-mediated responses of predators
with higher vigilance and larger group sizes in
areas with reintroduced or remaining predators
relative to predator-void areas.
The authors emphasize predator persecution
which has occurred across much of the world.
Using case studies in the Serengeii. they demon¬
strate the need to study remote, more natural areas
where intact ecosystems containing top predators
and mega-herbivores still remain. It is only in
these systems that we can truly observe the
potential impacts of top predators and trophic
cascades without the huge anthropogenic impacts
found in about 90% of the world's ecosystems.
Part four is a synthesis of the findings of this
book that highlights the implications associated
with accepting the paradigm shift that predators
are critical in ecosystem diversity and stability, and
the conservation and management considerations
that will help revive degraded ecosystems. It is
in this section that the editors and contributing
authors summarize evidence from previous chap¬
ters on a variety of ecosystems that top predators
and trophic cascades are important in understand¬
ing ecosystem functions with the recognition there
are different levels of strength to cascading effects
based on community composition and complexity.
Evidence is presented throughout this book that
predators can have immediate impacts on fitness
and provide an immediate fitness consequence that
shapes prey populations directly and indirectly.
Oversimplification of processes as mutually exclu¬
sive top-down or bottom-up drivers will not result
in scientific progress; rather, we need to re-evaluate
the ingredients of truly natural systems and what
has been lost in the human-dominated landscape.
We must recognize we can not erase the human
footprint to be able to properly conduct conser¬
vation and management. We can. however, work
to maintain habitat connectivity and encourage re¬
establishment of top predators and critical players
to ecosystems to attempt to prevent further de¬
gradation of ecosystem functions. — SUSAN N.
ELLIS-FELEGE. Assistant Professor. University
of North Dakota, Department of Biology, 10
Cornell Street. Stop 9019, Grand Forks, ND
58202, USA; e-mail: susan.felege@email.und.edu
A FIELD GUIDE TO THE BIRDS OF NEW
ZEALAND. By Julian Fitter and Don Merton.
Princeton University Press, Princeton, New Jersey,
USA 2011: 288 pages, more than 600 color
photographs, 3 maps. ISBN: 978-0-691-15351-3.
$24.95 (paper). — This new addition to the Prince¬
ton Pocket Guide Series covers New Zealand
(North. South, and Stuart islands), the Kennadec
Islands to the north, and the islands as far south as
the sub-Antarctic Campbell Island groups. New
Zealand has a long history of bird exploitation and
extinction, beginning with the arrival ol the Maori
and subsequent annihilation ot the Moa species
(Order Dinornithi formes), followed by the wave of
European immigrants with a species extinction as
recently as 1972. It is not surprising this is
discussed in the introductory material which
applauds recent conservation initiatives, including
those by the late Don Merton, one of the authors,
and highlights the sanctuaries and reserves that
offer birders an opportunity to see birds that
otherwise might be extinct.
648
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124. No. 3. September 2012
The introductory material includes sections on
geography, geology and climate, flora, habitats,
human history, conservation, and alien species, and
three maps, one showing New Zealand and its
offshore islands, and one each of the North Island,
and South and Stewart islands. A long series of
abbreviations (which 1 initially found daunting, but
soon got used to) help compress the species
accounts. These accounts, two-to-four per left-
hand page, begin with a small line diagram which
outlines the number and arrangement of photo¬
graphs on the facing page with the species’ share of
the photographs identified in gray. The typical
species account includes a description with the
critical identification features in italics, differences
in female and juvenile plumage, sections on voice/
call, feeding, breeding, breeding range, and estima¬
tion of breeding numbers, threats and management,
habitat where best viewed, and status in New
Zealand. The number of facing page photographs
varies from two to nine with one to five photo¬
graphs per species. About a quarter of the species
covered are listed as vagrant, occasional, or chance
sightings, mostly of Australian birds. Following the
species accounts are a list of extinct species and
‘Notes for the Visitor,' which includes an annotat¬
ed list of island sanctuaries, mainland sanctuaries
(each surrounded by pest-proof fences), a long list
of ‘Other Birding Spots.' ‘Offshore Boat Trips,'
national parks and other protected areas, birding
tour operators with contact information, environ¬
mental and conservation organizations, a bibliog¬
raphy, a glossary, and an index — all very useful
information.
One of the great strengths of this book is its size-
at 115 X 189 X 18 mm it fits easily into most
jacket pockets and is an actual ‘field' guide. The
sequence of bird species is not laxonornically
arranged, which may annoy some people, but
rather starts with a section on ‘Seabirds.' fol¬
lowed by ‘Waterside and Wetland Birds,' and
finally ‘Landbirds.' The Waterside and Wetland
bird section begins with the shorebirds (waders),
followed by grebes, spoonbills, ibises, cranes,
pelicans, and rails before getting to ducks and
geese. The photographs tire generally of excellent
quality, but there arc exceptions. For example, the
white neck of the White-necked Heron (Aniea
pucij'ua) is in deep shadow, neither photograph of
the White-chinned Peu-el ( Procell aria aequinoc-
tialis) has even a hint of white, and the white on
several birds is huffy. I personally prefer painted
plates to photographs, partially because photo¬
graphs make visual size comparisons among spe
eies problematic, it is difficult to standardize poses
for comparison purposes, and foreshortening in
other than side view' causes problems. That said, I
think the selection of photographs for this book was
well done with a lew exceptions — three photo¬
graphs of the Rock Dove (Col umbo livia ) are a bit
much, especially when only a single photograph of
the endemic New Zealand Pigeon (Kercru) (Hcmi-
phaga novae seel and! ae) was presented on the
same page.
This field guide is not perfect, but it is loaded
with information and will allow you to identify
the vast majority of New Zealand birds. 1 will
have one in my pocket on my next trip to New
Zealand.— WILLIAM E. DAVIS JR., Professor
Emeritus, Boston University, 23 Knollwood
Drive, East Falmouth, MA 02536, USA;
e-mail: wedavisl l@gmail.com
The Wilson Journal of Ornithology 124(3):649, 2012
ANNUAL MEETINGS OF THE WILSON ORNITHOLOGICAL SOCIETY'
1“ 1914, Chicago. Illinois
2nd 1914. Chicago, Illinois
3rd 1915. Columbus. Ohio
4“’ 1916, Chicago. Illinois
5* 1917. Pittsburgh. Pennsylvania
6* 1919. St. Louis. Missouri
1920. Chicago. Illinois
8th 1921. Chicago. Illinois
9® 1922. Chicago. Illinois
10® 1923. Cincinnati. Ohio
11* 1924, Nashville. Tennessee
12® 1925. Kansas City. Missouri
13® 1926. Chicago, Illinois
14® 1927. Nashville, Tennessee
15® 1928, Ann Arbor. Michigan
16* 1929, Des Moines. Iowa
17® 1930. Cleveland. Ohio
18* 1931. New Orleans, Louisiana
19® 1932. Columbus. Ohio
20* 1934. Pittsburgh. Pennsylvania
2I'1 1935. St. Louis, Missouri
22nd |936. Chicago. Illinois
23rd 1937, Indianapolis, Indiana
24® 1938, Ann Arbor. Michigan
25* 1939, Louisville, Kentucky
26® 1940, Minneapolis, Minnesota
27® 1941, Urbana, Illinois
28* 1946. Omaha. Nebraska
29* 1947. Columbus. Ohio
30"' 1949. Madison, Wisconsin
31’’ 1950, Jackson’s Mill. West Virginia
32"d 1951. Davenport. Iowa
33rd 1952, Gatlinburg, Tennessee
34* 1953, Cheboygan. Michigan
35* 1954, Cape May, New Jersey
36* 1955. Stillwater. Oklahoma
37* 1956. Buffalo. New York
38® 1957, Duluth, Minnesota
39* 1958, Wheeling. West Virginia
40* 1959. Rockland. Maine
41" I960. Gatlinburg. Tennessee
42nd 1961, Huntsville. Ontario
43'd 1962, Lafayette. Indiana
44* 1963. Charleston. South Carolina
45* 1964, Kalamazoo. Michigan
46* 1965, Sylvan Lake, South Dakota
47* 1966. University Park. Pennsylvania
48lh
1967. Crawford Notch. New Hampshire
49lh
1968. Carhondale. Illinois
5Q,h
1969. Williamsburg. Virginia
51"
1970. Fort Collins. Colorado
52nd
1971, Dauphin Island. Alabama
53rd
1972. Cape May. New Jersey
54,h
1973. Chapel Hill. North Carolina
55'h
1974. Cheboygan. Michigan
56"’
1975. Bozeman. Montana
57’"
1976. Ithaca. New York
58,h
1977. Mississippi State. Mississippi
59,h
1978. Jackson's Mill- West Virginia
60"'
1979. Omaha, Nebraska
61"
1980, Corpus Christi. Texas
62nd
1981. Saekvillc. New Brunswick
63rd
1982. Blacksburg, Virginia
64"'
1983. Green Bay. Wisconsin
65"’
1984. Wilmington. North Carolina
66"’
1985. Boulder. Colorado
67"’
1986. Gatlinburg. Tennessee
68"'
1987. Utica. New York
69'"
1988. Rosemont. Pennsylvania
70"'
1989. Notre Dame. Indiana
71*'
1990, Norton. Massachusetts
72nd
1991. Norman, Oklahoma
73rd
1992. Kissimmee. Florida
74'"
1993, Guelph. Ontario
75"'
1994. Missoula. Montana
76"'
1995. Williamsburg. Virginia
IT"
1 996. Cape May. New Jersey
78'"
1997. Manhattan, Kansas
79"'
1998. Si. Louis, Missouri
80'"
1999, Walerville. Maine
81"
2001). Galveston. Texas
82"d
2001. Fayetteville. Arkansas
83,d
2002. Fort Myers. Florida
84'"
2003. Delaware, Ohio
85'"
2004. Ithaca, New York
86‘"
2005. Beltsvillc, Maryland
87'"
2006, Veracruz. Mexico
88'"
2007, Wakefield. Massachusetts
89'"
2008, Mobile. Alabama
90’"
2009. Pittsburgh. Pennsylvania
91"
2010. Geneva. New York
92 nd
2011. Kearney. Nebraska
93rd
2012. Vancouver. British Columbia
“ Based on Jackson (Wilson Bulletin UK): 640: 1988) but corrected for 1974-1988 and updated for 1989-2012.
649
THE WILSON JOURNAL OF ORNITHOLOGY
Editor
CLAIT E. BRAUN
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Penn State Erie
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MEMBERSHIP INQUIRIES
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THE JOSSELYN VAN TYNE MEMORIAL LIBRARY
The Josselyn Van Tyne Memorial Library of the Wilson Ornithological Society, housed in the University of
Michigan Museum of Zoology, was established in concurrence with the University of Michigan in 1930. Until
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from members and friends of the Society. Two members have generously established a fund for the purchase
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Library currently receives over 200 periodicals as gifts and in exchange for The Wilson Journal of Ornithology. For
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be sent to the Treasurer.
This issue of The Wilson Journal of Ornithology was published on 4 September 2012.
Continued from outside back cover
547 Nesting biology of the Yellow-olive Flatbill (Tyrannidae, Elaninae) in Atlantic Forest fragments in
Brazil
Marina Anciaes, Thais Maya Aguilar, Lemuel Olivio I.eite, Renata Domelas Andrade, and
Miguel Angelo Marini
558 Species, functional groups, and habitat preferences of birds in five agroforestry classes in labasco,
Mexico
Hans van der Wal, Beatriz Pena-Alvarez, Stefan L Arriaga- Weiss, and Salvador Hernandez- Daumds
572 The composition of mixed-species bird Hocks in Alto Quindfo, Colombia
Enrique Arhelaez-Cortes and Oscar H. Marin-Gomez
581 Biology of invasive Monk Parakeets in south Florida
Michael L. Avery, Eric A. Tillman, Kandy L Keacher, John E. Arnett, and Kelli J. Lundy
589 Variation in the diet of Western Barn Owls ( Tyto alba) along an urban-rural gradient
Pablo Teta, Carina Hercolini, and Gerardo Cueto
Short Communications
597 Incidence of wing deformities (Angel Wing’) among Masked Boobies at Clipperton Island: life
history consequences and insight into etiology
Robert L. Pitman, Lisa T. Baltance, and Charles A. Bost
603 Fledgling Peruvian Pelicans {Pelecanus thagus) attack and consume younger unrelated conspecifics
Maximiliano Daigre, Paulina Arce, and Alejandro Simeone
608
611
614
620
Malicious motherhood: instance of infanticide by a female Barn Swallow
Joanna K. Hubbard and Audrey /.. Tobin
Intraspecific brood parasitism of the Pale-breasted Thrush ( Tardus leucomclas)
Paulo V. Davarifo, Livia M. S. Souza, Leonardo S. de Oliveira, and Mercival R. Francisco
Estimation of female home-range size during the nestling period of Dark-eyed Juncos
Dustin G. Reichard and Ellen D. Ketterson
Movement and cover-type selection by fledgling Ovenbitds (Seiurus aurocafilla) after independence
from adult care
Henry M. Streby and David E. Andersen
626 Asymmetries in mobbing behavior among nuclear fiockmates
Jason R. Courier and Gary Ritchison
630 Eastern Screech-Owl responses to suburban sprawl, warmer climate, and additional avian food in
central texas
Frederick R. Gehlbach
633 Diurnal activity of the Austral Pygmy Owl ( Glaucidium nana) in southern Ch.le
Heraldo V. Norambuena and Andres Munoz-Pedreros
636
640
Raptor migration at Concepcidn, Bolivia
Matias A. Juhant
Simultaneous multiple nests of Calliope Hummingbird and Rufous Hummingbird
Ned Batchelder, Gigi Batchelder, Dale A. Livezey, and Jeffrey S. Mark >
643 Editorial News
644 Ornithological Literature
Margaret A. Voss, Book Review Editor
649 Annual Meetings of The Wilson Ornithological Society
The Wilson Journal of Ornithology
(formerly The Wilson Bulletin)
Volume 124, Number 3 CONTEN TS September 20 1 2
Major Articles
429 Gaudy juvenile plumages of Cinereous Mourner (Lmiocera hypopyrra) and Brazilian I .miisonu
(/ Mniisoma elegans)
Fernando Mendonfd d' Fiona, Guy M. Kirwan, and Dante Huzzetti
436 Temporal and spatial patterns in abundance of the Wedge-billed Woodcreepcr ( Cdyphorynchus spirurus)
in lowland Ecuador
John G. Make and Bette A. Loiselle
446 Repertoire site and syllable sharing in the song of the Clay-colored Thrush ( Turdus grayi)
l.uh F. Vargas -Castro, Natalie V. Sdnchez, and Gilbert Barrantes
454 Silvcreyc* {Zoiterops lateralis) song differentiation in an island-mainland comparison: analyses of a
complex cultural trait
Myron C. Baker
I
467 Age-dependent orientation to magnetically simulated geographic displacements in migratory Australian
Silvcrcycs ( Zoiterops I. laterals)
Mark F.. I )eutu blander, John B Phillips, and Ursula Munro
478 Restoration of movement patterns of the Hawaiian Goose
Steven C. Hess, Christina R. Leopold, Kathleen Misajon, Darcy Hu, and John J. Jeffrey
487 Ecology and habitat selection of the Magellanic Plover (Pluvianellus socialis): a little-known Patagonian
shorehird
Carmen Fishman and Frica Not
49 Behavioral activities of male Cerulean Warblers in relation to habitat characteristics
Petra BohaU Wood and Kelly A. Perkins
506 Microhabitat nest cover effect on nest survival of the Red-crested (Cardinal
Luciano N. Segura. Diego A. Masson, and Mariela G. Gantchoff
513 Nest-site characteristics affect probability of nest predation of Bull-headed Shrikes
Sachiko Fndo
9
518 Capsaicin as a deterrent against introduced mammalian nest predators
Shane M. Baylts, Phillip Cassey and Mark F. Flauber
525 Historical and current status of laughing Gulls breeding in New York State
Brian F Washburn, Martin S. Lowney, and Allen L Gasser
531 Breeding biology of the Southern House Wren on Chile* Island, southern Chile
Silvma Ippi. Rodrigo A. I ’dsejuez, Juan Moreno, Santiago Merino, and Camila P. Villavicencio
538 Breeding biology of the Red-bellied Crackle ( Hypopyrrhus pyrohypogaster)-. a cooperative breeder of the
Colombian Andes
David Ocampo. M. Camila Fstrada-F. Jenny M. Munoz, Laura V. Londoho. Santiago David,
(novanny Valencia. Paula A. Morales, Jaime A. Garizdbal, and Andr/s M. Cuervo
Continued on made back
s ^ Wilson Journal
v.124 ^ _ _ f f
of Ornithology
Volume 124y Number 4y December 2012
Ewell Sale Stewart Ubraay
DEC Z 7 2012
Academy of Natural Science®
of Philadelphia
Published by the
Wilson Ornithological Society
M2l
tyu
til
v.l^t
THE WILSON ORNITHOLOGICAL SOCIETY
FOUNDED 3 DECEMBER 1888
Named after ALEXANDER WILSON, the first American ornithologist.
President — Robert C. Beason, P O. Box 737, Sandusky, OH 44871, USA; e-mail: Robert. C.Beason@
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First Vice-President — Robert L. Curry, Department of Biology, Villanova University, 800 Lancaster
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© This paper meets the requirements of ANSI/NISO Z39.48- 1 992 (Permanence of Paper).
preserved specimen. Top ad^Tm^le ( MCZ ^0995 (£irid°ps a™a) based on the three 1
subadult male (AMNH 459008). Bottom row: adult female (aSh^P^ byTuli^RH,
Of Wm
LIBRARY
philadelp^
Wilson Journal
of Ornithology
Published by the Wilson Ornithological Society
VOL. 124, NO. 4
December 2012
PAGES 651-878
The Wilson Journal of Ornithology 1 24(4):65 1 -674, 2012
HISTORY, STRUCTURE, EVOLUTION, BEHAVIOR. DISTRIBUTION,
AND ECOLOGY OF THE EXTINCT HAWAIIAN GENUS CIRIDOPS
(FRINGILLIDAE, CARDUELINI, DREPANIDINI)
STORRS L. OLSON1
ABSTRACT. — The extinct drepunidine genus Ciridops is known from five historically taken specimens of Ciridops
anna from the island of Hawaii, the last in 1892, and from fossil populations on Molokai, Oahu, and Kauai. The origins of
the historical specimens and the taxonomic history of the genus are reviewed. The plumages of C. anna are interpreted as
highly sexually dimorphic (red males vs. greenish females); the juvenile plumage of males included brownish feathers that
appear to have been retained and mixed with the incoming definitive plumage. The thigh musculature and pelvic and
hindlimb osteology show that the strong legs and feet of Ciridops were probably used to move plant debris in search of
insects. The closest living analog may be the Yellowltead ( Molioua uchrocephalu) of New Zealand. Analysis of stomach
contents of the single fluid-preserved specimen of C. anna disclosed remains of insects that are widely distributed in
Hawaiian forest ecosystems. The traditionally claimed association of Ciridops anna with palms of the genus Pritchurdia
suggests that Ciridops may have fed ill the accumulated debris in the axils of palm leaves. Hie patchy distribution of fossils
ot ( iridops may result Iroin the birds being associated with nearly pure stands of Pritrhnrclki that were in turn patchily
distributed. Vulnerability of Pritchurdia to introduced seed predators, including rats and humans, and to destruction of
lowland habitats by cutting and burning, may have caused the prehistoric extinction of Ciridops on all islands except
Hawaii. Received 2 March 2012. Accepted 25 May 2012.
Among the most beautiful (Frontispiece, Fig. I )
and enigmatic of the exuberant adaptive radiation
of Hawaiian cardueltne finches of the tribe
Drepanidini, is the extinct Ula-ai-hawane (Ciri¬
dops anna). This is among the rarest of birds,
being known historically only from live study
skins and remnants of a single skinned body
preserved in alcohol. Although Ciridops was
known historically only from the island of Hawaii,
fossils show that it also occurred at least on
Molokai. Oahu, and Kauai. Many new insights
' Department of Vertebrate Zoology, National Museum of
Natural History, Smithsonian Institution, P. O. Box 37012.
Washington, D.C. 20013, USA; e-mail: olsons@si.edu
into the structure and probable habits of the
species of Ciridops have been gained through
study of the fossil material and from new
dissections of the one fluid specimen. Additional
new information on the history and habits of C.
anna comes from archival sources. This paper
presents the new data and attempts to gather all
previous knowledge regarding the genus Ciridops.
reserving species-level revision of the fossil
material for future studies.
HISTORY AND DISPOSITION OF HISTORIC
SPECIMENS OF CIRIDOPS ANNA
The first published indication of the existence
ol the bird that became Ciridops anna was in a
651
652
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124. No. 4. December 2012
I^I?9 inwhichT"6 \CTIOP! T"al LC" C°,Umn: 'a,eral- ventraK
column (top 2 figures) lateral and ventn ,i. 1. f , , lhe rcds have faded ,n alcohol to an orangish hue. F
bottom figure: liwi (Ves.iaria cocci,, ea) (BMNH95 7^72) Zd °' ““ (BPBM l9)' Rl-ht coh
Note the light colored patch in the inner i '• U dorSal v,ew IO contrasl wir>g pattern with Ciridops a
Paintings by Julian P. Hume ^condartes „ on the outer webs in Ciridops and on the inner webs in Vesti,
Olson • THE EXTINCT HAWAIIAN GENUS CIRIDOPS
653
two-page catalog drawn up by Sanford Ballard
Dole, a Honolulu lawyer and amateur ornitholo¬
gist, later to become the first territorial governor
of Hawaii and then a Federal judge (Damon 1957,
Allen 1988). This list (Dole 1876) was drawn up
to accompany a collection of mounted birds
that formed part of a display of Hawaiiana for
the centennial exhibition in Philadelphia in 1876,
the birds having been collected and mounted by
James Dawkins Mills, an ardent amateur naturalist
and taxidermist who resided in Hilo, Hawaii, from
1851 until his death in 1887. He and his bird-
catcher Hawelu are believed to have collected
mainly in the Olaa area of Puna on the island of
Hawaii (Olson 1999b) with his greatest activity
probably having been around 1 859- 1 860 ( Manning
1978, 1979, 1981). Under the family Fringillidae,
in which was also included the drepanidine
Psittirostra psittacea, Dole (1876; 2) wrote the
following:
“Ulaaihawane. Not previously described. 5 'A
in.[ches] long. Bill short, straight. Toes 3 front,
1 back. Wing coverts and breast red: throat,
primaries and tail, black; secondaries white; head
grey; merging into white on the upper part of the
neck, and grey again on the back. Habitat Hawaii.
Probably belongs to the genus Fringilla."
It is uncertain which of Mills’ specimens were
actually on exhibit in Philadelphia; some in
Dole’s catalog were possibly omitted, whereas
others that were not listed may have been included
(Manning 1978, 1979). After the birds from the
Philadelphia exhibition were returned to Mills, the
naming of the new 'FringiHa* fell to Dole (1878:
49-50). who called it FrinpiUa anna, the account
being otherwise a verbatim repetition from the
1876 list, to which was added: “This is a bird of
remarkable beauty, its peculiar combination of
colors producing a most harmonious and elegant
effect." The type locality ’Hawaii’ refers to the
island of Hawaii rather than to the archipelago.
Nowhere in Dole's (1878) list of Hawaiian
birds does he mention the number of specimens
examined for the species listed.
Mills retained his collection probably up until
his death in 1887. after which portions were sold
at auction (Manning 1978), although the bulk of
it was later acquired by Charles Reed Bishop at
some time between 1884 and 1888, after which it
became the nucleus of the bird collections of
the Bishop Museum (Manning 1978). The first
indication that there were at least two specimens
of Ciridops in the Mills collection was supplied
by Wilson, who stated that “1 procured a
specimen from Hon. C. R. Bishop, which had
been obtained by the late Mr, Mills of Hilo. Mr.
Bishop has a very much finer example remaining,
with more grey about the head and neck taken by
the same gentleman.... The present specimen [is]
now in the collection of the Hon Walter Roths¬
child" (Wilson and Evans 1893: 23).
Bishop’s ‘much liner specimen’ is the one now
in the Bishop Museum (BPBM 19). The second
one Wilson obtained from Bishop in 1888. along
with several other rare birds obtained by Mills
(Manning 1978), in exchange for species Wilson
had collected that Bishop did not possess.
Wilson's specimen of Ciridops eventually passed
to Rothschild (Rothschild 1900:183), doubtless
through purchase, as Wilson sold a number of his
specimens to other museums, such as the
Rijksmuseum in Leiden (Olson and James 1986)
and museums in Paris and Liverpool (Olson
1999a). That specimen of Ciridops ultimately
went to the American Museum of Natural History
(AMNH 459008) in New York when Rothschild’s
bird collection w'as sold in 1931 (Murphy 1932). It
is not in definitive plumage, the secondaries being
brown rather than white and part of the belly dark
brown rather than red. It has been regarded as a
syntype or cotype of the species by numerous
authors (e.g., Hcnshaw 1902, Munro 1944,
Amadon 1950. Banko 1979), but it does not agree
with Dole’s (1878) original description and has no
status as a type. The Bishop Museum specimen is
thus the holotype (Olson 1994), as also stated by
Rothschild (1907a: 41).
Two additional specimens, one in the definitive
red plumage (MCZ 10995) and the other in a
distinctive greenish plumage (MCZ 10987 ex¬
changed to New York where it is now AMNH
230275), appeared rather mysteriously with a few
other Hawaiian birds among the old collections of
the Museum of Comparative Zoology at Harvard
(Bangs 1910). 1 proposed that this small collection
had its origin in the expedition of William T.
Brigham and Horace Mann Jr. to the Hawaiian
Islands in 1864—1865 (Olson 1992). I also built an
entirely circumstantial case for the specimens'
possibly having been taken on Molokai, owing to
some comments inserted by Brigham into Dole’s
(1869) first list of Hawaiian birds. I no longer
consider this to be a plausible geographical origin.
Newly examined correspondence in the Smithsonian
Institution Archives (RU 182. volume 1 86, page 355,
654
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 4. December 2012
box 40, folder 16) reveals that Brigham “tried hard
to purchase those birds (Mills’ collection] eleven
years ago |1865] when 1 saw them in Mr. Mills’
collection in Hilo, Hawaii, but his price was beyond
my means." ive existing spec¬
imens of Ciridops anna are all in remarkably good
condition with plumage that shows little or no
signs ot wear, although what this may mean in
terms ot timing of molt cycle is uncertain because,
except for the last specimen obtained by Palmer it
is not known at what time of year any of them
were collected. None of them shows any evidence
of shot damage and it is likely that all may have
been trapped alive by birdcatchers using tradi¬
tional means such as birdlime, snares, and other
means (Emerson 1894). The one obtained for
Pa mer and preserved in spirits must have been
kdled soon after capture Tor the stomach contents
to have remained undigested and in good
condition. The label indicates it was ‘shot by a
native and Munro (1892) reports that the natives
shot it while feeding” but I have not noticed any
shot damage in either the skin or the remaining
body in fluid.
SYSTEMATIC HISTORY
Dole (1878) reflected the opinion, long voiced
subsequently, that the bill of the Ula-ai-hawane
was finch-like by placing it in the genus Fringilla.
probably intending that usage in a more or less
Lijinaean sense rather than suggesting any close
relationship with the few species now restricted to
the genus Fringilla. Subsequent to Dole's (1878.)
description, which was reprinted by Sclater ( 1 880),
there was no further mention of the species, apart
from a query in a footnote by Sharpe (1888), who
wondered what Fringilla anna might be. Newton
( 1 892:469) placed it in the new genus Ciridops and
considered that “it probably belongs to the fauna
which I have above called "Columbian’ (for want
of a better name): but I cannot suppose it to have
been so early a settler as the Drepanididae, since it
has changed so little.” In this he may have meant
that it had changed so little from other finch-like
Hawaiian passerines, which at that time were not
recognized as being part of the drepanidine
radiation. In the final arrangement of pages of
Wilson and Evans (1890-1899), Ciridops was
placed at the beginning of the drepanidines.
followed by the species of the red-and-black group.
Gadow ( 1899: 243) considered there was nothing
to be gained by excluding Ciridops from the
Drepanididae, citing hearsay reports of its frayed or
tubular tongue. That information came from the
specimen received in spirits by Rothschild (1900:
181) who remarked that the “tongue seems to
piove that this genus belongs to the Drepanidae and
not to the Fringillidae, the only two families which
would have any chance of claiming it.” Perkins
< 1901, 1903) was the First to advocate that all the
Hawaiian birds then included in the Drepanididae.
plus the finch-billed species previously considered
fringilline, constituted a monophyletic radiation
regardless of the family in which they were placed.
Perkins divided the expanded Drepanididae into
two "divisions’ and included Ciridops in his
Division I (the "red and black' group later often
called a subfamily Drepanidinae). Its position he
regarded as “quite certain” (Perkins 1901: 585),
specifically mentioning similarities shared between
Ciridops and Vestiaria (scarlet plumage, black
wings and tail, while in wings) and also Palme ria
(black.sh-gray | lanceolate] throat feathers). Bryan
( 1 901 ) placed Ciridops in the Drepanididae at the
end ol the red group after Himatione and preceding
Olson • THE EXTINCT HAWAIIAN GENUS CIRIDOPS
655
Chlorodrepanis. Henshaw (1902: 57) placed this
"finch-like bird" at the end of the red-and-black
species. Amadou (1950: 174) considered the bill ol
Ciridops to be “finch-like” but that it was
otherwise “nearest Palme ria but without a crest
and with lanceolate feathers on the crown throat,
and cheeks only." Amadou (1950: 231) believed
the drepanidines had evolved from nectar-feeding
coeribid-like birds and. that within the red-and-
black group. Ciridops. with its supposedly "most
tanager-like" bill, was considered to be the most
derived member. Bock (1970. 1979) and Richards
and Bock ( 1973) acknowledged the drepanidines to
have been derived from the Carduelinae. and
considered Ciridops to be basal to the entire
radiation, having given rise both to the ‘red and
black' group and to Loxops and the remainder of
the radiation, including all the laxa that are much
more linch-like than Ciridops. Bock <1979: 65)
later placed Ciridops at the base of the red-and-
black group “which may be representative of the
founding stock of the Hawaiian honeycreepcrs.”
Raikow (1977: 115) argued that Ciridops must
have branched off among the slender-billed non¬
finch-like forms in the drepanidine radiation but
that the “finch-like or tanager-like bill.,, is
difficult to explain in conjunction with the fully
tubular tongue, especially since little is known ol'
its feeding habits" so that “perhaps the hill
shape... is only secondarily finch-like." The bill
shape of the then newly discovered Poo-uli
{MeUnnprosops phaeosomu) was considered to be
“closest to that of the extinct 'ula-'ai-hawane
( Ciridops anna)" (Casey and Jacobi 1974: 220).
An osteological analysis consistently grouped
Ciridops with ihe red-and-black elude ( Drepanis .
Vestiaria. Himatione, and Palme ria). usually in a
basal position but in a strict consensus tree in the
most derived position (James 2004). There arc no
reliable generic-level characters to separate the
highly curved-billed genera Drepanis and Vestiaria
(Pratt 1979a. 2005), and only size and plumage
characters appear to separate Palme ria from
Himatione. The argument for merging all four of
these genera in Drepanis (Fleischer in Pratt 2005:
77) has received strong recent support from
discovery of a natural hybrid between Vestiaria
coccinea and Himatione san guinea (Knowlton
et al. in press). Drepanis sensu Into and Ciridops
would thus represent a simple dichotomy so that
which one would be ’basal' becomes moot. The
hindlimb morphology of Ciridops is certainly
derived relative to that of Drepanis (s.l.) and if its
short bill evolved from a longer-billed ancestor,
then Ciridops would certainly appear to be the
more specialized genus compared with Drepanis.
Genus Ciridops Newton 1 892: 469.
Type Species. — Fringilla anna Dole ( 1 878), by
monotypy; gender, common, probably intended as
feminine by analogy with Loxops, although all
genera ending in -ops are now to be treated as
masculine by decree of International Commission
on Zoological Nomenclature (Pratt 1979b).
Authorship of Ihe Generic Name. — Newton
(1892: 469) introduced a note of ambiguity
concerning the authorship of Ciridops : "... there
is one very puzzling species, of which only a few
specimens seem to have been preserved, that needs
particular attention. This was described by Judge
Dole under the name of * Fringilla anna: but. of
course, is no true Fringilla. Mr. Wilson brought
home but a single specimen.... and. I believe will
establish for it a new genus. Ciridops." Despite
this, the name was clearly established at that
moment by Newton, who. I believe (Olson 2003),
was also the chief author of most of what was
written in Wilson and Evans (1890-1899), where
Ihe reference was died (1893: 23) as '"Ciridops
- , Wilson', Nature, xlv. page 469 (17 Mar
1892)". Rothschild (1900, 1907b), W. A. Bryan
(1901 ), Perkins ( 1903), and E. H. Bryan (1958), for
example, attributed the genus to Wilson, but
Richmond (1902: 673 ) more precisely lists the
author as “‘Wilson’ Newton." Later authors (e.g.,
Bryan and Greenway 1944. Amadou 1950, Green¬
way 1968, AOU 1998) correctly give sole author¬
ship of the generic name Ciridops to Newton.
Etymology.*- Pratt (2005: 273) evidently did
not consult the original description of the genus
and appears to have contrived an etymology,
stating that Ciridops is "most often translated as
‘shining face',” or that “the name probably was
intended to mean ‘looking like Scylla’s ciris’."
Ciridops had not previously, to my knowledge,
been translated as ’shining face* except by Pratt
(2002a), the Greek word for ‘shining’ being
lampros. Newton (1892: 469), however, explicitly
declared that Ciridops was “so named because its
bright coloration recalls the well-known Emberiza
ciris ol Linnaeus, the Painted Bunting of authors,
or ‘Nonpareil' of bird dealers."
Included Species. — Ciridops anna. Ciridops
tenax James and Olson 1991. Ciridops sp. (Oahu)
James and Olson 1991.
656
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124, No. 4. December 2012
Ciridops anna (Dole 1878)
Synonymy. — Ulaaihawane Dole 1876: 2; Frin-
gil/a anna Dole 1878: 49 [type-locality, Hawaii];
‘ Fringilla ’ anna.— Newton 1 892:468*; Ciridops
[anna], — Newton 1892:469; Ciridops anna.— Wilson
and Evans 1893:23. and all subsequent authors:
Ciridops anna. — Rothschild 1907a: 215 (lapsus)
Holotype. — BPBM 19, in (he presumed definitive
adult male plumage. AMNH 459008. in presumed
subadult male plumage, is not a syntype or cotype.
Etymology.— The specific name anna has been
widely and understandably assumed (Amadon
1944; Jobling 1991; Mearas and Meams 1992;
Pratt 2002a, 2005) to have been a tribute to Anna
Prentice Cate (b. 16 Jul 1842. Castine, Maine: d.
29 Aug 1918, Honolulu), who married Sanford
Ballard Dole on 19 May 1873, although Dole did
not publish any explanation for the name. Thus,
there remains a distinct possibility that anna could
have been meant to honor Dole’s cousin Anna
Ward. Dole traveled from New England to
California in 1868 with Anna and her daughter
May belle with both of whom he continued to
maintain close ties (Allen 1988). Dole named
Fringilla anna at a time when his wife was in
New England, their relations were strained, and
Dole was in the process of a Hawaiian 7 icmai'
adoption of 14 year-old Elizabeth Napoleon, an
arrangement that was not entirely satisfactory to
either Elizabeth or Mrs. Dole (Allen 1988). When
Elizabeth later married Eben Low, she named her
first daughter Annabelle Dole Low, supposedly to
commemorate Anna Dole and Maybelle Ward,
but there was ambiguity as to whether the
eponymous Anna was Mrs. Dole or Maybelle’s
mother (Allen 1988: 168-171). Dole may delib¬
erately have intended that the Anna of Fringilla
anna c ould not be pinned down with certainty
which is how it stands.
Vernacular Names.- On the island of Hawaii in
he 9th century, Ciridops anna was evidently
widely and consistently known as ‘Ulaaihawane’
or Ula-ai-hawane, with various usages of glottal
stops and macrons but correctly written in
Hawaiian as ‘ ula-ai-hawane . This was first made
known by D°le 0876. 1878), who doubtless
received his information from James Mills
Manning 1978), who in turn would have been
98lTw .y ?rdCa,Cher Mavvelu (Manning
1981). Wilson, who also interviewed Hawelu
reported that “I used to hear repeatedly of the
Ulaaihawane, by which name it is well known to
the natives, who told me that it feeds on the fruit
of the Hawane palm, whence its name — Ula (red),
ai (to cat), Hawane (the Hawane palm)” (Wilson
and Evans 1893: 23). The Hawaiian name loulu is
customarily used for the palm itself (Pritchardia
spp.). but. counter to the impression conveyed by
Pratt (2005), hawane may be used for the tree
also, as well as its more usual application to the
fruit ('nuts’) alone (Pukui and Elbert 1986).
Earlier ornithological writers usually used the
term hawane palm. Ihc preceding information
probably originated mostly in the Olaa District
between Hilo and the volcano of Kilauea. The
name Ula-ai-hawane was also used, or at least
understood, in the Kohala District in the north-
w'cstern pail of the island, where Hawaiians
collecting for Palmer obtained the last specimen,
as is evident from the diaries of both Munro (1892)
and Palmer (Rothschild 1893). There does not
appear to be any justification for Palmer’s emen¬
dation of the name to ‘Ulaaiwhane’ (Rothschild
1900: 184). Other apparent lapses are ‘Waaiha-
wane’ = (Bryan and Greenway 1944: 133), ‘ual-
ai-hawane* (Carlquist 1965:85), "Uha'aihawane-
(Banko 1987: title page), and ‘ulalhawane’ (Allen
1988: 59). Henshaw (1902: 58) called it the
“hawane finch.” Mathews (1930: 808) invented
many English names for birds out of flights of fancy
anil called Ciridops anna “White-naped Mano.”
w hich was a lapsus for ‘niamo.’ a name that he also
applied to Palmeria dolei (“Crowned Mamo”),
although no Hawaiian had ever referred to
either species as a ‘mamo.’ German vernaculars
include “Hawaii Fink” (Duncker 1953: 240)
and the ludicrous “Annakleidervogel” of Luther
( 1972: 1 79), Kleidervogel being German for drepa-
nidine birds from the use of their feathers by
Hawaiians in making garments ( Kleider ). so that
Luther s name might also be taken to mean ‘the bird
ol Anna’s clothing.’ Pratt’s (2005: 273. 275) “red
palmcreeper” for C. anna and “Kauai Palmeree-
per” for C. tenax are bookish inventions perhaps
reflecting a preference for continuing to call the
Drepanidini ‘honeycreepers’ rather than finches.
EXTERNAL MORPHOLOGY AND
PLUMAGES OF CIRIDOPS ANNA
External Morphology
Appearance and Proportions of Bill. Wings,
and Feet.- No aspect of the external morphology
is known for any of the fossil populations of
Cmdops and that of C. anna may be taken as
Olson • THE EXTINCT HAWAIIAN GENUS CIRIDOPS
657
TABLE 1 . External measurements (mm) of skin specimens of Ciridops anna. Oilmen length is from base of feathers to
tip. Width of culmen and depth of bill taken at level of anterior margin of nostril.
Museum number am! presumed sen and age
Wing chord
Tail length
Tarsus length
Culmen length
Culmen width
Bill depth
BPBM 19. adult male (holotype;
Wetmore’s measurements in
parentheses)
81.5 (83.0)
48.8 (49.0)
19.7 (21.0)
11.8 (11.0)
4.4
5.6
MCZ 10995, adull male
80.4
46.2
21.2
10.6
AMNH 459008. suhadull male
74.8
43.3
19.7
1 1.4
4.1
5.2
BMNH 1939.12.9.58. subadult male
77.1
42.7
22.3
9.9
3.5
4.6
AMNH 230275 (formerly MCZ
10987). adult female
72.0
45.4
20.9
9.3
3.9
4.4
representative for the genus. The most detailed
description available is from notes by Alexander
Wetmore when he visited the Bishop Museum
as part of the Tanager Expedition (Olson 1996).
His description was based on the holotype (BPBM
19) and is far more detailed and accurate than
Rothschild's (1900: 181), which was presumably
based on one or both of the specimens then in
his collection (AMNH 459008; BMNH 1939.
12.9.58):
Wing 83.0 [mm], tail 49.0, culmen from base
11.0, tarsus 21.0. Nostril set in a slight
depression only parlly concealed by frontal
plumes. Culmen slightly curved downward,
sides of bill nearly straight in outline: gently
rounded. Outline of maxillary tomium faintly
concave, slightly sinuate. Tip of maxilla acute
on sides, slightly broadened when viewed from
above. Lower mandible with sides rounded.
Line of gonys straight. Mandibular rami slightly
less that half | the length of the | gonys. Feathers
of forehead short and plushlike. Small rictal
bristles present. Wing formula 7, 8, 6. 5. 9. 4. 3,
2. 1. | Primaries! 6, 7. 8 nearly equal, 9 only
slightly shorter than 5. Wing tip about 20.0 mm.
Tenth primary on upper side of wing 8.0 mm
long. Tarsus scutellate. Basal joint of 4th toe
wholly adherent to middle toe. Basal joint of
2nd toe adherent to middle toe for slightly more
than one third length. Second toe with claw
reaching beyond base of claw on middle toe.
Fourth toe with claw reaching to base of claw on
middle toe. Hind toe and claw strong equal to or
slightly more than middle toe without claw. Tail
very slightly notched, rectrices 1 2. Feathers of
throat and ear coverts lanceolate with long
slender lips. (A. Wetmore Held notes. 31 Mar
1923. Division of Birds archives, Smithsonian
Institution).
Skin Measurements (Table 1 ). — Additional
measurements of the bill of Ciridops anna
(MCZ 10995) taken prior to the removal of the
skull from the skin (Olson et al. 1987) include:
culmen length from anterior rim of nostril,
7.9 mm; length of rostrum along tomium,
1 1.7 mm; mandibular symphysis length, 7.4 mm;
basal mandible width. 4.5 mm; basal rostrum
width. 6.1 mm. Middle toe with claw 0.76 inches
(19 mm), hind toe with claw 0.64 inches (16 mm)
(Rothschild 1900: 183, AMNH 459008).
Soft Part Colors. — Wilson reported the color of
the irides to be ‘"dark hazel” (Wilson and Evans
1893; 24), but that was either a guess used to
instruct his artist or a surmise based on the fact
that most drepanidines have brown eyes. He also
reported "bill and feet pinkish brown” presum¬
ably based on dried skins. Pratt (2002a: 9) gives
the bill and leg color as “brown.”
Plumages
Presumed Adult Male Plumage.— BPBM 19
and MCZ 10995 (Frontispiece, Fig. I). J. P.
Hume, H. D. Pratt (in litt. 20 Jan 2012), and I
consider these two specimens lo be identical in
plumage and Pratt's illustrations (Raikow 1977;
Pratt et al. 1987; Scott et al. 1988: Prall 2002a. b;
Pratt 2005, 2010) may be considered idealizations
of both (H. D. Pratt, pers. comm.). Illustrations in
Carlquist (1965) and Berger (1972, 1981 ) may
be based on BPBM 19 but are poor at best.
Underparts: throat and breast, extending onto
upper belly, black, grading to brownish on the
Hanks; the rest of the belly is scarlet, there is a
light patch at the anterior of the vent region that
has been described as tawny but in MCZ 10995 is
lemon yellow, the rest of the vent and undertail
coverts are rich brown. Upperparts: the lores,
torecrown, posterior portion of the mantle, wings
658
THE WILSON JOURNAL OF ORNITHOLOGY • VoL 124, No. 4. December 2012
(except innermost secondaries), and tail black:
feathers of the throat, forehead, and auriculars
stiffened and pale grayish along the shafts; the
occiput and anterior part of mantle are silvery
gray shading into gray-brown posteriorly; the
outer webs of the innermost secondaries are while,
narrowly fringed with scarlet. The white patch in
the wing is similar to but evidently not homolo¬
gous with that of Iiwi ( Vestiaria coccinea), in
which it is the inner webs that are white. The
scarlet portions ol the plumage are extremely
glossy, although less so in BPBM 19. which had
been on exhibit and exposed to light.
Presumed Subadult Male Plumage. — A M N H
459008 (Frontispiece). Original color illustrations
are in Wilson and Evans 1893 (copied by many
subsequent authors), Rothschild (1907a), and Pratt
(2002a, 2005). Described by Rothschild (1900:
183) as: “Lores and forehead velvety black, this
colour gradually shading into the ashy grey of the
crown, nape, and hind-neck, which colour again
shades oil into the dark sepia-brown colour of the
back. Rump and upper tail-coverts dark glossy
red. Tail-feathers uniform black. Primaries and
secondaries black, only the outer webs of the last
three secondaries earthy brownish buff (nearest to
Ridgway’s [ I886J ‘clay-colour’ on plate v. fig. 8);
scapulars and tips of some of the greater wing-
coverts of the same colour. Feathers on the sides
of the head and neck, chin, and throat black with
silvery-grey shaft-stripes. Breast down to the
middle of the uppermost part of the abdomen
black. Middle of abdomen, vent, and under tail
coverts tawny brown. Sides of abdomen largely
glossy red.” Pratt (2002a: 9) found that it “mostly
resembles the adult plumage except: black of
forehead and lores more extensive with black
breast band extending anteriorly through the
throat to include the chin; middle of back,
shoulder, flank, lower belly, crissum. outer webs
of temals, edges and broad tips of greater upper
secondary coverts tawny, remainder black.”
BMNH 1939.12.9.58 (Fig. l). Skinned from
alcohol and said by Rothschild (1900:183) to
agree with the preceding specimen “except that
the beautiful red has faded away in the spirits and
that apparently the head hits been darker.” It is
apparently this laded specimen that wa.s illustrated
by Ren Hathway to accompany the Foreword on
extinct birds by Fuller (2002: plate F20) This
(S19e037en Tm “ aS immature ^ Perkins
903) and Munro (1944). “The secondaries of
[this) specimen were almost certainly brown
(definitely not white), which was restricted to
the outer webs. There is a fine border of orange
(same colour as the other faded red colouration)
on the outer edge of the brown outer webs, which
may have also been more reddish in life.
Interestingly, the chestnut-brown on the belly is
clearly unaffected by alcohol” (J. Hume in litt. 1 1
Jan 2012). This specimen, despite fading, is
clearly in a plumage equivalent to that of the
preceding, the most obvious indication being the
brown coloration extending from the undertail
coverts up the midline of the belly to intersect the
black breast (this is scarlet in the adult), and the
brown portions of the inner secondaries (white in
the adult).
Presumed Adult Female Plumage.— AMNH
230275 (Frontispiece). Color illustrations; Pratt
et al. (1987), Pratt (2002a, 2005. 2010). This was
regarded as an adult female by Bangs (1910: 68-
69) who described it as: "Forehead clothed in
stiffened, pointed, semi-erect feathers as in the
adult male, lop ol head, nape and sides of head
cinnamon washed with dull olive-yellow on
forehead and with the lores and a narrow frontal
band more dusky: cheeks with paler shaft- stripes to
the leathers; lower back grayish cinnamon, grad¬
ually passing into the purer color of the head: rump
and upper tail coverts olive-yellow: tail dusky,
(ringed with olive-yellow; primaries blackish,
narrowly edged with dark olive-yellow; secondar¬
ies more broadly edged with the same, the
innermost nearly wholly dark olive-yellow; throat
dull cinnamon, the feathers w ith paler shaft stripes,
slightly washed with yellow-olive in lower middle:
chest and breast dingy-smoke-gray, somewhat
washed with olive, gradually passing into dark
olive-yellow on belly; under wing coverts, axillars.
under tail coverts and a small patch in lower middle
belly dilute rufous cinnamon. The general pattern
thus resembles that of the adult male, though the
colors themselves are very different.” The bill is
noticeably smaller and more gracile in this
specimen than in the subadult male AMNH
459008, which may be a sexual difference.
Discussion of Plumages of Ciridops anna
The specimen in greenish plumage is so different
Irom the other four known specimens that Bangs
.(l9,0) considered it to be the adult female; but,
because ,n the rest of the red-and-black drepani-
,!!!* th^ adult female is like the male, Amadon
(1750: 174) considered the green bird to be
immature and stated that the “remaining immature
Olson • THE EXTINCT HAWAIIAN GENUS CIRIDOPS
659
feathers” in “a specimen not quite adult” (AMNH
459008) "agree with the plumage” of ihe green
specimen, which is not irue. The most conspicuous
remaining feathers in the transitional specimen are
the brown inner secondaries and the brown midline
of the belly, of which there is no trace in the green
bird, whereas there is no trace of green, nor any
gray in the breast, in the supposedly molting bird.
Yet the green plumage continued to he regarded
as ‘immature' (Pratt el al. 1987) or ’juvenile' (Pratt
2002a. 2005). Pratt (2002a: 9) recognized “3
distinct plumages ... with one in transition." but in
the same paragraph he stated that the bird in red
plumage with brown inner secondaries * ‘cannot be
a transitional stage because it includes feathers not
present in either” of the other known plumages.
This was mooted by the discovery that at least parts
of the juvenile plumage of the Hawaii Mamo
(Drepanis paeifica) were of a decidedly brown
color, similar to that retained in the 'transitional'
plumage of Ciridops anna (Olson and Hume 2009).
The plumage of the exquisite greenish specimen,
which appears to be completely fresh and without
wear, shows no evidence of the fluffiness, pointed
rectrices. or other signs of a truly juvenile plumage
(Olson and Hume 2009). making acceptance of it
as being in the adult female plumage the only
reasonable conclusion — one that was then accepted
by Pratt (2010: 647, figure and legend).
The only possible indication we have of
breeding or molt cycles comes front the bird
taken 2 February in ‘transitional' plumage
(BMNH 1939.12.9.58). February is a time when
neither Apapane (Himatione sanguined) nor liwi
are undergoing any molt (Fancy and Ralph 1997.
1998). Thus, if Ciridops were on a similar cycle,
’transitional' male plumage with brown feathers
may not have been evanescent and possibly lasted
a full molt cycle so that ii may have taken 2 years
for males to attain the definitive plumage. This
gains support from half of known male specimens
being in non-definitive plumage. If Ciridops anna
were a highly territorial species, there would have
been a decided evolutionary advantage for fully
adult territorial males to be able to distinguish
females and non-territorial subadult males from
threatening conspeeific invaders.
INTERNAL MORPHOLOGY OF CIRIDOPS
Tongue Morphology
The tongue of Ciridops anna was first illus¬
trated by Rothschild (1900: plate 83. figs. 55,
55a — natural size and enlarged) who made no
further comment on it other than that it indicated
that Ciridops belonged with the “Drepanidae”
rather than the Fringillidae (Rothschild 1900:
181). Amadon (1950: 222) reproduced the en¬
larged view along with the tongues of other
drepanidines. Carlquisl (1965: 125) constructed a
’tongue phylogeny' by superimposing illustrations
from Amadon (1950) on Amadou’s tree of
drepanidine relationships, but many of the tongues
were redrawn in different views from the originals
and are probably in part fanciful. Bock (1972: 76)
illustrated the tongue in several views in great
detail and found the structure of the corneous
tongue in Ciridops to be similar to that in other
drepanidines with tubular tongues but that it
“differs from that of ‘coerebidsL . . in that no
eoerebid' possesses laciniae along the upturned
lateral edges of the corneous tongue.” The tongue
of Ciridops was fringed and tubular as typical of
the presumably nectarivorous tongues of its close
relatives but was shorter in accordance with the
short length of ihe bill.
Osteology of Ciridops anna
The skeletal morphology of Ciridops was
investigated using fossil material and also the
skull and mandible, humerus, tibiotarsus, and
tarso metatarsus removed (Olson et al. 1987) from
the remaining Harvard study skin of C. anna
(MCZ 10995), and the pelvis and femur from
BMNH 1939.12.9.58.
Cranial Osteology.— The skull and mandible of
Ciridops anna are decidedly not finchlike "but
are shortened versions of the thin weak structures
found in the nectarivorous genera Himatione,
Palme ria . Vestiariu , and Drepanis" (James and
Olson 1991: 73). Four characters were identified
that confirmed the placement of Ciridops with
that same ’red and black' group of drepanidines
(Division I of Perkins 1903), from which
Ciridops was distinguished "by its much shorter
bill, constricted dorsal nasal bar. upturned retro-
articular process of the mandible, deep mandib¬
ular ramus (middle part), and enlarged mandibular
foramen” (James and Olson 1991: 73).
The skull and mandible of Ciridops are
contrasted (Figs. 2, 3) with those of a typical
nectanvore. the Apapane, and the Poo-uli. which,
although not typical of the truly finch-like
drepanidines such as Telespiza, is a basal taxon
within the radiation (Lerner et al. 2011) and
660
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124. No. 4. December 2012
considerably more finch-like than Ciridops. The
bill of Ciridops is much weaker than in Melam-
prosops and. in many respects, is much more like
that of Himatione except that it is shortened. The
nostril is much larger with an ossified nasal
septum, and scarcely differs in size or structure
from that o f Himatione. whereas in Melamprosops
the nostril is smaller, rounder, and lacks a septum.
The dorsal nasal bar in Ciridops is even thinner
than in Himatione and quite unlike the much more
reinforced nasal bar ot Melamprosops. In dorsal
view, the mandible of Ciridops with its prominent
retroarticular processes, scarcely differs from that
of Himatione except in the shorter, wider
symphysis, contrasting with the much wider,
heavily reinforced and much more finch-like
structure in Melamprosops.
Postcranial Osteology.— No peculiarities were
noted in the humerus or other bones of the wing
and pectoral girdle of Ciridops. However, great
differences in the pelvis of Ciridops from that of
its near relatives (Fig. 4), reflect the much greater
development of the pelvic musculature described
heicin. The surface of the antitrochanter in
Ciridops is unusually large mainly due to greater
extension anteriorly. The pelvis of Ciridops is
decidedly broader and more robust with the
anterior iliac shield being much wider and more
rounded and the posterior portion of the ilium
shorter and much broader. The terminal process of
the ilium is short and triangular in Ciridops.
versus long and pointed in its closest relatives.
The great medial expansion of the anterior shields
cause the dorsal iliac crests almost to meet at the
midline, concealing most of the anterior portion of
the synsacrum. whereas in more typical drepani-
dmes the dorsal crests are fairly widely separated
with deep V-shaped grooves between them to
accommodate the posterior termini of the dorsal
vertebral musculature. The wider posterior sur-
aces of the ilia in Ciridops reduce the si/e of the
visible posterior portion of the synsacrum. which
appears recessed and has much larger interverte-
bral foramina. The great differences in the pelvis
of Ciridops reflect just part of the complex of
changes involved in the evolution of the hindlimh
for the active moving of objects with the foot
Fossils of exceptionally stout passerine femora
Le,re m°?xrZ,hng Whcn first encountered on
Kaua. and Molokai, being quite unlike the femur
IT”8 n HTVaiian passerinc fcnown at the
time (F,g. 5A, Dj. A supposition that these might
belong to species of Ciridops was eventually
confirmed by comparison with the femur of C.
anna that was revealed after dissection of the
fluid-preserved trunk specimen. It also became
apparent that equally stout fossil tibiotarsi and
tursometatarsi (Fig. 5B. C) were also referable to
Ciridops (Olson ct al. 1987: James and Olson
1991: fig. 35). The hindlimb elements of C. term
ol Kauai are somewhat less specialized than in
other taxa of the genus (James and Olson 1991).
The robust tarsometatarsus reflects the larger fool
observed by many authors from examination of
the skin specimens. Similarly robust hindlimb
elements occur in the unrelated species that
appear to be possible functional analogs of
Ciridops.
Myology of Ciridops anna
1 he only anatomical specimen in existence of
( iridops anna was examined to ascertain if the
peculiar stout lemora repeatedly encountered as
fossils really belonged to species of Ciridops. this
being the remnants of a trunk preserved in alcohol
in the British Museum (Natural History). Origi¬
nally, the entire bird had been preserved in fluid
but it ‘was skinned out of alcohol many years ago
while still in the Rothschild collection and is now
a skin Reg. no. 1939. 12.9.58*' (Cowles in Bock
1972: 61). The value of the resulting skin was
greatly compromised because the red pigments
rapidly faded in alcohol, but we can be grateful
thai as much of the internal anatomy was
preserved as remained with this fragmentary
specimen.
The tongue and related musculature of that
specimen was the subject of detailed dissections
by Bock (1972) with some modifications to the
descriptions being added later (Bock 1978). The
results revealed relatively little in the absence
°f comparisons across a variety of other drepani-
dines. Some resemblances were noted to species
ol Loxops * (which included a minimum of three
currently recognized genera) and to cardueline
finches in general (Bock 1970. Richards and Bock
1973) but without an assessment of how the hyoid
musculature of Ciridops might differ from that of
its presumed closer relatives such as Vestiaria or
Himatione.
Bock (1972: 77) considered that “little addi¬
tional morphological evidence can be cleaned
110111 the alcoholic remnant of Ciridops anna , so
that no new anatomical data will be forthcoming
unless additional anatomical specimens are found
which is extremely unlikely,” which put undue
Olson • THE EXTINCT HAWAIIAN GENUS CIRIDOPS
661
FIG. 2. Skulls and mandibles in lateral (left) and dorsal (right) views. (A) Himatione sanguined (USNM 1 18858); (B)
Ciridops anna (MCZ 10995); (C) Melamprosops phaeosoma (AMNH 810456).
emphasis on the importance of the tongue. I look a
more hopeful approach, and carefully dissected
the thigh musculature of this remnant and found
that it did yield important and interesting new
anatomical data.
When I examined it, the specimen consisted of
the pelvis and thighs, a few caudal vertebrae, and
a partial presacral vertebral column extending into
the cervical series. The ribs had been cut through
and all of the pectoral assemblage was absent. The
left thigh had been savaged by persons unknown,
the femur being cut through in at least two places
and the musculature mangled. Raikow ( 1976) had
previously been able to study the condition of M.
obturatorius lateralis from the left side. The thigh
musculature was relatively intact on the right side.
662
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124. No. 4. December 2012
ABC
FIG. 3. Skulls in ventral views: (A) Himalione sanguined (USNM I 18858); (B) Ciridops anna (MCZ 10995); (C)
Melamprosops pbaeosoma (AM NT) 810456).
although some of the origins of the more posterior
muscles had been cut through, and the cut below
the knee had destroyed the insertions of others.
Some ol the internal organs remained relatively
intact, such as the intestines and anus, gizzard,
and heart. The liver had been mangled. The
gizzard had been sliced through, revealing that it
was completely filled with food that miraculously
had not been washed out and lost and which I
removed and had analyzed. It seems incredible
that this step had not been taken earlier,
particularly in view of the considerable published
speculation on the possible food habits of the
species.
1 cm
FIG. 4. Pelves in dorsal view. (A) Vesli,
(USNM 553205); (B) Ciridops anna ( BMNH I
coccinea
12.9.58).
Each muscle of the right thigh was compared
directly with its counterpart in Himalione sangui¬
ned (hereafter HS) and Vestiaria coccinea
(VC) and with the descriptions in Raikow
(1976). Each muscle was removed and preserved
with appropriate labeling in individual plastic-
envelopes. Ultimately, the femur and pelvis were
removed and cleaned and these are discussed
under osteology.
I he descriptions below are strictly compara¬
tive. the typical pelvic musculature of drepani-
dines having been illustrated and discussed
adequately by Raikow (1976). The relative sizes
°f muscles between species were often subjective
due to differential preservation. The muscles in
the specimen ol Ciridops, as noted by Bock
(1972), were fortunately well-preserved and easily
dissected, which was not always the case with
some of the comparative material.
M. iliotibialis cnmialis (Fig. 6A, B. C).— This
muscle in Ciridops was markedly wider (5.2 mm
at widest point) than in VC (3.4 mm) or HS
(3.1 mm). It was also thicker. The relative sizes
differ considerably (Fig. 6C). The part of the
insertion on the medial part of the patellar tendon
was still intact but the remainder had been
destroyed in skinning.
M. ilioribialis lateralis (Fig. 6A. B). — Ciridops
differs from VC and HS in that the posterior 3 mm of
the origin was not fleshy but aponeurotic. The origin
then became fleshy from a narrow band just above
the antitrochanter; these fleshy fibers attached deep to
a strong tendinous raphe running ventrally from the
Olson • THE EXTINCT HAWAIIAN GENUS C1RIDOPS
663
FIG. 5. Hindlimb elements of Ciridops (A. B. C) compared with Vestiaria coccinea (D. E. F) (USNM 553205). (A)
Ciridops xp., fossil from Oahu (USNM 255124. image reversed to facilitate comparison): (B, C) Ciridops anna (MCZ
10995). Groupings are femora in posterior view, tibiotarsi and tarsometatarsi in anterior view. Note the shorter but much
more robust limb bones in Ciridops.
iliac crest, to which also were strongly attached fibers
from the cranial portion of M. iliolibularis (Fig. 6) —
unlike either VC or HS. The origin extended as a
broad aponeurosis over Mm. iliotrochantericii
(Fig. 6B). Fleshy fibers did not approach the iliac
crest except in the anterior 2.5 mm, where the origin
was almost fleshy. The width of this muscle at its
origin was 13.0 mm. as in VC'.
M. iliotroclumtericus caudciUs (Fig. 6D). — This
muscle was strikingly different in Ciridops. being
much larger with a distinctly squared posterior
margin (Fig. 6D), causing the cranial portion
of the iliac shield to assume a conspicuously
different shape (Fig. 4) as compared with VC or
HS. A portion of this muscle in Ciridops extended
into the gap between the corner of the iliac crest
and the antitrochanter, unlike the other genera
compared. With its greater area and thickness, this
muscle easily had twice the volume of that in
either VC or HS. The tendon of insertion was
considerably stronger and extended farther cau-
dally than in those genera, leaving a deeper scar
on the femur.
Mm. iliotroclumtericus cranialis et medius —
These muscles were essentially similar to those of
VC and HS hut were larger and more robust. The
origin of M. iliotrochantericus cranialis was more
extensive posteriorly in Ciridops.
Mm. femorotibialis externus et medius. — These
fused muscles did not differ greatly from those of
VC or HS but some of the fibers of the externus
originated farther proximally, about half way up
the shaft of the femur, possibly correlated with the
shortening of the femur.
M. femorotibialis interims. — Similar to VC and
HS but larger and considerably thicker.
M. iliofibu/ciris. — The origin in Ciridops ap¬
peared proportionately shorter but was more
aponeurotic: the belly w-as larger and thicker than
in VC or HS.
M. flexor cruris lateralis.— The posterior por¬
tions of both pars pelvina and pars accessoria had
been disturbed in skinning. Differences from VC
and HS w'ere difficult to detect, but the insertion
seemed to extend farther mediad and distad.
M. caudiliofemoralis.— The belly had been cut
in skinning and the origin was lacking. The
muscle was similar in size and position to that in
VC or HS but the insertion was more distad (the
gap between the tendons of insertion of M.
664
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 4. December 2012
A
B
(VC)
0. fib.
(CA)
il.tib.lat.
c
D
(VCund^ST, diagrams of thigh musculature of Ciridops anna (CA) compared with that of Vesnaria coccinea
Irio nrof M X fr'T 1 ;. (A; B) d0rSOla,Cral VicWi of thigh muscles emphasising the aponeurotic
I T r“UdBl mUSCU,alUre- d = dermal muscles, if Ub. cran = M. iliotihiaJis
.ha, is ha!d wi NHm ! ^ = M‘ iliofihu,ilris’ «■ A- Ob- = a tendon deep to the region indicated
sS and shape o M Z h n! “TT? T T *“** differcnCes in M Hiotibialis crania.is; comparative
appro'm eTto soIe^ caudal, ,n lateral view between three genera of drepan, dines. Figuresare all
caudiliofemordis and M. ischiofemoral is w
2.5 mm in Ciridops. 1.9 mm in VC and HS).
M- ischiofemoralis.— The belly was somewh
larger and deeper, corresponding with the slight
broader and more deeply cupped ischium; tend,
ot insertion broader and stronger than in VC or H,
M. flexor cruris media Us.— This had been ci
away from the origin in skinning. It was similar i
VC but perhaps slightly more robust.
M. pubischiofemoralis.— The pars caudalis was
similar to HS, whereas in VC the origin was less
discrete and lay partially under the posterior part
ol pars cranialis. The pars cranialis was similar to
the other species.
M. obturalorius lateralis.— Both pars dorsalis
and pars ventral is were present, as noted by
Raikow ( 1976:783). These were larger and better
developed than in VC or HS.
M. obturalorius medialis. — This appeared to be
slightly larger than in VC.
M. iliofemoral is interims.— There were no
detectable differences in this small muscle.
Olson • THE EXTINCT HAWAIIAN GENUS CIR1DOPS
665
M. flexor hallucis longus. — Only the origin of
the medial head remained. This appeared to be
exceptionally strongly developed, more so than in
VC or HS. and the more expanded distal end of
the femur would have acted to provide increased
area for attachment of this muscle.
Discussion of Myology
Almost all of the thigh muscles of Ciridops
were markedly better developed than those of its
nearest relatives Vestiaria and Himatione. These
muscles are mainly those involved in moving the
femur or holding it in position, although one is
involved in flexing the hind toe, all of which
indicate a much more vigorous use of the
hindlimb than in related species.
Functional Interpretation of Hindlimb Anatomy
and Morphological Analogs of Ciridops
The pelvis and hindlimb structure of Ciridops
diverge significantly from those of all other
Drepanidini. including especially its presumed
closest relatives (Vestiaria and Himatione). All of
the hindlimb elements are much more robust but
this is most evident in the exceptionally short,
stout femur. The pelvis is correspondingly
modified to accommodate the much more strongly
developed musculature of the thigh. This indicates
active use ol the hindlimb in some activity other
than simply perching or hopping from branch to
branch (or along the ground), which arc probably
the only major uses of the hindlimb in other
drepanidines.
Therefore, to hypothesize the activity in which
Ciridops may have been engaging it is necessary
to identify other passerines with similar adapta¬
tions of the pelvis and hindlimb, particularly the
femur. The most extreme adaptations of this
nature are found in the chowchillas (Orthonyx),
which occur in woodlands of Australia (familial
level relationships of Orthonyx . as well as
Bowdleria and Mohoua. are still unresolved,
although they are not closely related to one
another). The femur in Orthonyx is extremely
short and stout, appearing almost like that of a
loon (Gaviidae) and quite unlike that of most
other passerines (Olson 1990b. Boles 1993).
These birds have a specialized foraging behavior
in which one foot is used as a brace and the other
for vigorously scratching and removing forest
litter in a search for prey (Zusi 1978). Another
group with similar, although less extreme mor¬
phological and behavioral adaptations are the
New Zealand fernbirds of the genus Bowdleria
(Olson 1990b), which also use the hindlimb not
only to scratch and push away detritus but also to
pick up leaves with the feet (Rest 1979). Both
Orthonyx and Bowdleria are almost completely
terrestrial, however, which is unlikely to have
been the case with Ciridops.
A much better analog for Ciridops are the two
more specialized species of the New Zealand
genus Mohoua. the Whitehead (A7. alhicilla) and
Yellowhead (A/, ochrovephala). These are medi¬
um-small arboreal birds with a short bill with a
curved culmen that compares quite favorably in
overall shape with that of Ciridops, and with
large, strong feet. The pelvis and hindlimb are
specialized along the same lines as those of
Ciridops with the femur in particular being
notably short and stout (Olson 1990a). The
Yellowhead feeds in treetops but also roots
“through the accumulations of rubbish that fall
down and collect” in the forks of trees, at which
time they grip with one foot, use the tail as a prop,
and “scratch vigorously with the other foot,
sending down a shower of debris” (Soper 1976:
50).
The claimed close association between Ciri¬
dops anna and loulu palms ( Pritchardia ) is
perhaps best explained not by the bird eating the
fruit or any other part of the palm itself, the fruits
usually being much too large for a bird the size of
C. anna to process, but by the birds finding food
among the litter that accumulated in the axils of
the palm leaves. This 'rubbish’ was presumably
moved by the bird’s using its large and well¬
muscled feet and legs to expose invertebrates
hidden within the accumulation.
That the crowns of Pritchardia palms (Fig. 7)
act to accumulate debris has been observed in the
field by botanist C. D. Bacon (in litt. 14 Dec
2011):
“First are things that get trapped in the
crown — seeds, leaves, and debris from other
plants, small herbaceous plants and mosses,
and invertebrates, anything you can imagine
falling from other plants or the sky into a plant.
The second contribution is from morphological
attributes of the crown itself — the upper sides
of the leaf sheath and petiole are often very
fibrous and sometimes pubescent with dense,
woolly hairs. These fibers and hairs more often
than not, split off and break at the margins, and
fall into the crown and might also offer easy
666
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 4. December 2012
FIG. 7. Crown of the palm Pritchardia nuirtii, endemic
to Oahu, Hawaiian Islands showing the density of the bases
ol the petioles and inflorescences, and the amount and
potential for accumulation of debris in the leaf axils. This is
hypothesized to have been the specialized feeding niche of
the species of Ciridops , which may have used its
hypertrophied feel and pelvic musculature to move debris
in search of insect prey. Photograph by Christine D. Bacon.
access lo nesting materials. Furthermore, some
species, like P. viscosa , have short, stiff
inflorescences that likely drop mature fruits
into their own crown. The stem apex where
things collect is protected by the crown and the
surrounding leaves, and would maintain mois¬
ture and shade, and potentially provide a food
source for insects and other invertebrates that
would also be in the crown.”
Scott et al (1986) suggested that the affinity of
Ciridops for palm trees recalled the Point-tailed
Palmcreeper ( Berlepsehia rikeri, Furnariidae) of
South America, which is closely associated with
stands of palms of the genus Mauritia. I examined
several skeletons (USNM) of Berlepsehia and
found that it has none ol the hindlimb adaptations
of Ciridops and probably obtains its food by
probing with its long, slender bill.
BEHAVIOR OF CIRIDOPS ANNA
General Demeanor.— Little was recorded con¬
cerning behavior of Ciridops anna in the field
Emerson (1894: 103) in his treatise of ancient
Hawaiian bird hunters, who sought plumes for
feathered garments and symbols, remarked that
there "was, I am told, another red-feathered bird
called ula-ai-hawai w, a beautiful thine in scarlet
wild and shy, a great fighter, a bird rarely taken by
the hunter. Its plumage would have been a
welcome addition to the resources of Hawaiian
feather- workers had it been obtainable.” I assume
Emerson's information came from native hunters.
Perkins (1903: 405) had no personal experience
with Ciridops , but he heartily endorsed Emerson's
characterization, stating that the “reputed pug¬
nacity of this bird is quite in accord with what one
might expect, and is characteristic of the section
of the family to which it belongs, which seems
generally to consist of stronger birds, well able to
drive from their food those of similar habits in the
other section | his Division 2], If, as there is reason
to suppose, the Ula-ai-hawane obtained its chief
food supply from these palms, which arc them¬
selves by no means abundant and are known to
have been visited by other Drepanididae species,
this pugnacity may well have been developed to
an unusual degree.” This is highly speculative,
but aspects of the plumage and distribution of
Ciridops can be interpreted in the context of a
territorial bird dependent upon a patchy food
source.
Vocalizations. — The only hint of any vocaliza¬
tion of Ciridops anna comes from Munro ( 1892:
20 Feb) in which he describes a “sweet low
tweet” that turned out to be made by Akepa
( Loxops coccineus) but that natives had confused
with Ciridops. Munro ( 1944) later seemed to write
the whole incident off as bungling, but his journal
is more ambiguous. He had heard many Akepa in
the Kona District prior to his venture to the
Kohalas and yet he let himself be misled at the
time. Perhaps there was a note of Ciridops that
resembled a note of the Akepa.
Previous Speculation on Possible Food Habits. —
Wilson was told “that it feeds on the fruit of the
Hawane palm” (Wilson and Evans 1893: 23). “It
seems to have been found only in the neighbourhood
ol the Lou I u palms ( Pritchardia ), the blossoms of
which as well as the unripe fruit supplied it with
food (Perkins 1903: 405). The supposedly short,
thick bill of Ciridops “lends credence to the
statement that it had departed from the nectar-
I ceding habits ol its relatives and subsisted on fruit”
(Amadon 1950: 205). If Ciridops were frugivorous
“fruits of the palm Pritchardia are claimed to be its
l°°d source; if so, one of the smaller-fruited species
of Pritchardia is to be suspected” (Carlquist 1974:
162). “The short, straight beak of Ciridops. now
extinct, is believed to have been adapted for a diet of
palm fruits” (Carlquist 1982: 9). Fruit of some or all
Pritchardia is Uk> large “to have been swallowed
whole” by Ciridops (Pratt 2002a: 5), which has
Olson • THE EXTINCT HAWAIIAN GENUS CIRIDOPS
667
neither a particularly wide gape nor any adaptations
whatever for crushing or manipulating large objects
with the bill. Munro (1892) records the last
specimen being shot “while feeding on the lo|u|lu
berries which abound in that place” he also noted
that the fruits in that area were some 20 mm in
diameter, which is much too large for a Ciridops to
cat except for small pieces of exocarp and no such
food was found in the stomach of that same bird.
“No justification exists, however, for Ama-
don's statement (1950: 223) that some
drepaniids that rarely or never take nectar, such
as... and Ciridops anna , still have a tubular
tongue' [italics Bock's|. So little is known about
the feeding habits of Ciridops , that no one knows
whether or not this bird fed on nectar. In the
absence of any contrary factual information. I
would conclude from its tongue morphology that
Ciridops fed on nectar at least during pan of the
year" (Bock 1972: 75). 1 concur that it would
have been unlikely that Ciridops did not take
nectar when it was available, considering that
many birds with no special adaptations for
nectarivory are known to feed opportunistically
on nectar (Fisk and Steen 1976. Franklin 1999).
Speculation that Ciridops actually fed on fruit or
nectar of Pritcluirdia palms based solely on the
Hawaiian name is not supported by either the gut
contents of the single fluid specimen nor by the
morphological adaptations of the genus.
Gizzard Contents and Tlteir Interpretation. —
The gizzard in the alcoholic trunk specimen
(BMNH 1939.12.9.58) had been slashed open by
some previous examiner and could be seen lo be
crammed with food. The contents were carefully
removed and later identified by workers skilled in
identifying food items from droppings obtained in
field studies of Drepanidini. The overall insectiv-
ory indicated for Ciridops was mentioned briefly
by Scott el al. ( 1986: 156. and cited by Pratt 2005:
275) based on communication from me concern¬
ing these findings: I adult lepidopieran (wing
scales only), 13 adult psyllids (Hemipiera, jump¬
ing plant lice). 38 psyllid eggs, three adult psocids
(Psocoptera. bark lice). 26 adult ‘Drosophila- like’
Diptera, 2 mites (Acari), I spider. 6 seeds of
unknown fruit. I anther? (C. P. Ralph in litt. to
Olson 30 Jun 1981).
This collection of arthropods is similar lo the
food items taken by other drepanidines in forest
ecosystems on the island of Hawaii, including
Apapane (Fancy and Ralph 1997), liwi (Fancy
and Ralph 1998), Amakihi ( Loxops virens ;
Lindsey el al. 1998). and Akepa (Lepson and
Freed 1997). The first three are specialized nectar
feeders and Akepa feed occasionally on nectar as
well. Nectar, however, provides no protein so that
even the most nectarivorous of birds, such as
hummingbirds (Trochilidae), must feed on insects
and spiders as well.
The arthropods fed on by Ciridops and many
other drepanidines are probably dispersed nearly
throughout the forest ecosystems on Hawaii.
Thus, it may not be so much a matter of
specializing on a particular kind of prey as
becoming adapted to extract widely available
generalized prey from particular niches w ithin the
ecosystem. Ciridops differed from all of its
relatives in having strong feet and leg muscles
that I hypothesize evolved for moving vegetable
matter that accumulated in the axils of palm
fronds. It may have fed on the same kinds of
insects and spiders taken by Apapane and liwi. but
it could gain access to them in places that could
not be exploited by species whose hindlimbs were
adapted solely for perching.
DISTRIBUTION AND ECOLOGY OF THE
GENUS CIRIDOPS
Stejneger (1900: 72) wondered why Ciridops ,
along with Viridoitia. Loxioides . Rhodacanthis.
and Cliloridops. should be confined to Hawaii and
not have representatives on the other islands.
Carlquist (1974: 129) considered that “the rarity
and early extinction of some of the Hawaiian
honeycreepers may have left gaps in our geo¬
graphical distribution; Ciridops might have oc¬
curred on islands other than the island of Hawaii,
for example.” He could hardly have for, seen how
the fossil record would completely upend every¬
thing previously thought to be known about the
distribution of Hawaiian birds. The only direct
evidence of the distribution of Ciridops comes
from the scant historical record and from fossils
(Fig. 8).
Because of repeated hearsay reports of the Ula-
ai-hawane, Wilson ventured that "I have little
doubt that it will be found, perhaps in some
numbers, in the upland region of the interior,
which I was unable to explore... .My friend Mr
Francis Spencer, writing to me quite recently
[presumably about 1892], says that his natives had
seen the bird in the sw'ampy forest-region above
Ookala [Keanakolu District according to Banko
(1987: 248)] on Hawaii, and his description leaves
668
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124, No. 4, December 2012
G Kauai
re,, pi-. I i , . '"e,map " 'h.C 1 lawauan ,sIands shovvin8 ,hc known distrihution of the genus Ciridops. Stars indicate the
? h i n TC Were lukcn- whercas question marks represent dubious records-that in the
indicate wh r 't" |( ; ! i,nd thal in ,he caM is ,he °oki,,i* a<™ Wilson and Evans 1893). Solid circles
ontn ckc is inTltaTe £ T T C°" r0COycred (,hal <>ahu includes several separate but adjacent sites):
open circles indicate lossil sites with small passerines but lacking remains of Ciridops.
no doubt of its identity" (Wilson and Evans,
1893: 23). Jt is uncertain why Perkins (1903: 405)
icgatded Ciridops to have been “widely distrib¬
uted on the island of Hawaii... and to have
inhabited both the Kona and Hilo districts as well
as the Kohala mountains." I know of no other
information concerning Ciridops in the Kona
District. Perhaps Perkins was told that by a local
source that he failed to mention or surmised a
wider range based on the distribution of Pritch-
ardia, which he noted had persisted into the late
19th century "in the dense forests above Hilo.”
and “in the Kohala mountains and the Kona
district." There is no historic record of Ciridops
from the Kona District, where several species of
birds were last known before becoming extinct
(e.g.. Olson 1999a). Important fossils of passer¬
ines have been discovered in lava tubes on Hawaii
Hf*mgnaihus vorpalis, James and Olson
2003). but the fossil record on that island is
sporadic and incomplete and many historically
known birds have not yet been found as fossils
including Ciridops.
The accounts of Munro (1892) and Palnu
(Rothschild 1893) describe searching for Ciridon
I” the Kohala Mountains. At the place where th
last specimen had been taken shortly before b
nat.ve hunters. Palmer noted only eight Pritch
auha palms, and where four of them grev
together was the spot the last Ciridops was found
(Rothschild 1893: Diary 7). They made an
unsuccessful search for the bird at elevations
above this point and at 1,200 m and above
conditions were described as “almost living in the
water because of heavy rain and the tempera¬
tures were so low that they gave up the pursuit
(Rothschild 1893: Diary 7). Thus, perhaps, arose
the misperception thal Ciridops anna was an
inhabitant of “montane forest" (e.g., AOU 1998:
677). The cold, wet Kohala Mountains were
probably submarginal habitat for Ciridops at best,
much as the last few struggling individuals of
MeUimpmsops pliaeosorna passed out of their
miserable existence in the dank slopes of
windward Haleakala on Maui, when the fossil
record shows that the species throve at lower
elevations on the drier leeward slope of the
mountain.
In contrast with Hawaii, the fossil record on
Maui is extensive and reasonably comprehensive
as tar as it goes; yet no fossils’ of Ciridops are
known (James and Olson 1991). This may.
however, reflect the tact thal no productive fossil
sites have yet been found in the lowlands of
Mam, the lowest site producing quantities of
P i edat or-acc u mu I ated passerine fossils being Pun
ms-! CaVe at 305 m elev»tion (James et al.
987)- If Ciridops did occur on Maui, as its
Olson • THE EXTINCT HAWAIIAN GENUS CIRIDOPS
669
presence on Hawaii and Molokai would make
probable, the birds were probably confined to
lowland habitats.
Fossils of Cirul ops, apparently referable to C.
anna on Molokai, were found in the Moomomi
Dunes (Olson and James 1982) where suitable
forest habitat was probably adjacent at the time of
deposition, whereas no fossils of Ciridops were
found in the dune deposits at Iho Point, a
particularly isolated locality in a harsh, arid part
of the island where probably only beach scrub
habitat was able to persist. Given that Ciridops
was definitely present on Molokai, it seems likely
that a representative of the genus would have been
on Lanai as well, although on that island the fossil
record is scant (Dove and Olson 2011) and as yet
includes no passerines.
On Oahu, a species of Ciridops is fairly
abundantly represented in the sinkhole deposits
in the southwestern part of the island at Barbers
Point. The bill and hindlimb bones appear to be
somewhat shorter than in C. anna and it should
perhaps be recognized as a separate species but
has not yet been named (James and Olson 1991).
The fossil species Ciridops ienax James and
Olson (1991) was described from the Makawehi
dune deposits in southeastern Kauai, where the
diversity of species of various passerines indicates
the presence of adjacent dry lowland forest. Yet not
one bone of Ciridops ienax has yet been found in
the Quaternary lake deposits excavated at Malta' u-
lepu. about 2 km to the east of the Makawehi
dunes, despite a great abundance of fossil material,
including hawks and owls, and the exceptional
diversity of species and quality of preservation
(Burney et al. 2001 ). This suggests a rather strong
habitat avoidance by Ciridops ienax. Although
Prilchardia palms were present and abundant at
Maha'ulcpu. the flora was extremely diverse,
including several species of trees now restricted
to upland localities where they are evidently relicts.
The overall impression of the environment at
Maha'ulaepu is a diverse, moist, closed-canopy
forest. Therefore, the habitat preference of Ciri¬
dops may have been for drier, more open habitat in
which Prilchardia grew in monospecific stands.
Ciridops ienax may be the most primitive species
of the genus because of its apparently less
specialized hindlimb elements. Kauai is the oldest
of the islands on which Ciridops was know to occur,
suggesting that the genus may have originated there
and spread eastward with the formation of the
younger islands of the main Hawaiian chain.
The available evidence suggests that one form or
another of Ciridops probably occurred throughout
all the main I lawaiian Islands, although confirming
iis presence on Maui would certainly he desirable.
The fossil record also shows that potential avian
predators occurred throughout the range of Ciri¬
dops. The extinct, long-legged, bird-eating owls of
the genus Grallistris arc known from Kauai. Oahu,
Molokai, and Maui, but apparently did not occur on
Hawaii (Olson and James 1991). The presence of
fossils of Ciridops in the deposits on Kauai. Oahu,
and Molokai is almost certainly attributable in
whole or in part to those owls and bones of
Ciridops were found in what was clearly an owl
pellet on Molokai (Olson and James 1982). The
Hawaiian Hawk UJuteo solitarius ) of the island of
Hawaii is known from bones of the same or very
similar species from Molokai. Oahu, and Kauai,
and small forms of Circus adapted tor catching
birds are know n from fossils on Molokai and Oahu
(Olson and James 1991). Thus, the species of
Ciridops. like the other small passerines that shared
their habitat, w-ould have had to have as keenly
evolved predator-avoidance behavior as any of
their mainland ancestors.
Assuming a close, if not totally dependent,
relationship between Ciridops and loulu palms
( Prilchardia ). we may extrapolate more about the
probable inter- and intraisland range and habitat
preferences of the birds, albeit with a certain
degree of circularity, based on information on
Prilchardia from Hodcl (2007). The apparent
diversity of Prilchardia is centered on the
Hawaiian Islands, although there are scattered
outliers in Fiji, Tonga, Cook Islands, and the
Tuamotus whose distribution suggests there were
probably widespread human-caused prehistoric
extinctions elsewhere in Oceania. The nominal
23 species in the Hawaiian Islands consist almost
entirely of allopatric populations most of which
are severely restricted in range and now often
consist of only a few' living individuals. Specific
characters are extremely variable and are usually
only useful for defining species when used in
combination. Only three species occur on more
than one island and all of those occur on Maui
Nui. which included the combined islands of
Maui. Molokai, and Lanai during lowered sea
levels of glacial periods.
Prilchardia occurs naturally now on all the
main Hawaiian Islands except the small, ecolog¬
ically devastated island of Kahoolawe. and also on
the remote island of Nihoa. The plants may occur
670
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124. No. 4. December 2012
in dry to very wet forest but not above 1.400 m
and probably constituted a dominant aspect of the
vegetation only in lowlands. Evidence of this
comes from Holocene fossil pollen on Oahu, and
pollen and seeds on Kauai, indicating that
Pritchardia was one of the most prevalent plants
in the diverse lowland floras of those islands
(Athens et al. 1992. Athens 1997. Burney et al.
2001). However, Ciridops did not necessarily
occur in all places where Pritchardia grew, as at
Maha ulepu on Kauai, and the birds may have
preferred areas in which palms grew practically to
the exclusion of other forest cover (Fig. 9). Nearly
monocult ural stands may have been patchily
distributed resulting in patchy distribution of
Ciiidops on Kauai and Molokai and perhaps
contributing to our failure as yet to find Ciridops
anywhere on Maui.
EXTINCTION
Destruction of lowland habitats (Olson and
James 1982) by burning and clearing for agricul¬
ture and introduction of the seed predator Rati us
exulans following Polynesian colonization, doubt¬
less gave rise to the obviously relictual distribu¬
tion and extinction or near extirpation of popula¬
tions of Pritchardia , and probably explains the
disappearance of Ciridops everywhere but on
Hawaii during the prehistoric period. After
European colonization, the introduction of grazing
and browsing ungulates, additional species of rats
and mice as well as carnivores such dogs and cats,
and alien species of birds with their diseases.’
accelerated the destruction of Hawaiian habitats
and biota.
By the late 1800s on Hawaii, Pritchardia palms
seemed “to have been always of sparse or local
distribution, and still exist singly or in scattered
clumps in the dense forest above Hilo, where I have
often observed them, as well as in the Kohala
mountains and the Kona district” (Perkins 1903*
405)- Hartlaub (1896a, b) included Ciridops anna
among recently extinct or threatened species
affirming Newton's (1892) statement that it was
truly native, and remarking that the published
leU a s*ran£e impression (Hartlaub
Rothschild (1900: 1 83) considered the species to
be one of the rarest in the world,” but only 7 years
ater listed it under the category “011110 extinct”
(Rothschild 1907a: 200). Amadon (1944- p)
■ emarked that “The speedy disappearance of this
bud is puzzling. Possibly it was on the verge of
EKi. 9. The isolated and protected islet of Huelo, off
the non hern coast of Molokai, showing one of the feu
remaining nearly pure stands of toulu palm ( Pritchardia ).
fins stand has survived due to (he absence of seed predators,
such as rodents and pigs, and protection from human
disturbance such as tire and cultivation. Similar patchy
monocultura! stands of Pritchardia may have been the
preferred habitat of the species of Ciridops in lowlands of
the Hawaiian Islands prior to ihe arrival of humans.
Photograph of P. hlllebrattdii by Donald R. Hodel.
copyright 2006.
extinction when discovered.” Greenway (1958;
regarded it as extinct prior to the 1950s. Possible
sight and sound records mentioned from the island
o! Hawaii about 1937 (Banko 1987: 240) are not
credible. The extinction of Ciridops anna was
considered to have preceded the extinctions caused
when avian malaria in the Hawaiian Islands
reached epizootic proportions after 1920 (van
Rtper et al. 1986).
From both Monro's (1892) and Palmer’s
(Rothschild 1893) journals, it is evident that in
C t' ldops anna was beyond extremely scarce,
ibat the local hunters Palmer recruited in his
quest lor this bird were highly motivated is
indicated by Palmer’s account book (Bishop
Olson • THE EXTINCT HAWAIIAN GENUS CIRIDOPS
671
Museum Archives), which he kept in minute
detail with every indication of scrupulous honesty.
The last entry for 13 February 1892 is "Ulaaiha-
wane specimen [$150.00.” At that time a payment
of lifty dollars for a single specimen of bird would
have been a truly extraordinary amount that must
have excited attention throughout the island.
Palmer used a conversion rate of £1 British
sterling = —54.80, but there is probably little use
in trying to comprehend the 1 892 value of $50 in
Hawaii in current dollars or pounds sterling. More
useful is an indication of what that amount would
purchase locally then in goods and services. The
next entry in Palmer's account book was "Pur-
chaste] one horse [$]60.00,” when a horse was
probably the greatest single expense he had in the
field. At the same time, he was paying Munro, a
New Zealander. $25.00 per week for physically
demanding but diligent and skilled labor. For
local laborers, $50.00 must have represented an
astronomical sum and the offer of such remuner¬
ation is a near certain indication that no more of
the birds could be obtained regardless of the
amount of effort expended. As further demonstra¬
tion of just how much Rothschild must have
desired specimens of Ciridops, a little over
2 months later Palmer paid half us much ($25.00
on 20 Apr) for a living specimen of the Hawaii
Mamo, which, like Ciridops anna, was the last of
its kind ever taken. Without that last specimen of
Ciridops. however, our much-expanded knowl¬
edge of the morphology of the genus would have
gone unknown. Thus, in hindsight. $50 for the last
Ciridops anna may have been one of most
fortunate purchases Walter Rothschild ever made.
ACKNOWLEDGMENTS
This paper would not exist except for the generosity of the
curators in charge of the following museums holding
specimens of Ciridops. comparative material, and fossils:
American Museum of Natural History, New York, ( AMNH);
The Natural History Museum, London, U.K.. formerly
British Museum (Natural History t (BMNH): Bernice P.
Bishop Museum. Honolulu. Hawaii (BPBM); Museum of
Comparative Zoology. Harvard University. Cambridge,
Massachusetts (MCZ); and National Museum of Natural
History, Smithsonian Institution. Washington, DC.
(USNM). I am much indebted to Ellen Alers, Smithsonian
Institution Archives, for bringing the Brigham/Baird corre¬
spondence to light. I uni especially grateful to Julian P. Hume
for his excellent paintings, for details of descriptions and
measurements of certain specimens, and for inking my pencil
sketches of myology. Carol P. Ralph and Stephanie Nagata
deserve special commendation lor identification of gizzard
contents. Helen James and Megan Spitzer supplied data and
other information, especially for fossils. I thank Christine D.
Bacon and Donald R. Hodcl for information and photographs
of Pritchardiu palms and Warren Wagner for botanical
advice. H. Douglas Pratt kindly provided information on his
illustrations of C. anna. Stipple draw ings are by Jacquin B.
Schulz. I am most grateful to Christina Gebhard and Brian
Schmidt for photography and creation and composition of
many of the figures.
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as conducted between
dawn and 1 100 hrs, and halted w'hen rain. wind, or
gusts exceeded prescribed levels (light rain and
wind level 3 on the Beaufort scale).
‘Oma'o density estimates (birds/ha ± SE) were
calculated using Program DISTANCE. Version
5.0, Release 2 (Thomas et al. 2005). The
candidate detection function models were limited
to halt normal and hazard-rate detection functions
with expansion series of order two ( Buckland et al.
-001). Hall normal was paired with cosine and
I lei mite polynomial adjustments following Buck-
land et al. (2001 ). and hazard-rate was paired with
cosine and simple polynomial adjustments. Model
precision was improved by incorporating sam-
p mg covariates in the multiple covariate distance
sampling (MCDS) engine of DISTANCE
(Marques and Buckland 2004, Thomas et al.
Judge et at. • REOCCURRENCE OF ‘OMAO ON HAWAI I ISLAND
677
Mauna Loa
n_n_n
m
gt.
V s— -
3 000 n.
000
'Oma'o detections
0 incidental observations
# 2010 HAVO survey
A 1978 HFBS
•••••••other surveys with detections
. other surveys with no detections
Landcover
j ] Mesic/wet forest
[ | Dry shrubland/woodland
| 1 Alpine scrub or unvegetated
] Sub-alpine/alpine life zone
FIG. 1. Detections of ‘Oma'o during 10 forest bird surveys on Hawai'i Island. The species’ range is nearly continuous
in forests on the windward side of the island, while there have only been scarce detections on the leeward side. The species
was not seen nor heard for >30 years in leeward forests and woodlands until it was detected during the HAVO land bird
surveys in 2010. Tract areas are II Ilonomalino. P = Papa, and K = Northwest Kahuku. The graphic also depicts sub-
alpine and alpine incidental observations ol the species; as well as potential habitats that have not been formally surveyed.
2005). Covuriates included cloud cover, rain,
wind, gusts, observer, time of detection, canopy
cover, canopy height, panel member, detection type,
and tract. All co variates were trealed as a factor,
except lime of detection, which was treated as both a
factor and a continuous covariate. Assessing time of
detection as a continuous covariate helped ascertain
if the detection rate varied during the morning. Each
detection rate model in the candidate set was lit to
data pooled across tracts, including 269 detections in
windward tracts (Judge et aJ. 2011); the model
selected was that with the lowest second-order
Akaike s Inlomiation Criterion corrected for small
sample sizes (AICc) (Table I) (Buckland et al.
2001, Burnham and Anderson 2002). Data were
truncated at a distance where detection probability
was -10%. This procedure facilitated modeling by
deleting outliers and reducing the number of
parameters needed to modify the detection function.
Tract-specific densities were estimated from the
678
THE WILSON JOURNAL OF ORNITHOLOGY • Voi 124, No. 4. December 2012
global detection function using the post-stratifica¬
tion approach, and variances and confidence
intervals were derived by bootstrap methods in
DISTANCE from 999 iterations (Thomas et al.
2005).
We used incidental Oma'o detections to
identify suitable habitat to delineate the distribu¬
tion of “Oma'o in scrub alpine habitat. Formal
passerine surveys have not been conducted in
scrub alpine habitats on Mauna Loa (Camp el al.
2009, Judge et al. 2011). Incidental “Oma’o
detections were made during seabird nest search¬
ing and colony monitoring in the scrub alpine
habitat on Mauna Loa between 2006 and 2010
(Apr-Nov: SWJ, pers. obs.). We also compiled
‘Oma'o detections since the 1990s recorded by
HA VO, The Nature Conservancy, and USGS
researchers who conducted botanical surveys in
the Mauna Loa scrub alpine life zone (Ziegler
2002). Detection rates were not calculated be¬
cause observations were not enumerated.
RESULTS
Oma'o were detected in high elevation wood¬
land habitat on the leeward 'dopes of Mauna Loa
during point-transect surveys in 2010 after
>30 yrs of apparent absence in the region. We
detected 23 “Oma'o at 19 stations in the Papa
(9 birds) and Northwest Kahuku (14 birds) tracts
between 1,800 and 2,500 m elevation (Fig. I ). We
did not detect 'Oma’o in the Honomalino tract,
which is predominantly wet mesic forest. Our
detections occurred in the transition between
woodland and alpine zones in habitat dominated
by mamane. naio, and ’ohi'a trees. Canopy cover
was classed as scattered (5-25% cover) in both
tracts, and canopy height was mixed ranging
between 5 and 10 m in the Papa tract and 5 to
>10 m in the Northwest Kahuku tract. The
understory' in both tracts was primarily bare
ground due to ungulate grazing and lava flows,
yet native shrubs and introduced grasses were
present. Densities were relatively low at the two
leeward tracts with an estimated (± SF) 0 16 ■+•
0.05 and 0.50 ± 0.22 birds/ha in the Papa and
Noithwest Kahuku tracts, respectively.
Incidental sightings of ‘Oma'o in the Mauna
Loa scrub alpine life zone ranged from 2.000 to
3,200 m and only occurred on lava How substrates
that were 800 to 5.000 years before present
Oma“o were most often observed on puhoehoe,
or smooth rope-like lava, as opposed to “a“a that
consists of brittle and sharp chunks of lava.
“Oma'o were also detected on infrared motion¬
sensor cameras trained on Hawaiian Petrel
(Pterodroma simdwichensis) burrows at 2,850 m
(Judge et al. in press). We identified 74.700 ha of
potential habitat in the scrub alpine life zone on
Mauna Loa. given the elevation, substrate age.
and flow type where “Oma'o were observed
(Fig. 1 ). There may be several thousand ‘Oma'o
in the scrub alpine habitat based on our woodland
estimates.
DISCUSSION
We detected ‘Oma'o in woodland habitat in
relatively low densities during a 2010 bird survey
of HA VO after the species was absent from
leeward forests and woodlands on Hawai'i Island
for >3 decades. A previous survey in 2005 on the
fixed panel transects yielded no detections of
“Oma'o (Tweed et al. 2007). nor had 'Oma'o been
detected in any leeward forest or woodland during
10 point-transect surveys dating to 1978 (Gorre-
sen cl al. 2009). 'Oma'o detections in leeward
woodlands of Hawai'i Island are significant
because they comprise a major expansion in the
species’ known range. The species is now
distributed from windward wet, mid-elevation
forests up to sparsely vegetated, high elevation
scrub alpine and woodland habitats in both
windward and leeward regions.
It is likely the birds detected in the woodland
habitat came from one of two local sources:
colonizing individuals from leeward scrub alpine
or from windward forest populations. Banding
studies in mesic and wet forest habitats indicated
Oma'o were highly sedentary (Ralph and Fancy
1994, Wakclee 1996). Thus, it is possible the bird."
we observed were not migratory or transitory but
instead have dispersed into and re-colonized
woodland habitats. It is most likely the leeward
biids were from the nearby scrub alpine popula¬
tion that is now occupying the woodland-alpine
transition zone. ‘Oma'o dispersing from the
windward forests to leeward woodlands would
have to either cross high elevation alpine habitats
or lower elevation degraded forests (i.e., habitats
without fruiting trees and shrubs). There are no
data available to indicate if the birds migrated
through alpine or degraded forests. A likely cause
lor birds to disperse is that resources in the
windward forests may be limiting because of
drought (Timm and Diaz 2009) or habitat
degradation (PMG, pers. obs.). It seems unlikely
that 'Oma'o would have traveled 15-30 km across
Judge et al. • REOCCURRENCE OF ‘OMA'O ON HAWAI‘1 ISLAND
679
TABLE 1 . Model parameters and model selection results for ‘Oma'o from the 2010 HAVO survey. Models were sorted
hv differences in second-order Akaike’s Information Criterion after correcting for small sample si/e ( AAlCc) between each
candidate model and the model with the lowest AKY value. Models included: H-norm = hull normal and 11-rate = hazard-
rate key detection functions with scries expansions Cos cosine, IT-poly ~ hermite polynomial, and S-poly = simple
polynomial. Covariates were incorporated with the most parsimonious model to improve model precision. Covariates
included the continuous variable Time-con = time of detection. Categorical variables included Cloud = cloud cover. Cover
amount of vegetation cover. DectType = detection type. Height = height of vegetation. Rain = amount of rain,
Observer = observer. Panel = transect category. Time-cat = time of detection. Tract - HAVO tract, and Wind and Gusts
= Beaufort wind scale. The number of estimated parameters (Variable) and Akaike model weight (u7) are provided for
each model.
Model1
Variables
AAlCc
AICc
W'i
H-rate Key
2
0
2310
0.771
H-rate Key Tract
8
4
2314
0.104
H-rate Key Cloud
3
8
2318
0.014
H-rate Key Rain
3
8
2318
0.014
H-rate Key Cover
3
8
2318
0.014
H-rate Key Height
3
8
2318
0.014
H-rate Key Time-cat
3
8
2318
0.014
H-rate Key Time-con
3
8
2318
0.014
H-rate Key Observer
3
8
2318
0.014
H-rate Key Panel
3
8
2318
0.014
H-rate Key Wind
4
It)
2320
0.005
H-rate Key DectType
4
10
2320
0.005
H-rate Kev Gusts
5
12
2322
0.002
H-norm Key
1
29
2339
0.000
J Model failed lo converge or
parameters were highly correlated for the H
-norm
Cos. H-norm H-poly. H-rate Cos. and H-ratc S-poly models.
unsuitable habitat to reoccupy leeward wood¬
lands. Captive-bred releases of Puaiohi on Kaua'i
are generally successful, but most birds disperse
<5 km to release sites and pairs rarely expand
into new territories (Tweed e( al. 2003, Snetsinger
et al. 2005).
Little is known regarding the biology of the
scrub alpine ’Onia'o population. Incidental detec¬
tions of ‘Oma’o in scrub alpine habitat have
occurred over a long period. 1990s to present, and
from throughout the year (Fcb-Nov). ‘Oma'o
were detected since our 2010 survey in the scrub
alpine habitat above both the Honomalino and
Papa tracts (Mel Johansen. The Nature Conser¬
vancy. pers. comm.). ‘Oma’o were readily
observed during seabird surveys near lava tube
entrances, overhangs, and cavities, predominately
in pahoehoe flows. These flows have more
vegetation than a‘a flows because soil and
moisture can accumulate on the smooth pahoehoe
surfaces and in wash areas (Eggler 1971 ). ‘Oma'o
in alpine habitats likely subsist on berries of
‘bhelo (Vacciniiwi relit uUiimn), kukaenene
( Coprosnui emntleoides). and pfikiawe (LepteCo-
phylla tamdameiae ), as evidenced from drop¬
pings with these seeds found beside raised rocks
where the birds had been perching (SWJ and
JMG, pers. obs.), There is also a significant
arthropod component in the diet of scrub alpine
’Oma'o populations (Wakelee 1996). ’Oma'o
nesting in scrub alpine habitat would be vulner¬
able to feral cat and rat depredation, which is a
concern for this unusual solitaire population.
Hawaiian forests are patchily distributed and a
metapopulation framework can appropriately
describe avian processes (Flaspohler et al. 2010).
Bird populations in the Hawaiian Islands are
disrupted by volcanic eruptions, habitat degrada¬
tion. and disease (Pratt et al. 2009, Flaspohler et al.
2010). Habitat connectivity and dispersal rale of
each population affect the success of a species
(Gilpin and Hanski 1991). ‘Oma'o possess greater
resource plasticity and have retained connectivity
among wet mesic forest habitats, unlike Puaiohi
that have distinct nesting and foraging require¬
ments (Wakelee 1996, Snetsinger et al. 2005).
'Oma’o from the scrub alpine population would
have to undergo substantial physiological and
behavioral shifts to disperse to wet mesic forests.
The processes needed for ’Oma'o to disperse
between alpine and woodland habitats, however,
would not be as restrictive as birds could forage in
the mosaic ol dry woodlands and large lava Hows.
Polymorphic microsatellite loci (Eggert et al.
680
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124. No. 4. December 2012
2008) could be used to confirm the source of the
leeward woodland population, as well as reveal
taxonomic differences in the scrub alpine and
forest populations.
Avian frugivores and specialists on Hawaii
Island have had numerous extinctions (Banko and
Banko 2009), and -Oma‘o is currently Hawaii
Island's sole native seed disperser (Gorresen et al.
2009) . Gone are the Greater Koa-Finch (Rhoda-
canthis palmeri). Lesser Koa-Finch (R. flaviceps).
Kona Grosbeak ( Chloridopx kona ), and Ula-'ai-
hawane (Ciridops anna) (Banko and Banko
2009). The only other native omnivore capable
of seed dispersal, the ’Alala ( Corvus hawaiiensis),
is extinct in the wild and only persists in captivity
(Banko et al. 2002). Recognition of the full extent
°f the range and population size of ‘Oma'o is
encouraging because of the potential for conser¬
vation of the species, and restoration of its role in
native plant propagation and ecosystem function
in leeward habitats.
ACKNOWLEDGMENTS
We thank T. K. Pratt and F. R. Warshauer for
discussions on ‘Oma'o distribution and the scrub alpine
population. We thank C. M. Kudray. K. L. Kozar. and C. J.
Nash of the Pacific Island Network Inventory and
Monitoring Program. We thank R. K. Loh. H. M. Hoshidc,
and A. W. Ramos of the Resource Management Division
Of Hawa.-i Volcanoes National Park for site permission
and logistical support We also thank B. IT Hsu. N. C.
Chatterson. C. M. Jenson, and J. X. Wu for contributions
m the field. We thank P. J. Hart, T. K. Pratt, and two
anonymous reviewers for comments on an eurlv draft of
this manuscript. This project was conducted under a
cooperative agreement between the University of Hawaii
at Hilo (Hawaii- Pacific Islands Cooperative Ecosystem
Judies Unit), the U. S. Geological Survey and the National
Park Service, Coopentu'vc Agreement Number H8080090(X)8.
Any use ot trade, product, or firm names in this publication is
tor desenptive purposes only and does no. imply endorsement
by the U.S. Government.
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The Wilson Journal of Ornithology I 24(4):682-687, 2012
TWO MODES OF PRIMARY REPLACEMENT DURING PREBASIC
MOLT OF RUFOUS FANTAILS, RHIPIDURA RUFIFRONS
JAMES H. JUNDA.1-2 ANDREA L. CRARY.' AND PETER PYLE'
ABSTRACT.— We documented unusual variation in the sequence of primary replacement during the prebasic molt of
Rufous Fantails ( Rhipidura rufifrons ) captured in 2009 and 2010 on Saipan. Northern Marianas Islands. Most captures
(62%) followed a typical replacement sequence, starting at the proximal primary (P I) and proceeding distally to the
outermost primary (P 10), but some individuals (38%) commenced molt from medial leathers, either P 2. P 3. or P4 with
replacement proceeding bidirectionally from the point of origin in multiple molt series. The distribution of centers for
medtal origin was P 2 (3%), P 3 (77%), P 3 and/or P 4 ( 12%), and P 4 (8%), indicating this pattern was distinct from the
typical (PI) pattern and the commencement point was not fixed to a specific primary, females and individuals undergoing
the second prebasic molt were more likely to have a center among primaries 2-4 than males and older birds. Two females
that showed a center at P I during molt in 2009 showed a center at P 3 or P 4 during molt in 20 1 0 represented exceptions to
this finding hut also indicated the starting point could vary inter-annually in an individual. Multiple molt senes among
p. .manes are poorly documented in passerines and we provide the first evidence for this molting strategy in the
Rhtpidundae. Our results suggest a molt center among primaries 2-4 in younger and female Rufous Fantails niav have
evolved to enable more-rapid replacement ol primaries while maintaining belter foraging ability among selectively
disadvantaged individuals. Received 20 January 20/2. Accepted II May 2012.
Molt sequence among primaries of passerine
birds is largely fixed, replacement beginning
with a center at the innermost primary (P I) and
ptoceeding distally in a single series to the
outermost feather (P 9 or P 10). Prcformalive
molt can be incomplete and eccentric in some
species with molt commencing at a primary other
than P 1. but replacement continues to be distal
and in sequence (Pyle 1997). Multiple molt
centers or series among primaries have been
documented widely among non -passerine families
including albatrosses (Diomcdeidae). alcids (Al-
ctdae), falcons (Falconidae). parrots (Psitlacidae),
and owls (Strigidae) (Miller 1941; Langston and
Rohwer 1995; Pyle 1997, 2008; Thompson and
Kitaysky 2004,. but only a few exceptions to
distal and sequential replacement during complete
prebasic molts have been documented in north-
temperate passerines. The primaries of Spotted
Flycatchers (Muscicupa striata; Muscicapidae)
are replaced proximally (generally from P 10 to
P 1) and. in a few European shrikes (Laniidae)
and warblers (Lucostellidae), primary molt can
begin with medial primaries and proceed bidirec¬
tionally, displaying multiple molt series (Cramp
1992. Cramp and Perrins 1993, Jenni and Winkler
1994). American Dippers (Cinclus mexicanus-
Cincltdae). among North American passerines
have been reported to molt primaries out of
sequence commencing with a block of medial
leathers (Sullivan 1965). We are unaware of other
North American or tropical passerines that
diverge Irom a single distal replacement series.
Multiple molt series are thought to be an
adaptation lor increased foraging efficiency in
birds with time constraints for molting (Tucker
1991, Hcdenstrom and Sunada 1999. Pyle 2005,
Rohwer ct al. 2009); documentation of exceptions
within families may lead to a better understand¬
ing ol remigial-replacement strategies (Rohwer
1999),
Rufous Fantails ( Rhipidura rufifrons; Rhipi-
duridae) occur in Australia, Indonesia, and
islands of the southwestern Pacific Basin (Hig¬
gins et al. 2006). This passerine species is
insectivorous with short rounded wings and
i cites heavily on aerial foraging strategies. We
discovered some Rufous Fantails molting bi-
direclionally from a center among primaries 2. 3,
oi 4 during research on the demography of
landbirds on Saipan. Northern Marianas Islands
(Radley et al. 201 1). Other individuals displayed
a sequence more typical of passerines, com¬
mencing with P 1 and proceeding distally to P
10. Our objective is to document variation in the
primary replacement sequence of Rufous Fan-
tails on Saipan and discuss its possible evolu¬
tionary implications.
' The Institute for Bird Populations, P. O. Box 1346 METHODS
Point Reyes Station, CA 94956, USA Ri •
"Corresponding nndior; ™u: jamesJunda.graai,com Aprf| °P"7o "
682
Junda et al • RUFOUS FANTAIL PRIMARY MOLT
683
TABLE 1. Molt patterns of Rufous Fantails captured in 2009 and 2010 at TMAPS stations on Saipan. Younger (SCB)
individuals and females were more likely to have a primary 2-4 strategy then older (DCB) individuals and males.
n
DCB*-"
SCB"'
Males"
Females"
Primary 1 group
108
54
34
20
5
Primary 2^1 group
66
8
32
8
14
Primary 2d
2
0
1
1
I
Primary 3d
51
6
26
7
1 1
Primary 3/4d
8
1
2
0
1
Primary 4d
5
1
3
0
1
' !X’B (Definitive Cycle Basic) individuals are those Undergoing ai least their third prebasic molt.
b Age and gender could not be ascertained for all captures.
L SCB (Second Cycle Bavin individuals are those undergoing their second prebasic molt
■' Values for P 2, P 3. P 3/4, and P 4 represent subsets of die primary 2-1 group.
October 2010 on Saipan (15 12' N. 145 45' E). a
tropical Pacific island in the Northern Mariana
Archipelago (Radley et al. 2011). Each mist-
netting station was operated for 6 hrs once every
10 days following protocols established bv (be
Institute for Bird Populations (DcSantc et al.
2009). All unhanded birds were individually
marked with numbered aluminum leg bands and
many were classified to age and gender (Pyle el
al. 2008. Radley et al. 2011). Wing chord was
measured (± 1.0 mm) as unflattened right wing
from wrist to tip of the longest primary. Mass
(± 0.1 g) was measured using a digital scale.
Rufous Fantails typically have a partial preforma-
tive moll and do not replace primaries or
secondaries until the second prebasic molt. Age
was assigned based on extent of skull pneumati-
zation, plumage, and moll-limit criteria (Radley et
al. 2011), and verified through recapture data
when available. Age codes were defined based on
plumage cycle (Wolfe et al. 2010) and birds were
categorized as either second-cycle basic (SCB).
including (hose undergoing (lie second prebasic
molt, or definitive-cycle basic (DCB). including
(hose undergoing (lie third or later prebasic molt.
Individuals in breeding condition were assigned
as male by the presence of cloacal protuberance or
female by presence of a brood patch (Pyle 1997.
Radley et al. 2011).
The presence or absence of symmetrical flight-
feather molt was recorded for all birds captured.
Both wings were scored for most captures to
confirm sequence and assess symmetry between
wings. We categorized individuals based on moll-
score patterns (using the strategies ot Rohwer
2008) as either showing distal sequential molt
from P 1 (primary- 1 group), showing molt centers
at P 2, P 3, P 3/4, or P 4 and both distal and
proximal replacement (primary 2-4 group), or
showing distal molt between P 5 and P 10
(primary 5-10 group). A center at P 3/4 was
assigned when these two growing primaries were
equal in length, indicating molt had commenced
with both feathers at about the same time.
Replacement of primaries 1-3 can be rapid and
close to synchronous in passerines (Pyle 1997),
and wc were careful to ensure that P 1 was fresher
than P 2 (and thus replaced earlier) in those
categorized into the primary- 1 group and in which
both of these primaries were fully grown. We did
not identify commencement point among prima¬
ries 1 to 4 in the primary 5-10 group and these
birds are not considered further.
RESULTS
We captured 1.086 Rufous Fantails a combined
1,728 times during 2009 and 2010; 306 individ¬
uals were captured a combined 448 times when
primaries were molting, and we scored primaries
for 343 captures. Molt center and sequence among
primaries i-4 were categorized during 174 molt
episodes for 166 birds (8 birds were scored twice
during prebasic molt episodes in both 2009 and
2010). All documented molt sequences were
symmetrical between wings within one full-grown
feather, and no birds had varying molt centers on
different wings.
Sequential replacement from P 1 was recorded
lor 108 ot 174 molt episodes (62%) and a center
among primaries 2-1 from which molt proceeded
bi-directionally was recorded for the remaining 66
(38%) episodes (Tables 1, 2; Fig. 1). Most birds
in the primary 2-4 group (77%) initiated molt at
primary 3 (Table 1). and the distribution among
centers (including 3% at P 2. 12% at P 3/4. and
8% at P 4) was normal (Kolmogorov-Smimov test
for normality: D = 0.042. P > 0.15). The mean
starting point within this group was 3.1 1. or just
684
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 4. December 2012
TABLE 2. Examples of feather scores for primary molt sequence of Rufous Fantails based on individuals captured on
Saipan in 2009 and 2010 (following Rohwer 2008). Two examples of each primary center are shown. Numeric values
represent proportion of feather growth: notations are Nodal (N.) and Terminal (T). and arrows above notations indicate
sequence direction.
Primary center
Primary
i
2
3
4
5
6
7
8
9
10
1
(N)0.3
—*0.2
-*0.l
OLD
OLD
OLD
OLD
OLD
OLD
OLD
1
(N)NEW
-*0.7
—*0.4
-*0.1
OLD
OLD
OLD
OLD
OLD
OLD
2
T*— 0.6
(N)NEW
OLD
OLD
OLD
OLD
OLD
OLD
OLD
OLD
2
T<— 0.2
(N)0.6
OLD
OLD
OLD
OLD
OLD
OLD
OLD
OLD
3
T«M).l
*—0.7
(N)0.8
—*0.6
-*0.1
OLD
OLD
OLD
OLD
OLD
3
T<-0.3
*-0.1
(N)NEW
-*0.8
—»0.4
-»0.l
OLD
OLD
OLD
OLD
3/4
OLD
OLD
(N)0.2
(N)0.2
OLD
OLD
OLD
OLD
OLD
OLD
3/4
OLD
<—0.5
(N)0.8
(N)0.8
— *0.6
-»0.l
OLD
OLD
OLD
OLD
4
T<— 0.3
<—0.5
<-0.6
(N)0.7
-*0.4
-*0.1
OLD
OLD
OLD
OLD
4
T<— 0.1
<—0.3
<-0.7
(N)NEW
-*0.6
-^0.1
OLD
OLD
OLD
OLD
distal to P 3, when calculated according to
primary center number (P 3/4 scoring 3.5).
Younger (SCB) birds were more likely to
initiate primary molt among primaries 2-4 than
older (DCB) birds with a mean starting point of
2.01 versus 1.54 for older birds (ANOVA, C2,m
= 4.03, P — 0.019). Females (mean starting point
2.22) were more likely to initiate primary molt at
primaries 2-4 than males (mean starting point
1 .48: F2, 54 = 8.30, P = 0.006; Table 1 ). Mean (±
SE) wing chord among 3 1 males of our sample
was 67. 1 ± 1 ,41 mm and mean wing chord among
22 females was 63.9 ± 1 .73 mm (FXM = 57.32. P
- 0.000). Mean mass among 29 males was 8.4 ±
0.43 g and moan mass among 22 females was 7.9
± 0.37 g. (F )i49 = 14.44, P = 0.000). Wing chord
was also significantly longer among 81 DCB birds
(65.9 ± 1.96 mm) than among 62 SCB birds (64.7
± 2.42 mm; mo = 5,62. P - 0.004), but mass
did not differ with age among 79 DCB (8.1 +
0.47 g) and 62 SCB (8.0 + 0.45 g) birds (FU40 =
1.55, P = 0.216). The effects of age ( P = 0.052)
distal, y from P <7»neLs„ Wmaries^numb
FIG. 2. Number of individual Rufous Fantails captured on Saipan showing centers at P I (bar stippling) and primaries
2-4 (bar hatching), and proportion of individuals with centers at primary 2-4 (line) by month during February to
August 2009-2010.
and gender (P = 0.038) remained significant or
nearly so, but the effects of wing chord ( P =
0.170) and mass (P = 0.828) were not significant
when analyzed using multiple ANOVA (/A47).
The within-month proportion of individuals
captured in February to August that exhibited a
center among primaries 2-4 varied from 20 to
47% with little evident seasonality (Fig. 2). Six ol
eight birds captured during separate prcbasic molt
episodes had the typical sequence from P I during
both episodes, one DCB female had a center at P 1
in 2009 and a center at P 4 in 2010. and one SCB
female had a center at P I in 2009 and a center at
P 3 in 2010; these two individuals represented
exceptions to the age-specific pattern.
DISCUSSION
Multiple molt centers or series among primaries
are poorly documented in passerines and our
results indicating a center at primaries 2. 3, or 4
for some Rufous Fantails provides the first
evidence for multiple molt scries in the Rhipidur-
idae (Higgins et al. 2006). The only North
American passerine with an atypical primary molt
sequence may be the American Dipper, where
primaries 2-6 may drop simultaneously before P
1. an adaptation enabling rapid molt and resulting
in brief flightlessncss (Sullivan 1965). This should
be confirmed, however, because the well-studied
White-throated Dipper ( Cinclus cinclus ) report¬
edly molts rapidly, but in typical sequence from P
I (Cramp 1988).
The distribution of molt centers among the
primary 2-4 group of Rufous Fantails with only
3% initiating molt at P 2 and the remainder
showing a normal distribution, suggests this group
exhibits a different mechanism affecting replace¬
ment sequence from the primary- 1 group, rather
than the center simply drifting among P 1 and P 4.
The mechanism affecting center resulted in an
average initiation point just distal to P 3 among
our sample of individuals with medial molt
centers. Some individuals appeared to have
molted primaries 3 and 4 at or near the same
time, suggesting the molt center may not be fixed
at an individual primary, but can occur between
two primaries or along a defined area along the
alar tract. Fluidity in both molt commencement
point and directionality has not been fully
documented to our knowledge, although it appears
to occur in Savi’s Warblers ( Locustellu lusci-
"iodes ; Jenni and Winkler 1994). Passerines with
eccentric preformative molts among primaries can
vary their center of initiation but distal sequence
is maintained (Pyle 1997).
Mechanisms affecting molt strategies in birds
remain poorly known due to complex interactions
between physiological, environmental, and genet-
686
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 4. December 2012
ic factors (Payne 1972); remigial molt sequence
may be based on either neurophysiological events
(Voitkevich 1966, Rohwer et al. 2011) or an
endocrinological mechanism (Miller 1941. Bridge
2011). That two Rufous Fantails in our study
switched front a center at P 1 during one molt
episode to a center at P ? or P 4 during the next
episode suggests the sequence may be phenotyp¬
ical ly plastic and adaptive based on environmental
as well as genetic factors.
Regular molt centers other than P 1 have been
documented among Eurasian passerines, most
thoroughly for Brown Shrikes ( Lanins cristatus;
Stresemann and Stresemann 1971, Cramp and
Perrins 1993) and Savi's Warblers (Thomas 1977.
Cramp 1992. Neto and Gosler 2006); a few other
individual cases in other passerine species have
been reported (Jenni and Winkler 1994. Thomp¬
son and Kilaysky 2004). possibly representing
anomalies or based on injuries. Most Brown
Shrikes appear to have a center between primaries
4 and 3 (molt proceeding both distally and
proximally), but some have either a single or a
second center at primary I. Other Lanins shrikes
appear to have a normal distal sequence from P I
in all individuals (Cramp and Perrins 1993).
Commencement of primary replacement can be
variable in Savi's Warblers with some birds
having a distal sequence from P I and others
appearing to have centers among primaries 2 and
6; birds initiating the prebasic molt at P I tended
to commence molt earlier than those initiating
molt among primaries 2-6 (Neto and Gosler
2006).
Rutous Fantails with molt centers among
primaries 2-4 showed no apparent seasonal pattern
within our capture periods (Feb-Aug). However, a
complete assessment of seasonality would have to
account for annual breeding phenology (which
appears to vary between years; P. Radley and J. F.
Saracco. pers. comm.) as well as age and gender
variation m timing of molt; we Currently lack the
data to address this question. The greater proportion
of younger (SCB) and female Rufous Fantails with
a medial molt center compared to older birds and
males suggests they may have a selective advantage
in foraging that affects the molt commencement
point. Neto and Gosler (2006) did not separate
younger from older individuals in their study
s,milar age-specificity suggesting slower or later
molts in younger birds could indirectly explain the
tendency for medial molt centers to occur with
later-molting Savi's Warblers.
Multiple series in larger birds, constrained from
replacing all primaries in a single molting season,
allows more feathers to be replaced in a shorter
period without creating large gaps in the wing,
thereby maintaining wing-surface integrity and
greater ability to fly and forage (Tucker 1991.
Hedenslrom and Sunada 1999, Rohwer 1999. Pyle
2005). Our results suggest a center among
primaries 2-4 in younger and female Rufous
Fantails may have evolved as an alternate strateg)
in groups with a selective foraging disadvantage to
enable them to replace more primaries more
rapidly while maintaining better foraging ability.
However, direct correlation with wing loading
(mass and wing chord) was not evident in our study
alter controlling for effects of age and gender.
It may be advantageous for younger and female
fantails to have multiple molt series iT they are
under greater time or energetic constraints due to
poorer foraging ability or greater breeding con¬
straints. respectively. Female passerines may
initiate molt later than males on average because
males abandon their broods and mates in favor of
early molting (Svensson and Nilsson 1997,
Hemborg and Merila 1998); this could result in
the need for more rapid molting in breeding
lemale tantails, perhaps varying regularly on an
inter-annual basis. Rapid molt may be unusual in
tropical climates, where time constraints arc less
severe than in temperate climates (Ryder and
Wolfe 2009). Our results suggest an adaptation for
rapid replacement in some short-winged passer¬
ines that rely on flight to forage for aerial insects,
such as Rufous Fantails (Higgins et al. 2006).
Molt sequence among inner primaries is
difficult to document unless specifically looked
loi because molt among inner primaries is rapid
and few specimens have been collected at this
stage (Pyle 1997). It is possible multiple series
may occur more often than suspected among
passerines. Molt sequence is especially poorly
documented in tropical passerines (Rvder and
Wolfe 2009), and discovery of additional tropical
passerines with multiple molt series may shed
further light on the evolution and adaptation of
this strategy. We encourage further study to
document molt sequence among inner primaries
ol passerines, and to investigate evolutionary’
causes for variation within and among species.
ACKNOWLEDGMENTS
thank Paul Radley for providing funding and
immense logistical support for the TMAPS stations on
Junda et at. • RUFOUS FANTAIL PRIMARY MOLT
687
Saipan as well as editorial comments, and James F. Saracco
for overseeing protocols and data collection. We thank
James Bradley. Christine Carter. Nathan Banficld. Lauren
Helton. Caroline Poli, and Daniel Webb for collecting data
at the TMAPS stations relative to this study. Wc also thank
Karen Nassi for keeping the process moving, and Seivert
Rohwer and three anonymous reviewers for comments on
the manuscript. This is Contribution Number 3% of The
Institute for Bird Populations.
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The Wilson Journal of Ornithology 124(4):688-697, 2012
WINTER SONGS REVEAL GEOGRAPHIC ORIGIN OF THREE
MIGRATORY SEEDEATERS (SPOROPHILA SPP.) IN SOUTHERN
NEOTROPICAL GRASSLANDS
JUAN IGNACIO ARETA1
ABS TRACT.— The winter distribution of neotropical seedeaters (Sporophila spp.) known as capuchinos is pooriv
known. 1 here are cl.ff.cult.es to understanding their migration patterns: fieldwork is lacking in their wintering areas, their
eclipse plumages often make it difncul. to identify species, different spcc.es share habitats during winter, and there is little
or no genetic dtfferent.at.on of several forms. Vocalizations display a geographic signature ,i.c„ diagnostic acoustic
matures that arc found in a limited area during the breeding period) and can he useful as indicators of a specific geographic
ongm ot » wmitaing bird I prevent data that: III dcmiinvlialcs Thai iKin-breedinj male Dark-lhroalcd Sealcalcr is
ruficolhs). Rufnus-rumpad Seedeater (.V. hyiwchroma), and Tawny -he! lied Seedeater IS. h\poxunlha) in iMnlerine areas ran
be assigned to a particular distant breeding populwion based on vocalisations: (2) evaluate the potential conlribinion of
m er tuiTo u'V" “f *- *«* "'feato* btovenienls: and (31 use vocal, aanons 10 uflml
Cerado 1 V n,fic""ls fmm Hmre «°» regiolecl wen: iKoried in
r , *•**""• ™C' Bwil f the Beni savannas close to Trinidad. Bolivia. 5.
E«m R oIT. J, r "rf' wm Vila Bcl'' <*» Sann'ssima Trindude. and S. hypoxaMm from
loZn „ , r , " ,r” T ‘ OSe 10 ’***•«■ Li"“"» hrmli"e «l non-breeding areuv .hrough song-types is
7. TZfyZI. “**' “"J “ Prom”tt — "f — "">■ '""distance Vs- *&-
Stem-gleaner specialists are birds that feet
upon seeds still borne on the stalks of natura
grasses. Many of these species engage in short tc
long-distance seasonal migrations in response t<
temporal fluctuations in their food supply (Rem-
sen and Hunn 1979. Silva 1999). One group of
stem-gleaner specialists is the capuchinos, a
distinctive subgroup of the genus Sporophila.
This group is presently composed of 1 1 species:
Dark-throated Seedeater (S. ruftcollis ), Rufous-
rumped Seedeater (S. hypochroma ), Chestnut
Seedeater ( S . cinnamomea). Marsh Seedeater (.S'.
palustris), Tawny-bellied Seedeater (S. hypax-
antha), Black-and-tawny Seedeater [S. nigrorufa ),
Copper Seedeater (S. houvreuif), Pearly-bellied
Seedeater (5. pileata ), Ruddy-breasted Seedeater
(S. minuta). Chestnut-bellied Seedeater (5. cast a-
neiventris ). and Black-bellied Seedeater (S. me-
lanogaster) (Sick 1997; Lijtmaer el al. 2004-
Areta 2008. 2010; Machado and Silveira 201 1 ). *
Capuchinos are conspicuous members of di¬
verse neotropical grassland communities during
the breeding season. Some species are known to
m.gratefrom then breeding areas in winter, but
remarkably little is known about their distribution
migration ecology, and wintering areas (Ridgely
and Tudor 1989, Chesser 1994).
. pCICyJTP— CC)NICET’ Ma,eri y EspafSa, 3105, Diamati
te, Entre Rios. Argent.na; e-mail: esporofiIa@yahoo.com.ai
Many species of capuchinos gather in mixed-
specics (locks during migration to and from
breeding areas. These seasonal movements were
outlined by Silva (1999), who proposed that after
breeding in the grasslands of central Bolivia,
northern Argentina, Uruguay, eastern Paraguay,
and southeast Brazil they migrate to their main
wintering area; the Cerrado region. S. ruftcollis, S.
hypochroma . and .S’, hypoxantha at the local scale
were found mostly in spring in Concepcion,
Bolivia, and were considered transient long¬
distance migrants (Davis 1993). Similarly. S.
ruftcollis was (ound to be a complete migrant, 5.
hypochroma suggested to be a medium-distance
migrant, and S. hypoxantha to be a short-distance
migrant during the winter in the San Joaquin area.
Bolivia (Mitchell 1997). Wintering records of 5.
cinnamomea and S. palustris suggest they do not
venture into central Bolivia and western Mato
Grosso (Ridgely and Tudor 1989). but gather in
large (locks with other species including S.
hypoxantha . S. melanogaster. S. ruftcollis. S.
bouvreuil. S. castaneiventris , S caentlescens. S.
nigricollis , and S. alhogularis during mid Sep¬
tember in Minas Gerais, Brazil (Sick 1997). S.
ruftcollis, S. hypochroma. S. cinnamomea. and 5.
palustris are encountered only in migratory
passage in eastern Formosa. Argentina to and
• orn more southern breeding areas in eastern
Argentina, Uruguay, and southeastern Brazil
(Ridgely and Tudor 1989. Di Giacomo 2005).
Areta • SONG AND MIGRATION IN SEEDEATERS
689
At least two species have migratory and resident
populations: the population of S. hypoxantha of
eastern Formosa is resident with birds gathering in
wintering flocks and wandering over local grass¬
lands (Di Giacomo 2005 k and a presumably
resident population of S. ruficollis inhabits the
Alto Madidi Savannas (Areta et al. 201 1). These
data show the existence of complex spatial and
temporal associations of several species. For
example, some species migrate together in
mixed-species flocks, but later breed in close
proximity but in different habitats, and finally
take divergent migration routes to their non¬
breeding areas. The mechanisms and patterns
behind this bewildering complexity have yet to be
unraveled.
Three main reasons account for the scant
knowledge of migration of capuchinos. First,
sampling effort has been low in the relevant areas
(Silva 1999). Second, it can be difficult to reliably
identify capuchinos to species based on plumages
during winter (Pcarce-Higgins 1996, Sick 1997.
Areta 2009. Kirwan and Areta 2009). Third, the
birds are too small to follow with tracking devices.
Movements between breeding and non-breed¬
ing areas are unknown for any individual of the
migrant populations of capuchinos. Use of
vocalizations seems a potentially powerful way
to uncover the details of their migration patterns
given the lack of genetic differentiation reported
to date (Lijtmaer et al. 2004, Campagna el al.
2011). and the diagnostic differences in their
voices (Areta 2008, Areta and Repenning 2011,
Areta el al. 201 1).
Vocalizations have been used successfully to
reconstruct the migratory trajectory of some birds,
but this approach has seldom been used in the
Neotropics (Dowsett-Lemaire 1979; see Chu
2001. Marler and Slabbekoorn 2004: 129).
Schwartz (1975), in a unique study of the
Sporophila, demonstrated the existence of two
divergent migratory routes and breeding areas ol
Lined Seedealers (.S', lineula) based on their
vocalizations. This method allowed for a more
precise delineation of the migration routes of 5.
lineola (Silva 1994. Neto and Vasconcelos 2007);
it was later proposed that further work with
vocalizations of .S', lineola might show the
existence of other geographical variants (Areta
and Almiron 2009).
My objectives are to: (1) present data that
demonstrates that non-breeding male S. ruficollis,
S. hypochroma , and S. hypoxantha in wintering
areas can be assigned to a particular distant
breeding population based on their vocalizations,
(2) evaluate the potential contribution of vocal
variation in other capuchinos to understand their
migratory movements, and (3) use vocalizations
to unravel migration patterns in capuchinos.
METHODS
I recorded vocalizations of all species using
different microphones (audioTechnica 815b.
Sennheiser ME-67 protected with a Rycote 6 Kit
| shock-mount, windshield, and windjammer],
Sennheiser ME-62 mounted on a Telinga Univer¬
sal Parabola or on a 60-cm parabola), and tape
recorders (Marantz PMD-222. PMD-661, and
Sony TC-D5M). Spectrograms were prepared
using Syrinx 2.1 (John Burt, www.syrinxpc.
com). Additional recordings were provided by
other investigators (Appendices 1. 2). All record¬
ings by JIA are archived at the Macaulay Library
of Natural Sounds (MLNS, Cornell Laboratory of
Ornithology. Ithaca. NY. USA). The comparative
data set for this study consists of recordings of the
vocalizations of 348 individuals of all species of
capuchinos from 49 localities (Fig. 1; Appendices
I. 2; Areta 2008, 2010; Areta and Repenning
2011; Areta et al. 2011).
Songs of capuchinos include many different,
non-repetitive, and morphologically complex
notes. 1 characterized notes which, based on shape
(including duration and frequency distribution)
and relative position in the songs, could be
identified unambiguously despite variation among
individuals. The frequency of occurrence of these
notes in individuals was compared within and
among populations. The analysis was limited to
sexually mature males, identified based on the
possession of fully adult plumages. Only male
capuchinos arc known to sing regularly, while the
repertoire of females usually consists of high-
pitched notes (Areta 2008; JIA, unpubl. data).
Males of three species of capuchinos. S. ruficollis ,
5. hypochroma, and S. hypoxantha sing different
songs depending on where they breed, and
different macrogeographic song variants or re-
giolects ("song variants encompassing extensive
subpopulations of a species and all individuals
within this large range’' Martens 1 1996:221 1)
have been defined based on the presence of
diagnostic notes in their vocalizations. The known
song types of 5. ruficollis have been separated
into; (1) Mesopotamia (Argentina), and (2) Apolo
Madidi Savannas (Bolivia) regiolects (Fig. I A;
690
THE WILSON JOURNAL OF ORNITHOLOGY • Vo/. 124, No. 4. December 2012
Areta • SONG AND MIGRATION IN SF.EDEATHRS
691
0 250 500 1.000 i.500 2.000
brackets indicate recording localities. Bold numbers indicate recording locality of shown spectrogram. Shaded areas indicate
approximate limits of regiolccts ( precise localities in Appendices 1 . 2). Gray circles indicate sampling localities of vocalizations
for all species of capuchinos in southern South America. Black circles indicate localities where song-types recorded durine the
breeding season match those recorded during the non-breeding season. Dark squares indicate localities where song-types
recorded during the non-breeding season match those recorded during the breeding season.
40°0’0"S
692
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 4. December 2012
60 ww 50WW 40ww
FIGURE I. Continued.
Areta • SONG AND MIGRATION IN SEEDEATERS
693
Areta et al. 2011). Songs of S. hypochroma have
been separated into: (1) Corrientes (eastern popu¬
lations. Argentina), and (2) Bolivia (western
populations. Bolivia) regiolects (Fig. IB; Areta
2010). Songs of S. hypoxantha have been separated
into: (1) Entre Rios (Argentina). (2) Corrientes
(Argentina), (3) Formosa (Argentina). (4) south¬
east Brazil (Brazil), and (5) Bolivia (Bolivia)
regiolects (Fig. 1C: Areta and Repenning 201 1).
Vocalizations display a geographic signature
(i.e.. diagnostic acoustic features that are found in
a limited area during the breeding period) and
could be useful as indicators of a specific
geographic origin. I investigated the correspon¬
dence between songs recorded during the breed¬
ing season in known breeding areas and songs
recorded outside the breeding season in presumed
wintering areas of S. nificollis. S. hypochroma,
and S. hypoxantha.
RESULTS
Dark-throated Seedeater (.S', nificollis). — I tape
recorded a mixed-species Hock in the Beni
savannas on 26 October 2006, close to the city
of Trinidad (64 54' W. 14 50' S). Beni, Bolivia.
1 visually identified adult males of .S', nificollis , S.
hypoxantha. and S. hypochroma as part of the
flock which had —200 Spomphila individuals. I
found songs identical to that of 5. nificollis.
belonging to an undetermined number of birds. I
tape recorded a male on 16 June 2008 in the
seasonally inundated cerrado of the Campos do
Encanto (59 48' W. 15 03' S), close to Vila Bela
da Santissima Trindade, Mato Grosso, Brazil. The
bird was heard singing and was immediately
identified as S. nificollis. I observed the singing
male after the tape-recording. It had a yellow base
to the lower mandible, light brownish-gray back,
gray cap. light creamy-rufous belly, and had a few
dark-brown feathers in the throat, making it
identifiable to species based on plumage. The
voice-type of both recordings is known to exist in
males breeding in Entre Rios. Santa Fe. Buenos
Aires (Argentina), Paysandu (Uruguay), and Rio
Grande do Sul (Brazil). The minimum distances
between wintering localities and the breeding area
is — 1 .800 km (Vila Bela-Paysandu) or 2,300 km
(Vila Bela-Saladillo) (Fig. I A).
Rufous-rumped Seedeater (S. hypochroma). — I
tape recorded a male on 16 June 2008 in the
seasonally inundated cerrado of the Campos do
Encanto, close to Vila Bela da Santissima
Trindade, Mato Grosso, Brazil. The bird was
heard singing and was immediately identified as
S. hypochroma. 1 observed the singing male after
tape-recording and it only displayed a few
somewhat lighl-orangish feathers on the otherwise
creamy throat. The belly had a few light-orangish
feathers, and the back and cap were light-brown.
This male was not possible to identify to species
based on plumage features. This voice-type is
known from males breeding in Corrientes and
Santa Fe (Argentina). The minimum distances
between the wintering locality and the breeding
area is —1,500 km (Vila Bela-Esteros del Ibera)
or 1.700 km (Vila Bela-Campo del Medio)
(Fig. IB).
Tawny-bellied Seedeater (S. hypoxantha). — I
tape recorded a male in the Beni savannas on 26
October 2007. close to the city of Trinidad (64
54' W. 14 50' S). Beni. Bolivia. The bird was
heard singing and was immediately identified as
.S', hypoxantha. The bird could not be seen while
singing as it was hidden amid vegetation. Three
birds were Hushed from the precise spot where the
bird appeared to be singing. At least one was S.
hypoxantha, but it did not show any diagnostic
plumage feature. This voice-type is known
exclusively from Entre Rios (Argentina), although
presumably transient individuals were also re¬
corded at a locality in Santa Fe (Argentina). The
minimum distance between the wintering locality
and the breeding area is —2,150 km (Trinidad-
Gualeguaychu) (Fig. 1C).
DISCUSSION
The large geographic area over which capuchi-
nos are distributed during the non-breeding
season, acquisition of confusing ‘eclipse’ plum¬
ages, sharing of habitats among species during
w inter, and lack of, or scant genetic differentiation
of several forms pose difficulties to understanding
their migration patterns within South America.
Vocalizations can partly overcome these difficul¬
ties, and reveal important biogeographic and
ecological relationships between distant breeding
and non-breeding areas for S. nificollis , S.
hypochroma . and 5. hypoxantha (Fig. 1). Sample
sizes of recordings of wintering birds are small,
but geographic coverage and sample sizes of
breeding birds are satisfactory: thus, the migration
patterns uncovered are unequivocally supported
by my data.
The Cerrado region and the upland Amazonian
savanas ot Humaita (Brazil) were recognized as
two important wintering areas for S. nificollis
694
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124. No. 4. December 2012
(Silva 1999). S. ruficollis overwintering in the
Cerrado region arc, at least in part, from the
southern and easternmost breeding areas in Entre
Rios, Santa Fc. Buenos Aires. Paysandu, and/or
Rio Grande do Sul. However, there is no evidence
suggesting where birds wintering in Humaita
breed. The wintering populations of S. ruficollis
in the cerrado of central Bolivia are completely
migratory (Davis 1993. Mitchell 1997). and the
source of these populations remains unknown.
The main wintering areas identified for S.
hypochroma are the Cerrado region and central
Brazil (Silva 1999). Populations from Corrientes
(to which 1 add Santa F6) that Short (1969)
attributed to S. hypochroma seem to overwinter in
the Cerrado of eastern Brazil, but precise evidence
of the source populations of birds in central Brazil
is lacking. The western populations of S. hypo-
chroma have been considered mid-distance north¬
ward austral migrants during winter (Mitchell
1997). At least two populations with distinct vocal
types are involved within S. hypochroma as
currently delineated (JIA, unpubl. data). Further
recordings of S. hypochroma should prove
rewarding to elucidate both the systematics and
the migration of this poorly known species.
The Cerrado region is also considered an
important wintering area for S. hypoxantha (Silva
1999). Possible short- and long-distance migrant
populations of 5. hypoxantha might coexist in the
Cerrado during winter. This seems to be the case
in the Trinidad grasslands where presumably
resident or short-distance migrants from the
lowland Bolivia regiolect co-occur together with
long-distance migrants from the Entre Rios
regiolect. The overall seasonal patterns of S
ruficollis, S. hypochroma. and S. hypoxantha ii
Concepcion (Bolivia; Davis 1993) were interpret
ed as consistent with different migratory move
ments; "long-distance temperate-tropical migra
tion, intraregional migration, local wandering o
several of these categories applied to the saim
individuals or populations over several years'
(Joseph 1996:190). My vocal data support the
long-distance migration hypothesis for .S’ hypo¬
xantha in Trinidad, and for .S. hypochroma anc
5. ruficollis in Vila Bela. Neither my data, no.
previously published studies (Ridgely and Tudoi
1989, Davis 1993, Pearce- Higgins 1996. Mitchell
1997, Silva 1999) support Short’s (1973) claim
that 5. hypoxantha (including .S', ruficollis and 5.
palustns) and .S’, hypochroma are non-migratory at
a wide scale. The general pattern suggests at least
some populations of these species migrate long
distances, but some resident local populations
may remain at or close to their breeding areas in
wintering flocks.
The lack of geographic variation in vocalizations
of S. cintuunomea and S. palustris (Areta 2008)
suggest that, whereas voices can aid in identifica¬
tion of wintering males, they cannot be used to
identify the origin of individuals of these species.
The locally-breeding 5. nigronrfa and S. niela/w-
gaster have little or no geographic variation in
song-types (Areta 201 0; Repcnning et al. 2010; JIA.
unpubl. data). Geographic variation in vocalizations
of populations of S. houvreuil and S. pileata could
provide useful guidance to allocate wintering birds
to a specific breeding area (Areta 2010; Machado
and Silveira 2010; JIA. unpubl. data).
Vocalizations have three advantages that make
them promising tools to unravel the migration
patterns of capuchinos. First, they can he detected,
recorded, and identified from a fairly longdistance,
partially overcoming the problems associated with
surveying a large wintering area. Second, they do
not vary seasonally for sexually mature males.
Third, they are geographically structured for some
species (Areta and Repenning 2011, Areta et al.
2011). In contrast, plumage traits vary seasonally
and seem lairly uniform over the geographic range
of the species. Vocalizations may prove to be a
uselul tool to uncover migration patterns of
capuchinos. Future migration, biogeographic, eco¬
logical. evolutionary, and conservation studies of
seedeaters will benefit enormously from this source
of information.
ACKNOWLEDGMENTS
I am most grulelul to all who made possible my field"
work outside Argentina: Sebastian Herzog and Bennett
Hennessey in Bolivia, L. F. Silveira. Vitor Piacentim. Erika
Machado. Marcelo Pena Padua. G. N. Maurfcto, C S.
Fontana, and Marvin Repenning in Brazil, and Joaquin
A Idaho in L ruguay. Heman Povedano. Leticia Haudemand,
Violcta Gomez Serrano. Guadalupe Garriz, Joaquin Areia.
Diego Isaldo, Enrique Carnba, Bemabe Lopez Lamb, Jorge
Noriega, Roscndo Fragu. Marcio Repenning. Marcelo Pena
Padua. L. F. Silveira, Vitor Piacentini. Erika Machado, and
Ingrid Hol/mann are thanked for sharing fieldwork.
Agradczeo muy especial mente a Luis Pagano por compartir
el arcnal. la ciudad dc las mujeres de Zitairosa y los
gavilanes bidbn. y a J. Noriega por su apoyo consume
durante las csporofilcadas. Comments by K L. Cockle
greatly improved a previous version of the manuscript.
Fieldwork in Mato Grosso (Brazil) was possible (hanks to
funding from the Frangoise Vuilleumier Fund (Neotropical
Ornithological Society).
Areta • SONG AND MIGRATION IN SEEDEATERS
695
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696
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 4. December 2012
APPENDIX 1. Recording localities that corre¬
spond to numbers in Table 1.
ARGENTINA. Buenos Aires. I-Saladillo (59
56' W. 35 30' S). Entre Rios. 2-Ibicuy (59 09’
W, 33 44' S), 3-Arroyo Nancay (58 44' W, 33
23' S), 4-Estancia La Marita (58 35' W, 33 20'
S), 5-Gualeguaychu (58 : 30' W, 33" 00' S). 6-Las
Piedras (58" 33' W, 32° 53' S). 7-Larroque (59
00' W. 33 : 02' S), 8-Urdinarrain (58 53' W, 32
41 ' S), 9-Puerto Liebig and Arroyo Caraballo (58
1 1' W. 32 09' S), I0-PN El Palmar (58 18' W,
31° 55' S). II -Arroyo Barn (58 27’ W, 31 52'
S), 12-San Salvador (58 30' W, 31 37’ S). Santa
Fe. 13-Sauce Viejo (60 50' W, 3D 46' S), 14-
Campo del Medio (60 08' W, 31 08' S).
Cordoba. 15-Laguna Mar Chiquita (62r 43' W.
30 57' S). Corrientes. I6-Mercedes (58 05' W.
29 10 S), I7-Eslancia Rincon del Socorro (57
10' W, 28 32' S), 18-Colonia Pellegrini (57 10'
W. 28° 35' S), 1 9-Cam ba Trapo (56° 51' W, 28
27' S), 20-Cuenca del Rio Aguapey (56 56' W.
28 36' S), 21- Estancia San Juan Poriahu (57 1 1 '
W, 27 42' S)/PN Mburticuyi (58‘ 05' W, 28' 00'
S), 22-Rincon Santa Marfa (56 ' 35' W, 27' 30' S).
Formosa. 23-Estancia F.I Bagual (58 56' W. 26
10 S). URUGUAY. Rocha. 24-Laguna Negra
(53° 40' W. 34 00' S), 25-Banados de la India
Muerta (53 50' W, 33" 45' S), 26-Cebollatf (53
38' W, 33 15' S). Paysandu. 27-Lorenzo
Geyres-Quebracho (57 55' W, 32 04' S), 28-
Queguayar (57 50' W, 32 00' S). BOLIVIA.
Santa Cruz. 29-Lomas de Arena (63 10' W. 17
56' S), 30-Pampas de Viru-Viru (63 08' W. 17°
39' S). Beni. 3 1 -Trinidad-Mamore (64 54' W,
14 50 S). BRAZIL. Parana. 32-Faz Chapadao-
Rio das Perdizes (49 51' W. 24 17' S). Santa
Catarina. 33-Coxilha Rica (50 15' W. 28 18'
S), 34-Estancia do Meio (50" 15' W. 28 18' S).
35-Rio Sao Mateus (50 13' W. 28 21' S). 36-
Pedra Branca (50 02' W, 27 55' S). 37-Sao
Joaquim/Lages (49 55' W, 28° 17' S). Rio
Grande do Sul. 38-Capao Alto (50 58' W. 28
12' S), 39-Sao Pedro (50 56' W. 28 13’ S) 40-
Capao Bonito (51 16' W. 28 04' S), 41-Antma
Esta^ao Ferrea-Bom Jesus (50 44' W, 28 19' S)
42-Fazenda Socorro/Rio Santana (50 48' W. 28
22 S), 43-Cachoeira dos Baggio (50 28' W. 28
40' S). 44-Guaeho (51 05' W, 28 40' S) 45-
Distrito Areal-Quaraf (56 23' w’ 30" 26' S). Mato
Grosso. 46-Campos do Encanto-Vila Bela da
Santfssima Trindade (59 48' W, 15 03' S). Sao
Paulo. 47-Mogi das Cruzes (46° 07' W, 23" 33' S)
48-Estagao Ecologica Itirapina (47 55' W. 22 12'
S). Bahia. 49-Boa Nova (405 13' W, 14° 21' S).
APPENDIX 2. Recordings analyzed in this
study. Number in square brackets denotes number
of individuals and number in parentheses indi¬
cates reference number in the data base. All
recordings by .11 A except those indicated by AJ =
Alvaro Jaramillo. BH = Bennet Hennesey. BO =
Brian O'Shea, CD = Charles Duncan. CM =
Curtis Marantz, I)M - Diego Monteleone. EVI =
Eugene Morton, F.) = Fernando Jacobs, FS =
Fabio Silva. HR = Heimz Remold. LD = L.
Davis, MR = Marcio Repenning. MP - Mark
Pearman. PAS = Paul Schwartz. RF = Rosendo
Fraga, SD = Susan Davis, SM — Sjoerd Maijer,
TP = Ted Parker 111. and QV = QuillenVidoz.
S. casta neiventris [2]. BRAZIL. Bajo Rio
Uaipas. Amazonas [1| (CMI: MLNS-1 13196-
113197), Careiro do Castanho. Amazonas |I]
(CM2: MLNS- 1 27641).
S. melanogaster [12]. BRAZIL. 2007-2009:
Pedras Brancas 1 1 1 ( I ). Sao Joaquim/Lages
1 1 1 (2), Coxilha Rica [6J (4-9), Bom Jesus |1]
(3), Fazenda Socorro HJ (10). 1979-1982: Sao
Francisco de Paula |2] (FSIl: MLNS-25401,
TP 1 2: MLNS-32 160-321 61).
S. ‘ xttmanxti ' [4]. BRAZIL. Coxilha Rica ID
(MR1), Estancia do Meio [l| (MR2), Bom
Jesus [If (MR3). Rio Santana [I] ( MR4).
S. mi nut a [23]. VENEZUELA. Caracas [19|
(PAS 1-19: MLNS- 1 5470- 15484, 15486-
1 5489), Santa Elena de Guairen [I] (CD1:
MLNS-1 10188). GUYANA. Rio Corantyne [1]
(BOl: MENS- 134808). MEXICO. Chuhuites
IIJ (LDI: MLNS- 15485). PANAMA. Toeu-
mun |1| (EMI: MLNS- 15490).
S. hypoxantha [103+]. ENTRE RIOS REGIO-
LEC1 [14|. ARGENTINA. Estancia La Mar¬
ita [ 1 3 1 (1-5. 7. 32-37), Campo del Medio [lj
(38). BOLIVIA. Trinidad (I) [631. FOR¬
MOSA REGIOLECT [19], ARGENTINA.
Estancia F.I Bagual [16] (43-58), Estancia La
Marita 1 1 ] (6), Campo del Medio [2] (39. 40).
CORRIENTES REGIOLECT [24]. ARGEN¬
TINA. Colonia Pellegrini (8. 9, 12-13. 17).
Camba Trapo [2] (10, 11). Mercedes (14-16.
28). Estancia Rincon del Socorro [14] (18-27.
29-31, 42). LOWLAND BOLIVIA REGIO¬
LECT. Trinidad [2+] (SM68-69. + several in
non-breeding mixed species Bocks). SOUTH¬
EAST BRASIL REGIOLECT [43]. BRAZIL.
Areta • SONG AND MIGRATION IN SEEDEATERS
697
1971: Guacho/Vacaria [3]. (PAS 123- 125:
MLNS 67596-67598). 2004-2009: Coxilha Rica
[23] (MR89-90. 93-95, 97, 99-105, 108-113,
118, 120-122), Estancia do Meio(4) [MR86.9I.
96. 98]. Fazenda Socorro/Rio Santana [3] (80,
82, MR88. 1 14), Lages [ 1 1 (MR64), Capao Alto
[3] (MR85, 115-117), Capao Bonito 1 1). Sao
Pedro [2] (MR84-85), Cachoeira dos Baggio 1 1 1
( 107). Rio Sao Mateus [ 1 1 (MR1 19). Guacho |2|
(MR87, 92). Fazenda Chapadao-Rio das Pcr-
dizes [1] (MR 106).
S. * Uruguay a ' [2]. CORR1ENTES RECIO-
LECT. Estancia Rincon del Socorro 1 1 1 (2).
SOUTHEAST BRAZIL REGIOLECT. Cox¬
ilha Rica [1| (MRI).
S. hypochroma [28], CORRIENTES REGIO¬
LECT [20], ARGENTINA. 1993: Esteros del
Tbera [AJI8-19], 2004-2008: Colonia Pelle¬
grini [6] (2-5, 7-8), Estancia Rincon del
Socorro [7J (9-15), Campo del Medio [2]
(16-17), Esteros del Ibera [2| (20-21). BRA¬
ZIL. 2004-2008. Vila Bela da Santissima
Trindade |l| (25). BOLIVIA REGIOLECT
[6]. BOLIVIA. Pampas de Viru-Viru |2|
(SD22, 29). Trinidad 1 1 1 (30). Lomas de Arena
[3 1 (QV26-28).
S. cinnamomea [24]. ARGENTINA. 1992-1993:
Mercedes [2] (AJ2I. AJ22), PN El Palmar 1 1 1
(MP23), Caza Pava-Corrientes |l| (MP24).
2003-2007: Estancia Rincon del Socorro |9]
(1-5, 7-10). Mercedes |l| (I). Colonia Pelle¬
grini 1 2) (11.12), Gualeguaychu Ml (13).
URUGUAY. 2003-2007: Lorenzo Geyres [5|
(14-18), San Javier-Rio Negro |1] (RFI9),
Villa Soriano-Rio Negro 1 1 1 (RF20).
S. ruficollis [83], ENTRE RIOS REGIOLECT
[79]. ARGENTINA. Arroyo Baru |8| (4-11),
Larroque-Urdinarrain 1 1 1 1 (20-27,38-40), San
Salvador |6| (12-17), Gualeguaychu 15] (33-
37), Estancia La Marita |4| (1,2.18.19). Puerto
Liebig and Arroyo Caraballo 1 1 1 (3), Sauce
Viejo [5] (28-32), Saladillo (10] (41-50).
BOLIVIA. Trinidad 1 1 ] (94). BRAZIL. Vila
Bela da Santissima Trindade [1] (92). URU¬
GUAY. Lorenzo Gcyres-Quebracho [261 (51—
76), Queguayar |2| (77,78). BOLIVIA RE¬
GIOLECT [41. BOLIVIA. Apolo-Madidi [4J
(BH88-91).
.S'. ‘ caraguata ’ [3]. ARGENTINA. Las Piedras
1 1 ] ( 1 ). Ibicuy 1 1 1 (2), Gualeguaychu 1 1 ] (3).
S. patustris [341. ARGENTINA. 1991-1993:
Mercedes |l| (AJ30), Gualeguaychu [2]
(MP32. MP34). Banco Caraballo-Entre Rios
1 1 ) (MP33). 2003-2007: Estancia La Marita [2]
(1.2), Colonia Pellegrini (2] (3.4), Estancia
Rincon del Socorro [1M (5-14, DM31),
Estancia Santa Isabel-Corrientes {1] (RF28),
Bahado Santa Rosa - Corrientes [1] (RF29).
URUGUAY. 2003-2007: Banados de la India
Mucrta [6] (15-20), Cebollau [7) (21-27).
S. ‘ zelichi ’ [31. ARGENTINA. 1992: Gualeguay¬
chu |l| (MP3). 2003-2007: Gualeguaychu [11
( 1 ), Estancia Rincon del Socorro 1 11 (2).
S. nigrorufa [9|. BOLIVIA. Flor d'Oro. PN Noel
Kempff Mercado (2| (SMI-2). BRAZIL. Vila
Bela da Santissima Trindade [71 [3-9].
S. bouvreuil [(>]. SAO PAULO REGIOLECT.
BRAZIL 14 1. Mogi das cruzes [1] (1),
Taia?upeba |3] (2-4). BAHIA REGIOLECT.
BRAZIL [21. Boa Nova [2] (5-6).
.S', pileata [13]. GUARANI REGIOLECT [2].
ARGENTINA. 2005: Campo San Juan 1 1) (6).
PARAGUAY. 2002: Estancia La Yegrena
(Itapua) |1! (RF1 1). CORRIENTES REGIO¬
LECT [6]. ARGENTINA. 1997: Estancia San
Juan Pori ah u [1] (RFI2). 2005-2007: Rincon
Santa Maria [5] ( 1—5). SAO PAULO REGIO¬
LECT. BRAZIL [51. 1999: Serra da Canastra
[3] (CM14: MLNS 1 1 3420- 1 1 3422, TP13:
MLNS-39143, HR16: MLNS-1 14653). 2007:
Esta?ao Ecologica Itirapina [4] (7-10).
The Wilson Journal of Ornithology 124(4):698-703, 2012
IDENTIFYING MIGRATORY PATHWAYS USED BY RUSTY
BLACKBIRDS BREEDING IN SOUTHCENTRAL ALASKA
JAMES A. JOHNSON,1 6 STEVEN M. MATSUOKA,1 DAVID F. TESSLER.2
RUSSELL GREENBERG,3 AND JAMES W. FOX4-5 6
ABSTRACT.— We placed light-level geolocators, on 17 Rusty Blackbirds < Euphagus carolinus) in 2009 to track their
migrations from nest sites near Anchorage, Alaska to wintering areas and back. We recaptured three of these birds in 2010
and found they departed breeding areas during the first hall of September, spent 72-84 days migrating to overwintenng
areas, but only 16-30 days on their northward migration to Alaska. Birds took similar Central Flyway routes on southward
and northward migrations, which were not previously described for this species. The birds used a series of stopover sites
across the prairie region from southern Saskatchewan to Iowa over a 4 to 5 week period on their southward migration to
wintering areas that spanned from South Dakota to northern Louisiana. We found upon recapture in 2010, the geolocator
attachment harnesses had abraded the surrounding feathers on all three birds. This coupled with the low return rate (18%)
lor instrumented birds indicates a better harness method must be developed before this technology is more widely used on
Rusty Blackbirds. Received S February 2012. Accepted 10 June 2012.
Understanding migratory routes and how they
link breeding, stopover, and wintering areas is a
key component ol effective conservation for
declining populations of migratory birds ( Webster
et al. 2002). 1 his task is complicated for songbirds
by their small size, large ranges, and inconspic¬
uous behaviors, which make them difficult to
effectively track using conventional mark-recap¬
ture techniques or radio or satellite telemetry.
Recent advances in light-level geolocators (Bur¬
ger and Shaffer 2008) have provided new
opportunities to study die migration pathways of
songbirds (Stutchbury et al. 2009, 2011;
Heckscher et al. 201 1: Ryder et al. 201 1 ; Bairlein
et al. 2012; Seavy et al. 2012). We used this
technology to track annual movements of Rusty
Blackbirds (Euphagus carolinus), a species of
high conservation concern (Greenberg et al.
2011), from their breeding areas in southcentral
Alaska to wintering areas and back.
The Rusty Blackbird breeds in wetlands
throughout the Nearctic boreal forest from
northeastern North America across Canada to
U.s. Fish and Wildlife Service. Migratory Bird
Se”1' 1011 EilsI T^'”r Road. Anchorage, AK
Alaska. It winters in wooded wetlands in the
eastern half of the United States where wide¬
spread wetland loss and degradation is believed lo
be the principal cause for the 90% decline in
population size (Greenberg and Droege 1999.
Niven et al. 2004, Greenberg et al. 2011, Sauer
and Link 2011). Feather isotopes suggest the
species may comprise western and eastern popu¬
lations with individuals breeding from Alaska
through central Canada wintering in the Missis¬
sippi Alluvial Valley, and those breeding east ot
Manitoba wintering along the Atlantic Coastal
Plain (Hobson et al, 2010). Little is known,
however, about timing of migration or important
migratory stopovers. The latter may be particu¬
larly important given the species is a temperate
migrant and may spend extended periods of time
at stopover locations before settling in wintering
areas in the southeastern U.S. (Hamel and
Ozdenerol 2009).
We used geolocators to provide the first
detailed look at the migratory movements of
Rusty Blackbirds over an entire annual cycle. We
also chronicle general habitats used for stopovers
and wintering, and the potential adverse effects of
geo locators on this species.
J Alaska Department of Fish and Game, Wild
Diversity Program. Anchorage, AK 99518, USA
'Smithsonian Migratory Bird Center. Smithsonian C
servation Biology Institule. National Zoological ?c
Washington. D.C. 20008, USA.
4 British Antarctic Survey, High Cross, Madingley Ro
Cambridge CB3 0F.T, UK.
'Migrate Technology Ltd., p. o. Box 749 Con
Cambridge CBI 0QY, (JK.
6 Corresponding author; e-mail: jim_aJohnson@fws.g
METHODS
We captured 17 adult Rusty Blackbirds (12
females and 5 males) in June 2009 near
Anchorage, Alaska (61 N, 149 W) using mist
nets placed near their nest sites. We attached 1.2-g
light-level geolocators (model MklOS with 10-
tiim sensor stalk at a 30 angle, British Antarctic
Survey, Cambridge, UK) to each bird using a
698
Johnson et al. • MIGRATION PATH OF RUSTY BLACKBIRDS
699
synsacrum harness (Rappole and Tipton 1991) of
5-inin tubular Teflon ribbon (Bally Ribbon Mills.
Bally, PA. USA). Harness si/e was calculated
using allometric equations (Naef-Daenzer 2007)
and adjusted in the field for individual fit. The
geolocator and attachment harness weighed 2.0 g.
or 3.4% of a Rusty Blackbird's body mass ( v -
57.8 g. n = 16 birds). We monitored each
instrumented bird over the nesting period for
evidence of poor fit or abnormal behavior. We
located three birds fitted with geolocators and
recaptured them at their nest sites in June 2010
following intensive, repeated surveys of the study
area (Matsuoka et al. 2010).
The MklOS measured light-level data at 60-sec
intervals and stored maximum values every
10 min. Geolocators were calibrated during a 5-
day period that preceded deployment. We esti¬
mated the average sun elevation angle that
corresponded to our chosen light threshold from
clean sunrise/sunset events during the calibration
period (Fox 2010). We analyzed the data on
ambient light levels from the geolocators to
identify daily locations using BasTrak software
with the single threshold method (Fox 2010). We
visually inspected the transitions at each sunrise
and sunset, and removed any that appeared to be
influenced by shading events and other sources ot
interference. Latitude was estimated from the
length of each solar day/night and longitude from
the liming of each solar noon/midnight. We did
not estimate latitude from data recorded 15 days
before and after spring and autumn equinoxes
because latitude estimates during equal day and
night lengths are highly inaccurate (Stutchbury
et al. 2009. Fox 2010).
Rust> Blackbirds are believed to move during
the non-breeding season in response to changes in
weather and availability of foraging habitats and
food resources (Hamel and Ozdenerol 2009.
Luscier et al. 2010). We estimated core areas
used by each individual during the non-breeding
season, rather than a single averaged location. We
used Home Range Tools ( Rodgers et al. 2007) and
ArcGIS 9.3 (ESRI 2009) to estimate kernel
probability densities of home ranges during
autumn stopover and winter periods. We used a
fixed-kernel parameter with least-squares cross
validation for calculating the smoothing parame¬
ter (h). This has performed well for simple
mixtures (< 16 components) of points with the
precision of fitted surfaces approaching an asymp¬
tote at a sample size of 50 locations (Seaman and
Powell 1996, Seaman et al. 1999). Variances of the
,v and v coordinates were unequal, and we rescaled
data after Rodgers et al. (2007). The grid size was
1 km. We conservatively defined each bird's core
area for stopover and wintering periods using the
50% density contour (Seaman et al. 1999). We
used landcover data from the North American Land
Change Monitoring System (2005) to characterize
the general habitats within core ranges. We
identified long-distance movements from breeding
and wintering areas as migration events and
delineated stopover areas as clusters of locations
recorded during 2:3 days. We used the center of
core ranges to estimate distances among breeding,
stopover, and wintering locations, and summed the
individual flight segments to estimate the total
distance traveled.
RESULTS
All 17 birds fitted with geolocators were alive
and behaving normally when we last observed
them in breeding areas as late as mid-July 2009. 4
to 6 weeks following attachment. Individuals with
geolocators were associated with 13 nests; two
were abandoned ( I pair re-nested and successfully
Hedged young), three were depredated or flooded,
and eight fledged young. We recaptured two
females and one male in June 2010, but did not
observe any of the remaining 14 birds (82%) in
either the 2010 or 2011 breeding seasons. The
original mean (± SD) weight of the three birds
that relumed ( v = 57.7 ± 0.8 g) was similar to
birds (n = 13) with geolocators that did not return
(,v = 57.9 ± 3.8 g). We found harnesses to be
loose fitting upon recapture and to have worn
away the surrounding feathers on the synsacrum
and inner thighs of each of the three birds.
However, each of the birds behaved normally in
breeding areas in 2010, and all three fledged
young from separate nests.
The distance between the filtered geolocator
locations and known nest sites during the breeding
season averaged 145 km (range = 128-175 km,
it — 3). The routes and timing of migration were
similar for all three birds (Fig. I ). The three birds
departed breeding areas during 7-9 September
and used a series of stopover sites from 1 9 October
to 29 November spanning the Prairie Potholes,
Badlands and Prairies, and Eastern Tall Grass
Prairie regions that included southern Saskatch¬
ewan. North Dakota, South Dakota, and Iowa.
Each bird stopped in either North or South Dakota
or both (Fig. 1). Mean habitat composition of core
700
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. !24. No. 4. December 2012
Johnson et at. • MIGRATION PATH OF RUSTY BLACKBIRDS
701
stopover areas was 60% cropland, 36% grassland,
2% water. 1 % wetland, and 1 % other.
The birds arrived in wintering areas between 20
and 30 November; 72-84 days following depar¬
ture from breeding areas. Wintering areas differed
among the three birds and included South Dakota,
Nebraska. Kansas. Oklahoma. Arkansas, and
northern Louisiana (Fig. 1 ). Distance from breed¬
ing sites to wintering areas ranged from 3,854 to
5.027 km (x = 4.430 km). Core winter ranges for
the male and one female wintering in the Central
Mixed Grass Prairie and Prairie Potholes regions
were 99% cropland and grassland habitats,
whereas the winter range of the female in the
Western Gulf Coastal Plain contained 51%
coniferous forest, 17% deciduous woodland,
18% wetland. 4% other, and only 10% cropland
and grassland.
Spring departure from core wintering areas
occurred during 1-13 April. The male and lemale
that wintered in the Central Mixed Grass Prairie
and Prairie Potholes stopped in northwestern
Alberta during 20-26 April before flying the
remaining 1,820-1.840 km to Anchorage in 4—
5 days (.v = 366 km/day; Figs. 1A and 1C). The
female that wintered in the Western Gulf Coast
Plain migrated through this same area, hut did not
appear to stop (Fig. IB). Instead, she stopped in
southeastern Saskatchewan and northwestern Brit¬
ish Columbia between 13-19 April and 1-4 May.
respectively. All three birds followed spring routes
that approximately matched their migration routes
the previous autumn. The two birds that wintered in
the Central Mixed Grass Prairie and Prairie
Potholes arrived at their Anchorage breeding areas
on 30 April and the bird that wintered in the
Western Gulf Coast Plain arrived on 6 May.
Duration of spring migration was 16-30 days.
DISCUSSION
We provide the first description of the annual
movements of the Rusty Blackbird, a temperate
migrant we documented to move in stages over a
prolonged autumn (72-84 days) and briefer spring
migration (16-30 days). The Prairie Potholes
region, from southern Saskatchewan to Iowa,
was an important stopover region during both
autumn and spring migrations; all three birds
stopped in North or South Dakota or both. Our
data indicate at least these three Alaska breeding
birds overwintered along the western portion of
the species' principal wintering range. I wo birds
overwintered in areas shown by Christmas Bird
Count data (1946-2011) to have relatively high
occurrence of Rusty Blackbirds — (I) the Arkansas
River Valley along the Kansas-Oklahoma border,
and (2) the Western Gulf Coast Plain from the
Ouachita Mountains south to northern Louisiana
(Hamel and Ozdenerol 2009). A third bird
overwintered in an area spanning South Dakota
and Nebraska, a region with a lower rate of
occurrence during winter (Hamel and Ozdenerol
2009). The species has recently been found, based
on feather isotopes and band recoveries, to have
separate Mississippi and Atlantic flyways (Hamel
et al. 2009, Hobson et al. 2010). Data for our
Alaska breeding population indicate the additional
possibility of a Central Fly way route, which is also
supported by limited numbers of band recoveries
(Hamel et al. 2009: fig. 1). Alternatively, the
western distribution of wintering birds in our study
may have reflected an interannual shift in the core
winter range that is thought to occur in response to
variation in winter weather across years (Hamel
and Ozdenerol 2009. Luscier et al. 2010). The
winter of 2009-2010 was particularly cold in the
eastern U.S. (NOAA 2011) and may have pushed
birds farther west than during a typical year.
The duration and timing of autumn stopover
estimated from geolocators (19 Oct to 29 Nov)
was similar to observations of migrating Rusty
Blackbirds using wetlands farther east at Buckeye
Lake, Ohio (15 Oct to 15 Nov; Trainman 1940).
Rusty Blackbirds complete prebasic moll by late-
September ( Mettke-Hofmann et al. 2010). Thus,
late autumn may be a distinct phase in the annual
cycle during which Rusty Blackbirds rest from
migration to forage in wetlands and agricultural
areas over a I -month period before traveling to
overwintering areas farther south. Populations
may be susceptible to habitat losses and alter¬
ations in key stopover regions as hypothesized for
wintering areas (Greenberg and Droege 1999,
Greenberg et al. 201 1). The species uses similar
routes for spring and autumn migration, and
disturbances in stopover areas may have com¬
pounding effects on populations. Rusty Black¬
birds are typically associated with wetland
habitats throughout the annual cycle (Avery
1995), but the core areas used by each of the
three birds for stopover during autumn migration
and by two birds during winter were in landscapes
largely converted by agricultural use. Other
researchers also occasionally found the species
in agricultural fields primarily adjacent to wet¬
lands (Trautman 1940, Luscier et al. 2010).
702
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 4. December 2012
Identification and conservation of key habitats,
particularly at stopover sites, may he additional
considerations for recovering populations of
Rusty Blackbirds (Greenberg et al. 201 1).
Additional tracking of Rusty Blackbird migra¬
tions from other breeding locations would further
identify migratory linkages and important non¬
breeding areas tor stopover and overwintering.
This information could test more specific hypoth¬
eses of the species’ decline, (e.g., the effect of
differing migration strategics on demographic
variables, such as overwinter survival) and be used
to coordinate conservation across the species'
annual cycle (Greenberg and Matsuoka 2010,
Greenberg et al. 2011), The winter distribution of
the species tends to vary both within and between
years (Hamel and Ozendero! 2009. Luscier et al.
2010). Multi-year tracking of individual Rusty
Blackbirds could add information on the plasticity
ot migratory movements and perhaps climatic
events that trigger them. However, the benefits
Irom this potential information should be carefully
weighed against the potential harm to birds fitted
with these devices. Only 18% of the Rusty
Blackbirds we fitted with geolocators in 2009
returned in 2010, much lower than the 60% of
Rusty Blackbirds banded in 2008 that returned in
2009 (SMM, unpubl. data). This was similar to
differential return rates reported for Purple Martins
(Progne snbis ; 10% return rate with geolocators,
54% for banded only), but contrary to Wood
Thrushes (Hylocichla mustelina: 50% return rate
with geolocators, 33% return rate for handed only
Stutchbury et al. 2009. 2011). Other studies that
used geolocators to irack annual movements of
songb.rds found return rates did not significantly
differ between tagged birds and individuals that
were banded and released without geolocators; e.e„
orthem Wheatear (i Oenanthe (tenant he: 12 5%
return rate with geolocators. 6.0% for banded only
Ba,rle,„ et al. 2012), Vcery
, retllni rate w“l» geo locators, 62% for banded
only; Heckscher et al. 2011), Gray Catbird
(Dumetella carotinemis ; 31.8% return rate with
geo locators 29.9% for banded only; Ryder et al.
-OH), and Golden-crowned Sparrow (Zonotridiia
anu-c.pdla: 33% return rate with geolocators, 39%
loi banded only; Seavy el al. 2012). Thus species
may vary in suitability for this technology and
subtle differences m harness materials and methods
may be critical to survival success
Al! three Rusty Blackbirds upon recapture in
-010 had loosely fitting harnesses that had
abraded the surrounding feathers along the
thighs and synsacrum. Body mass was lower in
2010 for the male and the female that wintered in
the Western Gulf Coast Plain (by 4 and 12%.
respectively), but not for the second female.
Rusty Blackbirds often forage in water, which
may have made the birds in our study more
vulnerable to a combination of feather wear and
reduced thermoregulation. This coupled with (he
cold weather conditions of the 2009-2010 winter
may have been particularly detrimental to birds
in our study. The weight of the geolocator and
harness we used were below 4% of body mass.
However, we recommend future studies using
geolocators on Rusty Blackbirds should consider
sub-grant devices. A thorough evaluation of
materials used for harnesses is also warranted.
Plastic cord that could maintain a tight fit by
accommodating seasonal changes in body mass
could be easily damaged by Rusty Blackbirds.
Elastic cord threaded through tubular Teflon
ribbon (3 mm; Bally Ribbon Mills, Bally. PA.
USA), however, may possibly produce a better
lining harness that allows for changes in body
mass yet is sufficiently durable.
ACKNOWLEDGMENTS
We are grateful to Niels Dau. Luke DeCicco. Larry
I loarc. Russ Oates, Lisa Pajot. Marian SniveJy, Kim Trust,
and Jen Wiley for assistance in the field. Herman Griese
and C hris McKee of (lie Department of Defense provided
access to study areas on Elmendorf Air Force Base and the
US. Army s Fort Richardson, respectively. We appreciate
Ihe helpful comments of Brad Andres. Clajt Braun. Jesse
Conklin, and an anonymous reviewer that improved earlier
dratl.s ul the manuscript. This study was funded by Hie
Alaska Department ol Fish and Game's Nongame Program,
t e U.S. Department ol Defense’s Legacy Natural Resourc¬
es Program, the Smithsonian Migratory Bird Center, and
Ihe U.S. Fish and Wildlife Service. Migratory Bird
anagement (Region 7). The findings and conclusions in
t us article are those ol the authors and do not necessarily
represent the views of the U.S. Fish and Wildlife Sendee.
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The Wilson Journal of Ornithology 124(4):704-712, 2012
MIGRATION ROUTES AND NEW BREEDING AREAS OF
BLACK-NECKED CRANES
QIANG LIU,1-5 FENG-SHAN LI,2 PAUL BUZZARD,' FA- WEN QIAN,4 FAN ZHANG.3
JIAN-LIN ZHAO.6 JUN-XING YANG,1 7 AND XIAO-JUN YANG1-7
ABSTRACT. — We equipped five Black-necked Cranes (Grus nigricollis) with satellite transmitters between February
and November 2009 to investigate their migration routes between breeding areas and wintering area at Napahai Marsh
(3,260 m asl). China. We identified the Shaluli Mountain region (southwest Sichuan), including Daocheng, Litang, Baiyu.
and Xinlong counties as a new breeding area with a mean elevation of 4.330 m asl. Four of five tracked cranes spent the
summer in Daocheng County. The fifth crane was there briefly and then moved north to Baiyu and Xinlong counties. The
distance between Napahai Marsh and Daocheng County ( — 180 km) is one of the shortest migration routes among crane
species, but covered an elevation increase of — 1,200 m. The migration route of the fifth crane was -400 km in length and
occurred over 2 or 5 days in spring 2009 and 2010, respectively, and 19 days in fall 2009 with five stopovers. Received I
November 2011. Accepted 15 June 20/2.
The Black-necked Crane ( Grits nigricollis)
lives al altitudes of ~ 1 ,900-4, 500 m asl (Li and
Li 2005) and is the only species of cranes endemic
to the Qinghai-Tihet and Yunnan-Guizhou pla¬
teaus. This species with -8,000 individuals
remaining in the wild is listed as ‘Vulnerable’
on the 1UCN Red List (IUCN 201 I). The summer
breeding range of Black-necked Cranes includes
much of the Qinghai-Tibet Plateau in China with a
small number in neighboring India. Black-necked
Cranes winter mainly in three subpopulations: (1 )
eastern population (EP; northeastern Yunnan and
northwestern Guizhou provinces), (2) central
population (CP; in northwestern Yunnan), and
(3) western population (WP; southern Tibet and
Bhutan, Li 2005).
The migration routes of Black-necked Cranes
have remained unknown until recently, because of
their remote distribution in high elevation areas.
State Key Laboratory of Genetic Resources and
Evolution. Kunming Institute of Zoology, Chinese Acad-
«lfScienCes’ 32 Jiaochangdong Rd., Kunming. Yunnan
650223, China.
International Crane Foundation. E- 11376 Shady lane
Road, Baraboo, W1 53913. USA.
China Exploration and Research Society, B 2707-08
SouthMark. 1 1 Yip Fling Street. Wong Chuk Hang, Hong
Kong, China. 6
4 Institute of Forest Ecology. Environment and Protec¬
tion, Chinese Academy of Forestry. Beijing. 1 0009 1 , China
5 National Plateau Wetlands Research Center, Southwest
Forestry University, Yunnan, 650224. China.
"^n®rj;La Furcs,ry Bureau, Shangri-la. Yunnan,
674400, China.
7 Corresponding author; e-mail: yungxj@mail.kiz.ac cn or
yangjx@mail.kiz.ac.cn
The first efforts to document Black-necked Crane
migration included banding cranes and. more
recently, satellite tracking (Wu el al. 1994.
Archibald 2005, Qian et al. 2009; Drolma
Tsamehue. pers. obs.; Cl. W. Archibald, pers.
comm.; Wangmo Rinchen. pers. comm.). These
cl torts identified three migration fly ways: (1)
Irom eastern subpopulation wintering areas to a
breeding area at Ruoergai Marsh in northern
Sichuan, (2) from the western subpopulalion
wintering areas to a breeding area in central anti
northern Tibet, and (3) from the central subpop¬
ulalion wintering area to a breeding area in south
Qinghai (Fig. 1).
I he central subpopulation is the least under¬
stood. but also the most endangered with —300
individuals. This subpopulation formerly wintered
at seven wetlands and lakes in northwest Yunnan
(Li 2005). Currently, however, cranes are com¬
monly observed at only two sites: Napahai Marsh
and Bitahai Marsh, with the former having the
largest number (Wei and Wu 1994, Hun 1995. Li
1996, Yang 2005). However, numbers at these
two locations are declining: the wintering popu¬
lation at Napahai Marsh declined from -700-800
birds before the 1960s to -300 in 1978-1979 and
to 60-70 in 1981. due largely to drainage of
wetlands and hunting (Li "and Bishop 1999).
Recent efforts have allowed the population to
recover to —300 individuals, but the percentage of
juveniles in the subpopulation has been decreas¬
ing, based on monitoring conducted from 2004 to
2010 (Liu 2007. Wang 2008, Liu 2010). The
percentage ol juveniles was only 8.4% in winter
2009, lower than estimates in a 2002 International
Crane Foundation report of 18.9% for the central
704
Liu et al. • MIGRATION ROUTES OF BLACK-NECKED CRANES
705
FIG. 1. Distribution and migration routes of Black-necked Cranes in China. Areas circled in green are breeding areas;
areas circled in red are wintering areas (remapped from Li and Li 2005). Black dots indicate locations of Black-necked
Cranes from Birdlife International (2001). Occasional records from outside normal range are excluded when <1.900 m asl
(Li and Li 2005). Blue lines indicate migration routes of Black-necked Cranes documented by satellite tracking or banding
(Archibald '’OOS Qian et al. 2009; Drolma Tsamchue. pers. obs.; F. Li. pers. obs.; G. W. Archibald, pers. comm.; Wangmo
Rinchen, pers. comm.). Areas with oblique lines are new breeding areas discovered in our study (rectangle denotes
study area).
subpopulation and 1 6. 1 % for the eastern subpop-
ulation (Li and Li 2005), indicating productivity
of this subpopulation is declining. Thus, improv¬
ing knowledge of migratory routes, and resting
and breeding areas of these cranes is crucial to
conserving this endangered species.
We used satellite telemetry in 2009 and 2010 at
Napahai Marsh to study the migration ol the
central subpopulation. Our objectives were to: ( I )
identify migration routes and stopover sites ol
Black-necked Cranes wintering at Napahai Marsh,
and (2) assess the overall habitat characteristics at
stopover and breeding sites.
METHODS
We captured five Bluek-nccked Cranes with
noose-carpet traps, as described by Sutherland et
al. (2004), between 2 1 February and 16 November
2009 at Napahai Marsh (27 48 '-55' N, 99 37 -
41' E: 3,260 in asl). a seasonal lake dominated by
open water, shallow water marshes, wet meadows,
dry grasslands, and 1 arm lands in northwestern
Yunnan Province (Liu et al. 2010). All captured
cranes were released immediately after the
satellite transmitters were attached. Each satellite
transmitter or platform transmitter terminal (PTT)
(Model PTT- 1 00; Microwave Telemetry Inc.,
Columbia, MD. USA) weighed 95 g. PTTs were
attached to the backs of cranes with Teflon-treated
ribbons as described by Nagendran et al. (1994).
The satellite transmitters amounted to <2% of the
normal bird's body mass (mean = 5,390 g, /; = 5
individuals) and each transmitter had a unique
number (ID) used to identify individuals. The
pulse interval of PTrs was 60 sec with a duty
cycle of 6 hrs active and 12 Ins inactive. Color
bands were attached to the legs of each crane to
provide identification in subsequent field obser¬
vations. Location data were ranked in order of
accuracy from lowest to highest: Z. B. A, 0, 1, 2,
to 3. The ±1 SD accuracies reported by Argos
(2011) were: >1,000 in for location class (LC) 0;
350-1.000 m for LC 1; 150-350 m for LC 2; and
<150 m for LC 3. Accuracies for the lowest LCs
(A. B, and Z) were not guaranteed. We used LCs
1-3 for data analysis, but data for LCs 0 and A
706
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 4. December 2012
were included when they were close to prior
locations or along the logical migration path
(Dubinin et al. 2010).
We used ArcGIS (ESRI. Redlands. CA. USA),
Hawth Tools (www.spatiaIecology.com), and a
topographic map (Digital Elevation Model,
http://eros.usgs.gov) to plot crane movements.
We analyzed the relationship between migration
routes and topography with these data. We made
a rapid survey of staging sites along the
migration routes and identified habitat types at
the landscape level. We divided the landscape
into three types: valley swamp, valley swamp
along river, and lakeside swamp in accordance
with vegetation and hydrology. We used ArcGIS
to digitize the ETM satellite images, and
computed areas of each landscape. Data are
presented as mean ± SD.
C). The two spring migrations both started in
early April and covered 406.5 and 439.7 km in 2
and 5 days, respectively. Crane ID 79631
initiated fall migration on 17 October 2010 and
arrived at Nupahai Marsh on 4 November 2010.
19 days after initial departure from where it spent
the summer. Five stopover sites were used during
migration, one in Daocheng County, one in Baiyu
County, and three in Litang County, Sichuan
Province (Table 2). Different sites were used
each year and time spent at each stopover site
was highly variable, ranging from 0 to 10 days.
Crane ID 79631 backtracked during spring 2010,
leaving Napahai Marsh on 9 April and arriving at
Cuoma Pond on 13 April. The crane turned back
on 14 April to its last stopover site al Gehe
Valley before returning to Cuoma Pond on 29
April.
RESULTS
We received 9,158 (mean ± SD = 2,015 ±
288.1, range = 1,622—2,298, n - 5 individuals
location records from the five Black-neckec
Cranes between February 2009 and December
2010. About 21% (20.9%) of the records were in
the highest accuracy categories (LC 2 or 3).
21.2% were LC 1, 1 1.8% were LC 0. 19.8% were
LC A, and 26.4% were LC B or Z. Overall 6 74^
(mean ± SD = 1.483 ± 261.7, range = 1.153-
1 ’737, n = 5 individuals) location records
provided usable information.
Four ot the cranes tollowed the same migration
route from wintering areas at Napahai Marsh to
breeding areas while the other crane took a
longer route (Fig. 2). Four cranes (PT'T ID
79627, 79628. 79629, and 79630) completed
one spring migration from Napahai Marsh to
breeding areas at Haizishan Marsh in Daocheng
County, Sichuan and returned in the autumn.
Black-necked Cranes initiated spring migration
between mid-April and early-June and fall
migration between late-October and early-No-
vember. Migration lasted 1 day and covered a
mean distance of 174.5 km (n = 8. Table I). The
four cranes followed the same migration route
without stopover sites.
mnoT In I?63' W0S tracked ,rom 21 February
2009 to 19 2010. It completed two spring
Zlh'0;, r r fa" miSrati°" between
Napaha, Marsh and a summering area at Cuoma
ond, Sichuan. 1 his wetland included 37.9 ha of
akes.de swamp at an elevation of 4.476 m asl
(31 15 N, 99 52' E) (Tables 1, 2; Fig. 2A, B.
The snow-covered Bangmanyi Range with an
elevation of 4,200 to 5,300 m asl. 60 km east-
west from Napahai Marsh, presented a barrier for
crane ID 79631 on the first day of Spring
migration in both 2009 and 2010. Crane ID
79631 turned northwest and followed the lower
Jinsha River Valley until the confluence of the
.linsha and Xiangcheng rivers. Subsequently,
crane ID 79631 turned northeast and proceeded
around the Bangmanyi Mountains, eventually
continuing to the breeding area (Fig. 3). Most
Black-necked Cranes, based on our ground
observations, started migration when thermals
formed al noon (1000-1300 hrs). Thus, the
cranes were able to climb to higher altitudes
while expending little energy in the process by
flying in a spiraling circular path within the
thermals.
DISCUSSION
This study adds to our knowledge of the
migratory behavior and distribution of Black¬
necked Cranes. We identified the Shaluli Moun¬
tain region as a new breeding area of Black¬
necked Cranes. We also directly observed breed¬
ing pairs of cranes in this region’in June 2010. We
documented a migration route between the central
subpopulation wintering area at Napahai Marsh.
Yunnan and breeding areas in the Shaluli
Mountain region, southwestern Sichuan.
A migration route had been documented
between Napahai Marsh and Yushu County.
Qinghai based on a single banding recovery, and
Daocheng County was identified as the staging
area In this migration route (Wu et al. 1993.
Liu et al. • MIGRATION ROUTES OF BLACK-NECKED CRANES
707
FIG. 2. Migration routes (black lines) and stopover sites (black boxes) of the 5 Black-necked Cranes as revealed by
satellite tracking for (A) spring migration of crane 79631 in 2009, (B) fall migration of crane 79631 in 2010. (C) spring
migration of crane 79631 in 2010. and (D) migration of cranes 79627, 79628. 79629 and 79630. The date shows duration of
staging at each stopover site.
708
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124, No. 4. December 2012
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Liu et al. • MIGRATION ROUTES OF BLACK-NECKED CRANES
709
1994). None of our five tagged cranes traveled to
Yushu, and it is not clear whether cranes breeding
in Yushu pass through Daocheng during migra¬
tion; it is more likely the cranes breeding in Yushu
use another migration route via Changdu, Chaya,
Gongjue, and Mangkang counties in Tibet. This
route is shorter and follows the low altitude Jinsha
River Valley. Thus, cranes have no need to cross
over high mountains (e.g., Queer Mountain
between Yushu and Baiyu counties: peak
6,168 m asl) and there is a multitude of suitable
wetlands along this route (e.g., Mangeuo Lake at
Mangkang). Daocheng County has also been
listed as a wintering area for Black-necked Cranes
(Dolan 1939, Zheng 1987). This suggests migra¬
tory behaviors are more complex and/or migration
patterns may have changed recently. Collecting
additional multi-year satellite telemetry data from
multiple cranes would be beneficial in providing
definitive data.
Different populations of Black-necked Cranes
have shown different migration behaviors, For
example, the shortest migration route is from
Phobjikha in Bhutan to Phari/Bam-tsho in Tibet,
only -120 km, and the longest is from Caohai
Marsh in Guizhou to Ruoergai Marsh in Sichuan,
-1,351 km. The duration of the migration can
also vary' from I to 21 days (Zhang 2007;
Wangmo Rinchcn, pers. comm.). Our study
documented this variation can occur within a
subpopulation as well, as migration routes varied
from 175 to >400 km and lasted from 1 to
19 days. Movements in Tibet are sufficiently short
in many cases and Ludlow and Kinnear (1944)
described the species as “only locally migrato¬
ry". This variation in migratory patterns likely
developed because the topography of the Qinghai-
fibet Plateau is dynamic with high mountains and
low valleys within small landscapes, resulting in
climatic conditions that can differ significantly
over a 100-km area.
Migration routes of Black-necked Cranes can
be short hut require negotiating areas of high
altitude. Black-necked Cranes used air currents
such as thermals and other updrafts to complete a
180-km trip and climb over 1,200 m in altitude
from Napahai Marsh to Docheng County. Cranes
usually departed about noon to target the peak
ihermal period, gaining —500 m in the process
before (lying north (Liu 2010).
Soaring birds, such as Black-necked Cranes,
depend on geographic and topographic character¬
istics during migration for navigation. Thus,
knowing routes these birds use each year during
migration is important. However, these routes
often differ between spring and autumn as a result
of varying wind and weather condition (Newton
2008), Fall migration routes lor cranes in
Daocheng County, compared to the tortuous
spring migration, is direct with no detours
(Fig. 3). Cranes moved south to lower altitude
wintering areas where the high snow-capped
mountains no lunger presented immediate barri¬
ers. Crane ID 79631 took a longer route than the
others and continued in the spring to the Cuoma
Pond, 200 km north of Daocheng County. The
terrain between Daocheng County and Cuoma
Pond is relatively flat with several dispersed small
lakes and wetlands that can provide roosting and
feeding sites. Crane ID 79631 chose to take
advantage of these suitable habitats rather than
take the most direct route. Crane TD 79631, during
its next spring migration, moved back to a
stopover site after reaching its summering area
at Cuoma Pond. This retrogression could have
been due to abrupt local heavy snowfall.
Black-necked Crane families separate before
spring migration and juveniles do not follow their
parents to breeding areas (Liu et al. 2008).
Instead, juveniles flock together and remain
longer at wintering sites. Juvenile ID 79629 in
our study started the spring migration up to
2 months later than adults. Similar observations
have been made for Red-crowned Cranes ( Grits
japonensis ) (Kamata 1994) and White-naped
Cranes ( G . vipio) (Lleta et al. 2001). This
separation may decrease conflicts between off¬
spring and their parents in breeding areas (e.g., for
food) and demonstrates juveniles have the ability
to migrate to breeding areas without following
their parents.
Eighteen Black-necked Cranes, including this
study, have been tracked using satellite telemetry
in China and Bhutan. These cranes have provided
extensive and detailed information about the
migration ecology of Black-necked Cranes. This
sample, however, is small. More satellite telem¬
etry and traditional color banding are needed.
Our study identified a new breeding area and
important stopover sites of Black-necked
Cranes. These areas are essential for the long
term survival and conservation of the central
subpopulation. More research is needed in the
future; e.g., estimating population si/e, identi-
lying food resources, and documenting repro¬
ductive ecology.
710
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 4. December 2012
Daocheng
lowmountain
6,000 m
Baiyu
Pond Cuoma
5.500 m
5,000 m -
Xinlong
4,500 m
4,000 m
j .500 m
3,000 m
:.50o m
Batang
2.000 m
1,500m
Deqin
irv
Napah-afffi'^
*7 !»- Ttf'
FIG. 3. Topography of breeding areas
Napahai Marsh, China. The black line ^ Wintering areas °f Black-necked Cranes wintering a.
the spring migration route of crane 7963 1 in ^OlO- th • g ™8ratlon route of crane 79631 in 2009; the blue line represents
" ni. red line represents the fall migration route of crane 79630 in 2010.
Liu et al. • MIGRATION ROUTES OF BLACK-NECKED CRANES
711
ACKNOWLEDGMENTS
This study was supported by the National Key
Technolog, R & D Program of China (2008BAC39B03),
National Key Development Program for Fundamental
Research (#2007CB41 1600). Western Light Associated
Scholar Program of the Chinese Academy of Sciences,
China Exploration and Research Society, International
Crane Foundation. National Natural Science Foundation of
China (#40971285). and grants from the National Basic
Research Program of China-973 Program (2OI0CB434807).
We are grateful to Hong-Zhong Yu. Yuangee Hong, and
Kai Wang for help with crane capture. We thank Teresa
Olson and Andrew Willden for editing a draft of the
manuscript.
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The Wilson Journal of Ornithology 1 24(4):7 1 3 -720, 2012
VISUAL ASSESSMENT OF INTERBREEDING BY
AECHMOPH OR US GREBES
ANDRE KONTER1
ABSTRACT. — Population composition of Aechmophorus grebes was investigated in Utah and the occurrence of possible
intermediates between Western ( Aeclwwplwrus occidentalis) and Clark's (A. clarkii ) grebes was assessed. Individuals with
clearly intermediate traits represented an aggregated 6.5% (43 individuals) in the populations investigated while another
7.6% (46 individuals) did not entirely conform to the description of Aedunophnrus grebes provided by Storer and
Nuechterlein. The number of intermediates has increased in Utah in comparison to historical data. A similar survey in
California and Oregon in 2009 also found increased percentages of intermediates. The results a priori contradict growing
reinforcement of incompatibilities between both Aechmophorus grebes. Western and Clark's grebes in these major areas of
sympairy appear to interbreed as frequently as in areas of relative allopatry. No evidence against assortative mating was
found. Hybridization for Aechmophorus grebes may reflect adaptive mate choice rather than a mistake. Introgressive
hybridization may be important and mask real rates of hybridization. Received 22 Jamum 2012. Accepted R May 2012.
The American Ornithologists’ Union split the
two North American Aechmophorus grebes in
1985 into Western ( A . occidentalis) and Clark’s
grebes (A. clarkii) (AOU 1985). More recent
genetic investigations (Ahlquist et al. 1987,
Bledsoe and Sheldon 1989, Guerra and Speed
1996. Hebert et al. 2003, Savolainen et al, 2005.
Ralnasingham and Hebert 2007) found low levels
of differentiation between both grebe species and
the methods of DNA bareoding applied to North
American bird species suggest Western and
Clark's grebes are candidates for combination
(Kerr et al. 2007). Both grebe species arose from a
common ancestral population (Storer and Nuech-
terlein 1985) that divided into northern and
southern subpopulations that today are again
largely sympatric. Positive assortative maling in
mixed populations of Western and Clark’s grebes
was demonstrated by different studies (Ratli 1979;
Nuechterlein 1981a. b: Lindvall and Low 1982;
Nuechterlein and Storer 1982). Differences in
advertising calls were identified as critical to their
reproductive isolation (Nuechterlein 1 98 lb). The
taxonomic status of Aechmophorus grebes may
not be entirely settled and a crucial question to be
answered in the field is whether barriers to
random mating between Western and Clark's
grebes are increasing or vanishing. First genera¬
tion hybrids could be rare, but they arc viable and
produce viable offspring (Storer and Nuechterlein
1985, Nuechterlein and Buitron 1998).
I investigated population composition and
occurrence of intermediate Aechmophorus grebes
in California and Oregon in 2009 based on
1 Museum of Natural History, 25 rue Munster, Luxem¬
bourg. L-2150, Luxembourg; e-mail: pocliceps@pt.lu
subdivision of divergent areas in the plumage of
the face between Western and Clark’s grebes
described by Storer and Nuechterlein (1985). I
found increased numbers of intermediates and
mixed pairings (Konter 2011). However, these
geographically limited findings may not be
representative for both species more generally
and I repeated the study in Utah, another major
area of sympatry.
METHODS
Study Sires— Major sites visited having grebes
included three protected bays on the eastern shore
of Great Salt Lake (GSL); the freshwater and
brackish marshes of Farmington Bay within
Turpin Unit, Crystal Unit, and two ponds close
to the visitor center; Ogden Bay and Willard Bay,
an impoundment on the floodplain of the GSL;
and part of Bear River Bay. Also included were
Mantua Reservoir, an impoundment at the top of
Box Elder Canyon East of Brigham City, Yuba
Liike south of Nephi, Minersville Reservoir west
of Beaver. Panguitch Lake west of Panguitch,
Lake Powell only at one site when crossing it on
the way to Natural Bridges. Bottle Hollow
Reservoir near Roosevelt, and seven areas of
Strawberry Lake between Duchesne and Heber
(Soldier Creek, nearby marina. Chicken Creek
West, bay between Chicken Creek East and West,
Chicken Creek East. Mud Creek, and nearby
marina and campgrounds).
Additional wetlands visited having a few
Aechmophorus grebes that could be identified
were: Benson Marina on Bear River; a wetland
adjacent to Cache Junction and Hyrum Reservoir,
all close to the city of Logan; Jensen Park pond in
713
714
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 4. December 2012
TABLE 1. Characteristics of Aechmophorus grebe study sites in Utah. USA.
Geographical coordinates
Name
Water surface (ha)
Elevation (m asl)
N
E
Farmington Bay
7,300
1.280
40 56.841
111 56.151
Ogden Bay
8,000
1.280
41° 11.198
112 09.667
Willard Bay
1.280
41 25.259
1 12 03.454
Mantua Reservoir
1.585
41 29.837
1 1 1 55.920
Yuba Lake
2, (MX)
1.520
39 ’22.400
112 01.382
Minersville Reservoir
450
1.685
38 13.680
1 12 48.893
Panguitch Lake
1.600
2,510
37°43.343
1 12°38.046
Lake Powell
1.100
37 53.293
1 10 24.049
Bottle Hollow Reservoir
160
1.560
40 17.674
109 53.085
Strawberry Lake
7.900
2,315
40 10.497
1 1 TO 1.694
Benson Marina
3.340
41 47.21 I
1 1 1 57.245
Cache Junction
1,350
4 f 50.692
112 00.145
Hyrum Reservoir
750
1,420
4 1 ”37.602
111 52.315
Jensen Park pond
1,295
41 03.967
1 12°03.266
Pelican Lake
7(H)
1.470
40 1 12.002
109 41.519
Ouray NWR
500
1.420
40 07.248
109 38.519
Bullock Reservoir
1.610
40 21.144
109 49. 115
Cottonwood Reservoir
1 ,600
40 2 1 . 1 35
109 47.135
Deer Creek Reservoir
1,300
1.650
40 28.424
1 1 1 28.409
Syracuse; Pelican Lake; Wyasket Lake and pond
on Ouray National Wildlife Refuge, Bullock
Reservoir, Cottonwood Reservoir, all close to
Roosevelt; and Deer Creek Reservoir in the Heber
Valley near Heber. The results from these wetlands
were aggregated under other sites visited. Public-
access to Bear River Migratory Bird Refuge that
has an important Aechmophorus population was
closed due to road construction and a request for
exceptional access did not receive a positive reply.
Water surfaces, elevations, and geographical
coordinates of study sites varied (Table 1 ).
Timing and Recording of Data.— Study sites
were visited between 8 and 25 July 2010. I
stopped to identify grebes any time they were
encountered. Nesting grebes were only present at
Farmington Bay, Crystal Unit. No attempt to
completely assess pair composition was under¬
taken to minimize disturbance to this mixed
colony of Western, Clark's, Eared ( Podiceps
nigricollis), and Pied-billed grebes (Podilvmbus
podiceps). Aechmophorus families were encoun¬
tered at Panguitch Lake, Bottle Hollow Reservoir
Ouray National Wildlife Refuge, and Strawberry
Lake.
Total numbers of Aechmophorus grebes present
were counted at each site using Zeiss 10 x 25
binoculars or, in a few cases, their numbers were
estimated. All grebes sufficiently close for species
identification were scanned using a Konica
Minolta Dynax 7D camera and a Sigma AF
800 mm auto focus lens mounted on a tripod.
Species (Western, Clark’s or intermediate) was
recorded after identification by an assistant. Up
to three photographs were immediately laken
lor each grebe not entirely conforming to the
descriptions of Storer and Nuechlerlein (1985) for
Western or Clark’s grebes. Photographs were
visualized later using Program Photoimpact that
allows sufficient magnification with negligible
loss of quality. Species composition of pairs
encountered was also recorded.
Identification of Grebe Species ( Western vs.
Clark's). — Species identification of exclusively
adults followed the descriptions provided by
Storer and Nuechterlein (19S5). They subdivided
diverging areas of the plumage of the face
between Western and Clark’s grebes into lores,
above eye. behind eye and below eye (Storer and
Nuechterlein 1985:103; figure I). Their criteria
were complemented by review's in Ratti (1981),
Eichorst anil Parkin (1991 ). and Konter (2009).
Individuals were classified as Clark's Grebes if
they had while lores and w'hite feathers above,
behind, and below the eye so the black crown
ended clearly above the eye. and an orange-
yellow hill with a sharply defined black culmen.
Individuals were classified as Western Grebes if
they had a dull yellow -green bill and the black of
the crown extended to well below the eyes. Bills
Konter • INTERBREEDING OF AECHMOPHORUS GREBES
715
TABLE 2. Number
intermediate (IG) grebes
of Aechmophorus grebes observed and classified into Western (WG), Clark’s (CG), and
in Utah. USA.
Welland
Total grebes present
Total glebes assessed WG {%)
Species identification
CG {%)
IG (%)
Farmington Bay, Crystal Unit <100
58
39 (67.3)
9 (15.5)
10 (17.2)
Farmington Bay. other areas ±55
40
10 (25.0)
26 (65.0)
4 (10.0)
Ogden Bay
14
14
6 (42.9)
6 (42.9)
2 (14.2)
Willard Bay
±100
84
52 (61.9)
24 (28.6)
8 (9.5)
Mantua
±40
22
12 (54.5)
6 (27.3)
4 (18.2)
Yuba Lake
20-30
14
9 (64.3)
4 (28.6)
1 (7-1)
Minersville Reservoir
142
142
87 (61.3)
40 (28.2)
15 (10.5)
Panguitch Lake
±50
43
35 (81.4)
2 (4.6)
6 (14.0)
Lake Powell
15
15
12 (80.0)
1 (6.7)
2 (13.3)
Bottle Hollow Reservoir
18
18
12 (66.7)
0 (0.0)
6 (33.3)
Strawberry Lake
±200
174
138 (79.3)
11 (6.3)
25 (14.4)
Other sites visited
±70
36
12 (33.3)
14 (38.9)
10 (27.8)
Totals
829
660
424
143
93
Percent
100
79.6
64.2
21.7
14.1
of intermediate color and identifiable neither as
clearly orange-yellow nor as dull yellow-green
were qualified as yellow. Other trails less obvious
in the field were not primarily considered. Little
intermediacy and no overlap between both species
;tre observable from April to October (Storer and
Nucchterlein 1985). All grebes not entirely
conforming to the above characteristics of West¬
ern or Clark’s grebes were grouped separately
according to their diverging traits.
Paii- composition of nesting grebes or those
caring for chicks or displaying was recorded at each
location. A x'-tesl w as used to examine if pairing by
grebes was random or assortativc with VassarStats
(http://faculty.vassar.edu/lowry/VassarStats.htnil).
Assortative mating was defined as like- with like
pairing to overcome the problem of defining species
status (Randier 2008). All grebes deviating from the
description of either Western or Clark's grebes of
Storer and Nuechtcrlein (1985) were treated as
intermediates for the test. Bill si/e dimorphism w'as
used to discriminate between males and females
(Storer and Nuechterlcin 1985).
RESULTS
Numbers and Species Composition oj Popula¬
tions. — Eighty percent or 600 individuals ot all
grebes encountered were assessed ot which 424
(64.2%) were classified as Western Grebes and
143 (21.7%) as Clark's Grebes. Ninety-three birds
(14.1%) did not entirely match the traits of either
species of Aechmophorus grebes (Table 2).
Western Grebes were in majority at nine
locations. They were most numerous at Panguitch
Lake, Lake Powell, and Strawberry Lake (each
—80%). Only the Turpin Unit of Farmington Bay
had a majority of Clark's Grebes. Not entirely
conforming individuals represented between 7.1
and 33.3% of I he Aechmophorus grebes at the
different sites. Their numbers were most impor¬
tant at Strawberry Lake (n = 25) followed by
Minersville Reservoir (n = 15). Bottle Hollow
Reservoir had the most important population
of intermediate grebes (33.3%) and no Clark's
Grebes were recorded at that site (Table 2).
Occurrence of Intermediates. — Ninety-three
grebes deviated from the descriptions of either
Western or Clark's grebes provided by Nuechter-
lein and Storer (1985). The first subdivision
(Table 3) aggregated grebes displaying minor
differences to Western Grebes that were classified
as debatable Western Grebes. They were 7.0%
(46) of all grebes assessed. The second subdivi¬
sion (// = 43) included those grebes with clearly
intermediate traits between both Aechmophorus
species and classified as intermediates. They
represented 6.5% of all grebes assessed. The third
subdivision aggregated those showing minor
deviations with respect to Clark's Grebes and
classified as debatable Clark's Grebes. Four
grebes (0.6%) varied only slightly from Clark's
Grebes (Fig. ]).
Mixed Pairings. — Two pairs of Clark's Grebes,
five pairs of Western Grebes, and one pair
716
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 4. December 2012
TABLE 3. Intermediate Aechmophorus grebes (n = 93) and patterns of deviation. Utah. USA.
Facial pattern
Before eye _ Above eye Behind eye _ Below eye Eye interseclion Bill color
Debatable intermediates or Western Grebes (± WG) (// = 46)
black black black
black black black
off-white black black
off-white black black
off-white black black
off-white black black
off-white black black
off-white black black
black black black
black black black
black black black
black black black
off-white black
black black
Grebes with clearly intermediate
black black
off-white black
off-white black
off-white black
off-white black
off-white black
off-while black
off-white black
off-white black
black black
white black
black black
off-white black
off-white black
white black
black black
white black
black black
black far down, washed below
black, washed white backward
black
black
light gray
diffuse gray
light gray, thin line
diffuse gray
black
white, thin gray line
white, thin gray line
light gray
light gray
light gray
(IG) (n = 43)
white
white
w'hite
white
black, off-white in lower part
white, thin gray line
white
white
white, thin gray line
white
white
white
white
white
off-white
black
white
white
below eye
green
5
below eye
green
3
below eye
green
1
below eye
yellow
1
below eye
green
7
below eye
green
2
just below eye
green
1
lower eye
green
3
below eye
yellow
1
just below eye
green
12
just below eye
yellow
2
below eye
green
5
below eye
green
2
below eye
green
1
lower eye
green
3
lower eye
green
1
center eye
green
6
lower eye
green
5
just below eye
green
2
just below eye
green
8
lower eye
yellow
2
center eye
green
1
just below eye
yellow
2
center eye
green
2
center eye
yellow
1
center eye
yellow
2
center eye
yellow
2
center eye
yellow
2
center eye
orange
1
below eye
orange
1
upper eye
green
1
upper eye
yellow
1
debatable intermediates
white black white white
white white washed gray white
white light gray white white
upper eye
above eye
above eye
orange
orange
orange
light gray
light gray
characters
black
light gray
black
black
black
black
black
light gray
black
black
white
black
black
light gray
black
black
white
white
composed of an intermediate male and a West
Grebe female were recorded at the breed
colony in Farmington Bay, Crystal Unit
complete assessment of pair composition v
not attempted. Three other Clark’s Grebe p;
were nesting in a channel in the reeds at Tun
Unit and, at Strawberry Lake, two Western Grc
pairs with a nest were found. Most gret
encountered at Minersville Reservoir weredd
in groups or dispersed: at the east end, three si
rather baste platforms existed, all maintained
Western Grebe pairs.
Pairs with chicks were present at Panguitch
Lake six Western Grebe families, an intermedi¬
ate female with two chicks was together with a
Western Grebe male: Bottle Hollow Reservoir —
four Western Grebe families, a debatable Western
Grebe female with one chick was paired to a
Western Grebe male and a debatable Western
Grebe male was with a Western Grebe female and
(wo chicks; Ouray National Wildlife Refuge— two
Western Grebe families, a debatable Western
Grebe male had two chicks with a W'estem Grebe
female; and Strawberry Lake — nine Western
Konter • INTERBREEDING OF AECII MOPHORUS GREBES
717
WG DVO IG KG CG
FIG. 1. Subdivision of Aechmophorus grebes identified
into Western Grebes (WG), debatable Western Grebes ( '
WG), intermediates (IG), debatable Clark's Grebes ( * CG I.
and Clark's Grebes (CG) in Utah. USA.
Grebes, two Clark’s Grebe families, an interme¬
diate female with two chicks was paired to a
Western Grebe male, a debatable Western Grebe
male, and a Western Grebe female cared for two
chicks.
Additional pairs were recorded either display¬
ing or swimming. An intermediate male displayed
with a female Western Grebe at Strawberry l.ake
and at Lake Powell, and three Clark's Grebe pairs
and two Western Grebe pairs displayed at Farm¬
ington Bay, Turpin Unit. A debatable female
Western Grebe was with a male Western Grebe at
Minersville Reservoir, and an intermediate male
appeared to be paired with a female Clark’s Grebe
at Willard Bay. Two Clark's Grebe pairs were
recorded at Benson Marina and at Cache Junction,
one Western Grebe pair was at Lake Powell, and
one Clark’s and two Western Grebe pairs were at
Willard Bay. No clearly identifiable pairs were
present elsewhere (Table 4).
Observed and expected frequencies of pair
composition varied (Table 5). The x: Goodness
of fit test provided no evidence contradicting like-
with-Uke or assortative mating, whether consid¬
ering only grebes with platforms and pairs having
ollspring or including displaying pairs and grebes
in twos that seemed paired.
DISCUSSION
I found no evidence contradicting assortative
mating in the two Aechmophorus species. How¬
ever. 6.5% of 660 grebes assessed had apparent
intermediate traits and another 7.6% were either
debatable Western or Clark's grebes. These
represented 14.1% of the population assessed.
This percentage could be biased towards interme¬
diates as they could be over-represented outside
active breeding colonies. They could disperse to
non-breeding areas relatively more rapidly than
Western and Clark's grebes as sexual selection
may put them at a disadvantage (Nuechterlein
1981a). A comparison with historical occurrences
of intermediates in Utah and other major areas of
sympatry suggests present day numbers have
increased. Intermediates were few' in 1963 (Storer
1965) at Bear River Migratory Bird Refuge, Utah,
and they represented only 0.7% of the population
in 1975 in = 3.376; Ratti 1979). They were also
<1% in >8.000 observations in California,
Nevada. Oregon, and Utah (Ratti 1981). My data
from northern California and southern Oregon in
2009 confirmed assortative mating, but percent¬
ages of intermediates were increasing; 3.3% of the
grebes clearly had intermediate traits and another
0.4% did not entirely conform to either species
(/; = 1 ,293) (Konter 201 l ). This percentage is not
comparable to the 7.6% reported for Utah as the
methodology used in 2009 included a major part
of debatable individuals in the counts of either
Western or Clark's grebes; if used in Utah, only
1 .5% of the grebes were classified as debatable
whereas the remaining 6.1% were counted as
either Western or Clark’s grebes.
It is generally debatable to what extent
individuals displaying intermediate traits in the
field are hybrids between two closely related
species or represent phenotypic variation. Studies
of hybridization in other species based on visual
identification, whether constructing a hybrid
index (Hoffmann et al. 1978, Bell 1997) or not
(Rasmussen 1991. Baker and Boy Ian 1999). relied
TABLE 4. Pair composition differentiating among Western (WG), Clark's (CG). debatable Western (± WG).
debatable Clark's (± CG). and intermediate (IG) Aechmophorus grebes. Utah. USA.
Total of WG pairs
Total of CG pairs
Mixed pair composition
Pairs with platform/nest
10
5
1 IG X WG
Families
21
2
2 WG X IG. 3 ± WG X WG. I WG X ± WG
Gther pairs
5
8
2 IG X WG. 1 WG X ± WG. 1 IG X CG
718
THE WILSON JOURNAL OF ORNITHOLOGY • Vo l 124. No. 4. December 2012
TABLE 5. Observed and expected frequencies of pairings in nesting Aechmophorus grebes and grebes with chicks
among Western ( n = 69). Clark's (/i - 14). and intermediate grebes (// = 7). and in all pairs assessed among Western (n =
82). Clark's (n = 31). and intermediate grebes (n = II ).
Pair composition
Pairs nesling/tending young
All pairs assessed
Observed frequency Expected frequency Percent deviation
Observed frequency
Expected frequency
Percent deviation
WGXWG
31
26.36 +17.6
36
27.00
+33.3
WGXCG
0
10.85 -100
0
20.67
-100
WGXIG
7
5.43 +29.0
10
7.33
+36.4
CGXCG
7
1.02 +584.6
15
3.78
+296.8
CGXIC.
0
1.10 -100
1
2.77
-63.9
IGXIC.
0
0.24 -100
0
0.45
-100
X Goodness of fit test y2
= 48.41, df = 5. P < 0.0001
T = 59.5
1. df = 5. P < 0.0001
on intermediary plumages between species to
identify hybrids. DNA analysis could provide
more reliable results. Genetic data may not solve
the problem in the case ol Aechmophorus grebes.
Studies ot the genetic dissimilarity between
Clark's and Western grebes have had inconsistent
results (Guerra and Speed 19%, Nuechterlein and
Buitron 1998. Kerr ct al. 2007). The relaliv.
frequency of mixed species pairs of up to 5%
depending on populations (Nuechterlein anc
Buitron 1998), and the observations of mixec
pairs with viable offspring (Ratti 1979; Storer am
Nuechterlein 1985; Nuechterlein and Buitror
1998; pers. obs.) leave little doubt that hybrid)
exist. Observations of intermediates with yotin^
were sufficient proof for the fertility of mixec
species pairs' descendants for Nuechterlein ami
Buitron (1998). They considered that hybridiza¬
tion for Aechmophorus grebes may reflect an
adaptive mate choice rather than a mistake. Thus,
debatable individuals or intermediates can be
considered suspected (Eichhorst and Parkin 1991 )
or presumed (Nuechterlein 1981a) hybrids
Randier (2008), in his meta-analysis of avian
hybrid zones, concluded assortative mating was
-stronger m narrow hybrid zones compared to
wider ones. Th.s supports the presumed hybrids
"m n ~Sr,udy.and ,for Califomia-Oregon (Konter
-Oil) f°r largely sympatric Aechmophorus
populations. Lower percentages were recorded
n P'aine Canada, a region of relative allopatry
where Clark s Grebes represent only I -4% cp
the Aechmophorus population. Nuechterlein and
Buitron U 998) rePorted intermediates represent-
ed <4,o of the population in 1980 and in the
early iqqos at Delta Marsh. Manitoba. Konter
(2009), ln a survey of different lakes in
Manitoba and Saskatchewan in 2008. found
3% intermediates.
Reinforcement of incompatibilities by selection
in sympatry (Servedio and Noor 2003) should lead
to a taster reduction of interbreeding in sympatric
than in largely allopatric populations (Randier
2006). Increased percentages of intermediates in
Utah and Cali torn ia-Oregon a priori contradict
growing reinforcement of incompatibilities be¬
tween both Aechmophorus grebes. Hybridization
becomes an ongoing process acting against
narrowing of hybrid zones (Randier 2008) if. in
situations with limited choice. Aechmophorus
grebes do not pair assortatively.
Gene flow can prevent speciation even at low
rates (Winker 2010) and development of postzy-
gotic incompatibilities possibly originating ~-
million years after divergence (Price and Bouvier
2002). We may question whether the existing
prezygotic barriers to random mating in Aechmo¬
phorus species are not being lost as numbers of
intermediate Aechmophorus grebes generally in¬
crease (Konter 201 1 ). Repeated backcrossing may
give rise to individuals of mixed ancestry that can
^ UlOUIIgUIJIICU ..v*... ,,u,w . .
(Howard et al. 2003. Randier 2004) and they are
absorbed into one parental species. The process of
introgressive hybridization (Anderson and Hu-
bricht 1938). besides introducing new variation
into the parental population, may reduce differ*
ences in advertising calls between Western and
Clark s grebes. This is a possible reason for the
near total absence ot Clark's Grebes at Panguitch
Lake in 2010; only two of 43 grebes assessed
were Clark’s and six displayed intermediate traits.
Clark’s Grebes were a specialty at this lake in the
late 20th century (Mclvor 1998).
Konter • INTERBREEDING OF AECH MOPHORUS GREBES
719
Hybridization in the case of Aechmophorus grebes
seems to be progressing while in the Held its
real extent might be masked by the effects of
inlrogression. Mate choice may be less apparent
when the population consists almost entirely of
highly recombined hybrids (Barton and Hewitt
1985). Feerer (1977) found intermediates to be
extremely frequent representing 30 and 51% at two
lagoons in surveys of Mexican Aechmophorus
populations, generally dominated by Clark's Grebes.
Repetition of this study for Mexican populations,
coupled with genetic analyses, is needed in reviews
of the taxonomic status of Aechmophorus grebes.
ACKNOWLEDGMENTS
I thank my wife Maria for assistance during fieldwork in
Utah, and the referees and the editor of the Wilson Journal
of Ornithology for their welcome and useful comments on a
first draft.
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LANDSCAPE-LEVEL FOREST COVER IS A PREDICTOR OF
CERULEAN WARBLER ABUNDANCE
FRANK R. THOMPSON III,14 MARK B. ROBBINS,1 AND JANE A. FITZGERALD3
ABSTRACT. — We examined support for the hypothesis that abundance of Cerulean Warblers (Setophaga cerulea)
increases with percentage of bottomland and upland forest, and decreases with percentage of developed land at a local-
habitat scale (within a 250-m buffer) and increases with percentage of all forest at a landscape scale (within a 10-km
buffer). We conducted surveys along 16 rivers in Missouri and Arkansas from 1999 to 2006 and related habitat and
landscape factors to counts of Cerulean Warblers in 123 5-krn segments on these rivers. We detected 576 singing male
Cerulean Warblers and found support for both local and landscape effects on Cerulean Warbler abundance. Model fit was
good with an average correlation of 0,841 between predicted and observed values based on an eight-fold cross-validation
procedure. The abundance of Cerulean Warblers increased 390.7, X.7. and 4.1 limes across the observed range of forest
within 10 km. bottomland forest within 250 in. and upland forest within 250 m. respectively. Conservation and research
need to address large-scale forest patterns in addition to local habitat for Cerulean Warblers. Further research is needed on
abundance patterns across riparian and upland forests and demographic rales in this part of their range. Received 17 April
2012. Accepted 19 June 2012.
There is great conservation concern for the
Cerulean Warbler (Setophaga cent lea) (Hamel et
al. 2004). largely the result of range-wide declines
in their abundance (Sauer el al. 201 1). Loss or
alteration of breeding habitat has commonly been
assumed to be a cause of declines; however, little
is known about their wintering range and threats
during the non-breeding season (llamel 2000).
Recent demographic analyses indicated increasing
overwinter survival would have (lie greatest effect
on population growth and that increases in the
amount of forest cover in agricultural-dominated
landscapes may be required to increase fecundity
(Buehler et al. 2008).
Local habitat characteristics associated with
Cerulean Warblers include mature deciduous
forest with large trees and heterogeneous canopies
(Hamel 2000, Jones and Robertson 2001. Roth
and Islam 20()S. Bakermans and Rodewald 2009.
Hartman et al. 2009). Heterogeneous canopies
used by Cerulean Warblers have been associated
with riparian or bottomland forests (Hamel el al.
2004. Carpenter et al. 2011). upland forest and
ridgetops (Dettmers and Bart 1999. Weakland and
Wood 2005, Buehler et al. 2006, Newell and
' L'.S. Department of Agriculture. Forest Service, Nonh¬
em Research Station, 202 Anheuscr- Busch Natural
Resources Building. University of Missouri. Columbia.
MO 65211. USA.
University of Kansas Natural History Museum and
Biodiversity Research Center. 1345 Jayhawk Boulevard.
Lawrence. KS 66045, USA.
American Bird Conservancy. 14264 Reno Springs
Road, Reeds Spring, MO 65737, USA.
‘Corresponding author: e-mail: lrthompson@fs.fed.us
Rodewald 2011), and timber harvest (Oliarnyk
and Robertson 1996. Rodewald and Yahner 2000.
Bakermans and Rodewald 2009. Newell and
Rodewald 2012). Cerulean Warblers generally
prefer heavily forested landscapes and are con¬
sidered area sensitive. Landscape effects include
positive effects of percent forest or forested
wetlands in a I- to 8-km radius and negative
effects of edge anil open or agricultural land
(Hamel et al. 1998, Detimers and Bart 1999,
Thogmartin et al. 2004, Weakland and Wood
2005, Buehler el al. 2006. Wood et al. 2006).
Landscape requirements may vary across the
breeding range and Cerulean Warblers may
require larger patches iu more fragmented land¬
scapes with less forest (Hamel 2000).
Understanding how habitat and landscape
factors affect abundance of Cerulean Warblers
across their breeding range remains a research
priority (Hamel 2000; Hamel e( al. 2004, 2006;
Hamel and Rosenberg 2007). Local or landscape
factors affecting abundance of Cerulean Warblers
remain largely unstudied in Missouri. This state is
the western terminus of (he both the Cerulean
Warbler’s range and the central hardwoods forest
region, the most important forest region for the
Cerulean Warbler (Hamel 2000). Past studies
have spanned micro-habitat to landscape scales,
but none has directly compared support for the
importance of local habitat versus landscape
forest composition. A large proportion of Cerule¬
an Warblers breed in riparian forest in portions of
this species’ range such as Missouri and Arkansas,
which have been poorly sampled using conven¬
tional survey methods (Jacobs and Wilson 1997,
721
722
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124. No. 4. December 2012
Robbins et al. 1998). The latter (1998, 2010)
conducted river-based surveys in 1999-2006 in
Missouri and northern Arkansas to address this
lack of data and document occurrence of some
species of concern, including Cerulean Warblers,
in riparian habitats across the state. These surveys
are not a representative sample of forest in the
state but they do represent forests where Cerulean
Warblers are known to occur and reach modest
densities (Reidy et al. 2011). The study design
provided an opportunity to assess how local-
versus landscape-scale habitat composition affects
abundance in this previously unstudied region.
Our objective was to evaluate the relative
support for the hypotheses that percentage of
bottomland and upland forest had a positive
effect, and developed land a negative effect on
abundance of Cerulean Warblers in Missouri and
Arkansas. We compared support for effects at: ( I )
a local-habitat scale (within a 250-m buffer), (2) a
landscape scale (within a 10-km buffer), or (3) a
combination of local-habitat and landscape scales.
Chariton
Big Piney
Jack's Fork River
James River
North Fork
White River
r- Buffalo River, AR
Black River
HG. I Portions of rivers along which we measured effects
of habitat aiul landscape factors on the number of singing
Cerulean Warblers in Missouri and Arkansas, 1999-2006.”
ivitiJ II W LAS
Study Area. We conducted surveys along
rivers in Missouri and northern Arkan:
(Fig. l).We selected rivers that had at least so
riparian lorest along them, occurred across i
region and along a gradient of landscapes fr<
mostly forested to minimally forested, anil w.
accessible by canoe to allow us to conduct surve
across public and private land. Rivers in southe
Missouri and northern Arkansas occurred
landscapes of rolling hills covered primarily w,
hardwood toresLs interspersed with glades a:
woodlands and dissected by deep river valleys T
two rivers in northern Missouri occurred
landscapes dominated by cropland and pasta
with narrow corridors of riparian forest. Forests
the nver floodplains included oaks (Q, terms spp
hickories Katya spp.). ash (Fraxinus spp.). mapl,
ind Am-' hackbeny °r suSarbcrT (Cel, is spp.
Forei i r SyC;aTe {Plant™“s Occident 1
Northern A t ^ W 80uther» Missouri an
extremes (i.e.. after heavy rains which ZtJZ
ow and no.se. or during low water levels) and onK
under conditions of no precipitation and no or ve.y
light wind. Wc surveyed river sections that did not
exceed 20 km, with lew exceptions, to ensure
surveys were completed by -1000 hrs. River width
was generally <50 m ( maximum 90 m) and birds on
both sides of the river could be heard. Robbins etal.
(2010) estimated that Cerulean Warblers could be
heard 100 m in width on each side of the river
hank. Each Cerulean Warbler was heard singing at
least twice before being recorded to ensure it was
not confused with Type B (= Song Type II).
(Moldenhauer and Regelski 1996) of Northern
Farula f.S. americana). We calculated coordinates
°l each singing Cerulean Warbler by estimating the
direction and shortest perpendicular distance to a
bird from our position on the river with a laser
rangefinder; we measured our position on the river
w ith a global positioning system unit (Gannin 12,
Map Datum WGS 84). Observations were directly
marked on topographic maps on a limited number of
surveys. Lour observers conducted surveys but (he
same observer conducted all surveys on a river to
eliminate multiple surveyor bias (Sauer et aJ. 1994).
Habitat and Landscape Measurements. — We
partitioned rivers into 5-km segments and created
250-m and 10-km flat-ended buffers around each
segment in a geographic information system so
there was no overlap in buffered areas between
•segments. We partitioned rivers into segments to
account lor variation in land cover along the rivers
and 5-km was sufficiently large to capture variation
Thompson et al • LANDSCAPE EFFECTS ON CERULEAN WARBLER ABUNDANCE 723
in numbers of birds. We calculated the number of
singing Cerulean Warblers in each segment. We
created maps of selected land cover types for the
two different buffer sizes around each river from
Version 7-21-2000 of the National Land Cover
Data (NLCD: http://www.mrlc.gov/). We com¬
pared 2000 and 2006 versions of the NLCD since
surveys spanned 1999-2006 and there was <1%
decline in forest cover. Thus, wc used the 2000
NLCD for all analyses to avoid having to address
potential compatibility issues between classifica¬
tions. We mapped upland forest as all forested
upland classes from the NLCD, bottomland forest
as the woody wetland class from the NLCD.
developed land as all developed classes from the
NLCD. and forest as bottomland and upland forest
combined. We intersected each buffered river
segment with the land cover map in a geographic
information system and calculated percent cover¬
age of each land cover.
Statistical Analysis.— We used an information-
theoretic approach (Burnham and Anderson 2002)
to evaluate our three hypotheses concerning factors
affecting Cerulean Warbler abundance. We con¬
structed a set of three candidate models represent¬
ing our three hypotheses plus a null model
consisting of only an intercept term representing
constant abundance. We included percent cover of
upland forest, bottomland forest, and developed
land in the 250-m buffer as fixed effects in the
model for hypothesis # I (local effects). We
included percent cover of upland forest, bottom¬
land forest, and developed land in the 10-km buffer
for hypothesis # 2 (landscape effects). We included
percent cover of bottomland forest and developed
land in the 250-m buffer and percent forest in the
10-km buffer for hypothesis # 3 (local and
landscape effects). We combined forest types in
the 10-km buffer to reduce cross scale correlation
with bottomland forest in the 250-m buffer:
tolerance values were >0.48 for all variables in
the model indicating no substantial multicollinear-
ity (Allison 1999). We used percent forest cover in
a 10-km buffer as a metric of habitat availability
and fragmentation (sen.su Robinson et al. 1995)
because other fragmentation statistics are highly
correlated with percent forest cover in Midwestern
landscapes (Robinson et al. 1995, Thompson et al.
2002). Percent forest cover best explains variation
in nest predation (Lloyd et al. 2005), and is a strong
predictor of Brown-headed Cowbird ( Mnlothrus
uter) abundance and parasitism (Donovan et al.
2000, Chace et al. 2005, Lloyd et al. 2005).
We compared support for the models by
ranking models from most to least supported
using Akaikc's Information Criterion for small
sample sizes tAKV; Burnham and Anderson
2002). We evaluated the goodness-of-fit of the
selected model using a /.-fold cross validation
procedure (Boyce et al. 2002). We sequentially
removed 15 randomly-selected observations with¬
out replacement and evaluated how well predic¬
tions from a model fit to the remaining observa¬
tions, compared to observed values for the 15
observations, eight times and calculated the
Pearson correlations between observed and pre¬
dicted values We plotted predicted counts of
Cerulean Warblers for ~1() values across the
range of each supported covariate that had
biologically meaningful effects while holding
other covariates at their mean.
We fit a generalized Poisson model with
random intercepts by maximum likelihood (Proc
GLIMIX; SAS Institute Inc. Cary, NC. USA). We
initially fit both a standard Poisson and general¬
ized Poisson model (Joe and Zhu 2005) to our
global model and. since the generalized Poisson
had a lower AlCr and overdisperion parameter
(c*), we used it for all candidate models. We
specified rivers as the subject for the random
effect which allowed the intercept to vary among
rivers. A river was surveyed in 1 year by the same
observer and in a narrow range of dates; this
model allowed us to accommodate year, observer,
and date effects on detection probability. This
model also acknowledges the likely correlated
abundances of Cerulean Warblers among seg¬
ments on the same river. Counts estimated by this
model are an index of relative abundance, but the
random intercepts can account for difference in
detection among rivers (and hence observers)
when estimating the fixed effects. We acknowl¬
edge the desirability and benefits of methods that
directly consider the probability of detection
(Rosenslock et al. 2002); how ever, survey designs
that cannot estimate detection probability may
still provide useful indices of abundance (Johnson
2008).
RESULTS
We conducted surveys along 16 rivers from
1999 to 2006 that we subsequently divided into
123 5-km segments. We detected 576 singing
male Cerulean Warblers with an average of 4.7
singing males per 5-km segment. Land cover
varied among rivers ranging from 30.7% forest in
724
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124, No. 4. December 2012
s'lE '■ Descriptives,atistics for variables used in models to estimate the number of singing male Cerulean Warblers
o 10 L 7 k rri' ' W'2006- Habi“' VariahlCS lhe °f «* >"=* defined by
or lu-km buffer represented by that vegetation type. ’
Variable
Number singing males
Bottomland forest in 250 m
Developed land in 250 m
Upland forest in 250 m
Bottomland forest in 10 km
Developed land in 10 km
Upland forest in 10 km
Forest in 10 km
Mean * SD
4.7 ± 5.66
6.07 ± 8.05
0.27 ± 0.45
68.57 ± 18.92
0.67 ± 1.19
0.27 ± 0.34
80.27 ± 16.13
80.87 ± 15.35
Min Max
0.0
18.0
0.0
36.5
0.0
3.2
11.5
96.0
0.0
6.6
0.0
1.5
25.8
96.8
.30.7
97.3
a 10- km buffer in north Missouri to 97.3% fores
in southeastern Missouri (Table 1 ).
We found support for both local and landscape
effects on Cerulean Warbler abundance. The
model with both landscape and local effects had
overwhelming support (w, = 0.984; Table 2).
Model lit was good based on the £-fold validation
procedure with a mean Pearson correlation of 0.84
(range = 0.67-0.96) bclween predicted and
observed values and the overdispersion parameter
was dose to I (c = 0.83). Abundance of Cerulean
Warblers mcreased 390.7. 8.7, and 4.1 times over
the observed range of forest within 10 km
bottomland forest within 250 m. and upland forest
within 250 m. respectively (Fig. 2). The 95%
confidence mtervals for the effects, bottomland
and upland forest within 250 m. overlapped zero
e a), which indicated some uncertainty in
these effects. However, the weight of evidence for
he most supported model with the effects
bottomland and upland forest, was 61.5 times
that of the second most supported model without
those effects (wj/w2; Table 3). The model coeffi¬
cient for (he percent of developed land within
250 m was relatively large and negative compared
to other coefficients (Table 3) but. because
pei cent developed land only ranged from 0 to
1-5%, the overall effect on density was smaller
than other effects and the confidence interval was
large.
DISCUSSION
Wc found strong support for our hypothesis that
abundance was affected by both local and
landscape-scale habitat composition. The greatest
Ufeei on abundance was the amount of forest
within a 10-km buffer, followed by the effect of
riparian forest and upland forest within a 250-m
buffer. The strength of the effect for the amount of
orest in the landscape emphasizes rhe importance
of extensive forest areas for the Cerulean Warbler
and the potential negative effects of fragmenta¬
tion, edge, or imerspersion of non-forest land
uses. Counts of Cerulean Warbler were predicted
table 2
for small
II samples (AICc), differencTi^AIcJ !yom"he 2 2 X I?8 likelihood- Akaik«-*'-s Information Criteria adjusted
Parameter (o) for models estimating nT T*' ,(A)* Akaike "eights Or,*. and overdispirsion
Missouri, 1999-2006. nmber of s'"8'"S Cerulean Warblers in 5-km river segments in
-50 m + upland forest 250 m + forest 10 km
Intemepi. dcve.oped 10 km + bottomland fomst
10 km + upland forest 10 km
*^ + ***« 250 m + talomland forest
-50 m + upland forest 250 in
Intercept
560.42
578.61
573.14
584.81
A
H7
c
0.00
0.984
0.83
8.26
0.016
0.73
37.82
0.000
0.55
49.49
0.000
0.50
,lJ foresl- and "Plund deciduous foresi, respecmclv
ireAi
Thompson et al. • LANDSCAPE EFFECTS ON CERULEAN WARBLER ABUNDANCE 725
Percent bottomland forest in 250-m buffer Percent upland forest in 250-m buffer
20 40 60 80 100
Percent forest in 10-km buffer
FIG. 2. Effects of forest composition at a local and landscape scale on the number of singing Cerulean Warblers along
rivers in Missouri and Arkansas, 1999-2006.
to be essentially zero below 50% forest cover in
the 10-km buffer (Fig. 2). Other studies of forest
songbirds have found support for landscape versus
patch or habitat effects bill the strength of these
effects varies considerably (McGarigal and
McComb 1995, Howell et al. 2000, Hagan and
Meehan 2002, Lichstein et al. 2002. Betts el al.
2006). Landscape may have had a larger effect
on abundance than habitat factors because our
sampling was constrained to riparian areas where
forest is generally suitable for Cerulean Warblers.
The importance of landscape is also consistent
with the theory that habitat selection is hierarchi¬
cal anti landscape provides an important proxi¬
mate cue (Hilden 1965). Potential ultimate factors
affecting selection of more forested landscapes in
this region include lower nest predation and brood
parasitism (Robinson et al. 1995, Thompson et al.
2002).
Our finding that Cerulean Warbler abundance
was greater in extensively forested landscapes is
consistent with results elsewhere in their range.
TABLE 3. Parameter estimates for the most supported generalized Poisson model used to model habitat effects on the
number of singing male Cerulean Warblers along 5-km river segments in Missouri, 1999-2006.
Effect
Estimate
SE
95% CL
Intercept
-7.999
1.495
-1 1.187. -4.812
Developed in 250 m
-0.642
0.494
-1.622. 0.339
Upland forest in 250 m
0.017
0.0 1 1
-0.006, 0.040
Bottomland forest in 250 m
0.060
0.019
-0.021. 0.099
Forest in 10 km
0.088
0.016
0.056, 0.119
726 THE WILSON JOURNAL OF ORNITHOLOGY • Voi 124. No. 4. December 2012
Occurrence in the Lower Mississippi Alluvial
Valley is positively related to the amount of forest
cover within 4-8 km and negatively related to the
amount of agricultural land (Hamel et al. 1998).
Abundance in West Virginia is positively related
to the amount of forest cover in a 3-km radius and
negatively related to edge density (Wood et al.
2006) and distance to edge (WeakJand and Wood
2005). Our finding that the amount of bottomland
and upland deciduous forest at a local-habitat
scale positively affected abundance is also
consistent with patterns elsewhere in their range.
Cerulean Warbler abundance is positively related
to the percentage of forested wetlands and patch
size m a I -km buffer around North American
Breeding Bird Survey routes in the upper Midwest
(Thogmartin et al. 2004).
We surveyed riparian areas because they could
be easily accessed by canoe and previous experi¬
ence indicated Cerulean Warblers were rare in
upland forests in Missouri. Occurrence or abun-
ance in other parts of their range, especially the
Appalachian region, is associated with upper slopes
and ridges (Deltmers and Bart 1999. Weakland and
Wood 2005, Buehler et al. 2006) but, in the
southwestern part of their range. Cerulean War¬
blers are more common in bottomland or riparian
Jorest (Hamel et al. 2004, Carpenter et al. 201 1 ).
Cerulean Warblers in Missouri appear to select
landscapes and habitat similarly to elsewhere in
their range. The magnitude of the landscape effect
we observed reiterates the need for research and
conservation to consider landscape effects (e u
Buehler et al. 2008). We believe additional
research ,s needed in this part of the Cerulean
Warbler s range to better examine abundance
patterns across riparian and upland habitats and to
address key demographic parameters such as
fecundity and survival.
acknowledgments
co^lc;“rB^nrr,dfor
manuscript- a^u ^
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The Wilson Journal of Ornithology 124(4): 728-736, 2012
NESTING ECOLOGY OF SWAINSON’S WARBLERS IN A SOUTH
CAROLINA BOTTOMLAND FOREST
JENNIFER THOMPSON BISHOP,'" JOHN A. GERWIN.' AND RICHARD A. LANCIA'
South ^Caroijnai^JSA 1“ » M* **
Clutches averaged , ± SE) 3.19 - (, t0 e‘ and ^ ,Vf, XtlTl ""'T7 ^ “ Nmodal distribu,ioD
23-day cycle was 50% Lo<'isiic“exDosnn“'m‘ i t Hedglmgs per nest. 1 he Mayfield nest success estimate fora
(Molothrus ater) nest parasitism next arc and SUCCesS hc m,1M i'nPac'e‘J by Brown-headed Cowbird
and further from a swamp had the highest daily su^val'mleT^Vn 0^'^, ' '"purasi,ized nests ,hat were younger io age
Cowbirds with a 26% reduction in 8wain«nn- u/. ■ . n percent of nests were parasitized by Brown-headed
brooding was observed in 21% of 2000 and 200 1 slaLin^ 1,1 Produc,ion- Mul,iPle
the most common substrate used for nesting, although two-thirds of ih - n - , mes- such as -erecnbner (Simla* spp.), were
*i8a,Uea) within a 5'm ^ius. Received ,8 December 2-) 'As-
Kins _000, Benson and Bednarz 2010) The
iemaining three specialists: Carolina Parakeet
{Conn raps, s carolinensis ), Ivory-billed Wood-
princiP“lis and Bachman’s
exfin fi T™ bachma"i» are extinct or near
extinction as the result of habitat loss and other
factors (Askins 2000). Current assessments by
Partners in Flight (Panjabi et al. 2005) indicate
“ns in - s“
sssssre » DrnmM 2”'-
NC 27695. USA ^mvcrsuy, Box 7617. Raleigh.
Jones Street, Ra'leU1 NcTy^lT usa' Scienccs- 11 Wesl
On. vers, ty. Box 7646. Raleigh. NC 27695. wSA
Corrcsponding author; e-mait: bishopj@uni(,n.^'
728
Swainson s Warbler is a leaf-litter special!:
that breeds in the southeastern U.S. and winters i
the C aribbean Basin. Breeding habitat in bottom
land hardwood forests of the Atlantic and Gul
coastal plains and in high mountain riverine area
ol the Appalachian Mountains is disjunct. Severa
studies since Meanley’s (1971) seminal mono
graph on Swainson's Warblers have shed eonsid
viable light on this bird’s habitat preference anc
breeding biology (Graves 2002, Henry 2004.
Benson et al. 2010b). although gaps still exist,
pai ticularly in understanding of its breeding
biology. This warbler's secretive nature, inhospi¬
table breeding areas, and inconspicuous nests
have resulted in its classification as the most
pooi | y understood of the migratory warblers
(Brown and Dickson 1994. Graves 1996).
Hus species a I Unity for early-successional
habitat or disturbance gaps in primary forest
(Carrie 1996. Graves 2001, Henry 2004." Benson
ct al. 2009) could allow lor dual management ol
Swainson’s Warblers while concomitantly ex-
tracting timber through alternative forest manage¬
ment practices, (i.e., wildlife forestry), which
maintain habitat heterogeneity and ecological
integrity (Heltzel and Leberg 2006, Twedt and
Somershoe 2009). Only a few studies have
examined Swainson’s Warbler productivity in
industrial forests (Carrie 1996. Peters et al.
-0(b, Bassett-Touchell and Stouffer 2006). Most
studies have been in non-industrial forests (Eddel-
man et al. 1980. Thomas et al. 1996. Graves 2002.
■Somershoe et aL 2003, Lanham and Miller 2006.
enson et al. 2009). which are typically subjected
.° min‘mid harvesting when compared to more
ntensively-managed private lands. Understanding
Thompson Bishop et at. • SWAINSON’S WARBLER NESTING ECOLOGY
729
this species’ productivity in industrial hardwood
forests is valuable considering most of tile
population is likely located on private lands
frequently managed by timber companies.
The Swainson's Warbler is in need of manage¬
ment and monitoring attention, but the lack of
available information jeopardizes sound manage¬
ment decisions (Graves 2001). Our objectives
were to: (1) describe nest-site characteristics and
nesting phenology of Swainson's Warblers, (2)
assess nesting success in a managed landscape,
and (3) document the effect of Brown-headed
Cowbird (Molothrus ater) parasitism on Swain¬
son's Warbler nesting success.
METHODS
Study Area. — The Woodbury Wildlife Manage¬
ment .Area (WWMA; 33 52' N, 79 22' W) is^an
8,000-ha peninsula at the confluence of the Great
and Little Pee Dee rivers near Britton's Neck,
South Carolina. Elevation ranges from 0 to 25 m
above sea level and includes small isolated
wetlands, sand ridges, planted loblolly ( Finns
tueda ) and longleaf pine (P. palustris) stands, and
large expanses of riparian bottomland hardwoods
(Peters et al. 2005). WWMA bottomlands are
dominated by broad leaved deciduous trees,
consisting mainly of sweetgum ( Uquiilambar
styraciflua), red maple (Acer mbrum), and
ironwood (Carpi nits caroliniana) with an under
story of holly (Ilex spp.). numerous vine species
le.g.. Campsis . Vitus, Smiiax). blackberry (Rubus
spp.), and cane (Arundinaria tecta and A. gigantea
combined into a single classification). Our efforts
were focused on a 150-ha bottomland hardwood
stand that experienced drying in late summer to
early fall, followed by wet winters, and frequent
early spring flooding lasting up to 25% of the
breeding season (Martin et al. 1993).
WWMA was privately owned timberland until
purchased by the State of South Carolina in 2006.
Georgia Pacific Corporation harvested the site
between 1978 and 1983 by shearing all saplings
and stumps, and then allowed the site to naturally
regenerate (Peters et al. 2005; Wayne Smith, pers.
comm.). Even-aged regeneration of hardwoods
followed clearcuiting with interspersion of uncut
drainages resulting in a mosaic of young and more
mature hardwoods (Peters et al. 2005). These
stands had not been replanted, thinned, or treated
with herbicides since the last harvest.
Data Collection.— We began a study that lasted
five seasons (1999-2001. 2005-2006) starting in
mid-April and lasting through July. We used spot
mapping to locate Swainson's Warbler territories,
followed by systematic nest searches; some nests
were discovered opportunistically, while conduct¬
ing other activities including vegetation sampling
or mist netting. We used radiotelemetry in 2005-
2006 to locate nests instead of systematic
searches. Nest locations were recorded using a
Trimble GeoExplorcr II. Global Positioning
System (Trimble Navigation Limited 2001) and
exported into Arc MAP Version 9.3 (Environmen¬
tal Systems Research Institute. Redlands, CA.
USA).
Unknown nest outcomes were minimized by
increasing nest content checks from every 3 days to
daily nest observation 6 days post hatching. We
followed Martin and Geupel's recommendations
(1993) in an attempt to prevent observer-induced
nest failure, and replaced physical checks with
binocular observations at -5 or 6 days post
hatching. Nestlings whose hatching date was
unknown were classified to age by examining
leather development (Table 1). The potential
fledging interval began 8 days after hatching as
95% of the nestlings fledged after 8 days (Thomp¬
son 2005). We were careful not to assign a known
fate unless one or more fledglings were detected, or
the chicks reached the potential fledging interval as
late predation increases the risk of overestimating
nesting success (Williams and Wood 2002). A nest
was considered successful if si warbler nestlings
fledged (Mayfield 1975).
We collected multiple scales of nest-site data in
July, at least a week alter fledging, including nest
characteristics, description of the surrounding
plot, and neighboring landscape information. Nest
characteristics included; nest height (base of nest
to ground), nest cup diameter and depth, outer
nest diameter and depth, distance of the nest to
substrate stem, diameter at breast height (dbh) of
the substrate, and substrate species. All nest
measurements were recorded from tightly packed
leaves rather than the furthest leaf margins to
ensure standardization. We counted the number of
cane stems at the nest-site scale (5-m radius
surrounding each nest), and recorded the distance
of nests to roads, sloughs, and sw amps.
Data Analyses.— We calculated Swainson’s
Warbler daily nest survival rate at WWMA using
two methods: Mayfield's (1975) approach with
Johnson’s (1979) standard error estimator, and
Shaffer's (2004) logistic exposure method. Shaf¬
fer and Thompson (2007) discourage using
730
THE WILSON JOURNAL OF ORNITHOLOGY . Vol 124. No. 4. December 2012
*“» *— a, Woodbun
Day
0
Nestling uppcarance
Dark pink mass, head down
£S=S«“~s^sr.-—
Pin feathers he,„£ sarfaee *"» «" — *
’XS iZ7 d°W"y Pi" “ «*•• » "neign down midline of back
alUivcr telly"0 °f baCk and nCCk- SidCS °f brCaSt' chin’ ***** of ^
- Set ::tr,hshcr s ^ rr co,cm - ~ •* <-»
uTmS ' 5 £*-2 ~ “rs 2:,:
Two pronounced lulls of down on head' head f„|’|vV' rl ' a,,d other WI"S lathers still in feather sheaths
breas, fully feathered, T* ***" ^ °f ^ ‘>U1 offc-hr sheaths:
devcioping tha, nre short end s.uhhvf f,=^ *“■ ^ °” -* « *=■*■"
Mayfield’s ,1975) approach, bu, we included il
or comparison purposes with other studies of
Swatnsons Warbkrs. The logistic exposure
method, a binomial distribution, requires each
exposure interval to be assigned either a 0 or a 1
°r*~ intervals, respectively
(Shaffer -OWi. Exposure intervals of known and
unknown lale were truncated as suggested hy
Man ohs et al. ,2000). We assigned each day of the
breeding season a number starting with 28 April
the earliest nest initiation we observed Nest
observations were frequently >] day and we
eraged the exposure period to assign a date to
each interval. Observa.ions from the budding
stage were excluded from the analysis; thus nest
age began with the hatching day A wa
Zffo £ Tr* if 11 SL one
CBurhiins “ l ”"* "* pe™d
(BumVamanTA T Candid“'= models
urnnam and Anderson 2002), based on o..r n,mi
5&3F*3s&
2) day oi ,he -vear ^rant et al ?()05i Ju
or (3) nest age or stage (Gran, e, al. 2005) We dfd
not assume constant survival during the nesting
cycle and modeled linear, quadratic, and cubic
ellects of nest age as well as linear and quadratic
effects of date following Grant et al. (2005). The
biological models focused on Brown-headed
Cowbird parasitism. The features examined for
habitat and landscape models focused on nest
height, cane density, and distance of nests to edges
including roads, sloughs, and swamps.
We used logistic-exposure models in PROC
GHNMOD (SAS Institute 2004. Shaffer 2004) and
calculated Pearson correlation coefficients for the
oZble,S, USing PR0C CORR (SAS Institute
-004). Highly correlated variables (r > 0.70)
vvere not included in the same model. We used
Hie I losmer and Lemeshow (2000) goodness of fit
,eM lo SauSe 'he fit of the global model. Candidate
models were ranked according to Akaike's
Information Criterion for small sample sizes
(AIC ) (Bum ham and Anderson 2002). Models
with lower AAICr values and higher AIC, weights
were considered to he the best supported. '
\Ve used null hypothesis testing, setting P <
' fof significance, to compare the effect of
roun- headed Cowbird parasitism on hatching
an Hedging rates of Swainson’s Warblers. All
estimates relating to the length of nesting periods
MC l,"1Ch SIZe are exPressed mean ±95% Cl.
,;!y IC dai,y survival rates and microclimate
dta are expressed as mean ± SE.
Thompson Bishop el al. • SWAINSON’S WARBLER NESTING ECOLOGY
731
1 2
3 4 5
■ 2001
□ 2000
□ 1999
Week
FIG. 1. Swainson's Warbler nesl initiations based on initiation week for 1999-2001 nests at Woodbury Wildlife
Management Area. South Carolina. Week I began on 24 April and week 1 1 ended on 9 July.
RESULTS
Breeding Phenology and Cl ii roll Size.— We
located 144 nests of which 78 were active: 18 in
1999. 22 in 2000, 23 in 2001. 5 in 2005, and 10 in
2006. Most active nests were found during
incubation with 28 % discovered before egg
laying, 12% during egg laying. 40% during
incubation, and 9% during the nesl ling phase
(11% had an unknown discovery lime). The
excellent condition of 66 inactive nests indicated
Ihey were built in the discovery year.
Males arrived during the first 2 weeks of April
followed by the females several days later. First
nests were built in late April to early May, and the
earliest egg (nest initiation) was laid on 28 April
1999 and the latest on 12 July 2006. There were
two average peaks in nesting during 1999-2001,
one occurring the first week of May and the other
the second week of June (Fig. I ). There was
substantial yearly variation in nest initiations.
Nest initiations in 2001 and 1999 were bimodal.
Nests remained empty after completion for 1 to
6 days (x ± SE - 2.64 ± 0.99, n = 14 clutches).
Females laid one egg per day and began incubation
with the laying of the last egg ( A’incubatioii Icngdi
13.85 ± 0.54 days; n - 14 clutches). One female
continued to incubate three eggs during the 1999
Hood with flood waters I m below her nest. This
nest failed several days later, although she
remained incubating above floodwaters the entire
time. A clutch of seven eggs, the largest detected,
hatched six eggs but most nestlings disappeared
before the potential fledging period, leaving only
two fledglings. Clutches averaged 3.19 ± 0.20
eggs (// = 69 clutches. 220 eggs total). Hatching
was synchronous unless Brown-headed Cowbird
eggs were present, in which case the cowbird egg
hatched at least I day in advance of the Swainson’s
Warbler eggs ( v - 1,46 ± 0.23 days; range - 1-
3). Eighty-one percent of the eggs that survived the
incubation period hatched ( J 29/158). One hundred
and twenty-nine of the 220 Swainson’s Warbler
eggs laid produced nestlings of which 80 fledged.
The nestling period lasted 9.94 ± 0.20 days (n =
17 clutches) with 2,50 ± 0.33 fledglings per nest
(n — 32 clutches, 80 fledglings). Seven nests were
observed front start of incubation through fledging
and were used to calculate a 23.3 ± 1.19 day
nesting cycle.
Fewer than 10% (7/78) of Swainson’s Warbler
nests were singly parasitized by Brown-headed
Cowbirds. Only 10 of 18 Swainson's Warbler
eggs laid hatched in parasitized nests, a 26%
reduction in hatching rate from 81 to 55% (/ =
2.21. df = 6. P = 0.06). Parasitized nest outcomes
were: three depredated during incubation; two
Hedged cowbirds. but all host chicks disappeared;
and two nests reached the potential Hedging
interval, but no host fledglings were observed.
Assuming these two nestlings Hedged, the average
number of Swainson’s Warbler fledglings per
parasitized nest was 0.28 ± 0.14, a significant
reduction in fledgling production (/ = 8.87, df =
18, P < 0.001).
732
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124. No. 4. December 2012
for.S7inso"-^'ari>,ere a, Woodbuty Wildlife MaW
modification proposed by Manolis et al. (2000). ' Sl"VIVa ,dlLS E lncludc nests of unknown fate using the
Incubation
Year
No. nests
•IIVUIM
Nestling
Exposure days ( losses i
Daily survival
Exposure days (losses)
Daily survival
1999
2000
2(M)I
2005
2006
Totals
18
22
23
5
10
78
165 (7)
220 (5)
235.5 (5)
11.5 (1)
49.5 (6)
681.5 (14)
0.957 ±0.016
0.977 ± 0.010
0.979 ± 0.009
0.913 ± 0.083
0.879 ± 0.046
0.965 ± 0.007
75.5 (1)
119(4)
126.5 (2)
28 (0)
31 (1)
380 (8)
0.986 ± 0.013
0.966 ±0.016
0.984 ± 0.01 1
1 .000
0.968 ± 0.032
0.979 ± 0.007
Pooled
Daily survival
0.967 ± 0.011
0.973 ± 0.009
0.981 ± 0.007
0.975 ± 0.025
0.913 ± 0.031
0.970 ± 0.005
Nesting Success. The leading cause of nesi
failure was depredation (25/27). followed by
desert, on (2/27). Two predatory interne, ions were
observed during the study, both involving black rat
snakes (Elaphe obsolete,). One snake unsuccessfully
ined to cany away an 8-day-old nestling, while
another swallowed three eggs from a 5.5-nt high
nest. The nesthng was force-fledged, hut was
observed J days later being fed by one of the
parents. Twelve nest outcomes were unknown due
the flew* "“T™8 fmm fluwli"S °r 'he end of
fOT (»lT°n' T'Cighl nesls were observed
(Tabl’e a , ThP°HrC, “f Wi,h 32 'e*** observed
Tll? da">' MayfleW dutch survival
est mate tor all years was 0.965 ± 0 007 and tin-
daily Mayfield nestling survival was 0.979 ± () (M)7
The overall daily nest survival rate with combined
The M 0rUM neSthng phases WiJS 0.970 ± 0.005
The Mayfield survival estimate for the 23-dav
nesting cycle was 50% {95%. Cl = 45-5?%)' *
Goodness of fit tests indicated the global model
ade,„a,dy j, the ohserved va|ues qT “
raf-bm og,ca| mode| (]p = 3/79 . dr = g
7.48 . df = s"ep = 0 486a)npCaPe m°de' «* =
’ U 486)- Pearson’s Chi-square
statistic was <| for both the temporal-biological
(0.739) and habitat-landscape models (0.659)
indicating limited overdispersion of data. Twen-
ly-lwo candidate models were used to examine
temporal and biological effects on nest survival,
an t,ie ,,CSI Oiling models incorporated the
interactive effects of nest age and parasitism
a'ong with nesi stage (Table 3). Models examin¬
ing yeat, day of the year, whether linear or
quadratic, and the cubic and quadratic effects of
nest age were not strong predictors of nest
suivival. Daily survival rale was highest among
unparasitized nests o I the youngest age during
incubation. The variables from the best fit
temporal-biological models were incorporated
into ihe habitat-landscape models (n = 17)
•iol 3). We identified two candidate models
win ow AAIC values; the combined effects of
nest age. nest parasitism, and distance to the
nearest swamp w'ere most important for nesi
survival. Variables relating to cane density,
distance to the nearest road and slough, and nest
ivi^it received little support. Unparasitized nests
that were younger in age and further from a
swamp had the highest daily survival rates. The
w.Sy^ *, habitat vaHaite
- fury Wildlife Management Area, South Carolina. 1994-2001 and 200
_ Model
Temporal-biological models
parastat*nest_agexstage
Parastat*nest_age
Nest_age parastat 3 185.89 j p-, 0.5401
Habitat-landscape models 18896 4.192 0 0664
Parastat*nest_age dist.swp
Nest-age parastat dist_swp
0.7309
0.2511
Thompson Bishop el a!. • SWAINSON'S WARBLER NESTING ECOLOGY
733
TABLE 4. Swainson's Warblers nest-site variables and
measurements at Woodbury Wildlife Management Area.
South Carolina. 1999-2001 and 2005-2006. Values are ,v ±
SE: n in parentheses.
Vegetaiion variables
Measure menl
Range
Inner cup diameter, cm
5.95 ± 0.10 (92)
3.5-1 1
Outer nest diameter, cm
14.02 ± 0.36 (90)
8.7 25.5
Inner cup depth, cm
4.29 ± 0.07 (91)
2-6.9
Entire nest depth, cm
8.75 ± 0.27 (89)
5 I't
Distance from stem, m
0.38 ±0.12 (63)
0-2.55
Nest height, m
1.42 ± 0.06 (1 10)
0.36-3.8
Host height, m
2.77 ±0.18 (83)
0.95-10
Host dbh. cm
2.79 ± 0.72 (55)
0.3-35
overall daily nest survival rate was 0.968 (9597 Cl
= 0.940. 0.983; n = 78).
Nest-site Measurements. — Nest sites were mea¬
sured at 84 and 18 nests in 1999-2001 and 2005-
2006. respectively. Nests were in the understory at
a mean height of 1.4 ± 0.06 in (Table 4). and the
plant host species tended to he small (a\jh, = 2.79
~ °-72 cm) and short Cvhosl heipht = 2.77 ±
0.18 m) (Table 4). Nests were highly variable in
M/.e as evidenced hy an outer cup diameter
ranging from 8.7 to 25.5 cm. Nineteen species
representing 18 genera were used as nesting
substrate (typically more than one substrate used
per nest; n = 163 substrates) with cane used most
frequently (26%), followed hy greenhrier (Smi/a.x
spp.) (13%). holly (12%), and grapevine ( Vitis
spp.) (12%); 47% of nests were in vines. 26% in
cane, 18% in shrubs, and 10% in trees. Seventy-
one percent (72/102) of nests contained cane at
the nest-site scale. Significantly more cane was
found at the nest-site scale (x = 71.9 ± 12.2
stems) than if another species was used for nest
support (x = 18.4 ± 2.3 stems; t = 5.64. df = 30.
P < 0.001).
DISCUSSION
Our earliest indication of multiple brooding in
Swainson's Warblers was from our nesting
phenology data (Holmes et al. 1992). On average,
the first peak in nest initiations occurred the first
week of May and the second 45 days later in June.
The bimodal distribution implies a synchronicity
of brooding as nest failures would be expected to
■smooth out the peaks. This synchronicity could be
caused by food availability and social behavior
that would encourage pairs to nest at the same
time. Our subsequent observations from color
banding and telemetry work confirmed double
brooding, up to three rcncsting attempts by
females with earlier failed attempts, and several
bigamous matings (JAG. unpubl. data). Twenty-
one percent of nests were double-brooded (12/56)
in 2000 and 2001 (Thompson 2005). Miller
(2003) also observed an occurrence of double
brooding by a pair of Swainson’s Warblers in
South Carolina. Multiple brooding may be an
important strategy to maximize Swainson's War¬
bler fecundity rangewidc.
Many of our findings on nesting ecology are
consistent with those reported by Meanley (1969.
1971, 1 982) and other researchers. Our estimates of
incubation and nestling period lengths were within
Meanley's (1969) estimated ranges of 13-15 and
10 days, respectively. An average nesting cycle of
23.3 days was required from start of incubation
through Hedging. Clutch sizes (3. 1 1 eggs) averaged
slightly less than estimates from studies in
Louisiana (3.30; Henry 2004). Arkansas (3.43;
Benson et al. 2010b), and Missouri (3.65; Thomas
et al. 1996). One of our nests had an exceptionally
large clutch of seven, a potential sign of intraspe¬
cific brood parasitism; however, egg dumping is a
rare behavior used by <2% of avian species and
even fewer altriciul species (Payne 1977, Mac-
Whirler 1 989), Approxi mately one third of the eggs
laid produced a Hedgling. and the number of
fledglings produced per nest was slightly lower
(2.50) than most observed in comparable studies
(2.12; Thomas et al. 1996) (2.75; Benson et al.
2010b) (3.0; Henry 2004) (3.25; Lanham et al.
2006). Over 90% of nest losses were due to
depredation. Many potential nest predators used
the study site, but we observed only two instances
of predation by black rat snakes, which are
opportunists (Chalfoun et al. 2002).
Most nesting studies report apparent nest success
of Swainson’s Warbler, but relatively few examine
Mayfield nesting success (Thomas et al. 1996.
Henry 2004. Peters et al. 2005), and only one
examined nest survival using logistic exposure
(Benson el al. 2010b). Nesting success estimates
were corrected for a 23-day nesting cycle, and ours
was the second highest value (50.0%) when
compared to populations in Missouri (62.8%;
Thomas et al. 1996). South Carolina (40.0%;
Peters ct al. 2005). Louisiana (30.0-40.0%; Henry
2004). and Arkansas (32.2%; Benson 2008). The
weighted mean for all five studies was 39. 1%, well
below the nesting success calculated in our study.
The Peters et al. study (2005) is from the same
population and it is unclear whether the difference
734 THE WILSON JOURNAL OF ORNITHOLOGY . Vol 124. No. 4. December 2012
represents temporal variability in success or is an
artifact of limited sample size (n = 17). The
combined effects of nest age. Brown-headed
( owbird parasitism, nest stage, and distance to
the nearest swamp had the greatest effect on
Swainson’s Warbler nest survival in our study.
Brown-headed Cowbirds may follow swamp edges
to gain access into forest interiors explaining the
negative association between swamp edge and nest
survival: however, cowbirds can also use roads and
sloughs for the same purpose, but proximity to these
features did not affect nest survival in our study
Bc-nson el al. (20 1 IJa (observed a similar decrease in
Swam son s Warbler nest survival with age, an
observation that could be attributed to increased
act.vuy around nests as nestlings become older.
One of the most important determinants of
Swa.nson s Warbler nest success was whether or
not the nest was parasitized. Not only did the
presence ol cowbirds reduce the hatching rate of
eggs m parasitized nests by 27%, it also (/> <
0.001 ) reduced fledgling production by 89% (() ->*
r,."'5 flcd5l,n«* Pcr nest). Our estimate of
fledgling production in parasitized nests is liberal
nes,Ii"Ss we™ not rcobserved M
T ‘nle"SiVe searching. Hc„so„ et
al. (-01 Ob) observed a similar reduction in
Swamson s Warbler fledglings at nests in Ark-in
;™vs- r 75 nedg,ings ^
paras, t.sm status to be the most imporfml
predictor ot fledgling product! on. SwttLon's
Warblers can produce fledglings in singly „ara
nized nests. bu, a, a much diminished r e
(Benson et al. 2010b, . They appear be
particularly vulnerable to Brown-headed Cowbird
parasitism. Parasitized nests may also be Ta
greater depredation risk due to increased provi*
stoning rates of parents (Pappas el al. 2010^
JTcmZ T °n"e S'VainSon's Warbler nests
o.wb,rd"'otTudr::fs)bLdT'hL'iAi
studies at the wpsior,, „i y whereas,
n ks“sas (36%: eTar20l0b)reLV“riable:
!. “«r m> SSS
a critical habitat component i ,s
IQSn ti nun (Lddlenian ei jiI
>980, Thomas e, al. ,996). However, habitat
requirements of core breeding populations in
Georgia and South Carolina may differ. Graves
(2002) found no cane at a site in Louisiana with
the highest Swainson’s Warbler population den¬
sity on record, and also observed less cane in
territories compared to non-use plots in the Great
Dismal Swamp (Graves 2001). We observed
Swamson's Warblers using a variety of substrates
foi nesting with vines being most common
followed by cane. Cane was used as a substrate
at more than one-third of the nests and was found
m close proximity to two-thirds of the nests. Daily
nest survival rates were not influenced by the
amount of cane in the surrounding area orthetvpe
°' neslinS substrate used. Lanham and Miller
(_006) observed mountain populations using
hemlock ( Tsittfa spp.) for nesting. The diversity
ol Holistic results related to Swain son's Warbler
labitat pieference may indicate the importance of
vertical structure to habitat occupancy.
A major factor influencing Swainson's Warblers
is hydrology as it is the driving force behind
vegetative distribution, soil composition, and litter
launa in a bottomland hardwood forest < Martin et al.
D.l). Hydrology directly impacted nesting phenol-
<»gy with May flooding events delaying nest
initiation by as much u.s 3 weeks in 1999 and
affecting the abundance of leaf litter. Anich and
Raley (2010) observed Swainson’s Warblers feed¬
ing in novel ways during a flood and suggest this
species may have evolved the flexibility to survive
temporary flooding, and continue reproduction.
ew investigators have examined the litter
Guna ol floodplain Zones II through V (Martin
el al. 1993). and more research is needed to
compare Swainson’s Warbler distribution to
invertebrate abundance (Brown 200S. Savage et
al- -010). Several studies (Graves 2001. 2002:
Benson et al. 2010b) have examined the effects of
oo ing on occupancy patterns by Swainson’s
Warblers, and found them to be profoundly
impacted due to their characteristic ground
foraging and shrub nesting life history. Not only
l'lc Swamson’s Warblers negatively impacted by
flooding (Anich and Reiley 2010, Benson and
e narz 2010), but fewer understory -dependent
'’lit '- aie found in the frequently flooded zones
Wlen j°niPared to lllc bird communities of higher
giound (Wakely and Roberts 1996).
CONSERVATION IMPLICATIONS
Gin results suggest industrial forests can be
°i uctive areas tor Swainson’s Warblers. Not
Thompson Bishop el at. • SWAINSON'S WARBLER NESTING ECOLOGY
735
only is the fecundity of the population we studied
comparable to studies in non-industrial forests, in
many instances it surpasses those landscapes.
Additional breeding populations need to be
studied to assess the feasibility of the industrial
forest as a management scenario for Swain son's
Warblers. The principal impact we observed on
Swainson’s Warbler productivity was Brown¬
headed Cowbird parasitism. The effects of
parasitism on hatching and fledgling production
should be considered a significant threat to this
species. Cowbird abundance across the Swain-
son's Warbler range should be monitored.
AC KNOWLEDG M ENTS
We thank the many field technicians and volunteers who
assisted during the study, and recognize those who directly
contributed to the nest observations for this manuscript:
B. B Desjardins. L. C. Bruce. D. K. Bruce. S. C. Garriock.
and J. C. Norwalk. K. A. Peters provided valuable
instruction, support, and insight into studying Swainson's
Warblers. Funding was provided by International Paper
Co.. North Carolina Museum of Natural Sciences. National
Audubon Society. North Carolina State University, and
National Council for Air and Stream Improvement. Wc
particularly thank S. E. DuBose and W. T. Smith at
International Paper Co. for then support. Members of the
Woodbury Hunt Club provided logistical and moral
support, particularly L. E. Gunter, C. S. Easterling, and T.
L. and C. A. Lewis. We thank the reviewers, T. J. Benson
and G. R. Graves, and editor. C. E. Braun, for their critiques
of this manuscript.
LITERATURE CITED
Anich, N. M. and B. M, Ri ii ey. 201(1. Effects of flooding
on foraging ecology and population dynamics of
Swainson's Warblers. Wilson Journal of Ornithology
122:165-168.
ASKINS, R. A. 2000. Restoring North American birds:
lessons from landscape ecology. Yale University
Press. New Haven. Connecticut. USA
Bassctt-Touchell. C. a. and P. C. STOUtn-.K. 2006.
Habitat selection by Swainson's Warblers breeding in
loblolly pine plantations in southeastern Louisiana.
Journal of Wildlife Management 70:1013-1019.
Benson. T. J. 2008. Habitat use and demography of
Swainson’s Warblers in eastern Arkansas. Disserta¬
tion. Arkansas Stale University, Jonesboro. USA.
Benson, T. J. and J. C Bf dnarz. 2010. Short-term effects
of flooding on understory habitat and presence ot
Swainson's Warblers Wetlands 30:29-37
Benson. T, J.. J. D. Brown, and J. C. Bednarz. 2010a.
Identifying predators clarifies predictors of nest
success in a temperate passerine. Journal of Animal
Ecology 79:225-234.
Benson, T j„ N. M. Am6
Martin T. I, and G. R. GEUPKU 1993. Ncst-monitoring
P methods tor locating nests and monitoring
success. Journal of Field Ornithology 64-507 My
IS,WR s °- Bovra- ™ A c e—cht.
ol te MWhcnMcrn United States
New YcXwa ' J°hn W,l';-V ”"d Su"'-
Mayheld, H.F. ,975. Sngpestinns for MIculaIi„g „c„
success. Wilson Bulletin 87:456-466.
Meanley. B. 1969. Pre-nesting and nesting behavior of the
Swomson s Warbler. Wilson Bulletin 81:246-257.
A Warblef North . Nu,Ulal h,SIor-v oi‘ 'he Swainson's
MEANLLY B mf N DenCan *un" Seri«* Number 69.
the DifmM t V;,irn * Warblera,,d 'hecowbird in
tile Dismal Swamp. Raven 53:47-49
Mtu.BR. s. M. 201,3. Hi,,, report of a' do»ble-bmoded
o erlang a, G. S. Butcher. S. K. Davis n w
Demarest. R. Dt.mtF.Rs W Easton it r’
Silva gah/y f i »*,' - CASroN- *1. Gomez de
d n C. j.
i- M i. s S.
pdf 8 1 s/downloads/Handbook2005.
Pappas, S.. T J. Benson, and J. C. Bednarz. 2010. Effects
ol Brown-headed Cowbird parasitism on provisioning
rates of Swainson's Warblers. W'ilson Journal of
Ornithology 122:75-81,
Pay ne, R. B. 1977. The ecology of brood parasitism in
birds. Annual Review of Ecological Systems 8:1-28.
Peters, k. A.. R. a. Lancia, and J. a. Gerwin. 2005.
Swainson’s Warbler habitat selection in a managed
bottomland hardwood forest. Journal of Wildlife
Management 69:409-4 1 7.
SAS Institute. 2004. SAS Online Doc 9.1.3. SAS Institute.
Cary'. North Carolina. USA.
Savage, A. L., C. E. Moorman. J. A. Gerwin. and
C. Sorenson. 2010. Prey selection by Swainson's
Warbler on the breeding grounds. Condor 1 12:605-
614.
Shaffer, r. L. 2004. A unified approach to analyzing nest
success. Auk 121:526-540.
Shaffer, t. l. and f. r. Thompson III. 2007. Making
meaningful estimates of nest survival with model-
based methods. Studies in Avian Biology 34:84-95.
SOMERSHOB. S. G-. S. P. HUDMAN. AND C. R. CHANDLER.
2003, Habitat use by Swainson's Warblers in a
managed bottomland forest. W'ilson Bulletin 115:148-
154.
FhoMAS. B. Ci., E. P. WlGGERS. AND R. L. CLAWSON. 1996.
Habital selection anil breeding status of Swainson's
Warblers in southern Missouri. Journal of Wildlife
Management 60:61 1-616.
Thompson. J. L. 2005. Breeding biology of Swainson’s
Warblers in a South Carolina bottomland forest
Dissertation. North Carolina State Univcrsilv. Raleigh.
USA.
Trimble Navigation Limited. 2001. GeoExpIorer II
operation guide. Trimble Navigation Limited. Sunny¬
vale. California, USA.
J urnfr. R. k.. S. W'. Forsythe, and N. J. Craig. 1981.
Bottomland hardwood forest land resources of the
southeastern United States. Pages 13-28 in Wetlands
ol bottomland hardwood forests (J. R. Clark and J.
Benfurado, Editors). Elsevier Science Publishing
Company, Amsterdam, The Netherlands.
I Wl-irr. D. I AND S. G Somhrsiioe. 2009. Bini response to
prescribed silvicultural treatments in bottomland
hardwood forests. Journal of Wildlife Management
73:1140-1150.
W akely. J. S. andT. H. Roberts. 1996. Bird distribution
and lores! /('nation in a bottomland hardwood wetland.
Wetlands 16:296-308.
Williams. G. E. and P. B. Wood. 2002. Are traditional
methods of determining nest predators and nest fates
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ehla muste/ina) using miniature video cameras. Auk
1 19:1 126-1 132.
The Wilson Journal of Ornithology 1 24(4): 737-742, 2012
NESTING OF THE THORN-TAILED RAYADITO ( APHRASTURA
SPIN/CAUDA) IN A PINE PLANTATION IN SOUTHCENTRAL CHILE
CLAUDIO S. QUILODRAn.1 RODRIGO A. VASQUEZ,1 3 AND CRISTlAN F. ESTADES’
ABSTRAC I — We installed nest boxes lor I horn-tailed Rayaditos (Aphrastrum spinicauda) and monitored their use in
a Monterrey pine (Pin us radiata) plantation in the Manic Region, southcentral Chile. Thirty-four breeding pairs built nests
in boxes, of which 75*7 began laying eggs. Nest establishment began in early September and construction lasted 12.8 ±
A9 days in = 23). Rayaditos used mainly pine needles, together with mosses, epiphytes, herbs, and animal hair in their
nests. Clutch size ranged from two to four eggs (mode = 3) that were incubated for 15.8 ± 1.2 days. Brood size negatively
affected mass of nestlings, but was positively related to mass of the parents. Adults had higher body mass and built larger
nests than those reported previously for the species on Chilod Island, where broods are larger and the incubation period is
shoner. The provision of artificial cavities allowed Thorn-tailed Rayaditos to nest in the pine plantation. Nest boxes
combined w ith oilier management tools, such as maintaining snags and understory enhancement, may be important factors
in mitigation of negative effects of pine plantations on secondary cavilv-ncsling birds. Received IS February 2012.
Accepted 7 June 2012.
The Furnariidae consists of a large variety of
species that have colonized a wide diversity of
habitats from tropical rainforests to savannas and
deserts (Fjeldsa et al. 2005). They are mostly
insectivorous, socially monogamous, and territo¬
rial. Their plumage is typically brown or grayish-
brown, and males and females are morpho¬
logically similar (Zyskowski and Prum 1999,
Mezquida 2001, Remsen 2003. Rubio and de
Pinlio 2008).
The Thorn-tailed Rayadito ( A ph rostrum spini-
cauda) is an endemic member of Furnariidae from
South American temperate rainforests (Grigera
1982). It does not exhibit sexual dimorphism and
has high parental care of eggs and chicks ( Moreno
et al. 2007, van Dongen et al. 2009). Ii is
territorial during the breeding season (Ippi et al.
2011), but joins mixed-species flocks during the
non-breeding season where it is the dominant
'pecies fVuilleumier 1967, Ippi and Trejo 2003).
Plantations of exolic Monterrey pine (Pinus
radiata) have replaced (he original native vege¬
tation in southcentral Chile, affecting wildlife
diversity by homogenizing the landscape (Munoz-
Pedrcros et al. 1996, Vergara and Simonetii
2003). The Thom-tailcd Rayadito is considered
sensitive to habitat fragmentation and patch
vegetation characteristics (Vergara and Simonetti
Institutodc Ecoiogia y Biodivcrsidad. Departamento de
C'ienciaji EcolOgicas. Facultad dc Ciencias, Univcrsidad de
Chile, Casillu 653. Santiago. Chile.
‘ fahoratorio de Ecoiogia de Vida Silvestre. Facultad de
t iencias Forestales y de la Conscrvacibn de la Naturaleza.
Univcrsidad dc Chile. Casilla l>20b. Santiago. Chile.
Corresponding author: e-mail: rvasquez@uchile.cl
2004, Vergara and Marquet 2007), but also
frequently visits the pine matrix to forage (Estades
1999, Estades and Temple 1999). Rayaditos use
small and isolated remnants of native forest
during the breeding season, where there are
available tree cavities, a limiting resource for
nesting (Tomasevic and Estades 2004, 2006;
Cornelius et al. 2008).
Pine plantations represent usable foraging
habitat for Thorn-tailed Rayaditos and may also
enhance connectivity between remnant native
vegetation patches (Estades and Temple 1999;
Estades 200 1 h. c: 2006). However, the scarcity of
cavities in industrial forests severely restricts
breeding use by the species (Estades 2001b).
Thus, use of nest boxes has the potential to
become a habilnt improvement tool to allow
Thorn-tailed Rayadilos to nest in pine plantations.
Information about Rayadito breeding biology in
pine plantations is scant, despite its usefulness to
assess conservation status as well as species
responses to environmental disturbances in natural
and managed habitats (Vasquez and Simonetti
1999). Our objectives were to; (I) examine if
Rayaditos can breed in exotic pine plantations if
they have access to nesting cavities, and (2)
describe their breeding biology in pine plantations
for comparison with previously published data
from a native forest on Chiloe Island, Chile
(Moreno et al. 2005).
METHODS
Study Area. — The study was conducted during
austral spring 2009 in the Coastal Range of the
Maule Region. Constitucion Province, southcen¬
tral Chile (35 29' S. 72° 21' W) (Fig. I). The
737
738
THE WILSON JOURNAL OF ORNITHOLOGY . Vol.
124. No. 4. December 2012
LEGEND
Pine plantations
Native forest
Nest-box plot
Nothofagus forest (black) arc embedded i nT matrix°of exot ic^M "i SOUth<:enlral Chile' Fragmented remnants of nativ
* °f eXO,lc Mon,errey Pine (Pinus radiata) plantations (gray).
area was ortginally a deciduous forest of No,ho-
fagus glauca (Hualo), which began being exploit-
n 10 thf l9,h cenlury (San Martin and
r: ? ^ MaUle «ow contains
e of the largest concentrations of />, radiata
P antauons in the country, covering 76% of the
Coasta Range. Native forest remains in small
rev n, tragmenlS surroun^d by exotic Monter¬
ey p,ne Plamat,ons- The climate is warm
temperate with an oceanic influence. The average
m nimtim temperature is 5.9 C during winter
(Jul) and the mean maximum temperature is 2^ 7
u during summer (Jan). Mean annual rainfall is
881 mm (Estades and Temple 1999)
We worked in plantations that were 1 8 years of age
«£ »n"SPl^»r, ® l Samp,e
2009) n J r r°m l,e nest (van Dongen et al
between 2°5 tnd^m lrec «™nta
three boxes in sin !hc grOUnd *"> all
,e>"1 sin. wium ot i o cm, and
entrance hole of 3 cm in diameter ( Moreno et
2005, 2007).
Nt;st Monitoring.- We checked nest box
wee ly fiom the last week of August, recordir
any sign of nesting activity, including use of twit
and/or feathers to build die nest. We increase
frequency of monitoring once we observe
activity in the box to detect laying dates (date c
lust egg) and hatching dates (date of fir;
hatchling in the nest). The latter frequenc
depended on advancement of the nest buildin:
stage, from three times per week to daily when th.
nest was nearly completed. We weighed ant
measured eggs on the day they were laid. Lengtl
and width were measured to the nearest 0. 1 mn
WM 1 a , r Ԥl,al caliper. Egg volume was obtained
using Hoyt's (1979) formula: Volume = 0.51
(Length X Width?).
We captured adults with traps in the nest box
w en nestlings were 13 days of age and banded
mem with a combination of three plastic colored
an s under the authority of Servicio Agricola y
'unadero ot Chile. Adult mass was recorded with
‘ spnng balance to the nearest 0. 1 g. We measured
w:;hJS '!m. lea increase the abundance of cavity-nestim?
btrds as well as their frequency of Jo"
2003 m"' MU"°Z-Pedreros « “I- 1996, Bull
-003, Maicas and Haeger 2004). We observed
Thorn-tailed Rayadito using Monterrey nine
presem °nS ^ '***"* if nest b<>*^ were
Nestlings ( 13 days)
Adults
/
p
20.8 ± 0.7
26.4 ± 0.9
30 ± 5.1
20 ± II
69 ± 8
13.1 ± 1.3
22. 1 ± 0.6
30.6 ±0.7
58 ± 2
83 ± 6
135 ± 7
1 1.6 ± 0.3
6.5
13.2
23.3
17.1
26.3
-4.9
<0.001
<0.001
<0.001
<0.001
<0.001
<0.001
Pine plantations may differ from native forests,
m addition to scarcity of cavities, in other
breeding habitat aspects for Thorn-tailed Rayadi-
los. However, evidence of food abundance for
small msectivores suggests pine plantations in
southcentral Chile provide levels of foraging
resources similar to native forests f bstades and
Escobar 2003), Thus, the observed difference in
clutch sizes may be more consistent with ihe
hypothesis proposed by Lack (1968), which
predicts that at higher latitudes (Cliiloe --41 S
mid Const itucidn -35 S). clutch size increases,
presumably because of longer day length, which
pi ovules more time for parents to feed nestlings
and reduces the possibility of re-nesting (Dunn
and Machines 1987. Shamel and Tracy 1987,
r oung 1994. Piersma 1996). A recent study of
House Wren ( Troglodytes aedon chilensis) on
hiloe Island, also suggests that clutch size
increases with latitude in the Southern Hemi¬
sphere (lppi et al. 2012).
Lsludcs (2001b) argued that pine plantations
mtg t offci a safe place to nest for cavity-nesting
mds such as the Thom-tailed Rayadito/ because
Nest construction (days)
Incubation period (days)
clutch size
Brood size
Adult mass (g)
Nest dry weight (g)
Egg volume (cm3)
Hatching success (%)“
Breeding success (%)h
b cggs batched lor all nests
% young fledged for all egg* that hatched.
61 ± 4.8 (J5)
,2-8 ± 1.9 (16)
4- 1 ± 0.8 (30)
4.2 ± ().7 (22)
,(, x i 0.8 (41)
137 — 5.1 (12)
20 10 ± 200 (57)
?5'2 ± 10.2 (26,
7&.7 ± 3| (26)
Consiiiucidn
12.8 ± 4.9 (23)
15.8 ± 1.2 (20)
T3 ± 0.7 (22)
2.9 ± 0.8 (19)
1 16 - 0.3 (14)
416 ± 14 (15)
2010 ± 92 (16,
X9 ± J6 (|9)
72 ± 44 (19)
<0.001
<0.001
<0.001
<0.001
<0.001
0.05
0.99
0.15
0.69
Quilodran el at. • NESTING OF THE THORN-TAILED RAYADITO
741
both the structural simplicity and the low density of
breeding birds would limit nest predators present in
these artificial forests. However, we observed that
predation and breeding success rates were similar
to those in native forest. Potential Rayadito nest
predators in pine plantations include mice, opos¬
sums (Thylamvs elegans) (Estades 2001b). and
the long-tailed snake ( Phyloctrias chamissonis )
(Escobar and Vukasovic 2003).
We did not find any effect of distance lo native
lorest on the use rate of nest boxes or on nesting
success. Rayaditos breeding in native forest
patches usually move several hundred meters into
the adjacent pine plantations during the non¬
breeding season (Estades 2001b, 2006). Thus, it is
likely birds were able to detect the presence of
nest boxes throughout the entire range of
distances in our study.
Ise of an artificial habitat for nesting reflects
some level of behavioral plasticity by the Thorn¬
tailed Rayadito. Examples of the latter arc use of
pine needles as one of the main materials for nest
construction, and consumption of pine seeds by
this insectivorous species (Estades 2001a).
Our results support the use of nest boxes to
offset the scarcity ol cavities in a landscape
dominated by plantations of fast growing pine,
thus allowing nesting by cavity-dependent birds
(Munoz-Pedreros et al. 1996, White and Seginak
2000. Bull 2003. Maicas and Haeger 2004.
Woodley el al. 2006, Cockle el al. 2008). U se of
artificial nest boxes, together with other manage¬
ment tools such as maintenance of snags and
enhancement of the understory (Tomasevic and
Estades 2008), may he important methods to
mitigate the negative effects of pine plantations on
forest birds in Chile.
ACKNOWLEDGMENTS
rhis study was funded through grants to R. A. V.isquez
(FONDECYT 1090794. PFB-23-CONICYT). and grant P05-
0,)- Millenium Scientific Initiative of the Ministry of
Economy, Advancement and Tourism of Chile. C. E. Estades
hunks FONDECYT for grant 108046.3. Minineo kindly
granted access to the study area and provided cartographic
information. The School of Foa*st Science and Nature
Conservation of the University of Chile contributed with
lodging. C. S. Quilodnirt acknowledges .support from an IEB
scholarship. R F. Zuniga, C. I Venegas, and D I. Medina
helped set up the nest boxes, and F. M. Muureira. N. D. Von
Kunowsky, M. A. Chavez, and C A. Pernollet helped with
fieldwork We thank Kristof Zyskowski. an anonymous
reviewer, and C. E. Braun for valuable comments and
suggestions on an earlier version of this paper.
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The Wilson Journal of Ornithology 1 24(4): 743-749, 2012
FIRST DESCRIPTION OF THE NEST AND EGGS OF THE ISLAND-
ENDEMIC COZUMEL VIREO, VIREO BAIRD/
JOSHUA B. LAPERGOLA,1 4,5 JESUS GUSTAVO MARINA HIPOLITO,2
JUAN E. MARTINEZ-GOMEZ.' AND ROBERT L. CURRY1
ABSTRACT.— We report the lirsi description of the nest, eggs. ;md nesting phenology of the Cozumel Vireo {Viren
herd,), a passenne species endemic to Isla Cozumel. Mexico. We discovered three nests of this species in 2009 These open-
cup nests were woven onto branches and hung beneath forks. Clutch size was 2-3 eggs, and eggs were ovate and had a white
ground color with reddish-brown Hecks. These characteristics of nests and eggs are similar to those of most other Vireo spp
including other West Indian members of the Vireo subgenus. Breeding activities, including egg-laying, incubation and
nestling and post-fledging provisioning occurred from May to July 2009. We estimated the length of incubation to be -14 days
and length of the nestling stage to be 11-12 days. Much of the Cozumel Vireo’s breeding biology remains unknown and
further study of this single-island endemic is needed. Received 25 Mon h 2012. Accepted 6 July 2012.
The vireos (Vireonidae) comprise 32 species
that range from North to South America, includ¬
ing many islands (Brewer and Orenstein 2010).
Vireo. largest of the family’s four genera, contains
31 species with —61% mostly or wholly restricted
to tropical latitudes including the nine species
restricted to islands (Raffaele et al. 1998. Brewer
and Orenstein 2010). A temperate-zone bias (cf.
Stutchbury and Morton 2001 j characterizes
knowledge of the breeding biology of vireos:
species nesting in Canada and the United Slates
are overall better known than neotropical and
Southern Hemisphere counterparts. The nests and
eggs of several vireos breeding in Mexico and
Central and South America remain undescribcd
i Brewer and Orenstein 2010).
fwo recognizable groups are distinguishable
within Vireo on the basis of plumage (Hamilton
1962): ( 1) species with eye-rings and wing-bars in
(he subgenus Vireo. and (2) species with eye-
stripes and lacking wing-bars in the subgenus
Vireos viva. Johnson et al. (1988) recommended
abandoning this dichotomy based on allo/yme
evidence, but phylogenetic analysis using mito¬
chondrial DNA sequence data (Murray et al.
1^94) supported recognition of the two subgenera.
Department of Biology. Villanova University. 800
Lancaster Avenue. Villanova, PA 19085, USA.
L niversidad Autonoma Mctropolilnna-Xochimilco, Cal-
zatia del Mucso 1100, Colnnia Villa Quictud. Delegaci6n
Coyoacdn, CP 04960, D.F. Mexico.
Instituio de Ecologta. A.C., Red dc Interacciones
Multi trtificas, Apartado Postal 63. Xalapa, Veracruz
91000, Mexico.
'Current address: Department of Neurobiology and
Behavior and Cornell Laboratory of Ornithology. Cornell
University, Ithaca. NY 14853, USA.
'Corresponding author; e-mail: jbl96@cornell.edu
The -eye-ring' group includes eight little-studied
species endemic to the West Indies or the adjacent
Caribbean Coast of Mexico and Central America;
one of the most range-restricted species among
these is the Co/umcl Vireo ( V. hairdi).
The Cozumel Vireo is endemic to Isla Cozu¬
mel, Quintana Ron, Mexico (Howell and Webb
1995. AOU 1998). The species’ breeding biology
is wholly unknown (Brewer and Orenstein 2010).
Early records described the species as “very
common” (Griscom 1926:11) and “more fre¬
quently encountered than any other species in
woodland and secondary growth” (Bond
1961:45). The Cozumel Vireo remains abundant
(JBL, RLC, and JEMG. pers. obs.) despite the
presence of feral cats (Felts cants) and dogs
( Cam's familiaris) as well as other recently in¬
troduced potential predators, including a snake
(Boa constrictor, present since the early 1970s;
Martmez-Morales and Cuardn 1999, Romero-
Najera et al. 2007) and black rats ( Ratttts rattus;
Engstrom et al. 1989). Our objectives are to report
the first descriptions of the Cozumel Vireo’s nest,
eggs, and nesting phenology, and to compare our
observations with available data for other ‘eye-
ring’ vireos (if Hamilton 1962).
METHODS
Study Area.— We observed vireo nests during
fieldwork (May-Jul 2009) on Cozumel focused on
Black Catbird ( MelattoptUa glabrirostris ) breed¬
ing biology. Cozumel is in the Caribbean Sea,
— 17.5 km off the Yucatan Peninsula’s coast,
separated from the mainland by a deep channel: it
has a land area of -490 knr (BirdLife Interna¬
tional 2012). Most of the island's vegetation is
semi-deciduous or tropical deciduous forest with
743
744
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 4. December 2012
relatively low canopy height influenced by
hurricanes; recent hurricanes that have directly
impacted Cozumel include Gilbert (1988). Rox¬
anne (1995). Emily (2005), and Wilma (2005).
Our study site was a set of paths leading from an
area known locally as Pueblo Fantasma (20 26'
54" N. 86 57' 32" W), an isolated and mostly
abandoned residential development (Howell
1999:311) ~6 km south of San Miguel, the
island’s primary town. This area was easily
accessible with vegetation representative of Co¬
zumel’s interior forests.
Nes1 Searching and Monitoring. — JBL discov¬
ered three Cozumel Vireo nests while systemat¬
ically searching for catbird nests. We checked
nest contents every' 1-3 days (although one nest-
check interval lasted 8 days).
Measurements.— We measured nest height from
nest bottom and top. tree height, nest circumfer¬
ence, distance to stem, and angled distance to
stem using a tape measure. We used calipers to
measure nest and egg dimensions.
OBSERVATIONS
Nesting Cycle and Nesting Phenology.— JBL
tscovered the first Cozumel Vireo nest (#1 ) on 1
June 2009 (Fig, I) containing two eggs at 1136
and .830 hrs (COT). The nest contained*™ eggs
on 2 June 2009 at 1114 hrs. The last dav we
observed the nest with eggs was 15 June 2009 at
chVu • ,and WC °bserved tWo recently-hatched
chicks and one un-hatched egg in the nest on 17
June 2009 a, ,854 hrs. .negation latd !4 dall
it ue assume incubation began with clutch
comp ei, on (2 Jun 2009) and the chicks hatched
i June 2009, die day between the last
~of "T f8gS and ,he r,m “‘“crvation
£*£7 ’ ’6” ^ °" ^ -d 0731 te
^7 June 20°9 and |04() hjs on 28 ‘ JJ- ™
A second Cozumel Vireo nesi ’ .
one recently hatched chick and „n . / cont£nned
discovery (17 Jun 2009 at 0955° S°n d,ate °f
chicks and no eggs at the next n . ,u1f lvv°
2009 a, ,835 hrs). Thh 2
2
3
2 ± 1
2-3
14.4
17.6
19, 18
19.2 ± 0.3
May-Jul
14
13.8
May-Jun
12.5, 13
Jan-Jun
14.5 ± 0.7
Mar-Jul
11-12
17
11.2-14.6
8.9-13
9
8.6-10
11-16.2
" 10 nCSlS forclulch si“; Barl<'* «nd Nash < 1985). individual measurements.
366 cm); Maynard (1893:96). n = 4 eggs.
We collected ,wo nests after the chicks fl
We deposited nest #1 and its remaining esc
National Collection ol Birds (Inst, l, node ft!
de ia Cm vers, dad National Autdnoma dc M
CNAV: N029I40). an
ln the„Museo do Zoolog, ' a of HI Colegic
Fiontera Sur, Cheiumal, Mexico
Description of Eggs, Hatching Success
nest'#] 5.TCeW~Clutch size «hrec eg
,“* i ' 'wo e*f in neat #2. and two
#3. All observed eggs (n = 6) were o
short oval in shape (Baicich and Harrison 1997)
and had white ground color with reddish-brown
Hecks concentrated toward the broad end
(Eig. IB). The egg we collected measured 20.2
x 14 4 mro (length x width).
Hatching success varied. Two of three eggs in nest
hatchcd’ eggs in nest #2 hatched; and neither
cg^ in nest #3 hatched, likely because the parents
abandoned the nest prior to completion of incubation.
uients at two of the three nests appeared to
lave edged young. We inferred fledging success
LaPergola el al. • NEST AND EGGS OF THE COZUMEL VIREO
747
based on (1) the presence of adult Cozumel Vireos
emitting alarm or scold calls close to each nest
during the first days we observed them empty, and
(2) the highly developed state of nestlings (prima¬
ries and secondaries completely lacking sheaths) on
the last day observed in nests #1 and #2.
JBL and JGMH candled the eggs in nest #3
on 8 July 2009 using a headlamp. Neither egg
showed signs of development, but we returned
both to the nest. One egg had broken before we
checked the nest on 15 July 2009; we collected (he
remaining intact egg but it broke in transit.
DISCUSSION
Our observations represent, to our knowledge,
the first account of the nest, eggs, and breeding
phenology of the Cozumel Vireo. Sample sizes
are limited, but available data indicate that several
aspects of the species' breeding biology are
consistent with those of other 'eye-ring’ vireos.
including other members of the same superspecies
iAOU 1998) within the Vireo subgenus; White¬
eyed Vireo ( V . griseus) and Mangrove Vireo (V.
pa Ileus).
Cozumel Vireos, by suspending nests from
forked branches of a small tree and by using plant
fibers and spider silk for exterior walls and grass
fibers for lining, are typical of most Vireonidae
(Baicich and Harrison 1997). Incorporation of
more varied construction materials by White-eyed
Vireos. including use or rootlets and hair in the
lining (Hopp et al. 1995), probably reflects more
diverse contexts for nest-building across that
sister species' wide geographic range. The only
described nest of the Mangrove Vireo. from a
highland area in Belize, differed by having a
lining of pine needles (Figueroa and Albanese
-903). a resource not available on Cozumel. By
including prominent dead leaves in exterior walls.
Cozumel Vireo nests especially resemble those of
the island-endemic San Andres Vireo (V. car-
ihaeus) (Barlow and Nash 1985). although lacking
die dead leaves that hang from the bottom of San
Andres nests.
Measures of nest dimensions permit compari¬
sons with species for which data are available
'Table I ). Values from the three Cozumel Vireo
nests encompass those for Mangrove Vireo with
regard to four parameters, but front internal nest
depth and narrowest internal diameter were larger
tor the slightly heavier Cozumel species. Most
Cozumel Vireo nest dimensions were greater than
those for the considerably smaller San Andres
Vireo, whereas nests of the Thick-billed Vireo (V.
crussirost ris), with body size roughly similar to
that of Cozumel Vireo, appear to have smaller
interior dimensions but larger exteriors.
Precise data concerning canopy height on
Cozumel are not available, but the rather low
height of Cozumel Vireo nests (~ 1.5 m above
ground) may reflect use of small shrubs and
saplings (2-3 m tall) and not larger trees (up to
15 m) that are present in our study area, as in most
of Cozumel's forests (JBL. JEMG. and RLC. pers.
obs.). The tendency to place nests relatively low'
in vegetation is fairly consistent across other 'eye¬
ring' vireos (e.g.. < I m nest height in White¬
eyed Vireo; Hopp et al. 1995), including those on
islands (Table I ). although higher nest placement
(mean height = 4.9 in) by Puerto Rican Vireos (V.
latimeri) in montane habitat (Tossas 2008)
suggests flexibility within the subgenus. Detection
bias favoring low nests may complicate some
comparisons.
Cozumel Vireo clutch size appears to reflect
broad latitudinal trends (Martin 1996), but its eggs
may be comparatively large. Cozumel Vireos
produce smaller dutches, at two to three eggs,
than most temperate-zone congeners; for example,
clutch size in White-eyed Vireos averages four
eggs (Hopp el al. 1995). Cozumel Vireo clutch
size approximates that of congeners breeding at
similar latitudes (Thick-billed and Mangrove
vireos), but exceeds that of the more southerly
San Andres Vireo (Table I). The Cozumel Vireo
egg we measured was longer than that of the
similar-size Thick-billed Vireo and larger overall
than eggs of the smaller Mangrove. San Andres,
and White-eyed vitcos (Table 1; Hopp et al.
1995). but more data are needed to definitively
characterize egg dimensions of V. bairdi.
Our limited observations regarding breeding
success provide a preliminary basis for compar¬
isons. Hatching success (67%) in nest #1, which
yielded our most detailed information, was lower
than that of eggs in unparasitized Puerto Rican
Vireo nests (86%; Woodworth 1997). Our sample
suggested relatively high fledging success (67%
of nests producing at least one fledgling). Other
insular Vireo spp. may have higher rates of nest
failure; for example. 63% of Puerto Rican Vireo
nests were depredated (Tossas 2008).
The observed nesting period of the Cozumel
Vireo is somewhat shorter than other insular 'eye¬
ring' vireos, but the length of its incubation and
nestling stages are more typical (Table 1). Limited
748
THE WILSON JOURNAL OF ORNITHOLOGY . Vol 124. No. 4. December 2012
duration of fieldwork might account for our
relatively brief estimate of the Cozumel Vireo's
nesting period (— 2.5 months) and observation
of only one brood per pair. However, we predict
that Cozumel Vireos may attempt multiple broods
over a protracted season, as do some Caribbean
vireos (e.g., Puerto Rican Vireo; Woodworth 1997 )
and some other passerines in the Yucatan region
(e.g.. Black Catbird; JBL. ttnpubl. data). The
incubation and nestling stages of the Cozumel
V.reo were slightly shorter and longer, respective¬
ly, than those of the San Andres Vireo, but were
close to those of other ‘eye-ring* vireos including,
lor example, the White-eyed Vireo (incubation
1 995^ da'VS’ neSt,'ng Stage: 9-1 1 da7S; Hopp ct al.
The Cozumel Vireo is currently considered a
spec.es of Least Concern (BirdLifc International
2012), but insular taxa constitute a disproportion¬
ately large percentage of threatened bird species
with declines frequently attributable to newly
arrived predators and parasites (e.g., Blackburn
et al. 2004). Vireos and their nests may be
vulnerable to predation by boas and introduced
mammals on Cozumel, but confirmation is
needed. We detected no interspecific brood
parasitism m the three Cozumel Vireo nests we
observed. However, cowbird parasitism signifi¬
cantly affects several closely related vireos
including, for example. Black-capped Vireo (V'
wZTu1]' faraSitized by Brown-headed Cow-
birds (Molothrus ater) (Grzybowski 1995). and
birds Vire°* parasilized by Shi,iy Cow-
birds (M. bona nen sis) (Woodworth 1997) Recent
expansion of Shiny Cow birds into the Yucatan
represents a potential conservation threat for
Cozumel Vireos (Kluza 1998).
v bfhSiC natUral his,°^ data for Cozumel
olher P001^ k"own species will be
crucial f0r management decisions. Practical re-
ITT are raiSed h similarit5' between the
svm „ , tP V' bainti and of the
v- m ■ nmgister = I6 7_27s r> * c”
Orenstein 20,0) and belong to differemTubgen
era, but more data are needed to develop criteria
stedeTib„Tdb “ and «f the.,;
species in the absence of adults.
ACKNOWLEDGMENTS
We thank Blanca Rolddn-Clarii. Felipe Judrez, and
Rafael Chacon for logistical support in the field: I.
Acosta-Rosado for assistance wilh plant identification:
and C. E. Braun, C. C. Mineo. and two anonymous
reviewers for comments that improved the manuscript. The
Eundacidn do Barques y Museos de Cozumel. Fundacidn
Plan Estrategico de Cozumel. Direcddn de Ecologia
Municipal, and Island Endemics Foundation provided
generous logistical support. We completed fieldwork in
accordance with SEMARNAT permit #SGPA/DGVS/
03358/09 and Villanova University IACLC protocol #AS
08-06. Villanova University and a Florida Ornithological
Society William B. and Mary J. Robertson Fellowship
awarded to JBL provided funding. This research was
conducted while JEMG was a postdoctoral fellow at the
Institiito de Ecologia. A.C. JBL dedicates this manuscripllo
the loving memory of Thomas .1. Sullivan < 1 922-20 1 2 ).
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The Wilson Journal of Ornithology 124(4):750-757, 2012
HISTORIC PRESENCE AND ABSENCE OF PREDATOR AFFECTS CAI I
STRUCTURE OF BLACK-CAPPED CHICKADEES
JACOB A. SABORSE1 AND IAN J. RENNE1,2
{PrU' U,riCaPil,US) ^ CaP'Urcd presented
Populations („ = 4 and 8 chickadee,! “ to^s^hr /‘"t “T*-* “■* ***** «**
thls dangerous, regionally sympatric predator These learned vo-al Ch,C.k'd'dec c“l,s have a site-specific structure for
context is to denote information about predator threat level with nurnem! * T !" Van°US circums>ances and one
threat. Average number of D notes per call was 4 4 where chi k t ' ' IS ShWI an< lrcqueDt D no,es designating high
then, the average was 2.3. Dun,. ion of the f", D note and ime b u " """ *CTC*'™* ^ in — **
m areas without screech-owls. Diminution of Dredator J ■ ^ !* notes Were- respectively. 36% and 44% longer
chickadees elicit a threat-inappropriate present evidence that suggest'
repertoire for this predator and that nuances in ‘chick-a-dcc* e-41 !"? SCreech'owls because they have not learned the vocal
20/2. Accepted 14 June 2012. ‘ s LOnve> predator-specific identity. Received 2 February
Many animals produce variable calls in response
to potential predators (Bayly and Evans 2001
Yorzinski and Patricelli 2010). Some calls arc
structured to recruit individuals to harass predators
tom , he area via mobbing (Hurd 1996, Templeton
‘ id Greene 2007, Nolen and Lucas 2009) and
contain specific information important to survivor-
'h,p .such as predator type, location, or level of
threat (Gnesser 2008, Bartmess-LeVasseur et al
-010 Courier and Ritchison 2010). For example
Black-capped Chickadees (Poecile alricapillus]
feveUBak" "‘"hT ‘° designa,c Predation risk
A r ccker 2002' "Templeton et al
m“ed floT' * ?! ' ’• Thcse “«* ■* l«~d by
Greene 2007). TemP,clon a"d
The Black-capped Chickadee is a small non
Ame'ri ° SOngb,rd COmmon throughout its North
btrTwsittei„produce,oud^
^Ms^o'recru198^
Predator Hurt
et al. 20ft s . . 1 J9f)- Templeton
pi . ~ ’ empleton and Greene ^007)
important to survival. Templeton e, a”~
indicate number, rate, and duration of D notes by
chickadees correlate with the threat level posed by
particular predators (Avey et al. 2011): -50
species are known to respond to ‘chick-a-dee'
calls and join in mobbing (Gunn el al. 2000).
Eastern Screech-Owls {Megascops asio) in
northeast Ohio have historically been ahseni
t loughout large regions but a few areas main¬
tain persistent populations (R. C. Jones and R. J.
ovoiny, local park managers, pers. comm.:
Pc ter job n 2001). We assessed whether presence
oi absence ol the Eastern Screech-Owl, a small,
dexterous and dangerous predator of Black-
capped Chickadees and other small songbirds
(Smith 1947, VanCamp and Henny 1975. Ritch¬
ison and Cavanagh 1992), corresponded to
alterations in the ‘chick-a-dee* call structure. Pro¬
duction of the ‘chick-a-dee’ call appears mostly
learned by conspecifics and not innate (Hughes
cl al. 1998), and loss of structural components
resulting from predator absence may occur in as
hnle as one generation (Blumstein et al. 2004).
Screech-owls are a predatory threat to chickadees
ut their patchy distribution may locally relax
maintenance ot otherwise important vocalizations.
Uur objective was to test whether elements of the
chick-a-dee’ call structure differed in areas
istoncally lacking and harboring screech-owls,
c captured chickadees from each type of area
and analyzed components of their calls when
presented with a stuffed screech-owl model.
' Department of Biological Science v
University. Youngstown. OH 44555 - ^ ,H,nSM°wn Slate
■ Corresponding author; e-mail7ijrenne@ysi,edu
750
methods
... ^eto> Calls, — -Twelve unhanded Black
c-m!X. PVckadees °* unknown sex and age wen
re 1,1 ^rec counties in northeast 0 hit
Saborse ami Renne • HISTORIC PRESENCE AND ABSENCE OF PREDATORS
751
(Trumbull. Mahoning, and Columbiana) from
February through early May 201 1. including
locations in Poland Township, Yellow Creek
Park. Mosquito Creek State Park, Mill Creek
Metro Parks. Berlin Lake, and Beaver Creek State
Park (Fig. 1). We captured two instead of one
chickadee in three locations without and one
location with screech-owls; capture sites ranged
from 1.6 to 6 km apart. Two chickadees were
caught within 100 m of each other at two of our
10 sites; the time between these captures was at
least 6 weeks. The closest capture site with a
known Eastern Screech-Owl population to an area
without them was 17 km, a distance greater than
the screech-owl median natal dispersal distance of
2.3 km (Belthoff and Ritchison 1989) and average
circular home range radius of 400 m (Belthoff
et al. 1993). This greatly reduced the chance that
captured chickadees had not dispersed between
areas with and without screech-owls, particularly
since the median natal dispersal distance for
chickadees is l.l km (Weise and Meyer 1979);
their average circular home range radius in w inter
is 120 to 230 m (Smith and Buskirk 1988).
Chickadees were caught using a Sparrow Sled
Live Trap (Wildlife Control Supplies. East
Granby, CT. USA) which was hung near a
feeding station with a 1.8-m Sheppard’s hook.
The trap was covered with a sheet after an
individual was captured and the chickadee was
allowed to calm dowm for 5 min. Nearby I’lock
members can alter calling behavior (Frceberg and
Haney 2008) and this time was extended if Con¬
or heterospecific Hock members were within a
30-ni radius of the trap or could be heard. All
individuals were tested in isolation. A Sennheiscr
ME67 shotgun microphone w-as placed on the
■fap. the sheet was lifted and a stuffed Eastern
Screech-Owl mounted within 0.5 m of the trap
was revealed (the owl model, in a perched
position, was loaned from the Cleveland Museum
of Natural History by A. W. Jones). Calls pro¬
duced by the individual were recorded tor lip to
10 min using a Maranlz professional portable
s°lid state recorder (model # PMD670) and the
chickadee was released. We ceased recording if
an individual stopped calling tor 5 min because
we felt it had habituated to the model.
Call and Statistical Analysis. — ‘C!iick-a-dee
calls were analyzed using Raven Lite software
(Cornell Laboratory of Ornithology. Ithaca. NY,
USA). We recorded for each individual: (1) total
number of calls, (2) average number of D notes
per call. (3) average duration of the first D note,
(4) average length of time between the First and
second D note, and (5) average length of time
(see) between the ‘chick-a’ and D note. These
‘chick-a-dee’ structural components are known to
vary based on predator threat level (Templeton el
al. 2005, Soard and Ritchison 2009). We be¬
lieved a priori the acoustic structure initially
emitted would best represent the information
conveyed for that predator and only analyzed
components of the first five ‘chick-a-dee’ calls
(i.e.. before habituation may have occurred). We
caught chickadees across large spatial and tem¬
poral scales and treated each captured individual
as an independent experimental unit. Four and
eight individuals were respectively caught from
areas with and without screech-owls.
We initially used multivariate analysis of
variance (MANOVA) (Scheincr 1993) to assess
if historic screech-owl presence or absence af¬
fected response variables. All significant main
effects from the MANOVA were analyzed using a
one-way ANOVA in SPSS (2009) with screech-
ow'l presence and absence as treatment levels.
Treatment variances were heterogeneous for the
number of calls per individual ( P < 0.001,
Levine’s HOV test) and we analyzed this variable
using log-transformed data, which resulted in
homogeneous variances (P = 0.63). Homoge¬
neous treatment level variances in the ANOVA
w'ere found for the other four factors (P > 0.05)
and no other transformations were necessary. An
a priori a-lcvel w'as set at 0.05 for all statistical
tests.
Eastern Screech-Owl Survey. — Screech-owl
surveys were performed using methods adapted
from Takats et ai. (2001) to substantiate historic
reports of their presence or absence at sites in
which Black-capped Chickadees were captured
(Fig. 1 ). These areas w'ere fragmented deciduous
forests and woodlots of 4 to 260 ha. which is
deemed good screech-owl habitat (Sparks et al.
1994). Surveys began 30 min after sundown
between November 2010 and January 2012, a
diurnally active time for screech-owls (Deuser
2011), and each of 10 sites were sampled two to
four times during this interval (we stopped
playbacks if a response was detected). Eastern
Screech-Owl ‘trill' and ‘whinny’ calls were taken
from Peterson Field Guides (1990) (length of call
sequence: 24 see): this same series was played at
each site using a Foxpro Spitfire digital game call
(model # SF1). The volume was set so playback
752
THE WILSON JOURNAL OF ORNITHOLOGY • Vul. 124. No. 4. December 2012
calls could not be heard by a human at 225 m with
4nnaSSU7,i?n anowl could hear it ttt
4nn m P ayback lnaJ was conducted every
400 m along n ~2-kra transect at each site
followed by a I -min silent period. This was
repeated in each cardinal direction a elh
amplmg pom,. We only performed playbacks a.
four points in one small woodlot because of sire
transect. "I'' h“d P°<"“ P-
An Eastern Screech-Owl responded to our
playbacks a. each of our two sites a. Beaver
Cieek State Park, a location known for them.
Playback surveys at Berlin Center. 39 km from
Beaver Creek State Park, detected a probable
le.sponse and. given the park managers claim of an
active nest and injured Eastern Screech-Owls
have recently been submitted to Birds in Right
■Sanctuary, a local raptor rehabilitation center
(Heather Merritt, pers. comm.), we deemed this
area as having them. No screech-owls were
detected at any other site during our surveys; we
considered them as not present and these find¬
ings corroborate Peterjohn (2001), the unpublished
Saborse and Renne • HISTORIC PRESENCE AND ABSENCE OF PREDATORS
753
Ohio Breeding Bird Atlas II data, as well as
information from local park managers and
experienced ornithologists (e.g.. no screech-owls
have been reported in the latter sites in the last
10-30 years; R. J. Novotny and R. C. Jones, and
other local park managers, pers. comm.).
Sample Size.— We acknowledge our small
sample si/e could be problematic but believe
our findings are valid for three main reasons.
First, regional dialectical differences seem un¬
likely since chickadees in screech-owl areas were
sampled from populations separated by 39 km
and the only variable distinguishing these sites
from all others was screech-owl presence (Fig. 1 ).
Second, unlike song structures, which can vary
greatly over short temporal and spatial scales in
many songbirds (Slater 1986, Gammon et al.
2005), warning call structures exhibit remarkable
consistency across large areas and habitat types
(Ippi et al. 201 1). The 'chick-a-dee' warning call
of Black-capped Chickadees seems highly con¬
served throughout its North American range
(Hurd 1996 [Wisconsin], Baker and Becker 2002
[Colorado], Templeton et al. 2005 [Montana],
Avey et al. 2011 |Alberta, Canada], this study
[Ohio]), Third, small sample size can lead to false
positives and the likelihood of this would increase
if by chance young birds happened to be caught
that had not yet learned the calls from adults.
However, the 12 Chickadees were tested from
February to early May and nestlings Hedge in
May; thus, few if any young could have been
caught.
RESULTS
Call and Statistical Analysis.— We recorded
231 ‘chick-a-dee’ calls from 12 individuals.
Black-capped Chickadees from non-screech-owl
areas produced 93 calls (n = 8 individuals, mean
± SE = 11.6 ± 6.1) while chickadees from
screech-owl areas produced 138 calls (n = 4
individuals, mean ± SE = 34.5 ± 8.6). This
197% increase in average call number per
individual was only marginally significant when
using log-transformed data with homogenous
variances (Fig. 2A; Ft. io - 3,65. P = 0.085).
Individuals from areas without and with screech-
owls, respectively, averaged 2.30 and 4.40 D
notes per call (median = 2.22). which represented
a 91% higher number of D notes per call in areas
with Eastern Screech-Owls (Fig. 2B, Fig. 3; FUo
= 7.64, P = 0.020). The duration of the first D
note produced by chickadees in areas without
screech-owls was 36% longer than in areas with
them (Fig. 2C. Fig. 3 ; F,.,0 = 6.44. P = 0.030)
and the time between the first and second D notes
was 44% longer (Fig. 2D. Fig. 3; Fuo = 4.58,
P - 0.058). There was no significant difference in
length of lime between the ‘chick-a’ and the D
notes between the two groups (Fuo = 2.03. P =
0.19).
DISCUSSION
Faunal community structure is spatially and
temporally dynamic as predator composition
changes over space as well as generations of prey
(Griffin 2004). This raises a fundamental question
as to whether absence of a historically sympat-
ric predator results in loss of recognition or an
acoustical change in learned calls for that
predator. Evidence suggests it is not the former
and that deterioration in predator recognition can
be recalcitrant (Curio 1993, Blumstein 2006).
Maintenance of adaptive response to unfamiliar
predators is particularly likely for continental
species, as their lineages have been subjected to
different predator archetypes (Blackburn et al.
2004, Cox and Lima 2006); presence of a
functionally similar predator is also sufficient
for persistence of threat recognition for a currently
absent but historically sympalric predator (Blum¬
stein 2006).
Black-capped Chickadees have many similar-
sized avian predators such as Cooper’s Hawks
( Accipiter cooper'd). Sharp-shinned Hawks (A.
striatus), and American Kestrels ( balco sparver-
i„s), and it is unlikely the low-threat -chick-a-dee'
calls produced in areas without screech-owls
(Figs. 2. 3) reflect loss of predator recognition
but rather resulted from failure to learn vocaliza¬
tions for them. Learning call structures in many
songbirds is requisite for producing and respond¬
ing to them (Hughes et al. 1998, Gill and Sealy
2004. Avey et al. 201 1 ). and predator absence can
alter learned anti-predator vocalizations in one
generation (Blumstein et al, 2004). We did not test
different-size predator models or measure re¬
sponses to playbacks of our recorded calls and it
remains possible that chickadees in areas without
screech-owls coincidentally elicit calls with few
D notes which convey high threat. This is unlikely
because 'chick-a-dee' calls designating high
threat and the responses to them, albeit learned,
seem highly conserved throughout North America
(Hurd 1996. Baker and Becker 2002, Templeton
et al. 2005. Templeton and Greene 2007, Avey
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 4. December 2012
754
ESOWs
present
ESOWs
absent
ESOWs
present
ESOWs
absent
(in sec); and (D) timelength tetwwn tte ^ °f ° n°tCS per call; (C) lcnf?'h of the first D noIe
when presented with a stuffed Eastern Screech-Owl ’fESOW) t *eC) C,ICUed by caP,ured Black-capped Chickadees
Lh °Wl (ESOW) n,odcl "> arcas where screech-owls were present and absent.
et al. 2011). We also did not measure habitat
features (e.g.. extent of fragmentation), which can
affect sound transmission, but observed no
discemable differences in sites with and without
screech-owls and note alarm call structures do not
vary across habitat types in other taxa (Tppi et al.
Templeton et al. (2005) found Black-cap,
Chickadees convey high threat levels (based
predator size) by eliciting large numbers
frequent, short D notes and suggested tl
response was threat- but not predator-specif
Th,s remains plausible but if chickadees si
recogmze screech-owls as a dangerous predal
have lost threat-appropriate vocalizations I
hem, their call components may actually conv,
™PCC: C toea,S- n°' Sp
cies. Thus, the complex ‘chick-a-dee' call nu
uniquely con vey the identity of particular predat,
species, and can have survivorship value
dtosyncratues i„ predator-foraging behavior a
feet the adaptive nuances of predator-specific pre
lesponses. Local predator absence or presenc
should have no bearing on chickadee response i
chick-a-dee call structures convey information
about predator size only. We did not find this to
be the case and highlight this incongruence as
evidence for a predator-specific call structure,
^ hat seems apparent is that components of the
anti-predator behavior for this historically sym-
pau ic and dangerous predator have been altered.
Increasing interest is emerging to integrate
avian culture ( i.e., behavior acquired through
social learning; Laiolo 2010) with conservation
(Curio 19%, McLean el al. 1999. Ryan 2006.
Laiolo 2010). Information for many songbirds,
including anti-predator vocalizations, is transmit-
ted v'a social learning (Gammon et al. 2005.
Laiolo and Telia 2007. Nocera and Taylor 20081.
Survi vorship can be reduced if passage of social
learning is disrupted but sympatry is later realized
between predator and prey (van Heezik et al.
1999). Black-capped Chickadees elicit a threat-
inappropriate call for screech-owls in areas
aeking them and there is little opportunity for
ock members to learn a proper response
( Templeton and Greene 2007); thus, their survi¬
vorship may be compromised if they are later
Saborse and Renne • HISTORIC PRESENCE AND ABSENCE OF PREDATORS
755
K
H
z
Sec
FIG. 3. Representative spectrograms of ‘chick-a-dee’ calls from (A) Beaver Creek State Park, (screech-owls present)
and iB) Ford Nature Center (Mill Creek Metroparks), Ohio (screech-owls absent).
exposed to this predator. Achieving sympatry with
a predator is likely to result in quick spread ot
threat-appropriate calls, but the time necessary for
this is not trivial for small populations threatened
with extirpation. The rapidity with which this
transmission occurs can be accelerated by linking
naive populations lacking fitness- related vocali¬
zations with those ‘culturally significant units'
having them (Ryan 2006). This suggests manage¬
ment which increases population connectivity can
he of strong conservation value to many songbirds
'n decline by maximizing population growth
Potential, which in part is driven by facilitating
transmission of behaviors of high adaptive value.
ACKNOWLEDGMENTS
We express gratitude to J. N. Mager ot Ohio Northern
University for lending recording equipment and for com¬
ments on this project. We also thank A. W. Jones of the
Cleveland Natural History Museum for lending us a stuffed
Eastern Screech-Owl model. R C. Jones and R. J. Novotny
of Mill Creek Metroparks, and many other park managers as
well as experienced ornithologists are thanked lor commu¬
nicating their knowledge of the long-term, detailed screech-
owl records throughout our study region. J. D. Usis and F. P.
Diggins of Youngstown State University (YSU) are thanked
lor providing insightful comments as this project developed
and T. P. Higgins of YSU is thanked for detailed comments
on an earlier draft. The assistance from these people was
invaluable to our research. We appreciate the timely
approval of YSU's 1ACUC animal use protocol (# 05-10),
P. j. Kasvinsky (YSU) for funding of this project (URC # 07-
10). and the U.S. Fish and Wildlife Service and Ohio
Division of Wildlife for scientific collecting permits to
capture Black-capped Chickadees (#MBI7l55A-0and# 1 1-
363, respectively).
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Weise. c. M. AND J R Meyer. 1979. Juvenile dispersal
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The Wilson Journal of Ornithology 124(4):758-766, 2012
SPATIAL DYNAMICS OF THE RED-TAILED HAWK IN THE
LUQUILLO MOUNTAINS OF PUERTO RICO
FRANCISCO J. VILELLA1 ' AND WYATT F. NIMITZ1 2
ABS TRACT. The Red-tailed Hawk (Buteo jamaicensis) is a top predator of upland ecosystems in the Greater Antilles
Little information exists on the ecology of the insular forms of this widely distributed specie! wTslied nTvelen"
lm l0,2002 in *he “ northeastern Puerto Rico.
Moumls1 mS m dU,Ca,e h°mC rangC- C°rC ;irea shifl" ‘*"d macrohabitat use in the Luquillo
characteri/ed wide ranlinp e h T ,rct,UCn"-V pc, chcd ncar "* “»P of canopy emergent trees and were
h^actenzed by rang mg capabilities and extensive spatial overlap. Home range size averaged 5.022.6 = 832.1 ha
3 5 86 2- 348 5 u i f IV ** ' species had large mean wecklv movements
Fleeted f "rf t V'T °W «W~ fragmentation of contiguous fores, outside
protected areas ,n Puerto Rico may benefit the Red-, ailed Hawk. Received 28 Fehruan 2012. Accepted V Mas ViP
Oceanic islands are recognized as important
repositories of biodiversity and are a critical com¬
ponent of global conservation strategies (Myers
et al. 2000. Donazar et al. 2002). Raptors have key
toles in the food web of oceanic island ecosystems
given the virtual absence of native mammalian
predators (Losos and Ricklcfs 2009). The Red¬
tailed Hawk ( Buteo januiicensis) is one of the
most widespread raptors in the Americas (Johns-
gard 1990. Preston and Beane 2009). The eastern
Caribbean region of Puerto Rico and the Virgin
Islands (east to St. Kitts and Nevis) represents the
southeastern limit of the species’ geographic
range where the non-migratory subspecies B.
jamaicensis januiicensis occurs (Rat fade et al.
1998, Preston and Beane 2009). This species is
common in coastal and upland forests of Puerto
Rico where it coexists with six other resident
raptors including the endangered subspecies of the
Broad-winged Hawk (B. platypte/us bnmnescens)
and Sharp-shinned Hawk ( Accipiter striatus ventit -
i°r), Turkey Vulture (Cathartes aura). Puerto
Rican Screech-Owl (Orus nudipes), Short-eared
Owl (Asia flamnieus), and American Kestrel
(Fa/co sparverius). Little is known about the
ecology Of the Red-tailed Hawk in its neotropical
lange, including the Caribbean (Bildstein et al
1998, Raffaele el al. 1998). A number of studies
have examined movements of Red-tailed Hawks in
and p * ?fvey' Cooperative Fish
WM f F ,h M!nl S'°P96‘JI' of
W.ldlde, Fisheries and Aquaculture. Mississippi Siutc
University, Mississippi State. MS 3976'’ USA
“Current address: U.S. Fores, Service. Coconino Nation-
'Corresponding author; e-mail; fvilella@cfr.msstate.edu
North America, but information on spatial dynam¬
ics in neotropical environments is mostly absent. A
limited number ol studies have been conducted of
the Red-tailed Hawk in the Luquillo Mountains,
including dispersal of juveniles from natal areas
and temporal stability of territories in portions of El
'f unque National Forest (Santana and Temple
1988. Boal et al. 2003).
Our objectives were to: (1) quantify Red-tailed
Hawk spatial dynamics, and (2) habitat use in the
Luquillo Mountains, namely El Yunque National
Forest and surrounding private lands. Specifically,
we report annual and seasonal home ranges and
movements, including shifts in core area use, and
provide information on resource selection at the
macrohabitat level.
METHODS
Stiu/x Area. — Our study was conducted in the
Luquillo Mountains of northeastern Puerto Rico
including El Yunque National Forest (18 10' N.
63 30 W) and adjacent private lands (Fig. 1). El
Yunque National Forest (El Yunque) encompass¬
es 1 1 ,332 ha of subtropical rainforest in northeast
Puerto Rico with elevations ranging from 20
to 1.079 m. Mean annual precipitation is 200-
300 cm, increasing with elevation. Wind speed at
the highest elevations averages 18 km/hr. The
vegetation structure of El Yunque reflects forest
regeneration following agricultural abandonment
and serai responses to hurricane-induced distur¬
bances (Foster et al. 1999).
El \ unque encompasses five life zones char¬
acterized by lour dominant forest types along an
elevation gradient (Wunderle and Arendt 2011).
Life zones include: subtropical moist forest
(< 200 m asl) dominated by palma real
738
Vilella and Nimitz • RED-TAILED HAWKS IN THE LUQUILLO MOUNTAINS
759
Atlantic Ocean
FIG. 1. El Yunquc National Forest including reserve proclamation area boundary and forest types (adapted Irom
Wunderle and Arendt 20 1 1 ).
{Roystonea borinquena) and ruble bianco (Tube-
buia heterophylla ), subtropical wet forest ( 200—
600 m asl) dominated by tabonuco ( Dacryodes
excelsa ), subtropical rain forest (> 450 in asl)
dominated by palma de sierra ( Prestoea montaiui)
on steep slopes, subtropical lower montane wet
forest (601-900 m asl) characterized by palo
Colorado ( Cyrilla racemiflom), and subtropical
lower montane rainforest dominated by dwarf
cloud forest on high peaks and ridges (750-
1.079 m asl).
Trapping and Radio-! racking. — We trapped
hatch-year (HY). after-hatch year (AHY), sec¬
ond-year (SY), and after-second year(ASY) Red¬
dled Hawks in the Luqttillo Mountains during
May 2000-May 2002 using bal-chatri traps and
how nets (Thorstrom 1996. Vekasy et al. 2002).
Bow nets were bailed with adult Rock Pigeons
( Columba livia ) captured in the center ol nearby
towns and bal-chatri traps were baited with young
Helmeted Guineafowl ( Numida meleagris) pur¬
chased from local suppliers. We placed bal-chatri
traps along roads and established three stations for
bow-net trapping. Trapping stations were on
private lands west of the El Yunque boundaries,
in the Mameyes River Valley at 300 m elevation
in tabonuco forest, and in the Icacos River Valley
at 650 m elevation in palo Colorado forest.
We banded all captured hawks after recording
mass and body measurements with a USGS band
on the right leg and color-coded band on the left
lee. We instrumented Red-tailed Hawks with
radio transmitters using a Teflon backpack
harness designed to break away Irom a center
point over the keel (Vekasy et al. 2002, Klavittei
el al. 2003). Radio transmitters (Holohil R1-2CP:
Carp. Ontario. Canada) had a life expectancy of
~ 1 .5 years and were programmed with a 24-hr
activity switch. The 19-g harness and transmitter
packages averaged ~2.2% of body mass. Indi¬
viduals for which the radio transmitter exceeded
3% of body weight were measured, banded, and
released (Vekasy et al. 2002). We conducted
telemetry accuracy tests prior to tracking to
evaluate the equipment and estimate observer-
based location error. We estimated location error
760
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124. No. 4. December 2012
by placing radio transmitters on the ground and on
canopy-level observation platforms at known
distances and azimuths. We measured azimuths
to transmitters from telemetry stations with
known Universal Transverse Mercator (UTM)
coordinates, and compared true azimuths to
measured azimuths to calculate mean azimuth
error. Wc used homing whenever possible to
obtain visual locations of radio-marked hawks and
minimize telemetry error.
Wc located birds 1-3 times weekly by homing
and conducted systematic searches using omni¬
directional antennas mounted on trucks to locate
radio-marked hawks that had ranged outside our
search area (Samuel and Fuller 1994). We
recorded UTM coordinates when a radio-marked
hawk was visually located with a portable Global
Positioning System (GPS), recorded compass
bearing to the hawk, and measured distance in
meters with a range finder. Homing minimized
location and azimuth errors from telemetry tests
(~2 ) and allowed behavioral observations. We
searched for radio- marked hawks during a random
time period (0700-1 100. 1 101-1500, 1501-1900
hrs) every other location to reduce location bias
by time ol day. Wc generated UTM coordinates
for all locations once fieldwork was completed
(White and Garrott 1990. SAS 2001).
Statistical Analyses.— We calculated the mini¬
mum number of locations for home ranges to reach
an asymptote prior to analysis by randomly selecting
ocations for six hawks with the greatest number of
locations to create home ranges. We plotted each
home range area by the number of locations to
assess when home range area reached an asymptote
We pooled years for home range estimates due to the
relatively small sample size (n = 21) of radio-
marked hawks available for analyses.
All spatial analyses were conducted using
rcView' 3.2 Animal Movements extension Vcr^
sion 2.04 (Hooge and Eichenlaub 1999). We
estimated mean home range, mean weekly
movements and core area changes for the
breeding (15 Dec-30 Jim) and non-breeding
(1 Jul-14 Dec) seasons. Wc also estimated
aTm r T ,rave,cd from "-“PPing station
or, r '7 71 brec'di"« season cen,r°ids
or all individuals during the study. Home ranges
wfthl r a,ed US"li! "lc "sed-kemel estimator
With least squares cross validation (Worton 1989
Seaman and Powell 1990. Kernohan et al. 2001)
T7dtrm hreedin« centroids
y paired Rcd-taiied Hawks were examined to
learn if movements increased as energetic de¬
mands of nestlings and fledglings increased. We
examined distances moved by juveniles to mea¬
sure dispersal distances following the post-fledg¬
ling dependency period. We used mixed-model
A NOVA to test whether home range and weekly
movements differed between age and gender
(SAS Institute 2001). Seasonal core area shifts
ol Red-tailed Hawks among breeding and non¬
breeding seasons were calculated using a multiple
response permutation procedure tMRPP) in Pro¬
gram BLOSSOM (Cade and Richards 1999).
We used Euclidean Distance analysis to assess
Red-tailed Hawk patterns of habitat use (Conner
et al. 2003. Bingham and Brennan 2004). We used
the Animal Movements extension to generate
1,000 random points within the home range of
each hawk then overlaid each home range and
random-point home range on the landcover of El
unque and surrounding lands. We calculated
distance from each hawk location and random
point to the closest representative of each
vegetation type by querying one vegetation type
at a time (ESRI 2001 ). We used MANOVA to test
di defences in means of the ratio vectors (Conner
and Plowman 2001). Paired r- tests were used io
test disproportionately-used habitats and a ranking
matrix ol all possible pair- wise comparisons
constructed to rank habitat types. All values are
reported as mean ± SE (range); results were
considered significant when P < 0.05.
RESULTS
We captured 32 Red-tailed Hawks in the
Luquillo Mountains during our study of which
27 were radiomarked and 21 were used for
analyses (Table 1). A minimum of 25 locations
was required tor home ranges to reach asymptote.
Wc excluded two outlier individuals from analy¬
ses; a juvenile male (RTHA 13) and an unpaired
second-year female (RTHA 7). The outlier
juvenile male exhibited the greatest home range
(28,791 ha), ranging beyond the Luquillo Moun¬
tains to the Sierra de Cayey, 40 km to the
southwest (Table I ). Red-tailed Hawks were
monitored for an average of 5.9 ± 0.9 months
(2-14), yielding an average of 46.7 ± 5.7 (24-
1 10) locations per individual.
We located hawks perched 62.3% (7/ = 628) of
(he time, most frequently near the top of canopy
emergent trees. Maximum distance from trapping
■sites averaged 10,660 ± 1,291.3 in (range =
6,875-17,490 m). Home range of Red-tailed
Vilella and Nimitz • RED-TAILED HAWKS IN THE LUQUILLO MOUNTAINS
761
TABLE 1. Red-tailed Hawks captured and radiomarked. and home ranges
Capture date Months tracked Number of locations Gender'
1
6/20/00
8
79
u
2
6/29/00
2
29
u
4
3/05/01
14
84
F
5
3/07/01
14
110
M
6
3/12/01
11
65
M
7
4/03/01
5
32
F
8
5/04/01
8
63
F
9
5/14/01
12
69
F
12
7/06/01
7
44
F
13
7/13/01
10
60
M
14
7/13/01
7
42
F
15
2/14/02
5
33
F
16
2/20/02
5
50
F
17
3/12/02
4
37
M
18
3/14/02
3
37
M
19
4/04/02
3
37
F
20
5/15/02
2
37
M
21
5/16/02
2
37
M
22
5/20/02
2
37
F
23
5/31/02-
2
37
F
24
5/31/02
2
37
F
'' (iender: U
Age: HY
= unknown,
= hatch-year.
F = female. M = male.
AHY = after-hatch year. SY
second-year. ASY ;
= after-second
’ Home range: 95*5 fixed kernel (ha).
" Core area: 509!; fixed kernel (ha).
in the Luquillo Mountains, Puerto Rico.
Age" Home range' Core area'
AHY
8.635
SY
2,849
ASY
1.320
ASY
1.483
AHY
2,317
SY
14.734
AHY
5.724
AHY
1 .408
HY
1,853
HY
28.791
HY
7.401
ASY
8.854
AHY
8.644
SY
1.312
ASY
1 1.288
ASY
7.228
HY
1,660
HY
532
HY
571
HY
305
HY
362
520
427
236
150
312
1.883
598
190
317
3.601
519
1.226
925
210
1.230
1.047
149
69
62
40
80
Hawks in the Luquillo Mountains averaged
5,022.6 ± 832.1 ha (305-11.288 ha) and core
areas averaged 564.8 ± 90.7 ha (150-1,230 ha).
The home range of paired Red-tailed Hawks
averaged 4,584 ± 420.6 ha ( 1 ,3 1 2- 1 1 ,288 ha) lot-
males and 5,219.7 ± 1,395 ha (1,320-8.854 ha)
for females. Home range of juvenile males
U.096 ha) was more than twice that of juvenile
females (412.6 ha). Breeding season home range
of Red-tailed Hawks did not differ by age ( / ’ i .5 =
0.83, P = 0,40) or gender (F j.s = 0.02, P = 0.89).
Red-tailed Hawks in the Luquillo Mountains
exhibited high spatial overlap and essentially
complete coverage of LI Yunque (F ig. 2).
Weekly movements averaged 3,063.1 ±
348.5 m (range = 1.652-5.090 m). Movements
of juveniles during the post-fledging dependency
period averaged 1.348 ± 264.2 m (Table 2). Red¬
tailed Hawk weekly movements during the
breeding season did not differ by age (F t.6 =
0-01. P = 0.93) nor gender (F i.<, = 0.46, P =
0.52). We detected shifts in Red-tailed Hawk core
area use (Table 3). The breeding season core area
used by one after-second- year female (RTHA 4)
decreased 69% (6 = -6.53, P ^ 0.001) from
2001 (205 ha) to 2002 (64 ha) and differed from
the non-breeding season to the breeding season (5
= -8,90, p < 0.001). Similarly, one adult male
(RTHA 5) shifted core area used from the
breeding to non-breeding season (6 = -4.81. P
= 0.002) and from non-breeding season to
breeding season (6 = -4.29, P = 0.003). A
juvenile male (RTHA 13) exhibited the greatest
shift in core area (6 = -7.37, P ^ 0.001). Red¬
tailed Hawks in the Luquillo Mountains exhibited
non-random patterns in habitat use (Wilks’ X =
0.1346, /^i o f, = 3.86. P = 0.05) and used roadside
habitats more than palo Colorado forest (P —
0.001), agriculture (P = 0.002), rivers (P =
0.002), and pasture (P = 0.005). Roadside
habitats were used more than wetlands (P <
0.001 ). urban (P < 0.001 ), sierra palm forest (P =
0.001), and subtropical moist forest (P = 0.001).
DISCUSSION
Neotropical buteos generally search from
perches and initiate attacks once prey is detected
(Panasci and Whiiacre 2000). Retention of perch
hunting behavior has been documented in other
insular forms of the Red-tailed Hawk and closely
related species including the Hawaiian Hawk (B.
soliturius) (Walter 1990. Klavilter et al. 2003).
This behavior may be facilitated by the availabil¬
ity of perches in tropical forests (Wunderle 1997).
762
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 4. December 2012
FIG. 2. Composite of 21 Red-tailed Hawk home ranges
virtually complete coverage of El Yunque National Forest.
Most visual locations of radio-marked individuals
were near the top of canopy emergent trees,
suggesting Red-tailed Hawks in the Luquillo
Mountains readily use perches with an unob¬
structed view of their surroundings. This may
facilitate territory defense and improved hunting
success in the dense forest canopy of El Yunque
and the fragmented woodlands in surrounding
private lands. However, we repeatedly In = 27)
observed Red-tailed Hawks in El Yunque hunting
from a soar and making long sloops at Scaly-
naped Pigeons (Paiagioenas squamosa) and small
flocks of the critically endangered Puerto Rican
Parrot ( Amazona vitlata). White el ul. (2005)
reported predation by Red-tailed Hawks was one
of the primary mortality factors for parrots in El
Vunque. We also observed Red-tailed Hawks
soaring with rats in their talons in El Yunque and
adjacent lands. Previous studies have documented
high abundance of columbids and rodents in El
Yunque (Zwank and Layton 1989, Riveru-Milan
Red-tailed Hawks in the Luquillo Mountains
are smaller m body size compared to continental
conspecifics, reflecting the ‘island rule’ concept
in the Luquillo Mountains depicting high spatial overlap and
Puerto Rico.
ol body size variation in terrestrial vertebrates of
oceanic islands (Lomolino 2005, Vilella 2007).
Annua! home range was large compared to main¬
land counterparts and other similar-sized raptors
of the Americas (Reynolds et al. 1 994. Walls et al.
1999). Similarly, breeding season home ranges
were larger than reported for continental subspe¬
cies (Andersen and Rongstad 1989. Smith et ai.
2003). The largest home range (28,791 ha) was
exhibited by an unpaired juvenile male, a pattern
observed in other conspecifics (Bloom et al
1993).
Home ranges of Red-tailed Hawks in El
Yunque were markedly different from previously
reported estimates of territory sizes (Santana and
Temple 1988. Boal et al. 2003). Boal et al. (2005)
reported Red-tailed Hawk breeding territories in
the eastern portions of El Yunque averaged
1 24.3 ha. The authors also argued there was little
temporal change in the spatial distribution of
territories and considerable boundary overlap over
a 26-year period. Our results indicated Red-tailed
Hawks in the Luquillo Mountains use large areas
throughout the year. Core areas within Red-tailed
Hawk home ranges averaged 564.8 ha, almost five
Vilella and Nimitz • RED-TAILED HAWKS IN THE LUQUILLO MOUNTAINS
763
TABLE 2. Distance from trap sites and weekly movements of Red-tailed Hawks in the Lut|tiillo Mountains, Puerto Rico.
Bird ID
Gender1
Age”
Max D‘ (ml
B-MWM'1 (m)
NB-MWM' (in)
MWM1 (m)
1
U
AHY
6.875
3.263
3,058
3.481
2
U
AHY
7.348
2.1 19
2,1 19
4
F
ASY
8.881
1.595
1.913
1 .652
5
M
ASY
6,454
2.048
1.580
2.166
6
M
AHY
9.629
3,730
2,095
2.599
7
F
AHY
17.490
4.573
5.039
4.651
8
F
AHY
10.248
2.906
2,873
2.975
9
F
AHY
16.008
2.327
1.312
2.090
12
F
HY
8.014
3.028
3.258
13
M
HY
39,942
6.791
6.782
6,705
14
F
HY
8,089
3.758
3.628
15
F
ASY
16.576
5.090
5.090
16
F
AHY
8.096
3.754
3.819
17
M
AHY
8.818
2.073
1.954
18
M
ASY
15.308
3.967
3.967
19
F
ASY
12.066
4.085
4.085
20
M
HY
5.179
2.286
21
M
HY
5.276
1.188
22
F
HY
3.194
1.470
23
F
HY
1.959
877
24
F
HY
2,104
919
“ Gender: U
= unknown, F —
female. M = male.
Age: HV = hatch-year, AHY = after-hatch year, ASY after-second year,
j Maximum distance front trap site.
Breeding season mean weekly movement.
, Non-breeding season mean weekly movement.
Annual mean weekly movement.
limes grealer than territory si/.es reported by
Boal et al. (2003), a difference we attribute to
the benefits of radiotelemetry. Territory sizes of
Broad-winged Hawk pairs measured by spot
mapping (74.3 ha) in the Rio Abajo Forest of
north-central Puerto Rico were considerably
smaller than home range estimates (213.1 ha)
obtained from radiotelemetry (Vilella and
Hengstenberg 2006). Radiotelemetry generates
improved estimates of animal space use com¬
pared to visual estimation techniques ( i.e., spot
mapping) because individual birds can be
tracked and observed continuously below or
above the canopy over extended periods of time.
However, most estimates of home range size for
neotropical raptors with few exceptions (Valdez
2009) have relied on territory mapping and
ground surveys, not radiotelemetry (Mader
Table 3. Distance between centroids and core area shifts from breeding to non-breeding season for six Red-tailed
Hawks in El Yunque National Forest, Puerto Rico.
Bird ID
Gender
Age”
ST
D1STT
DIST2”
DIST3r
4
F
ASY
P
422.5
699*
569*
5
M
ASY
P
1.750.7*
1,385*
367
6
M
AHY
P
1.013.1
8
F
AHY
P
276.8
9
F
AHY
P
87.3*
13
M
HY
N
6.265.2*
Gender: F = female. M = male.
Age: HY = hatch-year, AHY = after-hatch year. ASY = after-second year.
Status: P = paired, N = not paired.
GIST I = distance (m) 2001 breeding season centroid to 2002 non-breeding season centroid.
D1ST2 = distance (tn| 2001 non-breeding season centroid to 2002 breeding season centroid.
DIST3 = distance (in) 200! breeding season to 2002 breeding season centroid.
" Significant core use area shifts estimated by Multi- Response Permutation Procedure.
764
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124. No. 4. December 2012
1982, Thiollay 1989, Panasci and Whitacre
2002). The extensive spatial overlap of home
ranges during our study suggests that, while
Red-tailed Hawk pairs may be highly territorial
in the immediate area around their nest,
individuals may move and forage over commu¬
nally-shared space. This may be a result of
reduced competition from the absence of other
species of similar-sized raptors (i.e., ecological
release) provided by the isolation of an oceanic
island setting and the soaring conditions in the
Luquillo Mountains (McNab 1994, Vilella
2007).
Home range size in raptors increases with body
mass and is influenced by prey composition in the
diet (Pecry 2000). Moreover, home range size
may be a function of prey availability, dominance
status, and territory acquisition. Female Red-
tailed Hawks in the Luquillo Mountains are
considerably larger than males averaging 199 g
more, suggesting they may be dominant during
interactions. Garcelon (1990) showed larger
females displaced smaller males during observed
interactions. Dominance and aggression in raptors
enhances territory acquisition and access to
limited resources in temperate regions (Janes
1994, Shelley et al. 2004).
Studies on resource availability of Red-tailed
Hawk prey in El Yunque have not been
conducted, but previous research suggests diet
varies with elevation. Santana and Temple (1988)
reported Red-tailed Hawks in lowland habitats
outside El Yunque consumed mostly mammals
such as small Indian mongoose (Herpes, es
auropunctatue ) and rats (Rent us spp.) in contrast
to the high elevation rain and cloud forests of El
Yunque where they relied on amphibians, reptiles,
and birds taken from the canopy. Food delivery
rates by parents tu nestlings can also be impeded
by rainfall and fog, contributing to nest failure at
high elevations (Santana and Temple 1988).
We documented substantial home range over¬
lap among radio-marked hawks during our study
(Fig. 2). Valdez (2009) reported a slight home
range overlap among five species of Micros, nr
forest falcons in the Peruvian Amazon. The Red¬
shouldered Hawk (H. lineatus) exhibited limited
amount of overlap between adjacent home ranges
in uiban and suburban environments (Dykstra el
. 2001) Alternatively, home ranges of nesting
Red-ta, ed Hawks in Wisconsin overlapped ex
tensively (Stout et al. 2006). The extent of spatial
overlap exhibited by Red-tailed Hawks in the
Luquillo Mountains may be related to high
population density, as well as distribution and
availability of prey (Zwank and Layton 1989.
Rivera-Milan 1992. Boal et al. 2003, Nimitz
2005).
Red-tailed Hawks in the Luquillo Mountains
moved considerable distances between weekh
locations, averaging 3.063 m per movement
(Table 2). Paired females had slightly greater
weekly movements compared to paired males and
may have been related to dominance status.
Unpaired individuals of some raptor species
exhibit larger home ranges and movement be¬
tween weekly locations (Bloom et al. 1993). Male
juvenile Red-tailed Hawks in our study had larger
average mean weekly movements than juvenile
females during the post-fledging dependency
period. I his could be related to earlier flight
leather development and active dispersal of
juvenile males (Hargis et al. 1994. Mar/lulT et
al. 1997). Radio-marked hawks frequently exhib¬
ited long distance flights (4-7 km) within a short-
time period (<4 min) and readily used areas
inside and outside El Yunque. This may reflect
the soaring conditions in the Luquillo Mountains
and the generalist nature of the species (Snyder et
al. 1987, Bildslein et al. 1998). We detected shifts
in core area use lor Red- tailed Hawks within and
between years (Table 3). Large range use shifts
have been reported for Northern Goshawk (4.
i’entiUs) outside the breeding season (Hargis et al.
1994, Drennan and Beier 2003). Resource de¬
pression in core areas and habitat alteration can
also influence shifts in range use by raptors
(Jaksic 1988. Rodriguez-Estrella et al. 1998).
Red-tailed Hawks in El Yunque and surround¬
ing lands were associated with roadside habitats.
Roadside vegetation in the Luquillo Mountains is
characterized by an open canopy of pioneering
tree species (e.g., Cecropia peltata) and a sun-
tolerant understory dominated by early succession
plants and ferns (Lugo and Gucinski 2000).
Compared to the surrounding dense forest vege¬
tation. openings along riparian forest and roads in
the contiguous forest of El Yunque and fragment¬
ed lowlands may facilitate resource acquisition
and benefit Red-tailed Hawks (Preston 1990). We
frequently observed hawks hunting along rivers,
roads, and in pastures. The Red-tailed Hawk is
considered a habitat generalist throughout its
tange; our findings suggest fragmentation of
contiguous forest outside protected areas may
benelit Red-tailed Hawks. Additional research on
Vilella and Nimitz • RED-TAILED HAWKS IN THE LIJQUILLO MOUNTAINS
765
Red-tailed Hawks in the Caribbean will improve
our understanding of the ecological role of this
upper level predator in the terrestrial ecosystems
of the Greater Antilles.
ACKNOWLEDGMENTS
\\ e are grateful to the U.S. Fish and Wildlite Service.
L'SDA Forest Service, Puerto Rico Department ol Natural
and Environmental Resources, and USGS Biological
Resources for financial and logistic support. We thank K
A. Jacobson and M. M. Rivera for field assistance. We are
indebted to the USDA Forest Service’s International
Institute of Tropical Forestry for access to climate data
and digital land cover. The manuscript was greatly
improved by comments from two anonymous reviewers.
Animal capture and handling procedures were conducted
under permits EPE-010 from the Puerto Rico Department of
Natural and Environmental Resources. USCiS Bird Banding
Laboratory Master Station Permit # 22456. and protocol #
00-093 of the Mississippi Slate University Institutional
Animal Care and Use Committee. The use of trade names
or products does not constitute endorsement b\ the U.S.
Government.
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The Wilson Journal of Ornithology 124(4):767 774, 2012
FIRST DESCRIPTION OF THE REPRODUCTIVE BIOLOGY OF THE
GREY-BELLIED HAWK ( ACCIP1TER POLIOGASTER)
ANDREA LARISSA BOESING,1 2 WILLIAN MENQ.1 AND LUIZ DOS ANJOS'
ABSTRACT— We observed an active nest of the Grey-bellicd Hawk [Acci/nter poliogaster) in the mixed rainforest of
southern Brazil during the 20 1 1 breeding season. The nest was a platform built in the branches of the upper part of a Parana
pine ( Araucaria angustifoha). The clutch size was two eggs, but only a single nestling survived and left the nest. ~49 days
post-hatching. The fledgling was fed by adults at the nest for at least 90 days post-hatching. Only the adult female incubated
the e22S and brooded the nestlings. Both female and male provided nest defense, the former up to 50 m from the nest and
the latter at 50 to 200 m. Only the male hunted and only the female fed the nestlings. The identified prey brought to the nest
by the male included eight birds and one young armadillo. Five voice types were identified: one alarm call, three tood-
related calls (performed bv adults), and one food-begging call (performed by the fledgling). The type of habitat where the
nest occurred suggested this poorly known species can possibly survive in disturbed areas. It seems to be naturally rare and
its' shy behavior contributes to its low detection, Received N February 2012. Accepted 12 July 201..
The Grey-bellied llnwk ( Accipiier poliogaster)
is a poorly known species occurring over a large
area in South America. This species inhabits
lowland tropical forest, humid secondary growth
and other dense woodland, and also riverine
strips, apparently almost entirely below 500 m
and is perhaps migratory (Ferguson-Lees and
Christie 2001). It is distributed from northern
Colombia, the extreme west and south ol
Venezuela and lowland Guyana and Surinam
southwards through east Ecuador, northeastern
Pern and the Amazon, and east Brazil, from south
to north and east of Bolivia, east Paraguay, and
the extreme northeast of Argentina (Ferguson-
Lees and Christie 2001). It is a rare species and is
poorly known throughout its range (Thiol lay
1994). and is also poorly represented in museum
collections (Lanzer et al. 2009). It is treated as
Near-Threatened by Collar et al. (1994). hut the
species was recently categorized as a species of
Least Concern by Birdl.ife International (2012).
Information on the nest and reproductive
biology of the Grey -bellied Hawk has not been
described (Bicrregaard 1994. Miirquez cl al.
2005). and the vocal repertoire and diet ot this
species are unknown. There arc several short
articles discussing the possibility of a Grey-
bellied Hawk nest in Ecuador. This nest was
described by Vries and Melo (2001) as belonging
to a Slaty-backed Forest Falcon t Micrastur
mirandollei), a species with a similar adult
Departamento dc Biologia Animal c Vegetal. Umversi-
dade Estadual de I-ondrinS. Rodovia Celso Garcia Cid.
Campus Universitdrio-Caixa Postal 6001, CEP 86051-980.
Londrina, Parana. Brasil.
'Corresponding author; e-mail: lari.boesing@gmail.com
plumage as the Grey-bellicd Hawk. Thorstrom
(2002) questioned this designation, because some
of the nesting habits reported by the authors differ
markedly from those of the genus Micrastur .
suggesting the nest described was misidentified as
belonging to a forest falcon, and instead possibly
belonged to either a Bicolored Hawk ( Accipiter
bicolor) or Grey-bellied Hawk.
We made observations on the reproductive
biology and behavior of the Grey-bellied Hawk
based on an active nest found in mixed rainforest
in southern Brazil. We provide the first descrip¬
tions of the nest, egg. nestling, and fledgling, as
well as information on the diet and vocal
repertoire of this poorly known species.
METHODS
Study Site. — The nest was in a disturbed area
within mixed rainforest in Santa Catarina State,
southern Brazil at 800 m elevation. This forest
area. —500 ha in size, has a heavily degraded
understory because it is used for livestock. In
particular, the area around the nest (— 200 m
radius) had a poor understory. Parana pine
( Araucaria angiislifolia) represented —50-60%
of the tree species in (his disturbed forest; the
density of this conifer in mixed rainforest is -40%
of the individual trees (Oliveira and Rotta 1982)
and it is the dominant tree species of this forest type
(Maak 1981. Oliveira and Rotta 1982). Other tree
species in the study area included Ocotea porosa.
Ilex paraguariensis, Cedrela fissilis, Lithraea
molleoicles, and Ocotea odorifera.
Field Observations. —We made observations
continually (4 days/week) between 16 September
and 27 November 201 1 with occasional observations
767
768
THE WILSON JOURNAL OF ORNITHOLOGY . Vol 124. No. 4. December 2012
until mid January 2012. Observations were usually
made by the same observer (ALB) and were a, I
libitum with all activities in the nest observed and
noted. Thus, we achieved continuous observation for
6 hrs/day. Observations were primarily front 06(X)
(sunrise) until 1200 hrs, and at a lower frequency
from LOO to 1900 hrs. The activities recorded
included: parental care and incubation, nestling/
fledgling development, hunting sessions, provision¬
ing sessions, and agonistic interactions. We built a
camouflaged blind 40 m from the nest from which to
make observations and not disturb the birds
Occas'ona1 observations were made until 15 January
S ' r, ay m the nest area- We used Zeiss
X a 42 binoculars, and a Canon PowerShot SX20
camera to describe and document observations and ,
digital recorder Panasonic RR-US 470 to record calls
and Raven Pro 1 .4 ( Bioacoustics Research Pre^rn
0 prodllce tlle spectrograms. Vegetation
n Tk-°"0WS M™ Boreal Curd n
RESULTS
blest Location and Description —T ho n
bellied Hawk pair was first known to be in'The
area on 14 September 2011. However the pair
and a juvenile had been observed in the v. o
at the end of September. 1 yearZitT^
was looted because of the aggressive behavior
the female m response to hum-m r, 1
perched high S T “ ^
direction of the observer's position 'n
duri„: 20,1
cons, meted ,8 m above ground Tvefl^ The
incubation and brooding, only when taking find
from the male or attacking potential predators and
intruders. The male remained close (10-20 m) to
the nest at all times when the female was off Ik
nest.
Only one nestling survived and. at the end of
the sixth week <5 Nov 201 1; - 42 days), wc found
the remains o| the oldest nestling on the ground
30 m from the nest. The surviving nestling left the
nest at the end of the seventh week 49 da) m
when its first flight was observed, The fledging
had a black cap and malar streaks, rufous cheeks
neck and breast, and a white throat and middle-
breast with the pattern of black streaks complete
mi the underparts in the eighth week (- 55 day.,
1 ig. ID). The lledgling stayed close to the rest
om 'he' eighth until the twelfth week, venturing
up to 300 m from it.
blest Defense.- Both the female and male
elended the nest, but while the former defended
up to a radius ol —50 m, the latter seemed to
defend a zone from -50 to 200 m. The female
was observed chasing a Grey-headed Kite (Up-
Union cayanensis) and a Southern Crested Cara¬
cul a ( C a meant pUtncus). Her aggression was
strongest towards the Grey-headed Kite with three
observed body contacts. She grabbed the kite with
jc* jaws on his back on one occasion, and Hew in
1 11 °c lion ol the conifer canopy and continued
to do so until -50 m from the nest.
he aggressiveness of the female against
raptors or humans continued throughout the
nesting period, from incubation until fledgling.
, e ’otinued to demonstrate this behavior after
hr., « 7 r “uuve ground level in u,> ° ,g,ing lcfl lfle nest until the tenth weel
■ nC es,° 1 lc‘ canoPy of a young Parana Pin * *?°St" ,atc*lm£ when aggressive behavior began t£
close ,o he top of the tee. and wasTuTou dedTT T™' *» ‘<4* Performed this betavio,
dense foltage. The nes, .. .... . . noundeJ ,n the twelfth week and i, watt difficult to find her
oi the fledgling in the nesting area.
i" ^'ao”d
Sticks that ranged front 0.5 to ‘cT b, '7^ “d
(Ftg. 1A. B). The inside of te „es, L "
°n 26 Sep 2011 and wc „bsTrvcd aT e ^
newly hatched nestling (Fij, , TL*" “d a
rounded oval shape md L ‘ ™ Cgg had a
e white ™
were overall beige in color , nest||ngs
nrent was followed for -dOday , oSff h'Vd°P‘
Incubation and Nest lino n #
female incubated the cZ The
during the period ofobsem, lots r d? a"d'
nest 96% of the time. She Tft d °n lhe
short periods (12 + 974 ° 10 nesl on,y for
/4 m,n’ n = 14) during
.. *- . . . uicj.
c also observed the male attacking potential
predators (Grey-headed Kite and Southern Crest-
l a,acara) on two occasions at a distance
c tween 50 and 200 m of the nest. Other raptors
wtn_ observed close to the nest but appeared to be
tolerated within the defended area. These included
£■ I low-headed Caracara (Milvago chimachimi).
<>ai sic e Hawk ( Buieo magnirostris ), Plumbeous
1 c (Ictinia plumhea). and Swallow-tailed Kite
anon is fo/ftcatus). These species were prob-
, y Ualed 'n lhe nest area because they were
,a -v 0 served flying above the canopy. A
m side Hawk approached the nest closely on
<- occasion and perched on a branch at a
Boesing et al • REPRODUCTION OF THE GREY-BELLIED HAWK
769
FIG. I . The nest of the Grey-bellied I lawk in the upper pari of a Parana pine in the mixed rainforest of southern Brazil.
IA) Inner nest: the newly hatched nestling (on the right) and an egg (on the left) on 26 September 201 I: (B) the nest and
female Grey-bellied Hawk: (Cl nestlings 6 weeks post-hatching (2 Nov 2011): (D) fledgling 9 weeks post-hatching (23
Nov 2011).
distance of 20 m before the female chased it away.
A juvenile Yellow-headed Cararaca in another
situation ventured close to the nest and was
frightened away by skimming of the female.
Hunting and Food Provisioning. —The male's
role during both incubation and post-hatching
periods was mainly providing food for both
female and nestlings/flcdgling. The male brought
prey to the female during the incubation period to
feed upon on the nest. The male continued to
bring food to the female during the nestling
period, which she used to feed herself and also
tore it into pieces before delivering it to die
nestlings (up to the sixth week: — 42 days). The
nestlings began to feed themselves at -20 days,
but female assistance, by tearing the prey into
pieces, was usually observed. The male let l the
food in the nest for the chicks to start feeding
themselves after -42 days. It was at this point
that the first sign of competition between the
nestlings appeared, normally occurring when the
male left the prey in the nest. The faster nestling
would take the prey using its claws and feed itself,
not allowing the other chick to feed. The other
chick would remain attentive and, if its sibling
was distracted, would steal the prey.
The prey was delivered by the male to the
female within a radius of -50 m of the nest
(during the incubation/nesting periods), or was
left on the nest (during the fledging period). The
hunts, undertaken only by the male, more
frequently occurred in the early morning and
before sunset (Fig. 2). Twelve of 22 occasions
when we observed the male bringing food were
early in the morning (0600-0900 hrs) and seven
were in the later afternoon (1600- 1 900 hrs). Prey
were brought outside of these times (at — 1400
hrs) on just three occasions. It was possible to
make a general identification of nine of the prey
items: eight were small birds, probably Columbi-
dae, and one was a mammal, probably a young
armadillo. The female dropped the carcass of a
770
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124. No. 4. December 2012
nIABLE: Means ' - of measurements of activities obtained while two nestlings of the Grcy-bellied Hawk wer
present m the nest an southern BrazH. Means were obtained from each continuous observation sesin (c^I^
Post-hatching
Nestling development
Female's time
in the nest
brooding (min)
Female's time
perched in die Parana
pine nest tree (min)
Number of prey
brought to the
ncst/pcruxl In = 22)
Tim: (Kilsy
thenedicgT
by frock (ram
~5 days
~ 12 days
Overall beige in coloration
Nestlings became whitish
with both bill and eyes
355.5 ± 3.09
163.7 ± 137.5
16 ± 14.5
12.3 ± 16.7
0.66 ± 0.81
0.50 ± 0.70
20 ± 105
30.5 z 3.33
—20 days
—25 days
clearly black, and legs yellow
Thc flight feathers became grayish
The upper parts of the wings
became predominantly black.
141 ± 69.7
174 ± III
0.60 ± 0.58
1 ± 0.00
46.7 ± 1.90
38 ± 16.3
the first black streaks appeared
on their flanks and the first
black band also appeared in
the tail; the first flecking on
the wings was observed
~35 days The top of the head became black with
increased streaking in the flanks
~40 days The pattern of black streaks on the
underparts was almost complete,
and the cheeks, neck, and sides
129 ± 86.9 1.25 ± 0.96 28 ± 10.7
04 ± 05.3 1.25 ± 0.00 13 ±04.5
of the breast begin to turn
rufous (Fig. 1C)
Ruddy Ground Dove (Columbine talpacoti ) <
one occasion during one of her aggressive attaci
in response to human presence during ||
incubation period.
Time spent by the female in the nest decrease
as the nestlings matured (Table 1), although sh
usually remained next to the nest perched on
branch (5-30 m distant). The time spent feedin
the nestlings appeared similar throughout thei
development (Table 1). We did not observe tl„
male directly feeding the young; his function wa
as a hunter. He rarely visited the nest, and ther
only lor a tew minutes, usually in the absence oi
the female.
Vocalizations.— The male, upon arriving in the
nest area with prey, emitted a call composed of
single notes (Fig. 3A) to alert the female which
responded with a similar call, also composed of
calls (Rr'3B)UtThh,Chr T* IODger than thc male
calls (Ftg 3B). Thus, both would be found in the
mid-level of the forest in the air emitting
distinctive, high-pitched calls (Fig. 3C)- the
female would then fly 50-100 « from the nest
with the prey and continue calling (varying
between 3 and II times/mi n). The female was
observed on some occasions emitting this call
when perched on a branch next to the nest in the
absence ol the male, possibly seeking delivery of
food.
We identified two other Grey-bellied Hawk
vocalizations during the reproduction period: an
alarm call performed by adults and a food-
beggtng call performed by the fledgling. The
alarm call was relatively long (almost 3 sec),
composed of seven to eight melodic notes
repeated in a rapid rhythm, and was given by
t e adults in response to intruders or potential
{!re a,ors -*D). The food-begging call of the
ctgling was given when receiving or seeking
°° ^8- 3E). The tood-begging call had varia-
ttons ased on the proximity of food; motivation
seemed higher when the male was arriving and
cn tng in the nest area and. alternatively,
motivation was lower when the fledgling was
seeking food.
Appearance oj Adults. — The female had a pure
w ute breast and neck with two dark stripes on the
n.ec ’ l",er hack was dark gray, as were also the
c ee s, having an almost black appearance. This
coloration extended until the top of the head
creating a 'helmet' effect. The area around the
eyes up almost to the bill was yellow. The male
was 30-40% smaller than the female. He also
had a while breast and neck, but his back and
Boesing et al • REPRODUCTION OF THE GREY-BELLIED HAWK
771
1912
1648 *♦♦♦♦♦
1424 4 ♦ 4
I 1200 -
Cl
5 0936
| 0712 Jt _ 4 ♦ ♦ ♦ ♦ ♦ ♦
I ♦ ♦ ♦
0448
0224
0000 _
0 5 10 15 20 25
Hunting sessions observed
FIG. 2. Time of day the male Grey-bellied Hawk hunted to feed the female and young during the nesting period in the
mixed rainforest of southern Brazil.
cheeks were light gray with only the wings and
the top of the head being dark gray. Both male
and female had three dark bands on the tail.
DISCUSSION
This is the first description not only of the nest
but also of some aspects of the reproductive
behavior of the Grey-bellied Hawk that were
previously unknown. The Grey-bellied Hawk has
been considered by many as an ‘aberrant'
Accipiier with obscure relationships with the rest
of the genus (S. H. Scipke, pers. comm.). Our
observations of its breeding biology and ecology
revealed it may be closer to other neotropical
Accipiiers than has been generally assumed.
Knowledge of this hawk is so sparse that, until a
few years ago. the juvenile, which has a plumage
similar to the Ornate Hawk-Eagle (Spi'cn'tns
oniatus ), was considered to be another species
(A pectoralis).
Sexual dimorphism between the male and
female was apparent with the latter being
noticeably larger ( — 40%). We believe the
surviving fledgling was also a female as on the
last occasion the male was observed to leave prey
in the nest (late Dec), the juvenile was taller than
the adult male. The juvenile 40 days post-
hedging) also had the dark bands that occur on the
neck of the female. Schulenberg et al. (2007)
described an important morphological feature
distinguishing male from female Grey-bellied
Hawks: cheek coloration. We observed the female
had darker gray and the male lighter gray cheeks
and agree with Schulenberg et al. (2007).
However, one important ieature is that the female
had a 'helmet' linked with the rest of the plumage
of the hack and head, forming a uniform dark gray
plumage. The male clearly had a light gray
•helmet' with the top of the head being dark gray.
The reproductive behavior of the Grey-bellied
Hawk seems not to differ from that of olher
Accipiter species. The nest of the Grey-bellied
Hawk was in the upper parts of a tall tree, as is
true for most of its neotropical counterparts (e.g.,
Bicolored Hawk. Thorstrom and Quixchan 2000;
Rufous-thighed Hawk |/\. erythronemius], Seipke
and Cabanne 2008; White-breasted Hawk \A.
chionogasier |. Jenner 2010). The Rufous-thighed
Hawk has similarly been observed to build its nest
close to the top of Parana pine (Seipke and
Cabanne 2008). Platt (1976) reported Sharp-
shinned Hawks (A. st rial us) also have a prefer¬
ence for nesting in conifers.
Parana pine is the preferred nesting tree of the
Rufous-thighed Hawk according to Seipke and
Cabanne (2008). These authors suggest many
factors could contribute to this choice and. of
these factors, one seems more important and
applicable to the Grey-bellied Hawk. These trees,
other than the nest tree, usually have variable
amounts of sticks in the upper branches, forming
platform-like structures that could serve to
confuse potential predators (Seipke and Cabanne
2008). This is consistent with our field observa¬
tions because potential predators flying above the
canopy were tolerated in the nest area by the
Grey-bellied Hawk, in contrast to those flying
through it. The Parana pine presents nearly
772
THE WILSON JOURNAL OF ORNITHOLOGY . Vot 124. No. 4. December 2012
Boesinget al. • REPRODUCTION OF THE GREY-BELLIED HAWK
773
horizontal branches radiating from the trunk at the
same height, providing a stable foundation for
nests (Seipke and Cabanne 2008).
The Grey-bellied Hawk nest seems no different
from those of other neotropical Accipiter (e.g..
Bicolored Hawk. Bierregaard 1994; Rufous-
thighed Hawk, Seipke and Cabanne 2008). Clutch
size is variable among species of Accipiter ; the
Bicolored Hawk varied between one and four
eggs, while the Sharp-shinned Hawk has 2-3 in
the Caribbean. 3-5 in Mexico, and 4-5 in North
America (Ferguson-Lees and Christie 2001).
Nestlings of the Grey-bellied Hawk appear to
remain longer in the nest ( — 49 days) than nestlings
of Bicolored Hawks (~ 35 days, Throstrom and
Quixchan 2000).
Thiollay (1994) reported fledglings are depen¬
dent on food brought by adults for at least several
days after leaving the nest. The fledgling Grey-
bellied Hawk left the nest and continued to
receive prey from the male for at least 60 days,
and possibly longer. Bicolored Hawk fledglings
similarly remain close to the nest and are
dependent on their parents for nearly 2 months
or more (Ferguson-Lees and Christie 2001 ).
The role of the male as hunter and the female as
feeder (Thiollay 1994) was observed for the Grey-
bellied Hawks we studied, similar to the majority
of Accipiter species. We did not observe the
female Grey-bellied Hawk bringing food for
nestlings while they were growing, as has been
described generally for Accipiter (Thiollay 1994).
It seems the Grey-bellied Hawk is a bird-hunter, as
suggested by Bierregaard (1994) and by associa¬
tion with its neotropical congeners (e.g.. Bicolored
Hawk. Throstrom and Quixchan 2000; Chilean
Hawk \A. chilensis], Rojas et al. 2004: White¬
breasted Hawk. Jenner 2010). Our observations (8
of 9 prey were birds) and the time of the day the
male Grey-bellied Hawk hunts, coincided with
higher activity of birds.
This was the second year the Grey-bellied
Hawk pair was known to have used the same
location to raise their young, and it is possible the
same nest was used, because the female defended
the same nest area in the presence of humans in
the previous year. We suspect this might be the
third year the site was used by this pair, because in
mid-September 2010. in addition to the pair of
Grey-bellied Hawks, we also observed one
.juvenile in the nest area. Many Accipitridae
species re-use old nests, to which they add new
material (Thiollay 1994). Gundlach’s Hawk (A.
guiullachi), a species endemic to Cuba, appears to
use the same nest for at least 3 years or more
(Bierregaard 1994). Whether or not a nest-site is
changed from I year to another is strongly related
to breeding success in the previous year (Thiollay
1994).
Our observations do not enable us to resolve if
the nest found by Vries and Melo (2001 ) belonged
to the Slaty-backed Forest Falcon or Grey-bellied
Hawk, as suggested by Thorstrom (2002). Mor¬
phological features reported by Vries and Melo
(2001 ) are general and a more precise description
is needed to reach a conclusion on species
identity; however, some ecological features re¬
ported by those authors are not consistent with our
observations for the Grey-bellied Hawk.
Our Field observations confirm the secretive
behavior attributed to the Grey-bellied Hawk
(Santos et al. 2009). This secretive behavior
would explain the rarity of records and why it is
easily overlooked. It became difficult to find the
adult pair or the fledgling in the nest area soon
after the fledgling had left the nest, and we were
barely able to detect the calls of the fledgling
seeking food. This species seems to be naturally
rare and its shy behavior contributes to its low
detection.
ACKNOWLEDGMENTS
We thank the Boesing Family lor assistance throughout
the entire field period with logistical and total support; the
farm supervisor Ladislau Cubas Jr. who gave permission to
access the area where the field work was performed; Artur
Battisti F'ilho who provided the photographic equipment
used during the field work, and Tiago Zaiden who helped
with improvement of the spectrograms. We appreciate the
valuable suggestions by S. H. Seipke, N. .1, Collar, and C. E.
Braun, which substantially improved die last version of this
manuscript. The first author received a research grant from
CAPES (Coordination for the Improvement of Higher
Level Personnel. DS). and the third author received a
research grant from CNPq (Brazilian Council for Develop¬
ment of Science and Technology. 305593/07-3). This paper
is dedicated to the first author's mother. Mse. Cila
Tere/inha Friedrich Boesing I In Mcnioriam ). who support¬
ed all of her field work.
LITERATURE CITED
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Cornell Laboratory of Ornithology, Ithaca. New York.
USA. http://www.birds.corneIl.edu/raven/
BirdLife International. 2012. Species factsheet: Accip-
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www.birdlife.org/
Collar. N. J„ Vi. j. Crosby, and A. J. St atter sfiei.d.
1994. Birds to watch. Number 2. The world list of
threatened birds. Birdlife International. Cambridge.
United Kingdom.
Fkkguson-Lf.es, J. and D. A. Christie. 2001. Raptors of the
world. Houghton Mifflin, Boston. Massachusetts USA
Gtu., F. AND D. Donsker. 2012. IOC World Bird Names
(Version 3.1). Princeton University Press. Princeton.
New Jersey, USA. http://www'. woridbirdnamcs.org/
Jennlr, T 2010. Life history of the White-breasted Hawk
MctTp/Ver chionoxaster). Ornitologia Neotropical
— I . I / — J o(J.
Lanzer. M . M. a. Villegas, and M. Alrelio-Sii va
-009. Pr.me.ro registro documentado de Acciniter
pol, ouster (Temminek. 1824) no estado do Parana
sul do Brasil ( Falcon i formes: Accipitridae). Revista
orasilctra deOmitologia 1 7: 1 37— 138.
Maak, R. 1981. Geografia ffsica do estado do Parana.
Segunda cdiyao. Jose Olimpio Editora, Rio de Janeiro.
MAR-riot a” F GAS,‘ V‘ Vaneoas- ANL) M. Bechard.
-00>. Avcs rapaces d.urnas de Colombia. Ins.ituto de
Jv*!?! dC RecursoS BioW«fcas Alexander von
Humboldt. Bogot.1, Colombia.
Missour. Botanical Garden. 2011. The plant list
M,s,°ur; Botanical Garden. St. Louis. Missouri!
USA. http://www.lropieos.org/
Ol.ve.ra Y, M. M. and E. Rotpa. 1982. Levantamento da
estrutura honzontal de uma mata de Araucaria do
primeiro planalto paranaense. Boletim de Pesquisa
Florcstal 4; I — 46.
Pi att. J. B. 1976. Sharp-shinned Hawk nesting and nest
site selection in Utah. Condor 78:102-103.
Rojas. R. A. F„ S. A. ORELLANA, $ C U UHJNG. and I.
SHEHADEH. 2004. Prey of breeding Chilean Hu»ks
(Accipirer chilen.sis) in an Andean Nothofa^ forest in
northern Patagonia. Wilson Bulletin 116:347-351.
Santos, R. e. p\. p. Scherer-Neto. and J L. B.
Ai nuoiTRyuE. 2009. Gaviocs. Pages 169-197 in
Instituto ambiental do Parana. Pianos de Cnnservafao
para Especies de Aves Ameayadas no Parana LAP
Projeto Parana Biodiversidadc. Brazil
SCHULENBERG. T. S.. D. F. STOTZ. D. F. I.ANt. J P.O’NEM.
AND T. A. Parker III. 2007. Biids of Pem. Pnnceton
University Press. Princeton. New Jersey. USA.
Seii’ke, S. H. and G. S. Cab anne. 2008. Breeding of the
Rufous-thighed Hawk (Airiprter eryilironemius I in
Argentina and Brazil. Ornitologia Neotropical 19:15-29.
7 hioixay. J. M. 1994. Family Accipitridae (Hawks and
eagles). Pages 52-205 in Handbook of die birds of the
world. Volume 2 (J. del Hoyo. A. Elliott, and J.
Sargatal. Editors). Lynx Kdicions. Barcelona. Spain.
Tiiokstrom. R. 2002. Comments on the first nesting record
ol the nest ol a Slaty-backed Forest Falcon (Mu rustur
miraru/ollei) in the Ecuadorian Amazon. Journal of
Raptor Research 36:335-336.
I morstrom, R. and A. QUixchAn. 2000. Breeding biology
and nest site characteristics of the Bicolored Hawk in
Guatemala. Wilson Bulletin 112:195-202.
kii.s. T and C. Mhlo. 2001. First nesting record of the
nest ol a Slaty-backed Forest-Falcon (Micrastur
mirandollei) in Yasunf National Park. Ecuadorian
Amazon. Journal of Raptor Research 34:148-150.
Tlw Wilson Journal of Ornithology I24(4):775 782, 2012
INTRODUCED SPECIES DOMINATE THE DIET OF BREEDING URBAN
COOPER'S HAWKS IN BRITISH COLUMBIA
JENNA A. CAVA,1 4 ANDREW C. STEWART,2 AND ROBERT N. ROSENFIELD3
ABSTRACT.— We used collection of prey remains, direct observations of hawks with prey, and video cameras at two
nests to assess frequency of occurrence and biomass of prey species taken by breeding Cooper s 1 lawks (Accipiter coopcrii )
in Victoria. British Columbia, Canada during 1995-20)0. Small 27 g) to medium-size (28-91 g) bird species
contributed the majority (79-94*7-) of prey recorded from collection of 3,231 prey remains. 437 direct observations, and 783
video items at 87 nest sites. Avian prey contributed over half of prey biomass recorded in direct observations and video data
(67*7 and 93%, respectively). One native and Luo introduced species provided most (> 85%) prey recorded in all samples
in which birds were identified to species; American Robin (Turdits migratoriiis). European Starling (St limits vulgaris), and
House Sparrow (Passer domesticus). Introduced species were an important component of the diet, contributing over half of
items identified in all samples. There was a temporal shift in age of prey used: the earlv-season diet (Mar-Apr) was
comprised of adult birds and subadull mammals, while avian young of the year dominated the diet from late May until the
end of the breeding season (70-100% of identifiable items). Mammals were inconsequential in terms of frequency and
biomass except at nests 16 of 87) on or near the University of Victoria campus where nearly all European rabbit
( Oryetolagus cuniculus) prey was recorded. Received 28 December 2011. Accepted 4 Ma\ 2012.
Urbanization is a major force in changes of
global land-use (Ortega-Alvarez and MacGregor-
Fors 2011). Urban environments are relatively
new habitats for Cooper's Hawks ( Accipiter
cooperii) and other birds of prey (Bird et al.
19%, Stout et al. 2007, Rosenfield et al. 2009).
These landscapes vary greatly in size, habitat
heterogeneity, prey populations, and other eco¬
logical factors that potentially affect reproductive
success of raptors (Stout and Rosenfield 2010).
Little research has been done on breeding raptors
in urban settings and fundamental ecological
understanding of these populations is lacking
(Stout et al. 2005. Rutz 2008, Stout and Rosen¬
field 2010).
Some of the highest nesting densities and
reproductive success for Cooper’s Hawks occur
in cities (Rosenfield et al. 2007b, Mannan el al.
2008. Stout and Rosenfield 2010). Investigators
have suggested high nesting densities and repro¬
ductive success of urban Cooper’s Hawks could
he related to abundance and type of avian prey in
cities (Marzluff et al. 1998, Stout and Rosenfield
2010). However, there are few reports of the diet
o! urban Cooper's Hawks. A 2-year investigation
by Estes and Mannan (2003) in Tucson. Arizona
appears to be the only published research that
provides a detailed study of the diet of urban
'V 174 N .8473 Schneider Drive. Menomonee Falls. WI
53051, USA.
: 1921 Doran Road. Cobble Hill, BC VOR IL5. Canada.
Department of Biology, University of Wisconsin,
Stevens Point. Wl 54481. USA.
4 Corresponding author: e-mail: jcava275@uwsp.edu
breeding Cooper's Hawks. Our objective was to
document the diet of Cooper's Hawks breeding at
high nesting densities in Victoria. British Colum¬
bia, Canada.
METHODS
All data were collected in the city of Victoria,
British Columbia, Canada during 1995-2010.
This is a 89-knv city with a human population
of ~ 300,000. It has a temperate, coastal climate
and is comprised of sparsely to heavily wooded
habitat dominated by tall coniferous trees includ¬
ing Douglas-fir ( Pseudotsugci menziesii) and
grand fir (Abies grandis) (Campbell ct al. 1990).
Nests were found annually by systematic searches
of the entire city and prey reported represent all
habitats therein (Stewart et al. 1996),
Direct Observations.— We recorded 437 inci¬
dental direct observations of adult Cooper’s
Hawks with prey items at 87 nest sites from
March through August 1995-2010. These obser¬
vations consisted of direct observations of prey
carried by hawks or prey dropped in mist nets by
captured hawks. Samples from each breeding
stage (pre-incubation, incubation, nestling, and
fledgling) for each year were pooled because of
small sample sizes and because proportions of
avian prey were similar among stages. We noted
items as native or introduced to the study area when
possible. Avian prey items were initially catego¬
rized into size classes (SC) following Storer
(1966), Kennedy and Johnson (1986), and Biele-
feldt et al. (1992) by known mass and bulk of
familiar species: SC 1 ^ 27 g and SC 2 = 28-91 g.
775
776
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124. No. 4. December 2012
Relatively few items were larger than SC 2 and
were categorized as >SC 2. We estimated biomass
ol each prey item. Biomass refers to live mass of an
item, not the mass delivered to the nest or
consumed by nestlings. We removed the data
collected at nests on or within 0.5 km of the
University of Victoria property (/? = 31 items)
from biomass estimates due to a site bias; nearly all
(8 of 9) European rabbits (Oryctolayus cuniculus)
were recorded at these few nest sites. Each rabbit
provided about live times the biomass of a single
avian item, inflating the biomass proportion
contributed by mammalian items and inaccurately
representing the extent of mammal consumption at
the majority of nests in Victoria.
We identified 189 (46%) of 408 avian prey
items to species. Adult masses of these items were
from Dunning (2008). The age of avian prey
items, when possible, was identified from feather
sheathing in nestlings and recent fledglings
distinctive Juvenal plumages, or the color of the'
tarsi for some species. We estimated mass of
avian items identified by species and age from the
.teuuure 0" growth rates (Clench and Ueberman
1978). Most species in SC 1 fledge at >90% 0f
aduU mass and we ignored age in these cases.
Altncial, open-nesting species in SC 2 were
divided into two categories of smaller (28-59
and large, (fiU-Sig, species. We calculated mass
at 70. 90, and 95% of adult mass lor smaller
species al nestling, juvenal. and unknown ages
respectively; and for larger species al 65, 85, and
90%. respectively. Juvenal and unidentifiable
Items larger than SC 2 were calculated a, 90%
la““ 10 If c°nservalive in our estimates.
We used assumed averages of 25 g and 65 g for
unidentified birds in SC I and SC 2. respectively
Only one unidentified partial item was larger than
SC and was not assigned a mass. Other
unidentified items that could not he assigned a
sue class were not included in mass estiuiLs
We .denufied 27 of 29 mammalian items (91%)
to genus or species: mosl were Eastern cottontail
(SyMagus Honda,,"*) or European rabbits, and
orway rats \Raltus norveeicus) \ mom
estimate of 350 g for the two rabbi. spec"s
obtained from measurements of semiTntact prev
remains ail rabbits were less than or about half
grown. We estimated adult mass of Norway and
black, lats [R‘ rattu«) from Nowak (1999)-
juveniles and unidentified individuals were esli'
mated a, 90 % of adult mass to be conservative'
Rats only identifted to genus were assumed to be
less than or about half-grown Norway rats based
on general observations and we estimated biomass
of each at 220 g. Adult masses of one deer mouse
( Peromyscus maniculatus) and one Eastern gray
squirrel (Sc i urns carolinensis ) were estimated
from Wilson and Ruff (1999).
Drey Remains. -We tabulated remains of 3.231
prey items from 44 active nest sites during the
pre-incubation through fledging stages in 1995-
1998. The items were mainly pluckings. and legs,
tails, or partial carcasses. We identified prey to
the lowest taxonomic class by comparing remains
to a reference collection of locally common prey-
si/.ed species and the Royal British Columbia
Museum's vertebrate collection. We included
items from reoccupied nest sites hut treat the data
as independent because no single nest site
contributed >7% of the total items over the 4
study years. We combined all stages of breeding
(pie-incubation through fledgling) and pooled
data from all years because proportions of avian
prey were similar (94-98%). Avian items identi¬
fied to species were categorized, based on adult
masses (Dunning 2008), into the same size classes
Irom Siorer (1966), Kennedy and Johnson (1986),
and Bielefeld! et al. (1992). We classified prey
items as native or introduced to the study area
when possible.
Video Analysis.— We used video cameras to
record prey deliveries in different years to two
arbitrarily selected nests >2.5 kin from the
University of Victoria property. The custom-made
camera fed into two VHS video recorders and an
Axis brand video server that recorded a still image
every minute. We placed cameras at an oblique
angle. 80 to 1 00 cm from the center of the nest
platform. The Torquay nest was recorded from 2
June through 21 July 2001. Recording start time
varied between 0800 and 0930 hrs from 2 June to
4 June, 0430 hrs during 6-15 June, and 0500 hrs
t e rest of the days. Recording continued until
T “ hrs- when the videotape ran out each day.
vn ol the 50 days had incomplete recordings.
I he Burnside nest was recorded from 4 June
lb rough 5 July in 2002. We recorded from 0500 to
- 00 hrs each day (excluding 6 incomplete
ays). Complete days for both nests averaged
6 his of footage and incomplete days ranged
Iroiri 6 to 12 hrs of footage. We obtained 750 and
467 hrs of video from the Torquay and Burnside
nests, respectively.
identified prey to the lowest taxonomic
eve possible, age, and categorized them into size
Cava el al. • DIET OF URBAN BREEDING COOPER’S HAWKS
777
TABLE !. Percent frequency of avian and mammalian
prey items by three sampling schemes at Cooper's Hawk
nests in Victoria. British Columbia. 1995-2010.
% Frequency
Prev remains
in = 3,231)
Direct observations
(n = 437)
Video analysis
(n - 783)
Avian
SC 1
32
46
62
SC 2
61
33
32
>SC 2
3
3
0
Unidentified
1
1 1
9
Totals
97
93
96
Mammalian
3
7
1
Unidentified
0
0
3
classes. We also estimated biomass for items
observed in the video with the same methods used
in direct observations. Data from the two nests
were pooled because proportions of avian prey
were similar (96% at both nests).
RESULTS
Small (< 27 g) to medium-size (2S-9I g) birds
provided most of the diet in terms of frequency
(79-94%) and biomass (67-93%) among all three
sampling schemes; mammalian items were a
small component of the diet at typical Victoria
nests (Tables I, 2). There was a silc bias
concerning one species of mammalian prey;
nearly all European rabbits (26 of 27) were
recorded from nest sites associated with the
University of Victoria campus (6 of 87 nest sites
over 16 years). Introduced species were a major
component of the diet, contributing >50% of the
TABLE 2. Percent biomass of avian and mammalian
prey items by direct observations and video at Cooper’s
Hawk nests in Victoria, British Columbia, 1995-2010.
Total biomass in grams is provided below sampling
scheme headings.
Cc Biomass
Direct observations*
Video analysis
(g = 21.086)
(g = 30.379)
Avian
SC 1
23
40
SC 2
44
53
>SC 2
14
9
Totals
81
95
Mammalian
19
5
Estimates do not
include data from nests
on the University of Victoria
campus due lo site bias.
items in terms of frequency and a similar
proportion of the biomass ol items identified as
introduced or native (Tables 3, 4). The most
prevalent avian prey species were House Sparrow
( Passer dome slum), European Starling ( Stumus
vulgaris), and American Robin (Jurdus migratorius)
(Table 5). These three species combined represented
85. 88. and 97% of the avian items identified to
species in direct observations, prey remains, and
video analysis, respectively. These species contrib¬
uted a majority of the avian biomass (69% in direct
observations and 91% in video analysis).
Young of Ihe year represented a majority of
identifiable avian items, contributing 76% of prey
remains. 63% of direct observations, and 92% in
video analysis. These young of the year also
contributed a majority of biomass in direct
observations (69%) and video (97%). The iden¬
tifiable mammalian items in the prey remains and
direct observations were mostly subadults (100
and 80%. respectively). Only one mammalian
item was classified to age in the video analysis; a
subadult rat. Avian young of the year were taken
w ith increased frequency in the prey remains and
direct observation samples as the breeding season
progressed. All identifiable items recorded before
late April were adult or subadult mammals, while
avian young of the year dominated in the diet
from late May to the end of July (Fig. 1). Nest
video data documented that high proportions of
young of the year prey (92%) were captured in
June and July, corresponding to similarly high
proportions of young prey recorded in the same
months by direct observations and prey remains
(Fig. I).
DISCUSSION
Small and medium-size birds 27 g and
28-91 g. respectively), and especially introduced
species, were the primary prey taken by Cooper’s
Hawks breeding in the city of Victoria, British
Columbia. Mammals were taken at low frequen¬
cies and did not contribute substantial biomass at
typical Victoria nests.
High variability of urban environments should
cause variation in the ecology of a raptor species
that inhabits different cities, which appears to be
the case for several investigations of the diet of
urban breeding Cooper’s Hawks. This species
preyed mainly on small and medium-size birds in
Victoria, many of which were introduced. Estes
and Mannan (2003) in Tucson, Arizona reported
nesting Cooper's Hawks mainly taking native
778
THE WILSON JOURNAL OF ORNITHOLOGY • Vul 124. No. 4. December 2012
TABLE 3. Percent frequency of introduced and nativi
prey items recorded by three sampling schemes at Cooper":
Hawk nests in Victoria. British Columbia. 1995-2010.
% Frequency
Prev remains
In = 2.893)
Direct observations
(n = 217)
Video analysis
l« = 155)
Introduced
Avian
50
52
54
Mammalian
3
12
4
Totals
53
64
58
Native
Avian
47
35
42
Mammalian
0
I
0
Totals
47
36
42
dove species and introduced species had little role
in the diet (7.3% frequency, 4.6% biomass)
Bielcfeldt el al. (1992) found Eastern chipmunks
(Tarnias striatus) contributed a majority of the
biomass at a semi-urban nest near a rural town in
Wisconsin and the Eastern chipmunk is a common
prey item of breeding Cooper’s Hawks in and
around the city of Stevens Point. Wisconsin
(Nicewander and Rosenfield 2006; RNR, unpuhl.
data). We found local variation within our study
population; only Cooper's Hawks nesting on the
Univeisity of Victoria campus preyed upon
European rabbits in addition to the avian prey
commonly taken at nests elsewhere in the study
area. The variation in diet among populations and
opportunistic use of locally abundant prey within
Victoria underscores the plasticity of Cooper’s
TABLE 4. Percent biomass of introduced and native
prey items by two sampling schemes at Cooper’s Hawk
nests in Victoria. British Columbia. 1995-2010 Total
biomass in grams is provided below sample scheme
headings.
% Biomass
Direct observations'
allincte( 7%), but no evidence of
the disease (or deaths) in nestling urban Cooper's
Hawks in Grand Forks, North Dakota. However,
sampling there in 201 I found -30% prevalence
of T. gal/inae (/? = 70 hawks at 13 nests), but no
documented deaths of nestlings due to trichomo¬
niasis (T. G. Driscoll, unpubl. data). Both the
Victoria and Grand Forks populations exhibit
some of the highest nesting densities and
production indices recorded for Cooper's Hawks
in North America (Rosenfield et ai. 2007a).
although the Grand Forks population could
potentially be affected by trichomoniasis in future
years (- 14% of the diet of Cooper's Hawks in
Grand Forks is columbid prev: T. G. Driscoll,
unpubl. data).
Bielcfeldt et al. ( 1992) challenged the assump¬
tion that birds were the most frequent prey of
Cooper’s Hawks as reported in pre- 1990 studies
°* '*1e biology of this species. They indicated
mammals provided a majority of biomass in some
studies and argued that previous studies could
iave overestimated avian prey in the diet due to
Cava et al. • DIET OF URBAN BREEDING COOPER’S HAWKS
779
TABLE 5. Prey species constituting frequency in any of three sampling schemes al Cooper s Hawk nests in
Victoria, British Columbia, 1995-2010. Total sample size of items identified to species is provided below sampling
scheme headings.
Prey species
Prey remains
In = 2.8%)
% Frequency
Direct observations
«t = 217)
Video analysis
(;t = 155)
.American Robin
Turdus migratorius
34.6
29.5
40.0
European Starling
Sluntus vulgaris
28.3
15.2
18.7
House Sparrow
Passer domesticus
18.8
31.8
34.8
0
Varied Thrush
Ixoreus naevius
1.1
0.5
Pine Siskin
Spinas pinus
0.9
0.5
0
Spotted Towhee
Pipila mandat us
1.0
0.5
0
House Finch
Carpodacus mexicanus
5.6
2.8
0
1 *2
Northwestern Crow
Carvus caurinus
0.4
0
1 .3
Chestnut-backed Chickadee
Poecile rufescens
0.7
0.5
0.6
Rock Pigeon
Columba livia
1.8
4.1
0
Northern Flicker
Colaptes auratus
0.6
0
0
Gra\ squirrel
Sciurus carolinensis
0.3
0.5
0
1 3
Black rat
Ratrus rattus
0
0.9
1.3
Norway rat
R. norvegicus
1.3
5.1
2.6
Eastern cottontail
Sylvilagus floridanus
0.8
1 .4
0
Deer mouse
Peromyscus maniculatus
0.1
0.5
0
European rabbi 1
Oryctolagus funiculus
0.6
4.1
0
methodological biases. Our samples of prey
remains, direct observations, and nest video each
show that avian species arc the most frequent
items and provide the majority of biomass in the
diet of Cooper’s Hawks in Victoria.
Other recent urban and rural studies have also
shown birds are the most frequent prey (Estes and
Mannan 2003: Roth and Lima 2003, 2006) and
provide the majority of biomass (Estes and
Mannan 2003), and it is likely that birds are also
important prey in other cities. The lack of
mammalian and other Mow agility' prey may be
due to reduced abundance or availability of such
prey in the areas at the time of those studies.
Hawks nesting on the University of Victoria
campus preyed upon European rabbits that were
present in large numbers (about IK-20 rabbits/ha
in non-forested habitats), yet elsewhere in the city
mammals were recorded infrequently. Bielefeldt
el al’s (1992) suggestion that much of the
breeding Cooper’s Hawk diet consists of vulner¬
able. inexperienced, and ground-foraging individ¬
uals is supported by our results. The three most
common avian species taken in Victoria (Amer¬
ican Robin, House Sparrow', and European
Starling) would be classified as frequent or
primarily ground-foraging species by Bielefeldt
et al. (1992), and inexperienced young ot the year
were the most commonly recorded prey when
they become available in the season. Cooper s
Hawks seem to be opportunistic predators but it is
unknown whether they target vulnerable prey or
that prevalence of these items in our samples was
due to higher attack success rates.
Roth and Lima (2003) reported introduced bird
species, especially European Starlings and Rock
Pigeons ( Columba livia), were important prey of
seven female and one male radio marked
Cooper’s Hawks wintering in Terre Haute.
Indiana. They indicated small birds (< 70 g) such
as House Sparrows were rarely attacked despite
being numerous in their urban study area; smaller
bird species in their study area were at low risk ot
predation from Cooper’s Hawks. Il is possible that
differences in size class used by Cooper’s Hawks
between our study and others may reflect disparity
in size of hawks and prey used. Breeding males
captured most of the prey documented in our
study, and males often take smaller prey than
females (Rosenfield and Bielefeldt 1993). It is
also possible that smaller, sparrow-sized birds
have a greater risk of predation from smaller
Cooper's Hawks in the western half of this hawk's
North American distribution. Smaller body size of
breeding Cooper’s Hawks in some western
populations (including in Victoria) appears to be
influenced by selective pressures ol size and
agility of their relatively small avian prey
780
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 4. December 2012
P rey remains
n
n
...
16-30 1-15
Jun Jul
(301) (319)
15-31
Jul
(257)
1-15
Aug
(75)
(B)
1
«. 0.9
B
^ 0.8
Direct observations
m
nn
3 0.7
CO
£ 0.6
J 0.5
o 0.4
J 0.3
I °’2
£ 0.1
"ssSaWlflfs
® Adult mammal I Subadult mamma. ■ Adult bW □ Avian young of the year
British Columbia by prey rem^n"'(A) an^d i rL'c-,.‘ ohs J r v' 1 J '' r’ 1 995-201 0 at CooPer s Hawk nests in Victor
penod is in parentheses. Prc-incubation. incubation nestlin,. ... i n , c1.number ot 'dcntifiable items recorded in each tit
to late- May, late-May to late-Junc, and July to August respectively § S,ageS OCCUr in March to early-April. mid-Ap
(Rosenfield et al. 2010, Sonsthagen et al. 2012).
Larger and less agile prey are taken by Cooper’s
Hawks in some eastern populations where Coo¬
per s Hawks are larger (Rosenfield et al ^OIO)
Roth and Lima's (2003) data mostly (141 of 179
attacks) were observations of wintering female
hawks in an eastern population. Wintering male
and female Cooper's Hawks capture House
Sparrows in Victoria, but males do so more than
females (ACS, unpubl. data)
Ours is the firs, study , o' describe introduced
species as a major component of the diet of urban
breeding ( ooper s Hawks. Introduced species are
noun (or causing damage to native ecosystems
and species (e.g.. Mack et aJ. 2000, Chace and
a sh 2006), but they can provide potential
benefits to ecosystems (Schlaepfer et al. 20111.
he mttoduced bird species in our study area are a
benefit as they provide a valuable resource for
native, breeding Cooper’s Hawks in Victoria,
ntroduced bird species, particularly House Spar-
tows and European Starlings, are predominant
?QOsI,na 'n many cUies (c*8” Marzlu,Y el aL
). and it appears these species are important
Cava et al. • DIET OF URBAN BREEDING COOPER'S HAWKS
781
prey for many nesting populations of urban
Cooper's Hawks. House Sparrows and starlings
are common prey of Cooper’s Hawks breeding in
Milwaukee. Wisconsin (W. E. Stout and RNR.
unpubl. data), and Grand Forks. North Dakota (T.
G. Driscoll, unpubl. data). House Sparrows are
also common prey of breeding Cooper's Hawks in
Albuquerque. New Mexico (European Starlings
are mostly absent from Albuquerque; B. A.
Millsap and R. K. Murphy, unpubl. data).
Apparent widespread use of House Sparrows
and European Starlings in association with
generally higher densities of birds in cities could
in part be responsible for urban Cooper’s Hawks
(including the Victoria Cooper’s Hawk popula¬
tion) attaining some of the highest nesting
densities and reproductive success known for this
raptor tRosenfield et al. 1996; Marzluff cl al.
1998: Rosenfield et al. 2007a: ACS, unpubl. data).
There is evidence that some cities serve as
population sources for Cooper's Hawks and prey
availability has been suggested as having a key
role in this demographic progress (Mannan ct al.
2008, Stout and Rosenfield 2010).
ACKNOWLEDGMENTS
We thank Phil Barker. Suzanne Benuchcsne. Eileen and
Tesa Campbell. Jason Clark, Bryan Gates. David Gaunt.
Laura Gret/.i tiger, Robert Hagel, David Hill. Neil Horne,
Ignocz. Kadar, Manami Kaktl. Paul I.eBlanc. Brian Low,
William Muekic, Lance Regan, Marie O'Sliadghnessy,
Mari Smuby-Stone. Boh Chappell. Bret Ferguson. Darren
and Gini MeKellar, Brad, Laura, and Irene Stewart. Audrey
Wellburn. George Whitman, and others for project
assistance. Michael MeNall provided access to the
vertebrate reference collection at the Royal British
Columbia Museum. Funding and logistical support was
provided by the British Columbia Ministry of Environment.
Habitat Conservation Trust Fund. Public Conservation
Assistance Fund. Saanich Parks Department, British
Columbia Hydro. James L. Baillie Memorial Fund. Shaw
Cablesystcms, Pacific Forestry Centre, and Victoria Natural
History Society. Financial support for RNR's participation
came primarily from the Personnel Development Commit¬
tee. Letters and Science Foundation, and the Department ol
Biology at the University of Wisconsin-Stcveas Point.
Financial support for JAC came from the Honors Internship
Program at the University of Wisconsin-Stevens Point We
thank C. E. Braun. R. W. Mannan, and an anonymous
reviewer for suggestions that improved this manuscript.
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Short Communications
The Wilson Journal of Ornithology 124(4):783~787. 2012
Protocalliphora (Diptera: Calliphoridae) Infestations of Nestling
Red-shouldered Hawks in Southern Ohio
Cheryl R. Dykstra,15 Jeffrey L. Hays,2 Melinda M. Simon,3 and Ann R. Wegman4
ABSTRACT.— We examined nestling Red-shoul¬
dered Hawks {Buteo lineutus ) in 56 nests ( 1 47 nestlings)
in suburban southwestern Ohio and in 25 nests (67
nestlings) in rural forested Hocking Hills in south¬
central Ohio. — 1 80 km east of southwestern Ohio.
Fifteen of 25 nests in Hocking Hills had Protocalli¬
phora avium larvae on one or mote nestlings and/or
pupae in the nest material. Nineteen nestlings had larvae
in one or both ears, an additional 14 had evidence of
larvae outside the ears, 32 were not visibly parasitized,
and iwo were not examined or their status was not
reported; in contrast, no nests and no nestlings were
parasitized in southwestern Ohio. Reproductive rate
(voting fledged/nest) did not differ between southwest¬
ern Ohio and Hocking Hills <2.4 t 0 I young/nest at
southwestern Ohio vs. 2.7 ± 0.2 at Hocking Hills; P -
0.214). Parasitized nests at Hocking Hills were no more
likely to have been used in ihe prev ions breeding season
than non-parasitized nests (x = 0.903. I' 0.342. n
22). Similarly, number o! young fledged/nest at
parasitized nests did not differ from that at non-
parasitized nests within Hocking Hills ( V 75.0. P
= 1.00. n = 25: mean (± SE) number of young 2,7
- 0.3 vs. 2.7 ± 0.3 at parasitized and non-parasitized
nests, respectively). The Protocalliphora loads we
observed did not appear to have a negative effect on
the fledging rate of nestling Red-shouldered Hawks:
however, we did not assess any other potential effects of
parasitism. Received 29 I'chntarv 2012. Accepted 29
May 2012.
Many raptor species are infested by one or more
species of ectoparasitic Protocalliphora Hies (Dip¬
tera: Calliphoridae), commonly called bird blow
flies (Sabrosky et al. 1989. Bennett and Whitworth
1992). Adults of these Diptera lay their eggs on
nestlings, typically when the nestlings are young
(Tirell 1978, Sabrosky et al. 1989). The fly eggs
hatch within 24-48 hrs and larval Protocalliphora
Raptor Environmental. 7280 Susan Springs Drive, West
Chester. OH 45069, USA.
RAPTOR Inc.. 1419 Holmanview . Wyoming. OH 45215,
USA.
9016 Winthrop, Cincinnati. OH 45249, USA.
‘Cincinnati Museum of Natural History. 1301 Western
Avenue, Cincinnati, OH 45203, USA.
Corresponding author; e-mail: cheryldykstra@juno.com
feed on nestling blood until they mature, when they
drop from the nestlings into the nest material and
pupate (Sabrosky et al. 1989). The larvae are
typically found in nestling ear canals, nares.
axillary area, and feather sheaths in raptors (Tirrell
1978. Sabrosky et al. 1989, Philips 2007) and also
in the nesting material (Sabrosky et al. 1989).
The effect of Protocalliphora on raptor nestling
health and survival differs among species and
studies. Researchers hav e blamed Protocalliphora
for impaired development, weakness, and death in
some eases (Philips 2007): heavily infested Red¬
tailed Hawk ( Buteo jamaicensis) nestlings in
North Dakota were smaller and weaker than their
siblings and died as a result of siblicide; one of
these nestlings had 213 larvae in multiple
locations (Tirrell 1978). Protocalliphora likely
caused the death of 26 nestling Prairie Falcons
(Falco mexiemus) in nine eyries in Utah (White
1963). In contrast, Protocalliphora infestations
apparently hud little effect on nestling Red¬
shouldered Hawks {B. Uneatus) in Wisconsin (King
et til. 2010). Broad-winged Hawks {11 platypterus)
in New York (Crocoll and Parker 1981). Red¬
tailed. Red-shouldered, and Cooper's hawks (Ac-
cipher cooperii) in New York (Sargent 1938), and
Red-tailed Hawks in Montana (Scidensticker and
Reynolds 1971). Typical infestations likely pro¬
duce only minor or no negative effects (Sabrosky
et al. 1989).
Protocalliphora avium occurs in northern and
northeastern North America and has been docu¬
mented in at least 12 species (Sabrosky et al.
1989). P. avium is replaced in western North
America by the closely related P. asiovora
(Sabrosky et al. 1989. Bennett and Whitworth
1992). However, the distribution of P. avium is
not well documented, and its presence and
prevalence on raptor nestlings has been typically,
although not exclusively, reported anecdotally
(Sargent 1938. White 1963, Seidenstickcr and
Reynolds 1971. Bohm 1978).
Our objective was to investigate the presence
and prevalence of Protocalliphora ectoparasites
783
784
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124. No. 4. December 2012
on nestling Red-shouldered Hawks in two regions
of southern Ohio: suburban southwestern Ohio
(SWOH) and rural, forested Hocking Hills (HH)
in south-central Ohio.
METHODS
Study Areas. — The SWOH study area is a hilly,
unglaciated area in the Interior Plateau ecoregion
(Omernik 1987). The hills are dissected by many
small streams in ravines and two large rivers, the
Great Miami River and the Little Miami River.
Native forests are dominated by second-growth
oak ( Quercus spp.)-hickory (Cary a spp.) and
beech ( Fagus gramlifolia)-sugar maple (Acer
saccharin,,) associations with lowland, riparian
forests characterized by sycamores ( Platanus
occidcmtalis) and beech. Elevation ranges from
~140 to 270 m.
I he SWOH study area consisted of Hamilton
County, Clermont County, and southwestern
Warren County. Ohio; the nests studied were in
a wide band of suburban development surround¬
ing the city of Cincinnati, Ohio. Suburban areas
varied from densely-populated (residential lots
20 x 35 m) to sparsely-populated (>2.5-ha
residential lots, as well as undeveloped private
land). Most residences and other buildings were
surrounded by lawns and other non-native vege¬
tation. but residences tended to he on level ground
with native vegetation on steep slopes and in
riparian areas.
Hocking Hills is a hilly, unglaciated region
withm the Western Allegheny Plateau ecoregion
m southeastern Ohio (Omernik 1987), -180 km
east of SWOH. This region contains numerous
small, high-gradient streams, as well as the larger
Hocking River and many mid-size streams
Elevation ranges from -200 t0 3 10 m The
dominant forest type is oak-hickory. Drier sites
include chestnut oak (Quercus minus) and black
oak (Q velutma). and mesie slopes are charac¬
terized by tulip-tree ( Uriodendroit tulipifera).
Plantations of white (Pinas strohus) and red (P
resmosa) pine are also common on public lands
Western portions of this study area also feature
sandstone gorges containing northern microcli¬
mates and habitats, including eastern hemlock
{Tsuga canadensis) and ferns. Lowland forests are
characterized by sycamores, silver maple (Acer
saccharinum), beech, and river birch (Betula
nigra). u
The HH study area consisted of Hocking
County, eastern Vinton County, northern Athens
County, and southern Perry County, including the
Athens District of Wayne National Forest,
Hocking State Forest, Zalcski State Forest, and
associated private lands. Proximity to human
activities varied widely with some areas contain¬
ing residential development, some with recrea¬
tional development such as picnic areas and trails,
and some areas were fairly remote.
Location oj Nests and Measurement of Nest-
/mgs. Red-shouldered Hawk nest locations were
previously known to us from an ongoing long¬
term study (Dykstra et al. 2000. 2004. 2009). Wc
visited known nesting areas at least once (but
typically 2-3 limes) between mid-February and
mid-May. 2009-201 1. and viewed nests from the
ground using 8 x or 10 X binoculars or a 20-60
spotting scope. Red-shouldered Hawks do not
always re-occupv the same nest in subsequenl
years, and it was often necessary to search for the
new nest within a nesting area in the following
year. We generally considered that a new nest
0.5 km from a previously active nest was within
Hie same nesting area. A nest 0.5-0.8 km from a
previously active nest was considered to he within
die same nesting area if additional evidence
supported that conclusion (e.g., a bird seen flying
between the original and new nests, a lack of
activity at the original nest in subsequent years, a
temporal progression of new nests moving in that
direction indicating a shift of the nesting area's
oundaries). We visited some nesting areas in
more than I year, but data from only the first year
were included in this study; thus nests in this
study were independent in that each represented a
unique nesting area.
^ e included only nests where young or signs of
young (excreta on ground and branches) were
observed. We climbed to nests containing young
m SWOH and in HH between 7 May and 15 June
“ ) )-_() 1 1 |0 examine and band young when
nestlings were -2-5 weeks of ace.’ We 'banded
nestlings with USGS aluminum bands and
weighed them using a 1.000-g spring scale to
the nearest 5 g. We used a standard 33-cm ruler to
mcasuie the length of the first and second
secondary to the nearest millimeter.
^ e examined the ears of each nestling and
classified their infestation status as: ( I ) no larvae.
G) larvae present within ear or ears, or (3)
'larvae-evidence7 outside of ear or ears, hut no
aiyie observed. 'Larvae-evidence7 was defined
us the presence ol black crusty material below the
ears (excreta from larvae). This material was
SHORT COMMUNICATIONS
785
usually accompanied by enlarged ear openings.
Nests were classified as ‘infested il they
contained at least one nestling with larvae or
larvae-evidence.
Larvae were not counted but. in some cases,
samples were removed from ears for identification
of the parasite. We also examined the decaying
nesting material in the bottom of the nest at one
nest in 2010 and six nests in 201 1 in an effort to
find pupal forms of the ectoparasite; the remain¬
ing nests were not examined due to time
constraints. Presence or absence ot pupae in the
nest material was recorded and pupae were
collected. Larvae and pupae were stored with a
small amount of sawdust in plastic zipper hags
and shipped to T. L. Whitworth of Washington
State University, Pullman, for identification.
Larvae and some pupae were raised until adult
Hies hatched; adult flies were identified by T. L.
Whitworth based on (Sabrosky et al. 1989); pupae
were identified based on a key to the puparia ol
Norih American Protocalliphora (Whitworth
2003).
Estimation of Nestling Age and Reproductive
Rate— We estimated nestling age based on first
and second secondary feather lengths, using the
age-feather length regression model lor Red¬
shouldered Hawks of Penak ( I9S2). We averaged
Ihe estimated ages of the nestlings in each nest to
create a mean nest-age. as nestling age may allect
the visibility and location of parasite larvae/pupae
(Sabrosky el al. 1989, Bennett and Whitworth
1991).
Nestlings were counted as Hedged il they were
at least 3 weeks of age. At sites where nestlings
were <3 weeks of age at handing, we viewed the
nest front the ground when nestlings were well-
grown (4.5—6 wks) and counted nestlings using a
spotting scope. Reproductive rate was defined as
the total number of Hedged young/number ol
nests examined.
Nest Re-use. — Some studies suggest nest re-use
can affect some parasite infestation rates (Bennett
and Whitworth 1992, Rendell and Verbeek 1996),
and we recorded whether each nest had been used
>n the previous breeding season. We used
information from our historical data base for
-909 nests (JLH. unpubl. data).
Statistical Analyses.— We used Kolmogorov-
Smirnov tests to compare infestation rates of nests
in SWOH and HH because data were non-
normally distributed. The nests were considered
ihe unit of measurement, as it was likely that
siblings’ infestation status were not independent.
We used a Munn-Whilney U- test to compare the
number of young Hedged per nest at SWOH with
that al HH.
We used a Chi-square test for nests in the
Hocking Hills region to examine whether infes¬
tation status of nests was related to nest use in the
previous breeding season. Nest use in the previous
season was unknown for three nests because these
nesting areas were first found by us in the year
that we studied Protocol I iphora infestation there,
these nests were excluded from this test. We used
Mann-Whitney U- tests to compare mean nestling
age and the number of young fledged per nest at
infested nests with that at nests that were not
infested.
RESULTS
We examined nestlings in 56 independent nests
(147 nestlings) at SWOH and 25 independent
nests (67 nestlings) at HH. Fifteen of 25 nests at
Hocking Hills were infested with Protocalliphora
avium. Nineteen nestlings were infested with
larvae in one or both ears, an additional 14 had
evidence of larvae. 32 were not visibly infested,
and two were either not examined or their status
was inadvertently not reported on the data sheets.
No nests and no nestlings were infested at SWOH.
which differed significantly from infestation rate
of 1-111 nests (P < 0.001 ). Reproductive rate (mean
± SE; young fledged/nest) did not differ between
SWOH and Hocking Hills (2.4 ± 0.1 young/nest
at SWOH vs. 2.7 ± 0.2 al HH; U = 813.0, P -
0.214. n = 56 and n = 25).
We checked nesting material for pupae at seven
nests at Hocking Hills. Pupae were found in five
nests, all of which also had nestlings with larvae
or larvae-evidence; the other two nests had neithei
pupae in nesting material nor larvae in the
nestlings’ ears.
Infested nests at HH were no more likely to
have been used in the previous breeding season
than non-infested nests (Pearson’s y = 0.903, P
= 0.342, n = 22). Mean nestling age at infested
nests did not differ from that at nests that were not
infested (U = 101.50. P = 0.140. n = 25: mean ±
SE nestling age = 22 ± I days vs. 24 ± 1 days at
infested and non-infested nests, respectively). The
number of young fledged/nest at infested nests did
not differ from non-infested nests ( U = 75.0. P =
1.00. n = 25: mean ± SE number of young = 2.7
± 0.3 vs. 2.7 ± 0.3 at infested and non-infested
nests, respectively).
786
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124. No. 4. December 2012
DISCUSSION
Red-shouldered Hawk nestlings in southern Ohio
appeared to he unharmed by infestations of Proto-
cutliphora avium. We did not count the larvae found
in ear canals, but we did not observe >10 in any
nestling’s ear (ARW, unpubl. data). Infestations
were apparently less intense than those reported by
Tirrell (1978) and White (1963), in which larvae
were found in multiple locations on the nestlings anti
nestling mortality occurred. The reproductive rate (in
terms ot young fledged per nest) did not differ
between infested and non-infested nests at HH and
did not differ from the reproductive rate at SWOH.
Sixty percent of Red-shouldered Hawk nests at
HH in south-central Ohio contained the blow fly
P. avium, but nests in SWOH. -180 km west,
were entirely free of this ectoparasite. This
difference was not an artifact of the study sample
size, as we have not observed P. avium at SWOH
and we have consistently found -50% of nests
parasitized at HH in out 15-year study of Red¬
shouldered Hawks nesting in both study areas
(CRD and JLH. unpubl. data).
One possible explanation for the presence of P
avium at HH but no. SWOH is that the suburban
landscape is somehow unsuitable for P. avium It
is not uncommon for Protocol liphora to be absent
from some areas, particularly where the host
population is relatively recently established or the
environment is unstable (T. L. Whitworth, pen.
comm.). Some parasite species are less abundant
in urban areas (Marcogliese 2005) and some
researchers suggest parasite communities may be
appropriate indicators of environmental health
(Lafferty 1997; Marcogliese 2004. 2005) How¬
ever. urbanization may affect parasite populations
and communities in diverse ways. Urban song-
birds had fewer Protocol liphora (>. sialia: Moore
). fewer ticks (Ixodes; Gregoire et al. 2002
Evans et al 2009, and fewer blood parasites'
(Fok'd's e' 2°08). Prevalence of one Dipteran
ectoparasite (Phil,, mi, /u.ru-ri, on Northern
Mockingbirds polygbnos) was not di-
etCI y ?om P° Urbanization in Rorida 7^' “ Polluticn: for
example, Fln|and, P. aiurea larva(. werc ,
complex r te “i"0* T"inss closer >° •' ^lory
complex releasing sulfuric oxides and heavy
metals into the atmosphere fEeva el al 19941 X
Another possible explanation for ,he absence of
p. avmm at the SWOH study area is that it may be
outside of P. avium’s distributional range, while
HH is within it. The genus Protocalliphora is
considered ’predominantly northern* (Sabroskv
et al. 1989) or ‘mainly boreal' ( Bennett and Whit¬
worth 1991 ) and the range of P. avium extends from
Alaska and Yukon Territory to Quebec and
( onnecticut and south to Pennsylvania and Nebraska
(Sabrosky et al. 1989). Reports of this species within
the United Slates are from New York (Sargent 1938.
Crocoll and Parker 1981). Minnesota (Bohm 1978).
Wisconsin (King et al. 2010). Michigan (Hamer-
strom and Hamerstrom 1954). and as far south as
Pennsylvania, northern Iowa, and northern Illinois
(Sabrosky et al. 1989). Our report of P. avium in
south-central Ohio is apparently the southernmost
report ol this species to date. However, published
reports on the presence of (his species are scattered
and mostly anecdotal and may not represent the full
distribution range. 1 locking Hills, particularly the
western pan ol our study area, includes gorges
containing northern microclimates and habitats, and
is connected by a corridor of semi -wooded habitat to
northeastern Ohio and western Pennsylvania. SWOH
is in the Interior Plateau ecorcgion and is bordered on
the north by Hat. primarily agricultural lands with
lew forests. Thus, it is possible SWOH is effectively
isolated from northern species. Red-shouldered
Hawks are not present or have an extremely limited
distribution in the counties north of SWOH. although
other hosts of P. avium. Red-tailed Hawks. Cooper's
Hawks, and Great Homed Owls (Bubo Virginians),
are present in those regions (Pcteijohn 2001).
Il HH in south-central Ohio is at the edge of
the lange ol P. avium . we might expect lighter
infestations and/or a lower proportion of nests
in ested. compared to more northern regions. We
lound 60% of nests infested with P. avium but.
in northern Wisconsin, 91% of Red-shouldered
Hawk nests were infested (King et al. 2010), and
m cent ral New York, nearly 100% of nests of both
e -tailed and Red-shouldered hawks were in¬
fested (Sargent 1938). We note it is possible that
we underestimated the prevalence of P. avium, as
we did not examine the nesting material at all
nests, and we did not examine areas of the
nestlings other than the ears; had we done so. we
may have found more nests infested.
We do not know the reason for the difference in
i ow fly abundance between our two study sites,
and hope this paper will encourage researchers to
examine the distribution of ectoparasites such as P.
tn """ anc* ,*le'r relationships to their raptor hosts
and to the environment. Additional information on
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787
the effects of urbanization on avian parasites may
identify mechanisms by which urbanization affects
survival and demographics of some raptor species.
ACKNOWLEDGMENTS
We thank Sara Johnson Miller and Sandra Stone for
assistance with fieldwork, and T. L. Whitworth and Greg
Dahlcra for assistance with identification of blow flies. We
also thank the many landowners of the Cincinnati and
Hocking Hills regions who allowed us access to their
private property to conduct this research. This work was
supported by grants from RAPTOR Inc. and Marilyn Arn.
T. L. Whitworth and two anonymous referees kindly
reviewed an earlier version of this manuscript.
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The Wilson Journal of Ornithology I24(4):788-792. 2012
Hematocrit Does Not Indicate Condition in Nestling or Adult
European Starlings
Kayley D. Smith1 and Colleen A. Barber1 2
ABSTRACT. Hematocrit, the percentage of packed
red blond cells in blood, has been used as a measure of
avian condition. We investigated the relationship
between hematocrit and condition in a wild, breeding
population of adult European Starlings (Sturnus vul
Xcms). and their nestlings (at 5- and 1 1 -days post hatch),
Hemal writ was not correlated with condition in adults
or nestlings at either 5- or 1 1 -days post-hatch. Adult
males and females had similar hematocrit values
Hematocrit increased with age; adults had significantly
higher hematocrit than both 5- and I I day old nestlings
and 11-day old nestlings had significantly higher
hematocrit than when they were 5 days of a«e
Hematocrit was not correlated with sampling date
ambient temperature, or relative humidity level, but was
positively conelated with sampling time in the day for
nestlings (but no. adults). Our findings caution against
usmg hematocrit as a measure of condition in birds
Rice,ved 30 November 20/1. Accepted 23 June 20/2.
Hematocrit, the percentage of packed red blood
cells m blood, characterizes the ability of blood to
carry oxygen; increased hematocrit (within the
normal range) results directly in increased oxygen
carrying capacity (Birchard 1997), and has been
positively correlated with energy expenditure
(Viscor et al. 1985, Saino et al. 1997). Using
ematocrit to assess avian condition would be
advantageous as blood is easy to sample (Cuervo
et al. 2011). and the procedure is inexpensive
Several studies of birds have found a positive
correlation between hematocrit and condition
(when within normal range) (e.g.. Merila and
Svensson 1995, Piersma et al. 2000). Others
bZT’ '!ave fOUnd n° associat,°n (C.g., Dawson'
and Bortolotti 1997. Amat et al. 2009), or have
2007) e011)
wVVoSnT (negalivdy: RichneTet al.’
793 positively e.g., Dawson and Bortolotti
l"7 ' reV,ewed ** e, al. 2007). and
’ Department of Biology. Saint Mary’s University
Rob,e tree,. Halifax NS B3H 3C3, Canada ’ ‘ ^
Corresponding author; e-mail: colleen.barber@smu.ca
dominance (e.g.. van Oort et al. 2007). all of
which relate to condition.
VVe investigated whether there was a relation¬
ship between hematocrit and condition in a wild
population of nest box-breeding adult (male and
female) and nestling (young vs. older) European
Starlings (Sturnus vulgaris). This species is a
facultatively polygynous passerine breeding in
cavities; they typically have two broods a year
(Kessell 1957). Both males and females incubate
the eggs and provision the offspring (Feare 1984).
Nestlings fledge when they are between 21 and
23 days of age post-hatch (Cabe 1993). Our
second objective was to examine if hematocrit
dil leied between mule and female breeding adults
and il it increased with age (nestlings vs. adults,
and nestlings when 5 days of age vs. when 1 1 days
ot age). The potential effects of sampling dale and
linte o| day, ambient temperature, and relative
humidity on hematocrit were also investigated.
METHODS
We studied a nest-box breeding population of
European Starlings on the campus of Saint Mary's
University in Halifax, Nova Scotia. Canada (44
.1 54.07" N. 63 34' 47.09" W) from May to July
■ ^a’rs are double-brooded, but do not
generally remain together for both broods: we
, L felon, termed the first broods ‘early’ and
second broods ‘later’. We checked nests daily
unti egg-luyjng, then monitored nests every 3 days
until 3 days prior to the estimated time of hatch:
we then checked nests daily through day 15 of the
neM ing period (checking nests after this time can
result m premature fledging).
We caught adults using a nest-box trap when
nestlings were 5 days of age. All adults and
nestlings were banded with a Canadian Wildlife
Service band and three color bands for Individual
identification. This study complied with CCAC
guidelines and was approved by the Animal Care
Committee at Saint Mary’s University (protocol #
07). We took morphological measurements
mass to the nearest 0.5 g with a Pesola spring
SHORT COMMUNICATIONS
789
scale, and tarsus length to the nearest 0.01 mm
with digital calipers) of adults and nestlings (when
they were 5- and 11 -days of age). However, we
only sampled 16 individuals at II -days of age,
and all came from later broods. We had
hematocrit data for 12 of these nestlings (6
broods) at both 5- and 1 1 -days of age. We also
collected a blood sample (25- 100 ul) between
0900 and 1800 hrs from the brachial vein in adults
and the metatarsal vein in nestlings in a 50-ul
heparinized microcapillary tube. These samples
were kept cool at 4 C until processing, 2 to 4 hrs
later. Blood in microcapillary tubes was spun in
a centrifuge (Sero-fuge, Model # 0591. Clay
Adams. Parsippany. NJ, USA) at 8.000 rpm lor
6 min. Two different measurements of hematocrit
percentages were taken to compare with total
blood volume. The first method involved mea¬
suring the length of the hematocrit and the total
length of the blood (hematocrit and plasma) with a
ruler to the nearest 1.0 mm to ascertain the
percentage of hematocrit (Cuervo ct al. 2007), and
the other used the standardized percentages
written on the centrifuge. The results for these
two methods were highly correlated \ = 0.91. ii
= 124, P < 0.0001), and were averaged to
calculate the percentage of hematocrit in the
blood. This average was compared to another
index of condition (residuals of mass vs, average
tarsus length) in adult males and females, and
nestlings. Residuals were calculated through
regressing mass on average tarsus length ol all
individuals captured in 201 1 (regardless ol
whether we had hematocrit data for them).
Regressions were calculated separately lor adult
males and females; males tended to have larger
tarsi than females (mean ± SE = 34.81 ± 0.22
vs. 34.32 ± 0.19. respectively; unpaired / =
1.707, df = 39. P = 0.10), and also tended to
weigh more than females (84.26 ± 1.19 vs. 81.44
~ 1.01 g, respectively: unpaired / = 1.804. dt =
39. P = 0.08). Residuals were similarly calculated
for nestlings with a different regression for day
5 and day 1 1 nestlings. We calculated mean
hematocrit and mean condition per brood lor the
5- and 11 -day old nestlings to avoid pseudorep¬
lication in the correlation analyses. Mean hemat¬
ocrit and mean condition per brood were calcu¬
lated using only those nestlings lor which we had
both hematocrit and condition scores.
Ambient temperature ( C) and relative humid¬
ity (%) data were obtained from the web site for
Environment Canada’s meteorological station at
the Halifax Stanfield International Airport (44
53' 00.000" N. 63 31 ' 00.000" W). Nova Scotia,
35 km from our study site. Both ambient
temperature and relative humidity are reported
on an hourly basis; we took these data at the time
when blood was collected, rounding up or down to
the nearest hour. Two adults were omitted from
this analysis as (heir capture times had not been
recorded.
Data were tested for normality with a D'Agos¬
tino and Pearson omnibus normality test. We used
Pearson correlations when both variables were
normally distributed, and Spearman rank correla¬
tions when al least one variable had a non-normal
distribution, to examine potential relationships
between hematocrit and ( I ) condition, and (2)
factors such as ambient temperature. We ran a
linear-mixed effects model with age/sex as a fixed
effect and subject as a random effect to test if
differences in hematocrit existed between: (1)
male and female adults. (2) 5-day old nestlings
from early and later broods, (3) adults and 5-day
old nestlings. (4) adults and 11-day old nestlings,
and (5) nestlings at 5 days of age compared to
when they were 1 1 days ol age (only 6 later
broods were sampled at both 5- and 11 -days ol
age). We included subject as a random effect, as a
subset of the later brood nestlings (// =12) was
measured on both days' 5 and 11. We used a
Tukey USD test to identify the location of the
differences. Data were analyzed using GraphPad
Prism Version 5.04 (GraphPad Software. San
Diego. CA. USA) and JMP Version 10 (SAS
Institute. Cary. NC. USA). All tests were two-
tailed. Results were considered significant when P
< 0.05.
RESULTS
The mass versus tarsus regression equation for
adult males was y = 3.585x-40.54 while for adult
females it was y = 3.152x-26.73. For 5-day old
nestlings, it was y = 2.9l7x-31.67 while tor 11-
day old nestlings it was y = 5.565x-l 16.2. The
slope was significantly greater than zero in all
cases (males: F = 1 1.28. dl = 1. 15, P = 0.0043;
females: F = 1 1.98, df = 1. 22. P = 0.0022; 5-
day old nestlings: F = 1114. dl = 1, 122, P <
0.0001; 1 1-dav old nestlings: F = 204.9. df = 1.
103. P < 0.0001 ).
Hematocrit was not correlated with condition in
adult males (r, = 0.25, n = 15, P = 0.37) or adult
females (r = —0.0997, n — 17, P = 0.70). Simi¬
larly, mean hematocrit/brood was not correlated
790
THE WILSON JOURNAL OF ORNITHOLOGY . Vol 124. No. 4. December 2012
TABLE 1 Mean hematocrit (%) (SE). range, and sample size (/,) for European Starlings of different sexes and ages.
Breeding males
Breeding females
5-dav old nestlings (early brood)
5-day old nestlings (later brood)
1 1 -day old nestlings
Brood means: 5-day old (early)
Brood means: 5-day old (later)
Brood means: 1 1 -day old
Mean ± SE
52.76 ± 1.58
52.37 ± 1.62
37.03 ± 0.86
33.64 ± 1.37
43.06 ± 0.73
36.44 ± 1. 16
34.30 ± 1.48
42.78 ± 1.31
Low
39. 1 7
42.24
23.00
24.45
38.53
25.20
28.80
38.53
High
59.92
69.63
56.15
48.19
48.59
47.55
43.89
47.88
15
17
51
24
16
17
9
6
with mean brood condition for 5-day old nestlings
(/• = -0. 152, n = 26 broods, P = 0.46) or 1 1 -dav
old nestlings (rs = -0.143, n = 6 broods, P =
0.80). although sample size was small for the
latter.
We found significant variation in hematocrit
among adults, 5- and 1 1 -day old nestlings (r =
0.63; P < 0.0001 ); fixed effect tests indicated that
hematocrit was significantly related to age/sex
(/r4, 90.16 ^ 43.96, P < 0.0001). Individual
explained 3.0% of the variation in hematocrit.
There was, however, no significant difference in
the hematocrit levels of adult males and females
(Table 1). AdulLs (both male and female) had
significantly higher hematocrit levels than 5- and
ll-dav old nestlings, while 11-day old nestlings
(from later broods) had intermediate hematocrit
levels that were significantly higher than 5-day
old nestlings from early and later broods.
Hematocrit was not significantly correlated
with Julian date (sampling date) for adults (r
- -0.129. „ = 32, P = 0.48) or 11-day old
nestlings (rv - 0. 1 77. n = 6 broods, /J = 0 71 )
However, mean hematocrit/brood tended to be
negatively correlated with Julian date for 5-day
old nestlings (r, = -0.341, „ = 26 broods P ~
0.09). Hematocrit was not correlated with
ambient temperature (adults; rv = -0.093, „ =
30, P = 0.62: 5-day old nestlings: rx = 0.032. n
- 26, P — 0.88; 1 1-day old nestlings; rv = 0.177
-= °'7I)’ °r reIative humidity (adults; r
- -0.096, « = 30, P = 0.61; 5-day old
nestlings: r = -0.180. it = 26, P = 0 38- 1 |-
day old nestlings: rs = 0.177, „ = 6. P = [)j\)
Hematocrit was also not correlated with sampling
time of day tor adults (/• = 0.117, n = 30 p =
0-54) or 1 1-day old nestlings (rx = 0.143 n = 6
for°5 d- ^ Th0 80;- bl" Was P°si‘^ correlated
for 5-day old nestlings (/• = 0.407, n = 76 P
0.04; Fig. 1). ’
DISCUSSION
We delected no significant correlation between
hematocrit and condition in adults or nestlings (5-
or II -days of age). We do note, however, that
sample size was small for broods of 1 1 -day old
nestlings. Our results agree with previous studies
where no association was found between hemat¬
ocrit and condition (e.g., Dawson and Bortolotti
1997, Aniat et al. 2009). Other studies have found
(hat supplemental ly- fed birds had higher hemat-
oeiits than non-fed birds (e.g., Merino and Potti
1998; but see Cuervo et al. 2011), or that
nun itionally-stressed birds had lower hematocrit
lhan non-stressed birds (e.g., Piersma et al. 2UU0).
( uervo et al. (201 1) in their study of the closely
tclated Spotless Starling ( Stunms unicolor) found
hematocrit was positively correlated with condi-
1,0,1 rinass controlled for body size) in a control
group ol nestlings. This relationship became non¬
significant when nestlings were provided with
supplemental feedings, but there was no signifi¬
cant reduction in the variation of nestling
condition. Cuervo et al. (2011) concluded that
■t£
50
40
30-1
20H
10i
10
— i —
12
14
16
18 20
Time of Day
fig. I. Mean hematocrit versus time of day when
oo was sampled for 5-day old ncstlina European
Starlings (/• = 0.407, n = 26 broods. P = 0.04).
SHORT COMMUNICATIONS
791
hematocrit varies across different nutritional
regimes. Hematocrit is clearly not a reliable
measure of condition in all avian species.
Breeding adult male and female European
Starlings did not differ in their hematocrit. Fair
dal. (2007) reviewed the published literature, and
found no differences in hematocrit between males
and females in 36 avian species. Some studies
reported males having significantly higher hemal
ocrit than females (e g.. American Robins | Turclus
migraiorius], Carey and Morton 1976: Brown¬
headed Cowbirds [ Molothrus clier\. Keys et al.
1986), while others found females had higher
hematocrit than males (e.g.. Great Tits \ Pants
major], Ots et al. 1998).
Hematocrit of European Starlings increased
significantly with age: breeding adults had
significantly higher hematocrit than 5- and 1 1 -
day old nestlings, and I I -day old nestlings had
significantly higher hematocrit than 5-day old
nestlings. These findings likely reflect the in¬
creased muscular activity and demand for oxygen
(Saino et al. 1997), and the increased production
of red blood cells (Campbell 1994) that occurs
with age. Hematocrit is also positively correlated
with energy expenditure (Viscor cl al. 1985. Saino
el al. 1997). Five-day old European Starling
nestlings are unable to thermoregulate, while I I
day old nestlings are almost 100% sell sullicient
at thennoregulation (Feare 1984). Older nestlings
expend more energy than younger nestlings
through thermoregulation and increased activity.
Older nestling Eurasian Tree Sparrows (Passer
muntanus ) had higher hematocrit than younger
nestlings (Kostelecka-Myrcha et al. 1997). He¬
matocrit also increased with age in Chinstrap
Penguins ( Pxgoscelis anlarclinis)', adults had
higher hematocrit than juveniles which had higher
hematocrit than nestlings (Merino and Barbosa
1997). Fair et al. (2007) reported published
studies found either an increase in hematocrit
w'lh age, or no association; no study detected a
decrease in hematocrit with age. Norte et al.
• 2009) found hematocrit increased with age
within adult Great Tils.
Adult and nestling hematocrits were not
correlated with Julian date of sampling, ambient
temperature, or relative humidity in our study.
Christe et al. (2002) found hematocrit of breeding
adult Common House Martins (Delichon urbi-
cum) decreased between first and second broods.
Hematocrit of 5-day old nestlings in our study did
not differ between early and late broods in
accordance with our finding no association
between hematocrit and Julian sampling date.
Dubiec and Ciehon (2001 ), however, found Great
Tit nestlings in second broods had lower hemat¬
ocrit than those in first broods, and proposed that
it reflected poorer body condition in second
broods. Williams et al. (2004) reported hematocrit
in breeding adult European Starlings was unaf¬
fected by ambient temperature, which concurs
with our findings. Hematocrit ol 5-day old
nestlings increased with time of day. hut we did
not find this association in adults or older
nestlings. Few studies have examined potential
hematocrit changes throughout the day. Dawson
and Bortolotti ( 1997) reported a negative correla-
lion between hematocrit and time of sampling in
adult American Kestrels (Falco sparverius). They
proposed this decline in hematocrit through the
day might he due to dehydration from fasting
overnight, and then replenishing plasma water
through their diet as the day progressed. Con¬
versely, an increase in hematocrit with time ot day
as seen in our 5-day old European Starling
nestlings might he attributable to either vigorous
begging at this age. resulting in a loss ol plasma
water through evaporation, or that their diet
consists of items that dehydrate them as the day
progresses. Further examination into the relation¬
ship between hematocrit and meteorological
variables is warranted, as we did not take ambient
temperature and relative humidity readings al our
study site, but relied on a weather station 35 km
distant.
Our study supports those that caution against
using hematocrit as an indicator ot condition. Fair
et al. (2007) suggest hematocrit can be uselul
when combined with other indices, but only when
potentially confounding factors such as energy
requirements, season, and disease are considered.
ACKNOWLEDGMENTS
We ihank all those who helped with data collection
including A. M. C. Ouedraogo. M A. W. Hornsby. J. W. G.
Slade. M. E. Lalouf, M. T. McCubbin. and L. K. Zou. This
studv was funded by a Discov ers grant to C. A. Barber from
the Natural Sciences and Engineering Research Council,
and a Dean of Science Research Award to K. D. Smith. J.
R. Foote provided invaluable help with statistical analysis
for which we are grateful. We sincerely appreciate the
insightful comments given by two anonymous reviwers,
and the editorial improvements made by C E. Braun. We
thank Saint Mary's University for logistic support and for
allowing us to conduct this study on campus.
792
THE WILSON JOURNAL OF ORNITHOLOGY • Vo/. 124. No. 4. December 2012
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Keys. G. C, R. C. Fleischer, and S. L. Rothstein. 1986
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.Sheldon. 2009. Variation of udult Great Til Parus
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Piers, via. I .. a. Koolhaas. A. Dekinoa, and E. G winner.
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F Moller. 1997. Experimental manipulation of tail
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Swallows (Hirundo rustica). Oecologia 110:186-190.
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SHORT COMMUNICATIONS
793
The Wilson Journal of Ornithology 1 24(4):793— 797. 2012
Growth Rate and Relocation Movements of Common
Nighthawk ( Chordeiles minor) Nestlings in
Relation to Age
Gunnar R. Kramer1 *-3 and Anna D. Chalfoun1 2
ABSTRACT. — Relocation by dependent young ts a
survival strategy that occurs among a wide range of
laxa. The Common Nighthaw k (Chordeiles minor) lays
its eggs on bare substrate and. once hatched, nestlings
may relocate to new sites daily. We located and
monitored eight Common Nighthawk nests in Grand
Teton National Park. Wyoming, quantified intcr-use-
site distances in relation to nestling age, and calculated
a nestling growth rate curve. Common Nighthawk
nestlings grow in a nearly linear fashion. Nestlings
moved up to 48 m in a single day and larger, older
nestlings tended to move greater distances between
daily use-sites. Received 2 December 2 1)1 1. Accepted 25
hme 2012.
Life history traits, including successful predator
avoidance behaviors by young, which promote
juvenile survival, should increase an organism’s
fitness and be favored by natural selection (Roff
1992). Relocation of dependent offspring to
increase the probability of survival is a tactic that
occurs in a broad range of taxa. However, the
ability of the non-precociul young of most avian
species to change their location is limited,
primarily due to construction of often elaborate,
stationary nests where they are fed and brooded
b\ adults (Collias and Collias 1984. Podulka et al.
2004). Relocation of young birds to limit
predation risk, while reasonable, is poorly docu¬
mented. Moreover, the details of this strategy in
avian species rearing dependent young remain
largely unknown.
Many species of nightjars (Caprimulgidae)
have semi-precocial nestlings hatched from eggs
laid on bare ground ( Holyoak 2001 ) without creat¬
ing any nest structure. Anecdotal observations
suggest Common Nighthawks ( Chordeiles minor)
1 Department of Zoology and Physiology. I niversity of
Wyoming. Laramie. WY 82071, USA.
3 U.S. Geological Survey. Wyoming Cooperative Fish
and Wildlife Research Unit. Department 3166. 1000 East
University Avenue. Laramie. WY 82071. USA.
Corresponding author; e-mail:
gunnarrkramer@gmail.com
move their eggs and coax their pre-fledge. semi-
precocial nestlings to move in response to
disturbance both by potential predators and
rnicrohabitat disturbances such as pooling water
(Pick well and Smith 1938; Fowle 1946: Rust
1947; Sutton and Spencer 1949: Dexter 1952,
1961; Weller 1958; Brigham et al. 2011).
However, factors influencing the distance and
frequency of pre-tledging chick movements are
unclear. We tested the hypothesis that nighthawk
nestlings' movements between daily use-sites
increase with offspring age. We also calculated
a Common Nighthawk nestling growth rate curve
using, for the first time, measurements obtained
from multiple chicks and broods.
METHODS
Study Area and Field Techniques.— Our study
occurred during May-August 2010 within sage¬
brush (Artemisia spp.) Hats in Grand Teton
National Park, northwestern Wyoming. Elevation
ranged from ~ 1,950 to 2.012 m and sites were
dominated by mountain big sagebrush (A. triden-
tata vaseyana). Nighthawk nests were located by
chance during systematic searches for nests ol
shrub and ground-nesling passerines.
Common Nighthawk nests and use-sites were
cheeked daily between 1400 and 2000 hrs MST,
barring inclement weather. We navigated to the
most recent known daily use-site using u handheld
global positioning system (GPS) and attempted to
relocate nestlings by initially searching within a
10-m radius from that point. We returned to the
most recent known use-site if the nestlings were
not relocated during the initial 10-m radius search
and walked four 50 m by 50 m quadrants centered
at the last known use-site, effectively searching an
area of 1 ,000 nr. We repeated the quadrant search
on each of the 2 days following the initial
disappearance of the nestlings and assumed the
nest was no longer active or had moved out ol our
search radius if we were still unable to locate the
brood. We Hushed the brooding female upon
794
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124. No. 4. December 2012
relocating a new daily use-site, and followed I
(usually "15 m) until she ceased her inju
display and left the area so she would not retu
while we handled the nestlings. We marked t
new use-site using a handheld GPS. We paced c
the straight-line distance between sequential us
sites if they were <15 m apart. We used GF
locations to measure the straight-line inter-us,
site distance if the new site was relocated >15
from the previous.
We considered the age of a brood to be the a*
of the first-hatched nestling. Nestling body masse
were obtained during each visit using a portahl
electronic balance (± 0.005 g, that was recali
brated following each relocation. We marked ,h
unders.de of the feet of the firs, hatched nestling
foi nests with two nestlings, using a non-toxi,
permanent marker. Marks were reapplied a
needed prior to Hedging. We replaced nestling:
where they were found and waichcd them unfi
they assumed a stationary, cryptic posture.
, We. codec, ed video of a single nesi-site
wMn 5nmy PfadnS “ fatnouflilSed video camera
within 5 m of an active use-site and recorded
brooding and movement activity from 1800 to
2100 hrs MST.
Statistical Analyses. — We calculated mean use-
site movement distances for each nestling age and
evaluated polynomial regressions before selecting
a cubic regression due to the high correlation
coefficient a,lL* correspondence with our observa¬
tions of nestling movement tendencies. We ft a
cufuc polynomial curve to the nestling growth
data because it maintained the linear nature of the
curve while allowing for a biologically accurate
representation of slower nestling growth both
early and late in the nestling stage. We used one-
tailed independent sample /-tests to assess signif-
,carlcc = ^-95 for all tests) of the correlation
coeflicients of the growth curve and movement
ala. We performed a two-tailed, paired sample
^ test to assess whether hatch order within
c utches influenced nestling growth rates.
RESULTS
Eight nest sites were found during incubation
and included in analyses. One brood was discov-
ere c*u,'ng the nestling stage but was omitted
SHORT COMMUNICATIONS
795
TABLE 1. Means (± SE), ranges, and sample sizes of
nestling movements of Common Nighthawks within three
age classes in Grand Teton National Park. Wyoming. 2010.
Daily nestling movement (ml
Age (days)
Mean ± SR
Range mil
It
1-5
1.57 ± 0.43
0—4
15
6-10
6.88 ± 0.96
0-14
16
11+
16.25 ± 3.39
5-48
14
from analyses due to our inability to relocate
subsequent use-sites. We observed one case in
which an egg of a two-egg-clutch was crushed by
an ungulate and the remaining viable egg moved
0.5 m from the original nest site. It is unclear
whether the egg was moved purposefully by the
adult in response to the disturbance or if it was
inadvertently moved by the adult Hushing during
or after the disturbance event (Jackson 2007). We
did not record any occurrences of egg movement
at any other nests (// = 7).
A growth rate curve (Fig. 1) was derived from
71 measurements of 10 nestlings from six
different broods. Nighthawk nestlings grew in a
nearly linear fashion (r* = 0.97. t - 48.6, dl =
68. r < 0.001). Common Nighthawk eggs hatch
asynchronously: however, across broods, second-
hatched nestlings weighed significantly more than
the older nestlings at the same age (t = 3.17, df =
14, P = 0.007).
Forty-five measurements t/i = 6 nests) of nestling-
stage movements were obtained from nestlings that
ranged in age from 1 to 18 days. Older nestlings were
more likely to move longer distances in a day (r =
0.66, / = 9.16. df - 43. /J < 0.001; Table 1. Fig. 2).
We observed two cases in which a likely predation
attempt was made on two different broods and in
both cases the nestlings moved nearly twice as far in
comparison to the largest previous site relocations (9
to 18 m. and 11 to 21 m). In the first case, a nestling
was observed to be severely injured, presumably due
to u predation attempt. In the second case, one
nestling was depredated.
FIG. 2. Common Nighthawk nestling movements as a function ([y - 0.0138x‘ - 0.1868x- + 1.2665x1; R- 0.66) of
chick age. Measurements (/i = 45) were collected for nests with 1 to 18 day-old young in Grand Teton National Park.
Wyoming. 2010.
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THE WILSON JOURNAL OF ORNITHOLOGY • Vo/. 124. No. 4. December 20/2
DISCUSSION
Nighthawk nestlings moved greater distances
between daily use-sites as nestlings increased in
age. Chicks ol 1—5 days ol age moved no more than
4 m a day from their previous use-site. However,
nighthawk nestlings regularly relocated greater
distances after day 5 between daily use-sites,
although short-range movements (- 5 m) were
recorded throughout the nestling period (Table I )
Common Nighthawk feet and legs are poorly
adapted for ambulation and these physical limita¬
tions may explain the reduced range of movement
observed during the early nestling stage. However
that short movements (- 5 m) occurred even for
young >11 days of age suggests there are likely
other factors influencing nestling movement. We
recognize that by regularly visiting the use-sites and
handling young we initiated disturbance that could
have influenced nestling movements. However ill
nest visits were conducted similarly and there was
still a clear movement distance pattern with respect
to nestling age. Our limited observations („ = ^ t)(-
nestling movements following severe disturbances
(partial predation, and a serious injury likely due to
attempted predation) suggest there may be a
relationship between the severity of disturbance
and the distance nestlings move. Common Night-
hawks may be able to differentiate between more
severe disturbance events and lesser ones, although
our protocol did not allow us to test this hypothesis
Which microhabitat features are important for
nest and use-site selection and inter-use-site
movement routes remains unclear as are the
spec, tie cues that elicit nestling movements We
were unable to discern any aural or visual cue that
prompted the nestlings to follow the female parent
trom the nest based on our video footage of a use-
site relocation. However, nestlings began to stir
and commence movement after the female parent
stopped brooding and began walking away from
the nestlings, suggesting that adults may be
responsible for use-site selection at least while
the nestlings are young (s 5 d)
The growth rate of nestling nighthawks is
comparable to reports for other young nightjars
such as Australian Owlet-nightjars { Aegothl/es
ensunus) (Brigham and Geiser 1997, and Com¬
mon I °orw, Ms (Pha/aenopti/us rwtiullii) fCsada
and Brigham 1994). Similarities in nes, predating
pressure and life history strategies have been
invoked to explain similarities in growth rates of
songbird species (Remes 2006, and may explain
the general likeness between the growth rates of
these nightjars. Common Nighthawk nestlings
overcame asymmetrical masses associated with
asynchronous hatching within several days of
hatching unlike Common Poorwill nestlings,
which are reported to take up to 14 days to reach
equivalent masses (Csada and Brigham 1994), We
did not observe feeding behaviors of Common
Nighthawk nestlings or adults and are unable to
comment on the potential role of food availability
and quality. However, selection may favor parents
with two equally developed nestlings that are able
to relocate similar distances.
Understanding the nature of nestling relocation
lias important implications for future survey
efforts, evaluation ol reproductive success, and
population analyses. Common Nighthawk nests
aie difficult to find and often just as difficult to
relocate. Having a general guideline for night-
hawk nestlings' movement potential will allow for
more certainty in identifying nest fates in future
studies. Daily nest survival rates and fecundity
estimates would also be improved. Our nestling
growth rate curve will provide a basis for
comparison across other ecological contexts,
Developing a better understanding of diverse
nestling behaviors in birds and other taxa enriches
om understanding of natural histories and important
selective pressures shaping life history strategies.
ACKNOWLEDGMENTS
Wc express our deep gratitude to members of (he
ha noun Laboratory for support at all stages of this
project. Funding for GRK during summer 2010 was
provided by a National Park Service Grant lo ADC. GRK
thanks the University of Wyoming Honors Prosratn for
providing a generous scholarship during this study. We
' un. ' * Braun, R. M. Brigham, C. P. Woods, and C.
' .iiiiriL/ Del Rio lor providing helpful comments on an
s.n u i \ vision ot this manuscript. Our study was performed
'"is 1 1 the auspices ot the University of Wyoming's
nstinuional Animal Care and Use protocol * A-32164N
. S 111,1 V'ok of bird biology. Second Edition. Cornell
Laboratory of Ornithology. Ithaca. New York. USA.
Ri:MES. V. 2006. Avian growth and development rates and age-
specific mortality: the roles of nest predation and adult
mortality. Journal of Evolutionary Biology 20:320-325.
Roil. D. A 1992. The evolution of life histories: theory
and analysis Chapman and Hull, New York. USA.
Rust. II. J. 1947. Migration and nesting of Nighthawks in
northern Idaho. Condor 49:177-188.
Sutton, G. M. and H. H. Spencer. 1949. Observations at a
Nighthawk’s nest. Bird-Banding 20:141-149.
Weller, M. W. 1958. Observations on the incubation
behavior of a Common Nighthawk. Auk 75:48-59.
The Wilson Journal of Ornithology 124(41:797-802. 2012
Nest Microclimate at Northern Black Swift Colonies in Colorado, New
Mexico, and California: Temperature and Relative Humidity
Carolyn Gunn.1 1 Kim M. Potter,2 and Jason P. Beason3
ABSTRACT. — The ecological nesting requirements
of Northern Black Swills (Cypscloldcs ni^cr borealis I
have been well documented, but little information exists
regarding the microclimate at Black Swift nests. We
placed 42 data loggers at 10 occupied Black Swift
colonies between 2006 and 2010 to measure and record
temperature and relative humidity, resulting in 19,181
usable records. Median temperature and relative
humidity at nine Colorado and New Mexico sites were
,J-4 C and 89.7%, respectively, and at one California
site were 13.4 C and 92.8%. respectively. Values were
quite stable throughout the breeding season with slight
changes reflecting the ambient temperature and humid¬
ity of the surrounding macroclimate. These baseline
data may prove useful for conservation of this species,
especially if predicted global climate changes occur.
Received 6 February 2012. Accepted I June 2012.
The microclimate at Northern Black Swift
( Cypseloides niger borealis) nests is believed to
he an important requirement for ncsl-site selection
hut there is a paucity of information on temper¬
ature and, especially, relative humidity (RH)
p. 0. Box 791, Dolores. CO 81323. USA
’White River National Forest. Rifle Ranger District. U094
County Road 244, Rifle, CO 81650. USA.
Rocky Mountain Bird Observatory . P. O. Box 1232.
Brighton’ CO 80601. USA.
4 Corresponding author; e-mail: cgunn@tone.net
(Lowther and Collins 2002). Knorr (1961) con¬
cluded Black Swifts occur only in isolated
colonics with specific ecological criteria, includ¬
ing proximity to water, high relief over surround¬
ing terrain, inaccessibility to predators, little or no
direct sunlight, and unobstructed fly ways. Levad
et al. (2008) analyzed 291 potential nesting sites
of Black Swifts and reported stream flow,
availability of potential nest platforms, amount
of moss, shading of potential nest niches,
topographic relief of surrounding terrain, and ease
of aerial access to potential nest niches each
significantly contributed to a higher probability
the site would he occupied by Black Swifts.
Neither of these studies mentioned temperature
and humidity, but low temperatures and high
humidity arc common characteristics of all
breeding sites for this species. Marin (1997)
suggested cool temperatures at a cave occupied
by Black Swifts could assist nestlings in main¬
taining a steady body temperature when adults
were away from the nest.
The first reference to temperature and humidity
at Black Swift breeding sites was by Murphy
(1951:448). who noted "considerable moisture”
and temperatures as low as 0-1.1 C at an
occupied colony in July 1949 near Silverton.
Colorado. Foerster (1987) recorded ambient nest
798
THE WILSON JOURNAL OF ORNITHOLOGY • Voi 124. No. 4. December 2012
temperatures at Lawler Falls in southern Cali-
tornia using Six’s maximum-minimum thermom¬
eters placed within 1 m of occupied nests and
measured RH using a sling psychrometer posi¬
tioned within 0.5 m of active nests during the
1985-1986 Black Swift breeding seasons. Am¬
bient temperatures near the nests ranged from
1 1.0-20.5 C for nests at drier sites to 1 1.5-17
C for nests at wetter sites, while RH near nests
was highly variable with a range of 54-96%
averaging 77% (Foerster 1987). Mann (1997)
measured temperatures with a portable thermom¬
eter placed near the center of a cave at Lawler
Falls occupied by Black Swifts during survey
visits from 1990 to 1992. He reported tempera¬
tures within the cave fluctuated no more than 2
C throughout the field season and readings
taken at night and early in the morning differed
only 1-2 C from those taken during the day
even though external temperatures fluctuated
daily by 10-20 °C; the actual temperatures were
not reported. A few humidity readings at this
same site early in the season ranged from 80 to
90%; the values decreased as the summer
advanced (Mann 1997).
The objective of our study was to document
microclimate parameters at Black Swift nests in
Colorado, New Mexico, and California by quan¬
tifying temperature and RH values.
METHODS
Study Sites. We reviewed known active colo¬
nies to identify sites that were amenable for data
logger placement, including accessibility with
reasonable effort and nests that could be reached
with aid of ladders. Colorado has 104 known
occupied colonies. New Mexico has three, and
California has -20. but most were unsuitable for
inclusion because of colony remoteness or nests
too high to reach.
We placed 42 data loggers over a period of five
breeding seasons (2006-2010) at one New
Mexico and eight Colorado breeding sites
levattons of these sites ranged from 2.231 to
:“7: "'1'“,|'*n8 Foothill, Montane, and
Subalp, „e Hie Zones (Levttd el al. 2008). Data
from these two states were analyzed together due
to habitat similarity. We placed two data loggers
for the entire 2009 breeding season a, Lawle?
Falls the San Jacinto Mountains of southern
California at an elevation of 1,620 m in mixed
comfer forest (Foerster and Collins 1990) This
was the most southern and western site from
which we collected data (Fig. 1).
Data Collection and Analysis. — We used Mi-
eroDAQ Log Tag model HAXO-8 humidity and
temperature recorders (MicroDAQ.com Ltd..
Contoocook. NH. USA) that are 86 8 54.5 x
8.6 mm and weigh 35 g. Data loggers can be
deployed inconspicuously in close proximity to
nests to collect season-long data and arc useful for
collecting temperature and RH values due to their
small si/e, accuracy, durability, battery longevity,
and case ol use. Specifications for the device can
be found on the company’s website (MicroDAO
20 J 2).
We programmed data loggers to collect tem¬
perature and RH data every 4 hrs which produced
three dusk to dawn and three dawn to dusk
leadings, capturing representative samples of
these values during each 24-hr period. Data
loggers were positioned as close to nests as
possible without disturbing nesting birds to obtain
the most accurate data of the nest microclimate.
\Ac placed data loggers in abandoned nests,
immediately adjacent to active nests, or on ledges
within 20 cm of nests. Reaching the nest was not
possible in some instances. We secured data
loggers in those cases within 20-125 cm of nests
or at an accessible site we felt was representative of
die nest microclimates for that colony. We placed
data loggers prior to onset of the breeding season
and retrieved them after the end of the breeding
season at most sites. We deployed data loggers
during one summer and retrieved them the
following summer at sites which were inaccessible
until alter the start of the breeding season due to
deep snow or streams that could not be crossed.
W e considered the potential for noise impacts
u| he|ieve units placed near nests did not produce
sufficient sound that would disturb swifts. The
primary' crystal oscillator, according to the
manufacturer, produces a sound of 32.768 Hz.
ut the crystal is physically dampened by a
si icone agent, further reducing sound production
(MicroDAQ.com Ltd., pers. comm.). All birds can
hear frequencies down to a minimum of —50 Hz
with the upper limit of hearing at -20,000 Hz;
cochlear potentials have been detected up to
30,000 Hz by using greater intensities of .sound
ih. in those normally encountered (Schwartzkopfl
1955),
We divided Colorado and New Mexico data
into live chronological segments of the nesting
season lor analysis based on breeding phenology
SHORT COMMUNICATIONS
799
FIG. 1. Historic and currently occupied Black Swift breeding colonies and data logger placement sites in the western
United States. 2006-2010.
at a site in Colorado including arrival at the colony,
egg laying, incubation onset, hatching, and Hedg¬
ing (Hirshman et al. 2007). We divided C alifomia
data into phenology periods previously published
lor this site (Foerster 1987. Schultz and Levad
2003). A 1-hr period in the afternoon (1500-
1600 hrs). considered the warmest time of day. and
a 1-hr period in the morning (0500-0600 hrs).
considered the coolest time period were used for
temperature comparison during each 24-hr period.
RESULTS
Thirty of 42 data loggers placed in Colorado
and New Mexico produced 17,826 usable records.
The two data loggers at the California site
produced 1 ,355 usable records.
Season-long (31 May to 7 Oct) median ± SD
temperatures and RH at Colorado and New
Mexico sites were 9.4 ±3.5 C (range =
0.11-26.2 °C, n = 17,826) and 89.7 ± 13.5%
(range = 23.5-100%, n = 17,826). respectively
800
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124. No. 4. December 2012
(A)
120
100
- 89,9 -
90 89 9
93.3
Q1 *)
B -
■■
- xLz
SO
1 - Bl -
*
60
40
20
- 5,2-5 - q.8 _
118
0
• -
- - - - -
- —
- • - -
- 8:2 - |
13 Jun Arrival
(n=142)
28Jur Egg 1 Jul Incubation 26 Jj| Hatching
laying (n=142) onset (n=140l ln=142)
-^-Temperature “C -*-Humidity%
13 Sep Fledging
(n=142)
( B )
(Fig. -A). We collected a substantial amour
ata at Fulton Resurgence Cave in Coloi
whose subterranean nature provides a st;
climate. Temperatures averaged 4 °C lower
RH averaged 6% higher within .he e
O da? r f, brfedins season when comp,
to dam from ail other Colorado and New Me,
Season-long, 15 May ,o4 Sep) median 4
wSe ,3 4™ , » col,
were 13.4 ± 2.89 C (range = 81-198 C „
.355) g ± ,5,4-angeT^8,^
n F-155), respectively (Fig. 2B).
Temperature and RH readings remained stable
within each 24-hr period at Colorado and New
Mexico sites. Temperature varied from a median
daily high of 1 1 .1 C to a median dailv low of 10. 1 C.
a difference of I C. RH varied from a median daily
high of 87.9% to a median daily low of 82.5%. a
difference of 5.4%. Similar data from the Califor¬
nia site were not available due to the times of day
for which data loggers were set to collect data.
DISCUSSION
Data loggers are a reliable method of obtaining
temperature and RH at Black Swift colonies.
SHORT COMMUNICATIONS
801
Their use revealed stability of both temperature
and RH, indicating little change in these values at
Black Swift nests within 24-hr periods or
throughout the breeding season. Nest tempera¬
tures from June through September at the colony
at Box Canyon, Ouray. Colorado, averaged
10.6 C lower than historic (1948-2006) ambient
temperature readings (Western Regional Climate
Center 2010) and RH averaged 45% higher than
recent historic (2001-201 1 ) ambient RH readings
MesoWest 2012). Our results show a close
relationship with the few data reported by
previous researchers (Murphy 1951. Foerster
1987. Marin 1997).
Median temperatures throughout the breeding
season at the California site were higher than at
Colorado and New Mexico sites and likely
represent elevation and latitude variations which
exist among North American Black Swift breed¬
ing sites across North America. Dates for
phenology events (onset of incubation, hatching.
Hedging) occur earlier at lower elevation and
lower latitude than at higher elevation and higher
latitude sites as demonstrated by review of Black
Swift phenology dates at locations throughout
North America (Wiggins 2004). However, great
variation in phenology can occur among nests at a
single site (Hirshman et al. 2007).
Eighteen percent of the data loggers were lost
during (lie first years of the study. Some fell from
their placement site, runoff from heavy rains
dislodged some devices, some slipped into cracks
in the rocks formed by freeze-thaw cycles making
them impossible to retrieve, and corrosion pre¬
vented downloading of data. We resolved the loss
"I data loggers by stabilizing deployed units with
a thin wire running from the data logger to a nail
temporarily placed in rock. Human tampering and
loss of battery power were not identified as
problems.
The choice of colonies for data logger placement
was not randomized. We chose colonies based on
ease of access to nests or niches that represented a
nest microclimate. This type of non-probability or
convenience sampling, where sampling units are
chosen based on tin arbitrary selection procedure
such as accessibility, time or budget constraints, or
study logistics, invariably introduces bias, and
makes it difficult to develop a statistically valid
estimate of surveillance parameters, in this case,
temperature and humidity (Nusser et al. 2010). The
somewhat broad elevation range, disparate loca¬
tions. and inclusion of one subterranean colony
decreased this bias, and allowed the study to be
conducted logistical ly.
There has been much speculation whether
Black Swift choice of nesting colonies near cool,
shady, damp waterfalls is an attempt to provide
optimal nest microclimate for incubating eggs and
rearing young, or part of some other life history
strategy (Knorr 1961. Marin 1997. Levad et al.
2008). Minimal temperature and humidity fluctu¬
ations may slow the metabolism of nestlings and
permit adults to leave them unattended for long
periods during wide-ranging foraging flights
(Levad et al. 2008); these suspected ecological
requirements may in turn limit nesting sites for
this species.
Some authors extrapolated the habitat require¬
ments of other Apodidac swifts to possibly allow
a reversible, temporary torpidity or partial poiki-
lothermy in developing Black Swift chicks and
adults (Koskimies 1948. 1950; Udvardy 1954) but
true torpor has not been identified in Black Swifts
(Lowther and Collins 2002). We have not
observed torpor-like characteristics in adult or
nestling Black Swifts (KMP, pers. obs.; CTC,
pers. obs.).
CONSERVATION IMPLICATIONS
The Black Swift nest microclimate material
presented, along with other physical ecological
requirements (Levad et al. 2008). provides infor¬
mation for modeling geographical range shifts lor
this species caused hy predicted climate change.
Identification and evaluation ot these potential
range shift areas in North America represent a vital
first step in protection o( these areas.
ACKNOWLEDGMENT'S
The authors are grateful to the U.S. forest Service for
purchase of data loggers that were used in the White Rivet
National Forest and other forests in the Rocky Mountain
Region. The Richard G. Levad Memorial Fund supported
data logger placement at St. Charles Falls. We thank J. E.
Bowers, J. G. Doerr. K. I. Giezentanner. R. W. Ghormley.
S. E. and W. K. Hirshman, the Maleug family. R. S. Noll.
K, D. Reid. R. E. Torretla. and J. G. Wargo for permits and
permission to access waterfalls and for help deploying and
retries ing data loggers. C. T. Collins. K S. foerster. Alicia
Mendoza. T. VV. Pairick. and J. F Toolen assisted with
logistics, placement, anil retrieval of data loggers at Lawler
Falls. K. H. Knudsen supplied access to research library
resources. M. M. Duffy and L. L, Jenks provided insightful
informal reviews of the manuscript, and .1 A. Frambach
assisted in mapping. C. T, Collins and an anonymous
referee generously reviewed the manuscript and provided
valuable comments. This paper is dedicated to the memory
802
THE WILSON JOURNAL OF ORNITHOLOGY . Vol 124. No. 4. December 2012
of Richard G. Levad. whose commitment to the Black Swift
encourages us to unravel the mysteries of this species.
LITERATURE CITED
FoHRsrtTt. K. S. 1987. The distribution and breeding
biology of the Black Swift ( Cypseloides niger) in
southern California. Thesis. California State Universi¬
ty. Long Beach. USA.
Foerster, K. S. and C. T. COLLINS. 1990, Breeding
distribution of the Black Swift in southern California
Western Birds 21:1-9.
Hirshman. S. E„ c. Ginn, and R. g. Levad. 2007.
Breeding phenology and success of Black Swifts in
Box Canyon. Ouray. Colorado. Wilson Journal of
Ornithology 1 19:678-685.
Knorr. O a. 1961. The geographical and ecological
distribution of the Black Swift in Colorado. Wilson
Bulletin 73:155-170,
KosKtMtEs. J. 1948. On temperature regulation and
metabolism in the swift. Micropus a. apus L... during
lasting. Fxperientia 4:274-276.
KOSK-Mtns. J. 1950. The life of the swift. Micro, no apus ( L )
m relation to weather. Annules Academiae Scientianim
Fennicae, Series A. IV Bioiogica 15:1-151
levad, R. G.. K. M. Potter. C. W. Shultz. C. Gunn, and
J. G. Doekr. 2008. Distribution, abundance, and nest¬
le characteristics of Black Swifts in the southern
Rocky Mountains of Colorado and New Mexico.
Wilson Journal of Ornithology 120:331-338.
Lowther, P. H. and c T. Collins. 2002. Black Swift
(Cypseloides niger). The birds of North America
Number 676.
Marin. M. 1997. Some aspects of the breeding biology of
the Black Swift. Wilson Bulletin 109:290-306
MESOWEST. 2012. Download KTEX data. University of
Ltah. Salt Lake City, USA. mesowcsi.utah.edu/cEi-
bin/droman/download_ndb.cgi?stn = KTEX&wwparam
= 1338494627
MicroDAQ.COM. 2012. Humidity and temperature data
logger. Contoocook. New Hampshire. USA. www.
mien KJaq.com/1ogtag/haxo- 8 php
Murrhy Jr., J. A. 1951. The nesting of die Black Swift.
Natural History 60:446-449.
Nusser. s. M.. W.'r. Clark. D. L. Ons, and L. Hianc.
2010. Sampling considerations for disease surveillance
in wildlife populations. Journal of Wildlife Manage¬
ment 72:52-60.
Schultz, c. and R. Levad. 2003. Black Swift monitoring
protocol. Unpublished report. USD.A, Forest Service.
San Juan National Forest. Bayfield. Colorado. USA.
Schwa RTZKOH-T. J. 1955. On the hearing of birds. Auk
72:340-347.
Udvardy, M. D. F. J954. Summer movements of Black
Swills in relation to weather conditions. Condor
56:261-267.
Western Regional Climate Center. 2010. Colorado
average monthly temperatures. W'RCC, Reno. Ne¬
vada. USA. www.wrcc.dri.ed u/h t in 1 files/co/cu.avg.
htinl
Wiggin.s. D. 2004. Black Swift ( Cypseloides niger): a
technical conservation assessment. USDA. Forest
Service, Rocky Mountain Region. Golden. Colorado.
USA. www.fs.fed.us/r2/projects/scp/assessments/
blackswift.pdf
The Wilson Journal of Ornithology 124(41:802-807. 2012
A New Method for Trapping Chimney Swifts and Other
Vertical Hollows
Birds That Nest in
Hazel E. Wheeler1
ABSTRACT.— Previous Chimney Swift ( Chae
pelagica) trapping efforts relied on chimney-top
traps at large roost sites, which were disruptive
tnefftciem when targeting individual birds. I design,
hoop net , or use a. nest chimneys to trap indivic
tn CnHgb n CaiAgh' 13 Swifls " different s
n Guelph Ontano, Canada over two summers with
sue abandonment. This trap is superior for trapp
individuals because it; (|, can be dep)oved ™
without scaling the chimney. (2) will work on chimn,
Trent Z ? ‘ ,Jfe Sdcnces Graduate Progn
Trent University. Environmental Sciences Buildi
Peterborough. ON K9J 7BS. Canada; e-mail:
hazel.wheeler@gmail.com
of different sizes and shapes, and (3) minimizes
is ur ance to birds. My results indicate this net is an
c icient. sale, and relatively simple method of trapping
m iv, ual Chimney Swifts at their nest chimneys.
e caved !7 March 2012. Accepted 22 May 2012.
Historically, Chimney Swifts ( Chaetura pelu -
gii a) were trapped mainly at chimneys where they
toost dining spring and fall migration using a
specialized chimney-top trap (Bowman 1952).
iese (taps were ellective in catching large
numbers of birds at roosts (e.g.. Peters 1937.
Calhoun and Dickson 1942. James 1950). but their
SHORT COMMUNICATIONS
803
use requires accessing the top of a chimney, they
are cumbersome because ot their size and number
of components (Bowman 1952), and installation
is time-consuming for targeted captures (e.g.. a
single bird). The use of chiinney-top traps has
caused birds to abandon roost sites en masse
(Zammulo and Franks 1979) suggesting this
method is stressful for birds and has, in some
cases, caused large-scale mortality events (up to
225 individuals reported) among trapped birds
(Worth 1 940. Zammulo and Franks 1979). Worth
1943) modified a chimney-top trap to be less
cumbersome, but it still required overnight use to
capture birds its they left the chimney in the
morning. Fischer (1951) developed a method ol
capturing Chimney Swifts singly throughout the
day by scooping them into a tethered can while
they roost. This method has been used with
success in some studies (Dexter 1969, Ramsey
1970. Zammuto and Franks 1979), but risks
sinking, and potentially displacing, nestlings or
the entire nest.
Most studies of Chimney Swifts that used
trapping and/or banding were conducted prior to
1980. However, since completion ol the last large
handing study (Dexter 1990). Chimney Swift
populations have declined across their breeding
range, and the species is designated as Threatened
in Canada (COSEW 1C 2007). Thus, extra care
must now he laken to ensure minimal disturbance
to birds during research, which requires develop¬
ment of new capture methods. I describe a new
trapping technique for catching indiv idual nesting
Chimney Swifts with a focus on minimizing
disturbance at the nest chimney, and improving
speed and ease of trap placement.
METHODS
Study Area.— I conducted this study from May
to August 2010 and 2011 in Guelph. Ontario.
Canada (43 33' N. 80 15' W). Guelph has a
large number of buildings built before the 20th
century, as well as the University of Guelph,
which has origins in the late ISOOs. The city is
divided by the Speed and Eramosa rivers, the
confluence of which is northeast ol downtown.
I focused my study on an ~-8-km diameter area,
centered on the downtown core (43 32 36 N,
80 14' 53" W). that is characterized by mixed
fcsidenlial/commercial land at the center, sui-
rounded mainly by older (50+ years ol age)
low-density housing and a small proportion ol
institutional land. Chimney Swifts occur mainly in
the downtown and university areas, where older
buildings provide suitable nesting and roosting
structures.
Site Selection. — I selected chimneys from a list
of previously identified nest sites from 2007 to
2009 (M. D. C adman, pers. comm.; Canadian
Wildlife Service-Ontario). Initially. I monitored
all chimneys used for nesting in past years,
following a standardized protocol (Bird Studies
Canada 2009). 1 gave priority to active chimneys
deemed more accessible (flat roof, roof access
from inside building, structurally sound chimney
and roof). I contacted property owners to secure
building access, and made an initial visit to those
chimneys to record physical characteristics
(height above roofline, internal and external
length and width, material, color, number of
flues), as well as to visually confirm the presence
of a nest, when possible. Chimney color was
defined as Might' (gray brick, stone, or cement; or
clay-lined) or 'dark' (red or dark brown brick).
Trapping. — I captured Chimney Swifts at their
nest chimneys after eggs had hatched, ascertained
by either direct observation of hatchlings in the
nest, or by observation of trequent visits by adult
swifts. I purposefully restricted trapping to this
period lo ensure the birds were invested, decreas¬
ing the chance of nest abandonment (Fischer
1958); nest abandonment instigated by researchers
would have meant immediate cessation ol any
trapping efforts, but nesting activity continued at
all sites following trapping. Restricting trapping to
this period also provided the benefit that adults
would he making frequent visits to the nest to
provision young, thus increasing trap success. I
trapped swifts with a hoop net (Colvin and Hegdal
1986). redesigned specifically for this purpose
(Fig. 1 ). as they entered their nest chimney during
daylight hours on fair weather days (no rain,
Beaufort wind score s-3). 1 made the net from
standard passerine mist-netting (38-mm mesh
size) suspended in a l -nr frame wilh black fabric
stretched between the frame and the opening of
the net. which was 50 cm in diameter. The net was
~ 1 m deep, and had a 1 5-cm diameter hoop (0.32-
cm clear PVC tubing) and a weight (four 0.79 cm
washers) at the bottom. 1 mounted the entire net
assembly on a telescopic pole (1.83-5.49 m
length) to facilitate placement at chimneys ot
various heights.
I placed the net (Fig. 2) after I observed a bird
exiting a chimney, and kept it in place until the
bird returned and was trapped, or a maximum ot
804
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124. No. 4. December 2012
1.0 m
Telescopic pole
mrara
[WmmW
VVWV vvV W\A/V"
AAA AAAAA A A A /\
A . I
mufmm
\numnt
0.15 m
1.0 m
Fabric-covered
wood frame
Net bag
Weight
FIG. 1. Modified hoop net design for trapping nesting Chimney Swifts.
2 his if no bird was caught. The trapping duration
of failed attempts depended on swift activity at
the chimney, where, if birds were making many
close approaches, I removed the net after 1.5 hrs
of unsuccessful trapping; only in cases where
there was little adult activity was the net left for
the full 2 hrs. I deferred further trapping at that
site to another day if no bird was caught by the
end of the second hour. The 2-hr maximum in-
place time was to minimize disruption to nestling
provisioning (Bull and Beckwith 1993).
Data Analysis. — I calculated trapping success
as a proportion ol sites at which trapping was
attempted each year (site success; N2m = 8,
^2011 - 10) and as a proportion of placements
(placement success; N2m) = 13. M0II = 22)
where a site could have the net in place numerous
times each year before a bird was caught. I tested
lot differences in placement success between
yeats and between chimneys grouped by color
with Fisher s exact tests at an alpha level of
0.05. All analyses were performed in R 2.12.2
(R Development Core Team 2011).
RESULTS
I caught individual Chimney Swifts at seven of
eight nest sites (88%) at which trapping was
attempted in 2010. and five of 10 nest sites (50%)
in 201 I . I attempted trapping in both years at six
sites with the remaining six sites targeted in only
I year. There was no significant difference in
placement success between years (Fisher's exact
test. /’ = 0.28) or between chimneys grouped by
color (Fisher's exact test. P = 0.14). "
I caught birds at five of the seven successful
Mtes in 2010 on the first visit, while the remaining
two sites required a second visit before a bird was
tiapped. Three of the five successfully-trapped
SHORT COMMUNICATIONS
805
FIG. 2. Net placement at a nest site in Guelph. Ontario. Canada (Jul 2010).
''iles had birds caught on the first visit in 2011.
whereas three or four visits were necessary for the
remaining sites. I terminated trapping on unsuc¬
cessful days at those sites requiring multiple visits
either because the sun had set or 2 hrs had passed
without any success. Pooling trapping effort (mins
net deployed) over both years. 1 had an average
effort of 125.38 min per bird caught.
Mean (± SE) time to trap a bird at a site on
successful trapping days was 38.08 ± 6.00 min.
and 84.6% of birds trapped were captured within
[ hr. 1 most often caught birds in the mid¬
afternoon (mean ± SE: 1528 ± 41 min EDT). and
they were released 12.85 ± 1.20 min after
capture. The average time ot capture may be
more an artifact of study logistics than an
indicator of the best time to attempt trapping. It
was necessary to coordinate building access with
property managers for six of the eight sites in
2010 and. due to inherent limitations, these
806
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124, No. 4. December 2012
trapping sessions were mostly relegated to the
afternoon. I attempted one site earlier in the day
(the trap was in place from 1140 to 1340 hrs)
without success; 2 days later. I caught a swift at
this site at 1824 hr.s. I made some earlier attempts
at trapping in 201 1. where the earliest a net was in
place was 0919 hrs, but did not catch any birds
before 1 100 hrs in either year. There may be some
value to avoiding trapping around noon, "as the net
may be more visible to approaching swifts at this
time due to more direct sunlight inside the
chimney. Three swifts were caught between
1 100 and 1300 hrs, although chimney color may
have been a factor in these cases; 60% of tailed
trapping attempts before 1300 hrs were at
chimneys where the interior was constructed of
light-colored material (gray brick or terra cotta
clay), whereas successful sites were of dark red
brick that would naturally obscure the net. Small
sample size prevented any formal analysis of
capture patterns at mid-day.
DISCUSSION
flic Chimney Swift trapping method I describe
here is superior to past methods for trappino
individual birds for several reasons; (I) it can be
installed easily by a single researcher in under
min without scaling the chimney; (2) it will
work on chimneys of differing sizes and shapes;
and (3) it minimizes disturbance to birds by
keeping trapping periods relatively short, targeted
to an individual, and spatially removed front the
nest within a chimney. This method has a
reasonable effort per bird (-125 min) for
species-specific trapping, considering that trap-
pmg effort can extend far beyond 2 hrs per bird
tor some species (Hernandez et al. 2006. Benfte/-
Lopez et al. 2010. Perkins et al. 2010). Most
swifts were caught within I hr. and I recommend
constraining trapping sessions to I hr to maximize
the catch to effort ratio.
The net described can easily be placed on
chimneys with an internal diameter of 50- 100 cm
and smaller chimneys in some circumstances. For
example. I caught one bird at a chimney with an
internal diameter of -30 cm; trapping proceeded
despue the small size because it had a clay liner
that created a smooth internal surface, and
snagging was less of a concern. Generally, care
needed to be taken to keep the net away from the
chimney s ulterior walls lest i, get caught and rip.
Chimney height could constrain placement, but ,o
a lesser extent than traditional trapping methods
that require access to the chimney top. This net is
eflective as long as researchers can gel within 5-
6 m of the chimney top (affected hy length of net
pole).
The presence ol researchers nearby did not
seem to aflecl swift behavior, as birds often
approached and immediately entered chimneys
during periods when I was observing from the
rooftop, or preparing the trap for placement.
However, there was some initial avoidance by the
approaching swift on most trapping occasions once
the net was in place. Typical adult behavior during
nestling provisioning involves foraging trips rang¬
ing Irom 15 min to 1 hr. depending on the age of
the young, at the end of which adults will return to,
arid quickly enter, the chimney (Fischer 19581
During trapping periods, a bird would often
approach within —0.5 m of the chimney opening
bclore veering off, circling in the area, then
icturning to the site. This could happen several
times before the adult actually entered the
chimney. There was no clear pattern in avoidance
behavior that suggested how it could be minimized
to expedite trapping, although using fabric of a
different color in net construction, to mimic the
appearance ol the chimney top, was considered.
Minimizing disturbance at nest sites to avoid
site abandonment was a primary concern. On
thiee occasions a bird trapped at one site was
tracked to another chimney nearby at night (via a
contemporaneous radiotelemetry study); although
in one case the bird was tracked to its original
chimney at a later date. However, these were not
\ iewed necessarily as abandonments, as it may be
that captured birds were actually "helpers’ to the
breeding pairs, which is a common behavior for
Chimney Swifts (Dexter 1969). Further. there w as
a case where two birds were caught at the same
site on di Herein dates with no abandonment. In a
comparable telemetry study on Vaux's Swifts
I [C/uietura vauxi ) nesting in natural cavities in
regon, multiple birds were also caught at the
same site on three occasions without abandon¬
ment (Bull and Beckwith 1993). This suggests
hupping multiple Chimney Swifts at the same
nesting chimney is a feasible option.
This net is an efficient, safe, and relatively
simple method of trapping individual Chimney
^witts at their nest chimneys. Trapping large
numbers of birds at a roost, however, would still
x* best suited to other methods as this net is
intended to catch birds singly. There is potential
Ibis trapping method could be used for other swift
SHORT COMMUNICATIONS
807
species that have similar nesting habits, such as
Vaux’s Swift in western North America: Sick’s,
Short-tailed, and Grey-rumped swifts ( Chaetura
mcridionalis, C. brachyura, and C. cinereiventris ,
respectively) in South America; and Mottled
Spineiait (Telecmthura ussheri) in Africa, which
have all been observed nesting in chimneys (Lack
1956. Chantler and Driessens 1995). Studying
individual birds can contribute to our knowledge
of fine-scale swift behavior and ecology in
breeding areas, and greatly enhance our ability
to develop effective conservation strategies.
ACKNOWLEDGMENTS
Funding for this project was provided by the Natural
Sciences and Engineering Research Council of Canada, the
Ontario Ministry of Natural Resources, and Trent Univer¬
sity. 1 thank my field assistants, S. K. Poole and A. F..
Bannister, the City of Guelph, the University of Guelph and
all pmperty owners who allowed unfettered access to their
chimneys. This research was conducted under Canadian
Wildlife Service permit tt 1 080 1 and was approved by the
Trent University Animal Care Committee (ACC# 10053).
The constructive review of J. J. Nocera, two anonymous
reviewers, and the editor improved this manuscript.
LITERATURE CITED
BenItez-LOpez, A.. F. Mougeot. C, a. Martin. F. Casas,
M. Calero-Riestra, .1. T. Garc ia, and J. Vinijela.
2010. An improved night -lighting technique for the
selective capture of sandgrousc and other steppe birds,
European Journal of Wildlife Research 57:389-393.
Bird Studies Canada. 2009. Chimney Swift ( Chaetura
pelagica) monitoring protocol. Port Rowan, Ontario,
Canada, www.hirdscanada.org/researcliyspcciesatrisk/
chsw/CHSW_Monitoring_Protocol.pdf
Bowman. R. I. 1952. Chimney Swift banding at Kingston,
Ontario from 1928 to 1947. Canadian Field-Naturalist
66:151-164.
Bull, E. L. and R. C. Beckwith. 1993. Diet and foraging
behavior of Vaux's Swifts in northeastern Oregon.
Condor 95:1016-1023
Calhoun, J. B. and J. C. Dickson Jr. 1942. Migratory
movements of Chimney Swifts. Cluietura pelugica
(Linnaeus) trapped at Charlottesville, Virginia. Bird-
Banding 13:57-69.
Chantler, P. and G. Driessens. 1995. Swifts: a guide to
the swifts and treeswifts of the world. Pica Press,
Sussex. United Kingdom.
COLVIN. B. A. AND P. L. Uegdal. 1986. Techniques for
capturing Common Barn-Owls. Journal of Field
Ornithology 57:200-207.
COSEWIC. 2007. Assessment and status report on the
Chimney Swift in Canada. Committee on the Status
of Endangered Wildlife in Canada, Ottawa. Ontario.
Canada.
DEXTER, R. w. 1969. Banding and nesting studies of the
Chimney Swift. 1944-1968. Ohio Journal of Science
69:193-213.
Dexter, R. W'. 1990. Composition of roosting Hocks of
Chimney Swifts at Kent. Ohio. 1944-1983. North
American Bird Bander 15:53-56.
Fischer. R. 1951. A new method of capturing Chimney
Swifts. Bird-Banding 22:79-80.
Fischer. R. 1958. The bleeding biology of the Chimney
Swill. Chaetura pelagica (Linnaeus). Education
Department. University of the State of New York.
Albany. USA.
Hernandez, F.. L. A. Harveson, and C. E. Brewer.
2006. A comparison of trapping techniques for
Montezuma Quail. Wildlife Society Bulletin 34:
1212-1215.
James. P. 1950. Spring flocking of Chimney Swifts
Chaetura pelagicci (Linnaeus) at Cornell University.
Bird- Banding 21:9-1 I.
Lack, D. 1956. A review of the genera and nesting habits
of swifts. Auk 7.3:2-32.
Perkins, M., S. King, and .1. Linscombe. 2010. Effective¬
ness of capture techniques lor rails in emergent marsh
and agricultural wetlands. Watcrbirds 33: 376-380.
PETERS. H. S, 1937. Chimney Swift banding in Alabama
during the fall of 1936. Bird-Banding 8:16-24.
Ramsey. J. .1. 1970. Temperature changes in Chimney
Swifts ( Chaetura pelugka) at lowered environmental
temperatures. Condor 72:225-229.
R Development Core Team. 2011. R: a language and
environment for statistical computing. R Foundation
for Statistical Computing. Vienna, Austria. www.R-
project.org
Worth. C. B. 1940. A warning to Chimney Swift banders.
Bird-Banding 11:61-62.
Worth, C. B. 1943. Notes on the Chimney Swift. Auk
60:558-564.
Z AM Ml 'TO. R. M. AND E. C. Franks. 1979. Trapping flocks
of Chimney Swifts in Illinois. Bird-Banding 50:
201-209.
808
THE WILSON JOURNAL OF ORNITHOLOGY • Vo I. 124. No. 4. December 2012
The Wilson Journal of Ornithology 124(4):808-8 1 I, 2012
Effects of Conspecifics on Feeder Choice by Northern Cardinals
David M. Millican,' Patrick G. McGovern,' and Mark T. Stanback1-2
ABSTRACT. — Inter- and intra-specific competition
are known to influence feeding decisions, but relatively
little research has investigated how inter- and intra-
sexual interactions can impact foraging. We studied
foraging preferences of male and female Northern
Cardinals ( Cardinalis cardinalis) during winter and
found they preferred sunflower seed to safflower seed
when presented with paired feeders in the absence of
conspecifics. Male Cardinals avoided feeders occupied
by other males and approached feeders occupied by
females, regardless of feeder contents. Female cardinals
avoided other females and especially males when
choosing feeders. These changes in foraging behavior
by male and female cardinals as a result of conspecific
presence indicate inter- and intra-sexual interactions
alter the attractiveness of a high or low energy food
source. Received 27 December 2011. Accepted 7 June
conspecifics altered the foraging behavior of male
and female Northern Cardinals (Cardinalis car¬
dinalis) using feeders during winter. For example,
males ot this species are known to be dominant to
females during winter (Nice 1927. Laskey 1944,
Rite hi son and Omer 1990,); thus we might expect
males to monopolize preferred foods — if nutrition
was their only consideration. We provided
Northern Cardinals with paired feeders containing
different foods (sunflower vs. safflower seed) to
lest the extent to which their foraging decisions
were influenced by the gender of other conspe¬
cifics present.
METHODS
Organisms must be discerning when presented
with conflicting options regarding foraging (Sih
1980. Lima and Dill 1990. Krebs and Kaeclink
1991, Cuthill and Houston 1997). Individuals
must optimize energy intake by trade-offs in
both food quality and vulnerability to predation
(Stanback and Powell 2010). Competition (both
inter- and intra-specific) can also have a substan¬
tial impact on tbe ability of individuals to access
food sources (Nice 1927. Lima and Dill 1990.
Shedd 1990. Belthoff and Gauthreaux 1991
Tarvin and Woolfenden 1997. Lima 1998. Rands
et al. 2006). Finally, inter- and intra-sexual
interactions, while often considered only in the
context of breeding, can have dramatic effects on
foraging in birds (Selander 1966. Schneider
1984). Inter-sexual niche separation, for species
that lack substantial morphological differences in
trophic structures, often results from social
dominance of one sex over the other (Desrochers
1989, Hogstad 1991). It js unclear, however,
whether males and females can cleanly separate
their foraging and sexual interactions, even durins
winter. We investigated how the presence of
NC 28036° USA f Bl°IOgy' Davidson CollcSe- Davidson,
2 Corresponding author;
e-mail: mastanback@davidson.edu
l iehl Procedures. — Northern Cardinals are
year-round residents in the southeastern United
States and common visitors to feeders (Halkin and
Lin vi He 1999). Pair bonds typically dissolve
dining the non-breeding season and cardinals in
an area form loose flocks (Halkin and Linville
1999). We observed Northern Cardinals between
15 and 21 January 2010 at five locations on the
Davidson College campus in Davidson. North
Carolina, USA (35 30' N, 80 50' W). The five
feeding sites were no closer than 500 tn from one
another. We set up two pole-mounted Absolute
hopper-style squirrel -proof bird feeders (1.5 m
apart) at each site, labeled A and B. Feeders were
kept filled lor 5 weeks prior to data collection. We
filled one feeder with unshelled safflower seeds
and the other with unshelled black-oil sunflower
seeds, buth from Wild Birds Unlimited. The
I ceding perch on each feeder was 29 cm long.
Wc adjusted the feeders to accommodate the mass
ol two cardinals, but cardinals rarely fed side by
side. We used 7 x 35 Nikon binoculars to observe
cardinals at feeders at each site for 1 hr twice a
day. once before and once after 1200 hrs. fora total
of 68 observation hours. We observed feeders
Irom a distance of 30 m to avoid disturbing feeding
individuals. We switched the position of the
feeders at each site alter 3 days of observations to
eliminate biases due to possible site preferences.
SHORT COMMUNICATIONS
809
1
Ot
C
Vi
O
o
£
U
VI u
V 41
5 *
£ =
>— ‘r
= P
o *
0.9
0.8
0.7
0.6
0.5
0.4
0.3
0.2
0.1
0
X2 = 10.96
P< 0.001
X2 = 20.54
P< 0.001
X2 = 12.24
0.UU1
X2 = 1.92
P= 0.165
X2 = 26.38
P< 0.001
Both Vacant
Fem. Saf.
Fern. Sun.
Social context
Male Saf.
Male Sun.
FIG. 1. Male Northern Cardinal feeder visitation in five social contexts: both feeders vacant (Both Vacant, n -^0h ®
female on the safflower feeder (Fem. Saf.. n = 85). a female on the sunflower leeder (Fun. an., n • _
safflower feeder (Male Saf.. n = 70), a male on the sunflower feeder (Male Sun., n - 104). All / tests wi ^ .
Vacant’ compared to a null expectation of no preference (1:1). All other distribut.ons compared to a null expectant
0,62:0.38 (Both Vacant).
We recorded the number of visits by male and
female cardinals to each feeder and noted the
location and sex of other cardinals present. We
defined a visit to a feeder as any time a cardinal
landed on the feeder perch and remained >1 see.
Cardinals are larger than and dominant to other
common feeder birds (e.g., Carolina Chickadee
\Poecile carol inensis], Tufted Titmouse \Baeolo-
phits bicolor]) and we assumed the occasional
presence of smaller species did not influence choices
made by cardinals. We excluded from our analyses
eases in which both feeders were occupied when a
third (focal) cardinal made a choice about which
feeder to visit. The cardinals we observed were not
individually marked, and wc sought to minimize
pseudoreplication by collecting data at five separate
locations and limiting the study to 1 week.
Statistical Analyses.- We used GraphPad
QuickCalcs software (GraphPad Software Inc.. La
Jolla, CA, USA; GraphPad.com) to perform /; tests.
We compared the proportion of visits to sunflower
versus safflower seed feeders (when both feeders
were vacant) to an expected equal preiportion. We
compared visitation rales to feeders with sunflower/
safflower seed to expected rates generated when both
feeders were vacant for our subsequent analyses.
RESULTS
Male Northern Cardinals visited the feeder
containing sunflower seeds significantly more
often (n = 360, *2, = 20.54. P < 0.001; Fig. 1)
than the feeder containing safflower seeds when
both feeders were empty of conspecifics. Females
exhibited a similar bias towards sunflower seeds
(„ = 473, x2i = 35.18, P < 0.001; Fig. 2).
Wc compared the feeder choices of males in the
presence of conspecifics to those made by males
when both feeders were vacant. Males visited the
safflower seed feeder significantly more often
when a female was present at the sail lower seed
feeder and the sunflower seed feeder was vacant
(y = 12.24. P < 0.001; Fig. 1). Males visited
the sunflower seed feeder significantly more
often than expected when a female occupied the
sunflower seed feeder (jr i = 10.96. P < 0.001;
Fig. I ). Males visited the sunflower seed feeder
as expected when another male occupied the
safflower seed feeder (x’i = L92, P = 0.165;
Fig. 1). Males visited the safflower seed feeder
significantly more often than expected when
another male was present at the sunflower seed
feeder Or, = 26.38. P < 0.001; Fig. 1).
Females visited the sunflower seed feeder as
expected when another female occupied the
safflower seed feeder (y:i — 2.95, P = 0.086;
Fig. 2). Females visited the safflower seed feed-
eAignificantly more often than expected when
another female was present at the sunflower seed
feeder (y\ = >9.04. P < 0.001; Fig. 2). Females
visited the sunflower seed leeder significant¬
ly more often than expected when a male occupied
the safflower seed feeder (/2i = 53.77. P < 0.001;
810
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124, No. 4. December 2012
QjC
0.9
C
0.8
e
o
■C
0.7
w
l/l
0.6
—
-
o
S
3
0.3
s
■
oSlok6 (BoTvafamr11 eXP“'ati'>" °f n° P"*""* All other distributions compared to a' null expect,®" of
Fig. 2). Females visited the safflower seed feeder
significantly more often than expected when a male
was present al the sunflower seed feeder and the
safflower seed feeder was vacant (y2, = 2P 7.5 p
< 0.001; Fig. 2).
DISCUSSION
We investigated how social situations in the
non-breeding season influence the foraging deci¬
sions by free-living male and female Northern
Cardinals. The birds we observed were not
individually marked, and it is possible that pre¬
existing dominance relationships among a small
number of individuals could have influenced the
overall patterns we observed. However, we at¬
tempted to minimize the probability of identical
dyads being observed repeatedly by collecting data
over a short period of time at five different feeding
stations, all visited by large numbers of cardinals.
Both male and female Northern Cardinals preferred
to visit feeders with sunflower seeds when
provided with a choice between sunflower and
safflower seeds when no conspecifics were present.
This is not surprising considering the higher fat
content of black-oil sunflower seeds (40%) versus
safflower seeds (29%) (Foster and Smith 2001 ),
Female Northern Cardinals avoided all conspe-
c.tics when visiting feeders, regardless of which
feeder they occupied. Females visited the saf¬
flower seed feeder significantly more often than
the sunflower seed feeder when the sunflower
seed feeder was occupied by another cardinal
either male or female. Females opted for the
unoccupied leeder, even if it contained the less-
preferred lood. Females appeared to be particu¬
larly averse to visiting feeders occupied by male
conspecifics.
’ - - ■'-wvjv.in WCVU|_UV.-U uy UUItl
visiting the safflower seed feeder significantly
more often than the sunflower seed feeder when
another male occupied the sunflower seed feeder.
Males preferentially visited feeders occupied by
leinales. even when these feeders contained the
I ess-pre fened lood. The interactions we observed
were, almost without exception, brief; the landing
of a new bird usually resulted in departure of the
original bird. The motion of the feeding perch upon
landing ol the second bird may have induced the
departure of the first, but there seemed to be a
disinclination to feed side by side. What does a
male gain by displacing a female from a less-
preferred food? We could And nothing in the
literature to explain our observations, and suspect
male cardinals are conflicted. January is the coldest
month at our study site, and males begin acting
territorial as early as February. It seems likely that
m«lcs may be under selective pressure to initiate
contact with females before females are willing to
reciprocate. Consuming a safflower seed for a male
cardinal with regular access to a feeder containing
sunflower seeds may he worth the opportunity to
interact, however briefly, with a female.
Both female and male Northern Cardinals
deviated from expected foraging behavior due to
SHORT COMMUNICATIONS
interactions with conspecifics. This is not surprising
as the idea that animals are automatons seeking
maximal caloric intake is. undoubtedly, naive
i Pierce and Ollason 1987 provide a critique of
optimal foraging theory). Most researchers reeog-
nize anuanced approach is necessary to appreciate
the variety of selective pressures operating on
foraging organisms (see Stephens et al. 2007). but
predictions based on simple assumptions are. for
better or worse, often the default. Our results
demonstrate inter- and intra-sexual interactions can
have a dramatic effect on observed resource use.
ACKNOWLEDGMENTS
We thank the students of the Davidson College 2010
Vertebrate Field Zoology class (Bio 322) for help in
conducting this experiment (Manelle Abalo, Farced
Cheema, Emily Copeland. Daniel Councell. Evan F.skew.
Marion Floyd, Shawna Foley. Alejandro Goiualez-Stcwarl,
Lucy Medley, Lauren Ivey, Currv Jones. Danielle Jordan.
Waller Kucera. Ross Lackey, Phil LaTourette. Chris Lima.
Meagan Madden. Kevin Mangum, Maddy MeCrcery.
Molly Mon-ill, Samantha Meyers. Tannhya Miranda, Shane
Purvis. Megan Reilly. Ben RilTe, Jeffrey Roth. Dairy
Spasova, Gabrielle Wallace. Abbey Webb. Zemis Wilson.
Colin Wint, and Lynea Wticzak). The manuscript was
improved by the comments of J. R. BeltholT, C, L, Braun.
E. L. Cline, and K. A. Turvin.
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risk of predation: recent developments from behavior¬
al. reproductive, and ecological perspectives. Advanc¬
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made under the risk of predation: a review and pro¬
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NICE. M. M. 1927. Experiences with Cardinals at a feeding
station in Oklahoma. Condor 29:101 103.
Pierce. G. J. AND j. Cl Oli ASON. 1987. Eight reasons why
optimal foraging theory is a complete waste of time.
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Rands, S.. R. Pettifor. J. M. Rowclifff. and G. Cow-
ushaw. 2006. Social foraging and dominance relation¬
ships: the effects of socially mediated interference.
Behavioral Ecology and Sociobiology 60:572—581.
RirrmsoN. G. and M. K. Omek 1990. Winter behavior of
Northern Cardinals ( Cnnliindi s cardinulis). Transac¬
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Schneider, K. J. 1984. Dominance, predation, and optimal
foraging in White-throated Sparrow flocks. Ecology
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Sblandf.R. R. K, 1966. Sexual dimorphism and differential
niche utilization in hirds. Condor 68:129-141.
SliF.DD, D. 1990. Aggressive interactions in wintering
House Finches and Purple Finches. Wilson Bulletin
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Sill. A. 1980. Optimal behavior: can foragers balance two
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Stanback, M, T. and E. M. Powra.i.. 2010. Predator
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Stephens. D. W.. j. S. Brown, and R. C. Ydenberg.
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812
THE WrLSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 4. December 2012
The Wilson Journal of Ornithology 1 24(4):8 12— 8 1 5, 2012
Kleptoparasitism of Nesting Material from a Red-faced Spinetail
( Cranioleuca erythrops) Nest Site
David L. S lager, 12 Molly E. McDermott,1 and Amanda D. Rodewald'
ABSTRACT. — We report observations of Thick¬
billed Enphonias (F.uphonia laniirostris) and a Gold
en-loced Tyrannulet ( Zimmerius chrysops) kleptopai -
asiti/ing nesi material from Red-faced Spinetail (Cra-
ni ole in a erythrops) nests in Antioquia, Colombia.
Thick-billed Euphonias (12 -t 1 m. n -= I I encounters)
and Golden-faced Tyiannulcts (10 ± | m. n = 19) at
our study site typically foraged at similar heights as the
Red-faced Spinetail nests they parasitized (9 in for both
nests), consistent with the idea that a klcptoparusile
might steal material from nests in its home stratum to
avoid predation risk associated with descending to the
ground in search of nest material. We encourage
ornithologists to continue reporting instances of nest
material kleptoparasitism so its prevalence in birds can
be rigorously assessed. Received 21 March 2012.
Accepted 18 June 2012.
Nest material kleptoparasitism commonly oc¬
curs among colonially-nesting birds subject to
intense competition for nest materials (Colliasand
Collins 1984. Moreno cl al. 1995). Reports of nest
material kleptoparasitism in solitary breeding
species tire much less frequent. We describe
observations ot Thick-billed Euphonias (Eupho-
nia laniirostris) and a Golden-faced Tyrannulet
(Zimrne tins chrysops) kleptoparasitizing nest ma¬
terial from a Red-faced Spinetail (Cranioleuca
cry l/i tops) nest site and discuss the potential
significance of the behavior.
METHODS
Nest material kleptoparasitism has been reporl-
ed for a variety of birds in scattered accounts, yet
the ecological context of the behavior remains
largely untested and speculative. Potential bene¬
fits ol nest material kleptoparasitism to the
parasite may include: ( I ) reduced competition
for a limited supply of nest materials, (2) easier
access to certain rare materials that may otherwise
be inaccessible to the kleptoparasite, (3) reduced
locomotive energy expenditure during nest build¬
ing due to decreased time and distance to nest
materials. (4) increased time available for nest
guarding due to less time spent away from the
nest, (5) reduced predation risk during nest
material gathering in less familiar microhabitats,
and (6) reduced risk of predators or brood
parasites detecting the kleptoparasile’s nest due
to fewer required visits or shorter flights (Ley
et al. 1997, Jones et al. 2007). Possible costs of
kleptoparasitic behavior to the parasite might
mdude: (I) aggressive interactions from the host
during nest defense, and (2) transmission of nest
Parasites (Ley et al. 1997).
'School of Environment and Natural Resources, Old,
Stale University. 210 Kottmnn Hall. 2021 Coffev Ron
Columbus, OH 432 1 0. I IS A. *
2 Corresponding author; e-mail: slager.4@osu.edu
We conducted observations at La Virgen de
Oro shade coffee plantation on the east slope of
the Western Cordillera of the Andes in the mu¬
nicipality ol Tame, sis. Department of Antioquia,
Colombia (05 44 ' 56.8" N. 75 42' 06.5" W;
1.500 m asl). We conducted 15 days of bird
observations from 26 January to 3 February 2011
and Irom 17 to 22 February 2011. systematically
traversing the farm at —500 m/hr. W'e recorded
foraging heights of individual birds upon encoun¬
tering mixed-species flocks. We estimated that
one or two pairs ol Red-faced SpinetaiLs occupied
the study site and that Thick-billed Euphonias
were common and Golden-faced Tvrannulets
were abundant. Nogal (Cordia altiodora) and
guumo (Inga sp.) trees dominated the open and
heterogeneous canopy in this agroforestry system.
A midstory was generally lacking with the
understory dominated by 2-m high coffee shrubs
(Coffea arahica) and a <0.5-m high herbaceous
layet. We measured foraging height. nest height,
and tree height using a Nikon Forestry 550
Hypsometer (Melville. NY, USA).
OBSERVATIONS
We discovered two Red-faced Spinetai Is adding
material to a nest (hereafter Nest A) on the
morning of 30 January 2011. Nest A was 9 m high
at the end ot a low hanging branch, 4 m from the
main H unk ot a 15-m tree. The nest was somewhat
SHORT COMMUNICATIONS
813
tubular, elongated, and messy, composed of dead
plant fibers, some green fern-like material, and at
least one piece of blue plastic ribbon. We
observed a male and female Thick-billed Eu-
phonia both remove nest material from Nest A
and fly off with the material while the Red-faced
Spinetails were out of view.
We observed two Red-faced Spinetails near
Nest A during the morning of 2 February 2011
and saw at least one of the birds enter the nest. We
also discovered an active Golden-laced lyrannu-
let nest within 30 m of Nest A.
We discovered a second Red-faced Spinetail
nest thereafter Nest B) on 20 February 2011 at
0945 hrs COT in the same tree as Nest A and began
a 30-min observation. Nest B was approximately
the same height as Nest A. but was 2 m distant in a
different fork of the same downward-hanging
branch. Nest B was more spherical than Nest A
with an obvious side entrance and long pieces ot
material hanging from the nest. We saw' a Red-
faced Spinetail remove material from Nest A
during the 30-min observation and fly trom sight
with the material. A Red-faced Spinetail was seen
returning from the same direction less than I min
later to Nest B with nesting material. We later
observed a Red-faced Spinetail remove material
from Nest A and bring it directly to Nest B.
We returned to the nest site on 20 February 2011
at 1123 hrs and conducted a 24-min observation
during which we did not detect any Red -laced
Spinetails. We observed a Golden-faccd 1 yrannu-
let perch on or enter Nest B at 1 1 33 hrs ami leave
without any material visible in its bill.
We visited the nest site again on 22 February
2011 at 1027 hrs and conducted a 167-min
observation. We observed at least two Red-laced
•Spinetails between 1027 and 1 124 hrs make lour
visits to Nest A and three visits to Nest B. The
Red-faced Spinetails adjusted the position ol nest
material in both Nest A and Nest B. but we did not
definitively see birds arriving or departing with
nesting material. We observed a Golden-faced
Tyrannulet at 1153 hrs fly 10 Nest B, remove
nesting material with its bill, and depart with the
material. We observed a Red-faced Spinetail at
1221 hrs 11 y to Nest A without material, remove a
piece of material from Nest A. bring that material
to Nest B. reposition some material in Nest B. and
periodically vocalize from inside Nest B until
leaving the nest at 1229 hrs. A Red-laced
Spinetail silently entered Nest B at 1244 hrs.
repositioned nesting material, and left at an
unknown time. We observed a Red-faced Spine¬
tail at 1248 hrs foraging and vocalizing within
30 m of the nest lice. The bird pulled epiphytic
plant material from a tree trunk, brought it to Nest
B. and left at 1250 hrs after repositioning the
material in the nest. A Red-faced Spinetail entered
Nest B at 1251 hrs and repositioned material
inside the nest until leaving the nest at 1257 hrs.
DISCUSSION
Reports of nest material kleptopurasitism in
non-colonial birds arc unevenly distributed across
geographic and phylogenetic space. The behavior
has been reported in the Eastern Hemisphere and
Hawaiian Islands in Meliphagidue, Pardalotidae,
Acanthizidae, Remizidac. Zosteropidae, Dicaei-
dae Fringillidae. and Remizidac (Ashton 1987,
Schleicher et al. 1993, Ley cl al. 1997. Vander-
Werf 1998). There are reports of nest material
kleptoparasitism in North America in Vireonidae.
Polioptilidae. Parulidae. and Icteridae (Jones et al.
2007). Relatively few studies report nest material
kleptoparasitism in neotropical birds despite the
region's high avian diversity: reports of the
behavior are available from Trochilidae (Skutch
1931, Haverschmidt 1952; F. G. Stiles, pers.
comm.), Furnariidae tRcmsen 2003), Tyrannidae
(Smith 1980; F. G. Stiles, pers. comm.), and
Fringillidae (F. G. Stiles, pers. comm.). The
scarcity of literature on nest material kleptopai-
asitism obscures whether such patterns aic
sampling artifacts or true biological phenomena.
Geographic trends in the prevalence of this
behavior may arise from regional differences in
habitat structure, resource availability, or com-
munity-wide life histories, whereas phylogenetic
trends could emerge due to evolutionary conser¬
vatism of nest-building behaviors.
We observed Thick-billed Euphonias and a
Golden-faced Tyrannulet klcptoparasitizing material
from a Red-faced Spinetail nest site. These obser¬
vations to our knowledge represent the first account
of nest material kleptoparasitism by the Golden¬
faced Tvrannulet (Goulding and Martin 2010). Nest
material kleptoparasitism has been reported previ¬
ously in Fringillidae and Tyrannidae, and out
observations are consistent with the possibility this
behavior may be more frequent or widespread in
these families than previously thought.
Nest building is often costly for birds, and
selection might favor construction strategies that
minimize costs of nest building (Gauthier and
Thomas 1993). Nest material kleptoparasitism may
814
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124. No. 4. December 2012
be one such strategy (Nores and Nores 1994. Jones
et al. 2007). Several accounts document kleptopar-
asites obtaining material from a single host nest
repeatedly, suggesting the behavior is not entirely
opportunistic but that kleptoparasites actively seek
out material from host nests, at least once a suitable
host nest has been found (Haverschmidt 1952. Lev¬
el al. 1997. VanderWerf 1998. Jones et al. 2007).
That we observed nest material kleptoparasitism
suggests its benefits outweighed the costs of
potentially aggressive encounters with the host
and possible transmission of nest parasites. Appro¬
priate nesting material seemed abundant near
ground level at the study site, suggesting kleplo-
parasitism was likely not driven by overall scarcity
oi material in the environment. However, birds
often build nests using highly stereotyped move¬
ments and may find only certain pieces of
ostensibly suitable material useful for construction
( Hansel 1 2000). Thus, by taking high quality
construction materials from hosts’ nests, klepto¬
parasites may reduce locomotive energy expendi¬
tures and search time, potentially increasing time
available for nest guarding. The kleptoparasites we
observed transported only a single piece of nest
material each time, suggesting kleptoparasitism did
not reduce predation risk at their own nest by
reducing the number of visits. We noted that
Red-faced Spinetails (8 ± 2 m. mean ± SE, ,, =
10 encounters). Thick-billed Euphonias (12 ±
1 m- n = 11), and Golden-faced Tyrannulets (10
± 1 m. n = 19) at our study site spent much of
their time in the midstory, the same stratum
occupied by the two Red-faced Spinetail nests
(9 m for both nests). This vertical overlap is
consistent with the hypothesis that kleptopara¬
sites reduce predation risk associated with nest
material gathering by stealing material from
existing nests in a familiar forest stratum and
avoiding gathering material from less familiar
strata such as the ground (Jones et al. 2007). We
also observed Red-faced Spinetails re-using
material from the older nest. Given that nest
material recycling carries a risk of transmission
of nest parasites, our observations of nest
material recycling suggest its benefits out¬
weighed its potential costs. Our observations of
nest material kleptoparasitism and re-use were
limited, and we encourage collection of addi¬
tional data that might refine the hypotheses
presented here.
Identifying the exact source of nest material is
often challenging under field conditions, which
makes the prevalence of nest material kleptopar-
asitism in birds difficult to assess. This behavior
may be further under-reported in the literature
because nest material kleptoparasitism is seidom
addressed as a major topic. Others have suggested
that nest material kleptoparasitism might have
important ecological roles such as shaping the
breeding seasons of bird species (VanderWerf
1998). We encourage ornithologists to document
instances ol nest material kleptoparasitism iii the
literature. Video camera studies at bird nests,
especially in the nest building stage, would be
useful for evaluating the prevalence of nest
material kleptoparasitism within a geographic or
phylogenetic comparative framework.
ACKNOWLEDGMENTS
Our observations were possible because ol funding
Provided by the U.S, Fish and Wildlife Service, (he
National Fish and Wildlife Foundation, and (he National
Council lor Air and Stream Improvement for an unreluted
project on Cerulean Warblers (Setop/uiga cerul«l). D. L.
Singer was supported by a Director's Associaleship Award
bom the Ohio Agricultural Research and Development
C enter. We thank J. M. Correa for access to field sites and
U. J. Colorado for logistical help. We thank F. G. Stiles for
sharing observations of nest material kleptoparasitism in
neotropical birds and two anonymous reviewers for helpful
comments on this manuscript.
literature cited
Ashton. ( B. 1987. The breeding of birds in the Aldinga
Scrub Conservation Park. South Australia. Australian
Bird Watcher 12:73-82.
COLLIAS. N. E. AND E. C. Cullias. 1984. Nest building and
biid behavior. Princeton University Press, Princeton.
New Jersey, USA.
Gauthier, m. and d. w. Thomas. 1993. Nest site
selection and cost of nest building by Cliff Swallows
( Hirumlo pyrrhonota). Canadian Journal of Zoology
71:1120-1123.
CiOLLDlNrj. W. AND T. E. Martin. 2010. Breeding biology of
tin. Golden-faced Tyrannulet ( Zimmerius chrysops) in
V cnezuela. Wilson Journal of Ornithology 122:689-098.
Hansi-ll. M. H. 2000. Bird nests and construction
behaviour. Cambridge University Press. Cambridge.
United Kingdom.
Haverschmidt. F. R. |952. Notes on the life history of
■ nui. ilia fimbriata in Surinam. Wilson Bulletin 64:
69-79.
Jonl-s. K. C.. K. L. Roth. K. Islam. P. B. Hamel, and
' Smith III. 2007. Incidence of nest material
kleptoparasitism involving Cerulean Warblers. Wilson
Journal of Ornithology 119:271-275.
Lev. a. J.. d. L. Oliver, and m. B. Williams. 1997. Theft
of nesting material involving honeyeaters (Meliphagi-
dae). Corel la 21:1 19-123.
SHORT COMMUNICATIONS
815
Moreno, J.. J- Bustamante, and J. Vinuela. 1995.
Nest maintenance and stone theft in the Chinstrap
Penguin ( Pygoscelis antarctica). Polar Biology 15:
533-540.
NORFS, A. I. AND M. Nokes. 1994. Nest building and
nesting behavior of the Brown Cacholote. Wilson
Bulletin 106:106-120.
REMSEN.J. V. 2003. Family Furnuriidae (Ovenbirds). Pages
162-239 in Handbook of the birds of the world.
Volume 8. Broadbills to tapaculos (J. del Hoyo. A.
Elliott, and D. A. Christie. Editors). Lynx Editions.
Barcelona. Spain.
Schleicher, B.. F. Valera, and H. Hoi. 1993. The conflict
between nest guarding and mate guarding in Penduline
Tits {Retni; pendulinus). Ethology 95:157 165.
Ski ten. A. F. 19.31. The life history of Rieffer’s
Hummingbird t, Amizilia i:ncatl I meat I) in Panama
and Honduras. Auk 48:481 -500.
SMITH. N. G. 1980. Some evolutionary, ecological, and
behavioural correlates of communal nesting by birds
with wasps or bees. Proceedings of the International
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Vanderwere. F. A 1998. Breeding biology and territori¬
ality of the Hawaii Creeper. Condor 100*541-545.
The Wilson Journal of Ornithology 1 24<4):8 1 5 817. 2012
A New Location for the Tody Motmot ( Hylomanes momotula ) in Costa Rica
Thomas K. Stevens1
ABSTRACT.— The Tody Motmot 1 1 Mommies mo¬
motula) has a fragmented range throughout Central
America. 1 present evidence from audio recordings lor a
new location for this species in Costa Rica. Individuals
detected likely represent a previously undiscovered
population in the foothills of the Caribbean Slope ol
die Tilardn Mountains. A small population ol tody
Motmots could easily be overlooked in foothill forests
drained by the Jamaical, San Lorencito, and San
Lorenzo rivers, which are exclusively on private land.
Received 6 January 2012. Accepted 21 May 2012.
The Tody Motmot (Hxlonutnes montotulu) is
uncommon in its fragmented range from the
Isthmus of Tehuantepec to northwest Columbia
(Snow 2001). This species is declining in parts of
its range (Patten et aJ. 2010). and is highly sensitive
lo logging and other forms of forest disturbance
(Parker et al. 1996. Whitman et al. 1998. Tejeda-
Cruz and Sutherland 2004). Strongholds for the
species are most likely ihe Caribbean Slope from
Veracruz to Honduras (Howell and Webb 1995,
Jones 2003) and the Darien region of eastern
Panama (Hilly and Brown 1986. Ridgely and
Gwynne 1989). The Tody Motmot in Costa Rica
is only found in a narrow elevational range (500-
1.000 m) on the Pacific Slope of the Cordillera de
Guanacaste. where it is uncommon and local (Stiles
and Skutch 1989; Fig. 1). There are no recent
records from Nicaragua (Martinez-Sanchez and
School of Geology. Energy, and the Environment. Texas
Christian University, Fort Worth. TX 76109, USA; e-mail.
tkstevens92@gmail.com
Will 2010). and the Guanacaste birds may represent
the only known population between Honduras and
Veraguas. Panama (Ridgley and Gwynne 1989.
Stiles and Skutch 1989. Howell and Webb 1995).
OBSERVATIONS
1 detected the Tody Motmot in March 201 1 at
l he Texas Christian University San Ramon
Tropical Research Station (10 15.12’ N, 84
33 3i ' W; Fig. 1 ). The station is on the Caribbean
Slope of the Tilardn Mountains (550-750 m asl)
in the transition zone between tropical wet forest
and premontane rainforest (Holdridge 1967). 1
recorded Tody Motmot vocalizations on 17 and
18 March 201 1 between 0600 and 0800 hrs CST
in mature primary forest (hUp;//www.xeno-canto.
ore/89088; Fig. 2). All vocalizations were repeat¬
ed" single calls at intervals of -1.25 sec, referred
to by Jones (2003) as a loud, penetrating, hollow
whoop'. Calling was continuous for up to 5 min at
a time, and I only noted calls early in morning
after dawn. A field assistant and I obtained
recordings on the morning of 18 March from
locations -700 m apart at similar times; indicat¬
ing that more than one individual was present.
Buff-fronted Quail-Dove ( Geotrygon costari-
censis ). the species most likely lo be contused
with the Tody Motmot based on vocalization, has
a minimum elevational range of 1 .000 m and has
not been recorded at this location. Other species
known from this site with similar vocalizations
( Gkntcidium g rise ice ps. Micrastur sp„ and Tro-
gon sp.) can all be distinguished from the Tody
816
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124. No. 4. December 2012
Motmot by differences in the pitch and or speed o
the repeated single calls.
DISCUSSION
Motmots have short rounded wings and do noi
make long distance migrations. The Tody Motmot
has not been recorded performing movements
or migrations of any kind (Snow 2001). Mv
recordings were ohtained ~65 km from the
nearest known location for the Tody Motmot.
the Pacific Slope of Tenoria Volcano. It j.s
unlikely the individuals present were vagrants
trom the Guanacaste population, which is on the
opposite slope of Costa Rica's continuous moun¬
tainous spine. It is more likely these individuals
represent a previously undiscovered population of
Tody Motmots. Foothill forests at elevations
between 400 and 900 m drained by the Jamaica!
San Lorencito. and San Lorenzo rivers are private-
l,argely i,,accessible lo ornithologists
and birdwatchers. Large tracts of unexplored
P unary forest could support a previously undis¬
covered population of Tody Motmots. Foothill
forests on the Caribbean Slope of the Til arm
Childrens fr ‘he M,,"evcrfc •*»»» Elena,
h" , - Internaljonul Ruinforesl. and Alberto
of hiahh TnrS RCSerVe C°rapk'x (40-™ ha
Of highland forestj are currently unprotected.
Disturbances or land use changes in this area
would jeopardize a population of Tody Motmots.
Pristine foothill forests are rare in the Neotropics
(Stot/ et al. 1996), and further study is needed to
assess the conservation value of foothill forests on
the C aribbean Slope of the Tilaran Mountains and
populations of Tody Motmots within these forests.
AC KNO W LEDG MENTS
I iliank E. S. Hatchett. D. K. Stevens, and H. C. King for
(heir excellent assistance in the field. I also thank Gustavo
Orozco and Katherine for their gracious hospitality at (he
research Mahon. The members of xeno-canto.org. especially
• . I anc. Patrick O'Donnel. Scott Olmstend. and Jay
VanderGaust assisted in identification of Tody Motmot
votalizaiions. This manuscript was improved by sugees-
hons from D. A. Williams, M. A- Patten. C E. Braun, and
an anonymous reviewer. Funding for this research was
provided by the ECU Institute for Environmental Studies
and fCL Graduate Studies.
literature cited
flu I V, S. L. AND W. L. Brown. 19X6. A guide to the birds
ol Columbia. Princeton University Press. Princeton.
New Jersey, USA.
Hoi.drjdge, L. R, 1967. Life zone ecology. Tropical
Science Center, San Jose, Costa Rica.
H<)Wr';l~ S N- G AN& S. Wkbb. 1995. A guide to the birds
ol Mexico and nonhem Central America. Oxford
University Press. Oxford. United Kingdom.
SHORT COMMUNICATIONS
817
(A)
11.0
kHz
8.2
5.5
2.7
*-
(B)
I7o~s 2 Jo s 3 Jo S 4.0 s 5.0 s
6 Jo s
7.0 S 8.0 S
11.0
kHz
8.2
5.5
2.7
<* i
1.0 s
FIG. 2. Sonogram of Tody Mo, mo, calls from (he TCU Tropical Research Station (A: calls of
an individual from the Guanacaste population in Cosla Rica (B; xeno-canto 7 1982. records. Andrew Spen ).
Jones. H. L. 2003. Birds of Belize. University of Texas
Press. Austin. USA.
Martinez-Sanchez, J, C. and T. Will (Editors). 2010.
Thomas R. Howell' s check list of the birds of Nicaragua
as of 1993. Ornithological Monographs 68. American
OmithologisLs’ Union. Washington. D C.. USA.
Parker ill. r. A., D. F. Sror/. and J. W. Fitzpatrick.
19%. Ecological and distributional databases. Pages
1 1 3—436 in Neotropical birds, ecology and conserva¬
tion (D. F. Slot/, .1. W. Fitzpatrick. T.A. Parker 111.
and D. K. Moskovils. Editors). University of Chicago
Press. Chicago. Illinois. USA.
Patitn, M. A.. H. Gomez pf: Silva, and B. D. Smith-
Patten. 2010. Long-term changes in the bird commu¬
nity of Palenque. Chiapas, in response to rainforest loss.
Biodiversity and Conservation 19:21-36.
Ridgfly. R. S. and J. a. Gwynnf. Jk. 1989. A guide to the
birds of Panama. Princeton University Press. Prince¬
ton, New Jersey. USA.
Ridc.ely. R. S.. T. F- AllNLTT. T. BWX)KS, D. K.
McNicol. D. W. Mi iilman. B. E. Young, and J. R.
Zook. 2007. Digital distribution maps of the birds ol
the Western Hemisphere. Version 3.0. NalureServc,
Arlington. Virginia. USA.
Snow. D. W. 2001. Family Momotidae (motmots). Pages
264-285 in Handbook of the birds of the world.
Volume 6. Mousebirds to hombilLs (.1. del Hoyo. A.
Elliott, and J. Sargatal, Editors). Lynx Editions.
Barcelona, Spain.
Stii i s. F- G. and A. F. SKUTC'H. 1989. A guide to the birds
of Costa Rica. Cornell University Press. Ithaca. New
York, USA.
Stotz. D. F.. J. W. Fitzpatrick. T. A. Parker 111. and
D. K. Moskovytn (Editors). 1996. Neotropical birds:
ecology and conservation. University of Chicago
Press, Chicago, Illinois, USA.
Tejf.da-Cruz. C. and W. J. Sutherland. 2004. Bird
response to shade coffee production. Animal Conser¬
vation 7:169-179.
Whitman, A. A.. J. M. Hagan HI. and N. V. L. Brokaw.
1998. Effects of selection logging on birds in northern
Belize. Biotropiea 30:449-457.
818
THE WILSON JOURNAL OF ORNITHOLOGY • Vo l 124. No. 4. December 2012
The Wilson Journal of Ornithology 124(4):8 18-820. 2012
Unusual Foraging Tactics by a Red-tailed Hawk in an Urban Environment
Renn Tumlison1
ABSTRACT. — Red-tailed Hawks ( Buteo jatnaicen-
sis) usually hunt from a perch and swoop down on prey.
I observed a novel foraging strategy in which the bird
deliberately, and successfully, attacked and deconstruct¬
ed nests of squirrels to flush or capture prey in an urban
environment. Received 9 March 2012. Accented 5 lime
2012.
five occasions. The corridor was lined by 21 mast-
Red-tailed Hawks ( Buteo januticensis) lend lo
be sit-and-wait predators, selecting perch sites
with less cover which may increase vulnerability
of prey (Leyhe and Ritchison 2004). Distribution
of the Red-tailed Hawk in central Arkansas
appears to be a response to availability of perches
and prey biomass (Preston 1990). Red tailed
Hawks are opportunistic predators that usually
prey on rodents including gray squirrels (. Scinnts
caroUnensis), small birds, and reptiles, but have
developed strategies to capture large birds, bats,
and insects by foraging in atypical habitats
(Murphy 1994. Jehl 2004. Preston and Beane
2009). I observed an unusual situation in which a
Red-tailed Hawk became habituated to people,
thereby altering typical life history traits (Ditchk-
off et al. 2006) to exploit the locally abundant
resource of gray squirrels.
1 observed an adult Eastern Red-tailed Hawk
foraging on the campus of Henderson State
University. Arkadelphia, Clark County. Arkansas
during October 2011 to March 2012. This bird
allowed close proximity with little apparent
concern. On two occasions. I was able to
photograph the bird from a distance of ~5 m.
Many students were able to watch this bird perch,
and occasionally pursue gray squirrels into their
leaf and stick nests. The objective of this paper is to
report the first observations of an aggressive new
foraging strategy used by this species of hawk.
OBSERVATIONS
I observed hunting behavior of a Red-tailed
Hawk in a landscaped corridor (120 X 30 m) on
'Department of Biology. Henderson State University
Arkadelphia. AR 71999, USA; e-mail: tumlison@hsu.edu
producing water oaks ( Quercus nigra) and two
mature loblolly pines ( Pinas taeda). Multiple
upright stems that grew after earlier pruning of the
oaks created several sites apparently preferred by
squirrels for construction of leaf and stick nests.
Twenty-five leal and stick nests were present, and
some trees also had multiple cavities in which a
squirrel could find shelter.
1 witnessed a Red-tailed Hawk chasing gray
squirrels by running along limbs of a laree pine on
25 October 2011 at -0900 firs CST. A flushed
squirrel ran into a cavity in the tree, and the hawk
perched over the hole and repeatedly (but
unsuccessfully) used its beak to probe the hole
in attempts to reach the squirrel. Within about
5 min, the hawk moved back along the limbs and
positioned itself on top of a leaf and stick nest.
Alter surveying the area for activity of squirrels,
the hawk then used its talons to shake the nest in
an apparent attempt to force any occupants to flee.
flic hawk perched in an oak between two nests
on 28 November 201 1 at —1215 hrs in the typical
upright position for surveying the foraging area.
Upon witnessing a squirrel move in a nearby oak.
the hawk assumed the pre-flight horizontal
posture, waited until the alerted squirrel ran into
its nest shelter, then flew- to the tree, landing
0.5- 1.0 m above the nest. The hawk walked
down the upright branches to the top of the nest,
positioned itself, and used its talons to tear the
nest apart. Falling leaves and small branches tom
liom the nest were enough to get the attention of
unaware students passing underneath the trees, but
t ie nest was substantial enough that the hawk
could not tear it completely apart, and the squirrel
did not exit the nest.
I observed the hawk again at 0830 hrs on 29
ovember 2011. ft landed in one oak and began
wa king down the limb Unvard a nest, flushing a
squirrel that scampered from the nest and down
a hmb- JumPing to another tree, the squirrel
s ie teied in a dense cluster of small branches and
remained there for several minutes with the hawk
remaining in its position watching the squirrel.
Jhe squirrel eventually ran up the limb to a leaf
SHORT COMMUNICATIONS
819
nest in that tree, whereupon the hawk flew to a
perch above the nest and climbed down the
upnght limbs to the nest. While the view of the
hawk was obscured by the nest, a squirrel exited
and ran down the tree, entering a cavity. The
hawk, having positioned itself on top of the nest,
began pulling the nest apart and a second squirrel
escaped behind the hawk. The hawk became
aware of this squirrel and w atched it run down the
tree, but it did not attempt capture. This squirrel
remained on the tree, but hid from sight on the
apposite side of the tree. The hawk returned to
decoastructing the nest until the nest was largely
tom apart and the hawk departed.
On the same day. at — 1630 hrs. the haw k returned
to the same oak. Less interest was show n in nests
(which had already been tom apart), but attention
was focused on the many cavities ol the old tree.
Tire Red-tailed Hawk hopped among branches as it
sought cavities that might afford refuge for squirrels.
Each of five cavities sufficiently large to shelter a
squirrel was probed by the bird's beak. In the case ol
a laterally positioned larger cavity, the hawk grasped
the edge with its talons while beating its wings to
maintain position and probing the opening with its
beak. These actions were search phase and not in
response to a visible squirrel.
The hawk again was observed tearing apart a
nest with no effect on 2 March 2012 at 1415 hrs.
The hawk flew to two other nests and behaved in
the same manner. However, at the latter site the
hawk reached into the nest, pulled out an adult
squirrel, and quickly threw it directly to the
concrete sidewalk (—10 m below). The squirrel
hit the ground solidly and was immobile, and the
hawk swooped down to the prey and secured it.
After looking about for —1.5 min. the hawk flew
to a limb and began to consume the prey.
After the trees had grown leaves, 1 again
observed the hawk tearing apart a squirrel nest
on 30 March 2012 at 1310 hrs. A squirrel emerged
and tied down the limb as three American Crows
( Corvus brachvrhynchos ) and one Northern
Mockingbird (Mimus polyglottos) arrived and
mobbed the hawk, causing the hawk to fly
without pursuit of the squirrel. The mobbing
behavior, not witnessed during the winter, may
have been related to the recent arrival and
development of territories by the birds.
people (i.e., synurbanized; Gliwicz et al. 1994,
Warren et al. 2006, Parker and Nilon 2008) and were
approachable to within 5-6 in. The elusive nature
more typical of gray squirrels was thought to
explain their low occurrence in the diet of Red¬
tailed Hawks in California (Fitch et al. 1946).
Tree squirrels have been captured through
cooperative hunting by mated pairs of Red-tailed
Hawks, when the two hawks guard opposite
sides of a tree and work together (Bent 1937).
My observation appears to be the first docu¬
mented case of this aggressive behavioral adjust¬
ment by a Red-tailed Hawk to a localized and
abundant urban prey source, as predators are
expected to hunt in profitable areas (Wakeley
1978). Squirrels were the only available prey in
the area, and the foraging strategy I witnessed
was focused on them. Rather than waiting to
locale prey, the hawk at times actively attempted
to flush, or capture, prey from their refuges. Leaf
and slick nests usually were reconstructed by
squirrels after an unsuccessful attack. The hawk
had habituated to the presence of humans, but
most (not all) of the observed foraging activity
occurred in early morning or late afternoon when
fewer students were on campus.
The Red-tailed Hawk was seen 12 times using
nest destruction as a technique of attempting to
access prey. The hawk was observed on two other
occasions in active search by repetitive examina¬
tion of eight cavities (2 in a pine. 6 in oaks).
Predation attempts regarding nests in this study
were not always initiated after location of prey
from perches, which typically are used tot
observations before a ground attack (Orde and
Harrell 1977, Preston 1990. Leyhc and Ritchison
2004). I witnessed successful capture ol three
squirrels, on 23 August 2011. 30 January 2012, and
2 March 2012, but the hawk was already on the
ground with the first two kills when observed and
the hunting strategy used could not be ascertained.
The 2 March 2012 observation conclusively
documented the direct success of the nest-attack
strategy. The successful strategy increases the
search area actively used by a solitary Red-tailed
Hawk to the canopy layer, and does not require 'sit-
and-wait' predation from a perch.
discussion
Numerous gray squirrels on the campus of
Henderson State University were habituated to
ACKNOWLEDGMENTS
I thank W. E. Stoul and an anonymous reviewer for
helpful comments on the manuscript, and T. G. Finley and
S. L. Russell for alerting me to the presence of the hawk on
some important occasions.
820
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124. No. 4. December 2012
LITERATURE CITED
Bent. a. C. 1937. Life histories of North American birds of
prey. Part i. U.S. National Museum Bulletin 167.
DrrctiKOFF. S. S.. S. T. Saalfeld, and C. J. Gibson. 2006.
Animal hehavior in urban ecosystems: modifications due
to human-induced stress. Urban Ecosystems 9:5-12.
Fitch. H. S., F. Swenson, and D. F. Tillotson. iy46.
Behavior and food habits of the Red-tailed Hawk.
Condor 48:205-237.
Guwiry. .1.. J. Goszczynski, and M. Luniak. 1994.
Characteristic features of animal populations under
synurbizaiion-the case of the Blackbird and the striped
field mouse. Memorabilia Zoologica 49:237 244.
Jehi. Jit.. J. R. 2004. Foraging by a Red-tailed Hawk along
a wetland edge: how large a duck can he captured?
Wilson Bulletin 1 16:354-356.
Leyhe, J. E, .and G. RrrCHISON. 2004. Perch sites and
hunting behavior of Kcd-lailed Hawks (Buteo jamai
censis). Journal of Raptor Research 38:19-25.
Murphy. R. K. 1994, Observations of Red-tailed Hawks
capturing w'ild ducks in North Dakota. Prairie Natu¬
ralist 26:313-314.
Orde, C. J. and B. E- Harrell. 1977. Hunting techniques
and predatory efficiency of nesting Red-tailed Hawks.
Journal of Raptor Research 11:82-85
Parker. T. S. and C. H. Nilon. 2008. Gray squirrel
density, habitat suitability, and behavior in urban
parks. Urban Ecosystems I 1:243-255.
PRES ion. C R. 1990. Distribution ol raptor foraging in
relation to prey biomass and habitat structure. Condor
92:107-112.
PRE.SWN. C. R. and R. D. Beane, 2009. Red-tailed HaWklfiww
jamaicensis), The birds of North America. Number 52.
Wakeley. J. S. I97S. Hunting methods and factors affecting
their use by Ferruginous Hawks. Condor 80:327-
333.
Warren. P., C. Tripi.kr, D. Boloek. S. Faeth. N. Huntly
C. Lepczyk. J. Meyer. T. Parker. E. Shocat. anpJ.
Walker. 2(M)6. Urban I'ood webs: predators, prey, and
die people who feed them. Bulletin of the Ecological
Society of America 87:387-393.
The Wilson Journal of Ornithology 1 24(4):820-824, 2012
WintD M|crohabltat Foraging Preferences of Sympatric Boreal and
Black-capped chickadees in Michigan’s Upper Peninsula
Zach G. Gayk1-2,3 and Alec R. Lindsay1 2
ABSTRACT.— We examined differences in microhab-
itat use between Boreal (Poeeile hiuisonicus ) and Black-
capped chickadees (P atricapillus ) where they co-occur near
Marquette. Michigan. USA. Twenty-four Boreal and 37
Black -capped chickadees were followed during 60 hrs of
field observation. Boreal Chickadees foraged only in three
conifer species. 76% of which were black spntce (Picea
mariana). while Black-capped Chickadees foraged widely
across six coniferous and three deciduous tree species.
Analysis of foraging data categorized by zones within
conifer trees indicated high niche overlap (0.676) between
Boreal and Black-capped chickadees across all foraging
zones. Individual comparisons on a zone-by-zone basis
revealed a significant difference in foraging occupancy in the
medial portion ol the crowns of conifer trees IP = ().(XX)2)
Our results indicate exclusive use by Boreal Chickadees of
den.se medial foliage within the top 3 m of conifer crowns
Received 22 March 2012. Accepted 3/ July 2012
1 Department ol Biology, Northern Michigan University.
University. 1401 Presque Isle Avenue. Marquette, Ml 49855.
2 Current address: Zoology and Physiology Department.
WYV8207,i°USA°min^ University Avenue, Laramie.
Corresponding author; e-mail: zgayk@sbcglobaI.net
Niche partitioning in birds has been widely
reported between species with similar morpholog¬
ical lealures, body sizes, and diets (Mac Arthur 1958.
Reynolds and Meslow 1984). or between males and
females ol the same species that have divergent
foraging strategies (Williams 1980. Radford and du
Rlessis 2003). Two congeneric species. Black-
capped and Boreal chickadees ( Poeeile spp.). often
loiuge together in mixed-species flocks within
boteal lorcsts ol Upper Michigan during winter.
Black-capped Chickadees (P. atricapillus ) are
abundant winter residents across a w ide spectrum
of Forested and scrub habitats, but Boreal Chicka¬
dees ( P . hudsoniem) are rare residents within
160 km ol their southern range boundary, they
(Kvut in lowland black spruce ( Picea manana )
forests which are localized within the predominantly
deciduous forest matrix of this region (Binford
2006). All members of the genus Poeeile have
similar food habits and body sizes, and forage for
arboreal insect larvae and seeds. Dhondt (1989)
concluded that non-overlapping distributions of
North American chickadees indicated either range
replacement (allopatry) or habitat partitioning, to
SHORT COMMUNICATIONS
821
avoid competition with closely related species.
Similar conclusions were noted by Alutalo et al.
1 1987) in Finland, based on elimination experiments
in winter Hocks.
Niche partitioning between Boreal and Black-
capped chickadees has not been studied during
winter, a period in which both species are in
greatest contact. Descriptive (Stewart and Aldrich
1952) or summer accounts (Vassallo and Rice
1982) suggest Black-capped Chickadees more
frequently occupy deciduous and less dense
forests, usually at lower heights within trees,
while Boreal Chickadees exploit regions of dense
conifer foliage most commonly in spruce crowns.
We investigated microhabitat partitioning in
mixed-species chickadee Hocks within boreal
forests at a McCormick Wilderness Area study
site in western Marquette County. Michigan, USA
in January-March 2011. We predicted the more
abundant Black-capped Chickadee might restrict
rarer Boreal Chickadees to confined regions ot
microhabitats.
METHODS
Study Area— Five primary study locations near
the McCormick Wilderness Area (centered at 4b
38' 39.04" N. 88 02' 40.87" W) were identified as
quality Boreal Chickadee habitat based on habitat
descriptions from Evers (1991) and lliekman
1201 1). and secondarily through analysis of aerial
photographs. Black-capped Chickadees also occur
in this urea and regularly use these habitats lor
nesting and foraging. The habitat consisted ot
mature boreal forest patches ranging from 1 .7 knr
in size to smaller, narrow belts of 0.35 knr. and
isolated boreal islands that were only 0.1 km in
size within a maple-yellow birch [Acer spp .-Helnla
alleghaniensis) matrix. All boreal lores! patches
were close to the Peshekec River or to Baraga
Creek, often forming narrow bands of boreal
habitat along streams. Tree species in the boreal
patches in decreasing order of estimated domi¬
nance were: black spruce, white spruce ( Picea
Klauca), tamarack (Liirix laricina). balsam Mr
{Abies huhamea), white birch {Be tala papyrifera).
white pine ( Piiuts strohus ), red maple (Acer
mbrum ), quaking aspen ( Populus tremuloides ),
white cedar ( Thuja occidentalis). and jack pine
( Finns banksiuna).
Data Collection. — Observers systematically
searched the study sites for chickadee flocks on
6 days between 24 January and 13 March 2011.
Flock size, species composition, general flock
location, and time of observation were recorded
once a Hock with chickadees was located.
Individual observers focused on one individual
chickadee of either species for as long as possible
(but <10 min) for each Hock. The lice species in
which a bird was foraging and estimated height of
tree were recorded. Observers visually divided
each tree used for foraging into zones by estimating
3-m vertical areas (c.g.. 21-m tree = 7 zones) that
each contained three horizontal /ones (basal,
medial, distal) per 3-m vertical zone. Observers
recorded the number of seconds using stop-watches
that a focal chickadee foraged in different zones of
the tree. Shifts to new zone positions and trees were
recorded as discrete observations. 1 iming stopped
when the focal chickadee stopped foraging. The
number of foraging observations within zones was
recorded per individual chickadee followed to
ascertain each bird's contribution to the data set.
Zones used to segregate chickadee foraging to a
specific location within trees were numbered from
tree crowns to the tree base following MacArthur
( 1958). Trees were numbered from the top so those
of varying height could be compared on a zone-by¬
zone basis while retaining as much similarity in
vegetation structure. Chickadees loraging in tiees
<10 m in height were not used in the data analysis.
Statistical Analysis.— We analyzed differences
between Boreal and Black-cuppcd chickadee
foraging time in nine tree species where chicka¬
dees were observed foraging. Chickadee Imaging
time in each tree species was scaled to the total
number of seconds chickadees were observed
foraging by species throughout the study, and the
total number of individuals observed. The numbei
of individual chickadees observed per species was
estimated from detailed records ot I lock locations.
Totals were based on the maximum number of
each species recorded each day plus addition ol
individuals recorded on subsequent days that were
>8 km from previous observations.
Differences in foraging zone occupancy between
Boreal and Black-capped chickadees within trees
in each of 21 zones were evaluated (unpaired t-
tests) with Bonferroni correction of the alplta-v alue
to account for repeated tests (Cabin and Mitchell
20(X)). We calculated niche overlap between Boreal
and Black-capped chickadees based on foraging
zone data using EcoSim 7.0 (Gotelli and Entsminger
2001 ) to evaluate the likelihood of niche overlap.
Each null model calculated niche overlap with
different assumptions about the specialization ol the
species compared based on Pianka s index (Pianka
822
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124. No. 4. December 2012
1974). The software generates upper and lower P-
values based on the number of observed niche
overlaps greater or less than the mean niche overlap
generated by random simulations. Model RA2
relaxes niche breadth from observed niche overlap
by assigning a random number for use, but retains
the resource stales where use was zero. Model RA3
retains the exact use in the original data, but
reshuffles the distribution of zeros. We also
analyzed foraging data using model RA4. which
retains both the use and zero distributions as in the
original data. Model RA4 reshuffles only the
distribution of each use within cells. This model
has the most stringent assumptions to satisfy and
may cause Type II error (Gotelli and Entsminger
2001 ). We reanalyzed evidence for niche overlap by
combining all horizontal zones using EeoSitn to
simulate niche overlap and eliminate arbitrary
distinctions imposed by the zoning system.
RESULTS
We observed chickadees on 6 days between 24
January and 13 March, totaling 60 hrs of field
observation time. This amounted to 1,875 and
1,074 seconds of timing foraging of Boreal and
Black-capped chickadee zone use, respectively.
Foraging zone data were recorded for 24 Boreal and
37 Black-capped chickadees that were in 20 different
flocks containing Black-capped Chickadees and 15
flocks containing Boreal Chickadees. This resulted in
72 (56.2%) Boreal and 56 (43.8%) Black-capped
chickadee zone observations. Data were drawn from
eight observations and 178 sec of individual chicka¬
dees within Boreal Chickadee flocks, 28 observations
and 484 sec within Black-capped Chickadee flocks,
and 92 observations mid 2.293 sec within mixed
flocks containing both species.
Microhabitat Use.— Boreal Chickadees foraged
in only three conifer tree species with 76% of total
foraging in black spruce. Black-capped Chicka¬
dees foraged widely across six conifer and three
deciduous tree species. Boreal Chickadees spent
36.5% of the total observation time in the top
vertical zone (zone I ) of trees when foraging,
while Black-capped Chickadees spent only 4.5%
°f the observation time in Ihis vertical zone
(Table I ). There was no significant difference in
foraging time between species in zone I when
alpha values were Bon ferroni -corrected (P ~
0 04 alpha = 0.0045). Neither Black-capped
(4.1% occupancy) nor Boreal (1.6% occupancy)
chickadees spent much time in the zones nearest
the ground (zones 5-6) (Table I). Boreal and
Black-capped chickadee foraging time was sim¬
ilar in zone 2 (P = 0.19) for 34.36 and 38.05% of
total observation time, respectively, largely in the
medial horizontal zone (2 medial). Foraging time
was similar tor both species in horizontal zones
with Boreal Chickadees spending less time in the
basal zone. Differences in foraging time between
chickadee species were significant only in the
medial portion of zone I (P - 0.0002).
Niche Breadth Analysis. — The observed niche
overlap was larger than expected (simulated) in all
three models assessed (Table 2). The observed
mean niche overlap was significantly greater than
expected by chance and observed niche breadth
was greater than simulated niche breadth in all
trials when foraging occupancy was reanalyzed
with broader zone use.
DISCUSSION
Use of black spruce, white spruce, and tamarack
(in decreasing order) suggests Boreal Chickadees
may prefer the highest quality boreal habitats of the
region (Evers 1991). This minimizes competition
with Black-capped Chickadees which preferentially
use the more common deciduous and mixed forests
(Grubb and Bronson 2001. Foote et al. 2010). A
more open branch structure and dispersed tree¬
spacing in deciduous forests appears to offer Boreal
C hickadees less-desirable habitat. Few data exist on
interspecific interactions between Boreal and Black-
capped chickadees, but Black-capped Chickadees
may be socially dominant to Boreal Chickadees in
congeneric winter flocks and limit Boreal Chickadee
foraging outside of high-density conifer regions.
Minimal differences in foraging microhabitaifl of
21 zones) arc shown in the medial region of dense
foliage within the top () to 3 m of conifer crowns. The
upper regions of spruce trees often contain the
densest foliage, cone crop, and branch structure on
(he entire tree, which Black-capped Chickadees may
be less able to exploit (Ficken et al. 1 996). This small
spatial area within conifer crowns may be the region
v\heie Boreal Chickadees have a competitive
advantage. Boreal Chickadees in Alaska and New-
loundland. where their habitat is far more common,
apparently forage in a wider range of tree heights,
suggesting ecological release (Haftom 1972. Vas¬
sal lo and Rice 1982).
Flic null model analysis of Boreal and Black-
eapped chickadee zone use indicates high niche
ovci lap (0.676), which is greater than the overlap
predicted to occur by chance alone. Pianka (1974)
and Glasser and Price (1988) prov ide explanations
SHORT COMMUNICATIONS
823
TABLE 1.
Boreal and Black-capped
chickadee foraging time in 21 distinct vertical
and horizontal zone
s corresponding
to spatial foraging position
in trees.
Percent lime per /.one
Vertical zones
Black-capped Chickadee
Basal Medial
Terminal
Vertical /ones
Basal
Medial
Terminal
1
2
3
4
5
6
7
2.42
1.77
10.88
2.51
0.00
2.79
0.00
0.74
28.65
6.51
20.19
0.00
0.93
0.00
1 .30
7.63
13.30
0.00
0.37
0.00
0.00
1
2
3
4
5
6
7
0.80
5.50
1.49
0.00
0.00
0.00
0.00
16.44
22.20
12.97
11.21
0.27
0.00
0.00
19.26
6.67
0.27
1.60
1.33
0.00
0.00
why these species may have more overlap than
predicted by chance: ( 1) Boreal and Black-capped
chickadees use resources that are in sufficient
abundance and each species can overlap spatially
without competing, or (2) these two species are
currently competing for food resources. Both s])ecies
appear to have similar diets, foraging heavily
(>50%) in winter for dormant caterpillars (hetero-
campids), pupae, and insect eggs (Bent 1946,
Haftom 1974. Oatman 1985. Smith 1991). Similar
foraging strategies (Moreno 1990. Ficken el al.
19%), and the general microhabitat used for foraging
support Boreal and Black-capped chickadees ap¬
parent overlap in use of food resources in winter.
Higher niche overlap was lound in our study than
in that conducted on Boreal and Black-capped
chickadee partitioning during summer (Vassallo and
Rice 1982). This may indicate foraging behavior
and extent of niche overlap varies seasonally.
We conclude niche overlap between Boreal anti
Black-capped chickadees its indicated by random
models is likely high. However, the macroscale
region within Black-capped Chickadee habitats
where niche overlap occurs is small as indicated
by: ( I ) Boreal Chickadees use of localized boreal
TABLE 2. Observed versus expected mean niche
overlap based on three null randomization algorithms
which use Pianka's index. Lower and upper probabilities
indicate the observed niche overlap is either less than or
greater than expected by chance (in the null model),
respectively.
forest regions, and (2) foraging overlap with Black-
capped Chickadees in only three conifer species.
Boreal Chickadees used the dense medially-located
foliage of conifer crowns significantly more than
Black-capped Chickadees. This may indicate dif¬
ferential resource use. hut further research is needed.
ACKNOWLEDGMENTS
We thank Joseph Youngman. Will Lewis, and Skye Haas
for field assistance, the NMU Department of Biology tor
supplies and equipment, and Scott Hickman. Alan Rebertus,
and Susan Fawcett for comments on the study design and
manuscript.
Model
Mean niche overlap
Probability
Observed
Expected
Lower
Upper
RA2
0.676
0.617
0.719
0.281
RA3
0.676
0.306
0.978
0.022
RA4
0.676
0.379
0.964
0.036
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Larsson. 1987. Exploitation competition influences
the use of foraging sites by tits: experimental evidence.
Ecology 68:284-290.
Bi-NT A C 1946. Life histories of North American jays,
croWS, and titmice. U.S- National Museum Bulletin
191. „ . ,
BiNr-ORD. L C. 2006. Birds of the Keweenaw Peninsula.
Michigan. Miscellaneous Publication 195. Museum ol
Zoology University of Michigan. Ann Arbor. USA.
Cabin, R. L and R. J. MITCHELL. 2000. To Bonferroni or
not to Bonferroni: when and how are the questions.
Bulletin of the Ecological Society of North America
81:246-248.
Dhondt. A. A. 1989. Ecological and evolutionary effects of
interspecific competition in tits. Wilson Bulletin
101:198-216.
Evers. D. C. 1991. Boreal Chickadee ( Poecile hudsonicus).
Pages 322-323 in The atlas of breeding birds of
Michigan (R. Brewer. G. A. McPeek. and R. J. Adams).
Michigan State University Press. East Lansing. USA.
Ficken, M. S.. M. A. McLaren, and J. P. Mailman. 1996.
Boreal Chickadee < Poecile hwbonicas). The birds of
North America. Number 254.
Foote. J. R.. D. J. Menniel. L. M. Ratcliffe. and S. M.
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Smith. 2010. Black-capped Chickadee (Poecile atri-
capillus). The birds of North America Number 39.
GlASSER, J. W. and H. J. Price. 1988. Evaluating
expectations deduced from explicit hypotheses about
mechanisms of competition. Oikos 51:57 70.
Goteuj. N. .1. AND G. L. Entsminger. 200). EcoSim: null
models software for ecology. Version 7.0. Acquired
Intelligence Inc. and Kesey-Bear. Jericho. Vennont. USA.
http://homepages.together.nel/~gcntsmin/ecosim.hlm
Grubb. 1. c. and C. L. Bronson. 2001. On cognitive
conservation biology; why chickadees leave a patch of
woodland. Journal of Avian Biology 32:372-376.
Haitokn, S. 1974. Storage of surplus food by the Boreal
Chickadee Pams hmkotriens in Alaska, with some
records on the Mountain Chickadee Pams yumhcli in
Colorado. Ornis Scan.liuuvica 5:145-161.
Hickman, S. C. 20Jl. Boreal Chickadee ( Poecile hudso-
tiictix). Pages not numbered in The second Michigan
breeding bird atlas (A T. Chartier. I J. Baldy, and J.
M. Brcnneman, Editors I. Kalamazoo Nature Center,
Kalania/oo, Michigan. USA. http://www.rnihirdullas.
org/MichiganBreedingBirdAtlasII/TaxonomicListing.
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MacArthur, R. H. 1958. Population ecology of some
warblers of northeastern coniferous forests. Ecology
39:599-619.
Moreno, E. 1990. The musculi flexor perforatus digiti Hand
flexor digitorum longus in Paridae. Condor 92:634-638.
Oatman, G. F. 1985. Boreal Chickadee. Pages 2 1 2-2 1 3 in
The atlas of breeding birds of Vermont IS. B. Laughlin
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England. Hanover. New Hampshire. USA.
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during breeding. Auk 101:761-779.
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Stewart, R. E. and J W. Aldrich. 1952. Ecological
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Vassallo, M. I. AND J. C. Rice. 1982. Ecological release
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The Wilson Journal of Ornithology 1 24(4):825 826, 2012
William and Nancy Klamm Service Award for 2012:
Doris J. Watt
The Wilson Ornithological Society (WOS) has
recognized outstanding commitment to the society
through the William and Nancy Klamm Service
Award since 2007. This honor was established to
acknowledge the history of service and dedication
to the society shown by the Klamms. Both of the
Klamms regularly attended Wilson meetings, Bill
served as Treasurer from 1068 to 1973, and both
served on the Auditing Committee during the
1970s and 1980s. The Klamms’ commitment to
the society later included a considerable bequest
that substantially increased the endowment and
continues to help support the activities of the
Wilson Society. However, for any professional
society to flourish, numerous individuals must
contribute their time, energy, and expertise. This
year, we are pleased to recognize the work ot
someone who attended her first Wilson meeting in
1973 while Bill Klamm served as Treasurer and
who has also served as WOS Treasurer.
Doris J. Watt attended her first Wilson Society
meeting as a graduate student at the University of
Arkansas. At that meeting, she co-authored a paper
with her advisor Douglas A. James about some ot
her Masters’ thesis research comparing foraging
techniques by Tufted Titmice ( Baeolophus bicolor)
and Carolina Chickadees (Poecile carolinensis).
Three years later she presented work on the role
of polymorphism in dominance relationships of
White -throated Sparrows ( Zonotrichia albicollis).
In 1980. as a Ph.D. candidate working with Gary D.
Schnell at the University of Oklahoma, she
825
826
KLAMM SERVICE AWARD
returned to the annual meeting of the WOS to
present some of her dissertation research on status
signaling in Zonorrichia sparrows.
Doris has shown an unflagging dedication to
the Wilson Ornithological Society Tor more than
two decades. She has volunteered in every
conceivable way to the varied activities of the
society. She hosted the Wilson Society’s annual
meeting in 1989 at St. Mary’s College in Notre
Dame. Indiana, where she has been a professor of
biology since 1982. During that meeting, she was
elected to a three-year term as a councilor. After
two years on Council, she agreed to run for
Treasurer, a position she held for 10 years from
1991 to 2001. Doris was elected Second Vice-
President in 2001 . She served two years as Second
Vice-President from 2001 to 2003, followed by
two years as First Vice-President from 2003 to
2005, and two years as President from 2005 to
2007. Doris, in her roles on Council, chaired the
scientific program committee, the Nice Medal
Committee, the Student Awards Committee, and
served on the steering committee for the 4th North
American Ornithological Conference in Veracruz,
Mexico and was President of WOS during that
meeting. In addition to her formal roles on
Council. Doris has contributed in many other
ways including judging student presentations
numerous years, four years of service on the
Edwards' Prize Committee that chooses the best
paper in the most recent volume of the Wilson
Journal of Ornithology , and stepping in to
moderate sessions as needed. She served as an
editorial assistant from 1998 to 2004 to Wilson
Bulletin Editors Bob Beason and John Smallwood
by reviewing accepted manuscripts for content
and format and proofreading the galleys. She
continues to attend meetings and participate in
council meetings. Doris J. Watt epitomizes the
Klamms’ spirit of service through her continuous,
varied, and substantial work for the Wilson
Ornithological Society.
To honor the recipient of the Klamm Service
Award, the Wilson Ornithological Society
commissions an original painting of a bird that
is important to the recipient. This year's award
is an original watercolor by Julie Zickefoose of
American Goldfinches (Spinus tristrs ), a species
Doris has studied for many years, on which she
has presented papers at Wilson Society meet¬
ings, and on which she has published. We are
grateful to Doris for many years of dedicated
service and arc pleased to honor her this year
with the William and Nancy Klamm Service
Award. — Sara R. Morris (Chair), Richard C,
Banks, Charles R. Blem, Leann Blem, and
Jerome A. Jackson (Klamm Service Award
Committee).
The Wilson Journal of Ornithology 124(4):827-828, 2012
In Memoriam
Pershing Benard “Jack” Hofslund (1918-2012)
Pershing Benard -'Jack" Hofslund was bom 13 April
1918 in Jeffers, Minnesota, and passed away on 21
April 2012 at the age of 94 in Duluth, Minnesota. Jack
began his interest in birds at an early age without
encouragement from others, without instruction, binoc¬
ular; or a field guide. He identified his first birds horn
Ann and Hammer Baking Six la cards and pictures
clipped from magazines and pasted into a pocket
notebook (Pcttingill. O. S„ 1965. Hu- Bin! Watchers
Anthology. McGraw-Hill Book Company. New York.
USA: 378-384). It was not until Ik- was a senior in high
school that he borrowed The Birds of Minnesota by T.
S. Roberts from the local library and read both volumes
from cover to cover in the allotted 10 days.
Jack graduated from high school in Jeffers,
Minnesota (1936) and received his B.S. Degree
from Mankato State Teachers College in Minnesota
( 1940). In 1940 he married Elaine Warner who died
827
in 2009 Many of us observed that Jack was nevet
really the same after Elaine passed away. Jack and
Elaine had a special relationship: the envy of any
married couple. He was absolutely devoted to her.
Jack taught high school in Pcquot Lakes and
Milaca, Minnesota, then served in the Navy
(1945-1946) during World War II. Shortly
thereafter he began his ornithological research
career, receiving an M.S. in 1947 and his Ph.D. in
1954 from the University of Michigan. His
doctoral dissertation, "A Life History Study of
the Yellowthroal," initiated his long interest in
parulid warblers and had a major influence on
countless students, including me. During his
graduate studies, Jack began his career at the
University of Minnesota-Duluth (UMD) in 1949
and retired as a full professor from UMD in 1982.
He then became professor emeritus. Upon retirement.
828
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124. No. 4. December 2012
Jack remained active at the Lakeside Presbyterian
Church and continued to teach in the University for
Seniors and die local chapters of AARP.
Jack Hofshind inspired hundreds of students,
colleagues, and friends with his expertise on birds
and his breadth of know ledge about life. He joined
the Wilson Ornithological Society (WOS) in 1944,
became a life member, and served WOS in several
capacities: elected WOS Council member (1957-
1960), Secretary (1962-1967), Second Vice Pres¬
ident (1968-1969), First Vice President (1969-
1971). and President (1971-1973). He also served
as chair ot the WOS Membership Committee
(1970-1971) and hosted the WOS meeting at
Duluth in 1957. Jack was also active in the
American Ornithologists’ Union (AOU) and was
made an elective member in 1959. He hosted AOU
(1967) and Raptor Research Foundation (1976)
meetings in Duluth. Jack also served as President
of the Minnesota Ornithologists’ Union (MOD)
(1963 to 1965) and as Editor of The Flicker, the
publication that preceded The Loon as the official
journal of the MOU, (1951 to 1958). Jack was
active in the Duluth Audubon Society, the board of
the Lake Superior Zoological Gardens, Duluth
Parks and Recreation, the Board of the Minnesota
State Zoo, and on the Boards of both the Raptor
Research Foundation and the Hawk Migration
Association of North America.
Among Jack’s major accomplishments was
aiding the establishment of Hawk Ridge Nature
Reserve in Duluth. He started the annual hawk
counts in Duluth, published some of the first
scientific articles on Hawk Ridge {The Wilson
Bulletin 78:79-87. 1966), and provided evidence
that Duluth was a major hawk migration route in
the United States. Jack along with many others in
the Duluth area began the long process to educate
the public about the benefit of raptors and the
protection of Hawk Ridge Nature Reserve. He
was recognized for these efforts with a lifetime
achievement award by the Duluth Audubon
Society in 2003.
Jack and Elaine loved traveling. They visited
all 50 slates, many Canadian provinces, and over
50 countries on every continent except Antarctica.
Besides birds. Jack enjoyed movies, bridge, the
Minnesota Twins and Vikings, and reading. Jack
is survived by his son, Jeffrey of Duluth, his
daughter. Jennifer Burla of Iromvood, Michigan,
and five grandchildren.
Jack will be remembered as a kind, loving, and
gentle man with a Hair for dapper dressing. He
encouraged and facilitated the development of
hundreds of students and colleagues during his years
at UMD, Hawk Ridge, and his other professional
activities. His efforts will long be remembered,
especially as one of the founding members of Hawk
Ridge Nature Reserve in Duluth.— GERALD J.
NIEMI, Professor, Department of Biology and
Natural Resources Research Institute, University of
Minnesota-Duluth, 5581 1, USA.
The Wilson Journal of Ornithology 124(4):829-834, 2012
Ornithological Literature
Margaret A. Voss. Book Review Editor
THE FEATHERY TRIBE. By Daniel Lewis.
Yale University Press. New Haven, Connecticut.
USA. 2012: 368 pages. 20 black and white
illustrations. ISBN: 978-0-300-17552-3. $ 49.50
(hardcover).— Science historian Daniel Lewis set
out to write a biography ot Robert Ridgway
(1850-1929), the Smithsonian's first curator ol
birds. Apparently finding that material about Ridg-
way would not fill a book. Lewis used Ridgway to
illustrate the transformation ol ornithology trom
the lyrical, poetic, and artistic study ol birds to
a scientific discipline. The material provided by
Lewis about Ridgway is rather fiat and superficial.
Little about the man's personality or temperament
is given, other than a number of statements about
his nearly crippling shyness. Perhaps this shyness,
combined with the time-intensive production of two
enomious works, a staggering number of papers,
and a small mountain of popular literature, limited
interaction with his colleagues, family, and friends:
little is visible in this book. He apparently did not
commit his thoughts to diaries or an extensive
correspondence. A few mentions of constant
struggle for money constitute the only personal
color. The most significant personal event ot
Ridgway's life-the death of his only son-seemingly
had little impact on Ridgway's daily file and career
trajectory, except perhaps an increase in the alt early
intense focus on work.
For lack of sufficient material about Ridgway.
the book moiphs into an analysis of the develop¬
ment of professional, scientific ornithology m the
second half of the 1 9th century as seen through
the lens of Ridgway. Elliott Coues, Joel Allen,
and the few others who constituted the innet cite c
of the nascent American Ornithologists’ Union.
After the first chapter— the basic outlines of
Ridgway's family, life before the Smithsonian
and into the survey work that ultimately brought
him to the Smithsonian— Ridgway makes scant
appearances until a chapter about bird pub ica
tions that describes, inter alia, the writing ot his
epic Birds of North America, modestly known as
Bulletin 50. The final of the seven chapters
recounts Ridgway's effort to standardize the
colors of birds. That Ridgway’s life and contri¬
butions are secondary is reflected in the title,
which reduces Ridgway to a subtitle and casts him
instead as a member of a 'leathery tribe.
The preface posits (page xv) that Ridgway s
career embodied the transition between the “lei-
surelv and aesthetic-driven pursuit of bird collect¬
ing and the later study of the living bird.' Ridgway
spanned the two eras and the rigorous taxonomic
and nomenclature work of his era formed the
critical bridge, but at least as told here, his life and
work seem isolated from the people and events ol
his profession at that time. The transformation, as
argued repeatedly throughout the book was
demarcated bv the development ol formal schemes
of classification that were accurate and non-
speculative. Uncertainty and re-classification per¬
sisted and new systems of classification emerged,
but Lewis refers to the underpinning of classification
with the Darwinian principle of common descent.
The establishment of authority— recognized sys¬
tems of classification, nomenclature, and proce¬
dure that all would follow— and accountability to
colleagues and institutions also characterized the
new era. Finally, the emergence of a specialized
vocabulary and the use of technical terminology
distinguished the professionals from the broader
group of individuals who observed birds and wiote
about their observations. Ridgway personified a 1
three of these hallmarks. His checklists-^
individually and later as a member of the AOU
committee-together with his exhaustive dassifi-
cation of the birds of North and M.ddle America
exemplified both author ity and the use ot evolu¬
tionary classification. Ridgway's use ot technics
language in Bulletin 50 drew one harsh review that
complained of the obtuse language even as his
colleagues celebrated the technical writing.
An earlier biography of Ridgway (Harris 19-8,
Condor 30:5-118) published during Ridgway s
lifetime also noted that Ridgway was little-known
and avoided the public stage. What is known of
Ridgway's early years appears in both accounts:
born in 1850 to a family in rural Illinois as the
oldest of 10. little formal education, and parents
who had misgivings about their son s intense
focus on birds and the likelihood of actually
building a career on this obsession. Ridgway’s
father inadvertently fostered his son’s interest in
829
830
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124. No. 4. December 2012
birds by taking him on walks through fields and
woods and teaching him to identify' birds. Father
also taught son to hunt, a skill critical for the
taxonomic studies of birds undertaken by Ridg-
way from about the age of 10. He began to shoot
birds and, mixing his own paints, taught himself
to paint birds. His interest was spurred by a book
given to him by an uncle.
The most charming story of Ridgway's early
steps to a lifetime of ornithological pursuit may be a
lesson lor those of us who receive e-mails from
students asking questions about birds. Ridgway,
wanting to know the name of a bird he'd seen
around his hometown of Mt. Carmel, Illinois wrote
to the Commissioner of Patents who turned the
letter over to Spencer Baird, then Assistant
Secretary of the Smithsonian. That first letter
sparked a running correspondence that ultimately
brought Ridgway to the Smithsonian, where he
remained for the rest of his life. Even today,
Ridgway’s handwritten letters and drawings hang in
a hallway in the Smithsonian Castle. The story
reminds us to respond to and encourage our young
correspondents seeking information about birds but.
then again, few of us are rewarded with a simple
message ol thanks, much less a series of letters
evidencing a dedication to learning the names of
birds, their anatomy, and technical terminology.
Baird recommended Ridgway to geologist Clar¬
ence King who was to conduct the Fortieth Parallel
Survey commencing in 1867. Ridgway was only 1 7
and had never been outside Mt. Carmel but Baird
thought he would make a suitable naturalist for the
survey. After a crash-course at the Smithsonian to
learn how to prepare study skins, Ridgway traveled
with the group surveying the Sierra Nevada from
Nevada to Wyoming. This section of the book is
relatively rich in details of Baird's experience.
During the trip, Ridgway gathered 769 skins and
753 nests and eggs, and contributed 366 pages to
the expedition report. Thereafter, he returned to the
Smithsonian to take a job as an illustrator, although
he also answered correspondence from the public,
worked on the public display areas, and managed
the bird collection. He undertook a number of
collecting expeditions in the eastern United States
and, «n 1899, joined the famed Harriman expedition
to Alaska. From this point forward, and apart from
some limited discussion of his marriage, his son
and his ever-pressing need for money, Ridgway
laigely recedes from die book.
Lewis moves into an in-depth discussion of the
development of ornithology as a science and the
establishment of the American Ornithologists’
Union, covered more completely by Mark Barrow
in A Passion for Birds (2000, Princeton University
Press, Princeton, New Jersey. USA). Lewis (page
86) devotes an entire chapter to America’s '‘first
bird organizations” noting that Ridgway was
busy with other matters." His intense devotion
to his work kept him distant from Coues’
maneuvering and plotting in the creation of rhe
American Ornithologists' Union. The discussion
ot the development of professional ornithology is
basically limited to the creation of the Nuttall
Ornithological Club and the subsequent develop¬
ment ot the American Ornithologists’ Union and
locuses largely on Coues. A bold and apparently
rather unpleasant character widely disliked by
his peers. Coues was, according to Lewis, the
constant engine ol change in ornithology in Norlh
America.
The founding ol the AOU elicited a deliberate,
although ultimately blurry, drawing of lines
between scientific professionals-especiaUy the
taxonomists-and all others who studied birds.
Lewis identifies three attributes that seem accu¬
rate enough in the absence of the formal education
credentials that would become de rigeur a few
decades later. He describes the professionals as
unsentimental, technical and precise in their use
ot language, had published in the technical
literature, and were respected by others who knew
them, or knew someone who knew them. At least
the first of these, according to Lewis (page 112),
served to exclude women who were seen as
delicate, emotional, and nurturing." This inter¬
pretation seems a stretch in that few women were
entering any profession, scientific or otherwise, in
the 1880s. Lewis names several female astrono¬
mers ol the time but disregards the fact women
could rarely undertake careers that entailed
lengthy absences from the home or unchaperoned
travel with men. as would have been the case for
most scientific collecting expeditions, even within
the United States. Barrow makes this point, but
goes on to name a number of women working in
ornithology including Graceanna Lewis, John
Cassin s only student; Fannie Chapman, Frank
Chapman s wife; and, although not mentioned by
Barrow, Florence Merriam Bailey, the first female
member of the AOU.
Lewis devotes his fourth chapter to scientific
collecting. It is the liveliest chapter of the book,
describing the need for specimens, the manner in
which collecting was undertaken, the preparation
ORNITHOLOGICAL LITERATURE
831
and preservation of skins — in graphic detail. The
difference between mercenary collectors and
those employed by museums is explained. The
concept of a subspecies and the role ot American
ornithologists in pressing for use ol trinomials are
discussed. The fifth chapter comprises a long
discussion of the battle for a single nomenclatural
system, checklist, and code. Despite Cones
machinations to garner favorable reviews tor his
checklist. Ridgway's checklist carried the stand¬
ing of the Smithsonian. Coues chaired the lirst
AOU Committee on Classification and Nomen¬
clature. The 1886 publication of the AOU
Checklist resolved many of the differences
between the Coues and Ridgway checklists.
The next chapter covers the era's publications
about birds. The reader is introduced to Ridg-
way’sbody of work, including The Birds of North
and Middle America , started by Ridgway in 1 894
and continuing through 1918, when Part 8 — the
last completed in his lifetime — was published.
The unfinished volumes, 9-11. were completed
by Herbert Friedman and the last was published in
1950, The planned volumes 12 and 13 were never
published. Lewis asserts (page 211) that Ridgway
"helped to put the nail in the coffin ot systematics
as the key means to study birds as a prolession.
because his work on Bulletin 50 was so definitive
that it wmuld remain unsurpassed tor decades,
leaving ornithologists to turn to other venues alter
Ridgway’s domination of avian systematics.
That this new profession was coming ol age
during the emergence of the study ot the role ot
behavioral characteristics in speciation surely
played a role; evolutionary shifts in the tocus ot
biological study respond to the change in resources
(tools, funding, publishing fashion) as do the
objects of their study. Moreover. Lewis overlooks
the enormous resurgence of systematics with the
advent of tools such as protein electrophoresis,
PCR, and equipment that sequences genomes while
biologists go out for a few beers. The significance
of the chapter, though, is the return to the
examination of Ridgway's work and file, including
his move in 1913 to southern Illinois. Lewis
attributes this move to the desire ot Ridgway and
his wife to live closer to nature. Ridgway continued
his work on Bulletin 50 despite failing eyesight and
poor health. His wife-who had helped him to till
orders for his color dictionaries by cutting and
pasting the hundreds of small squares ot color
samples to the pages of the sell-published Colot
Standards- died in 1927.
The final chapter of the book recounts at length
Ridgway's struggle to describe and standardize
bird colors. Like others who tried to create such
standards, he struggled with consistency of pro¬
duction of colors and the inability to prevent
fading of the printed page. His first eftort (1886)
illustrated 186 colors on hand-painted chips. The
second was published 26 years later, after many
false starts. Initially intended to be a Smithsonian
publication, institutional support and interest
swelled and waned over the years. When
published in 1913, the book included 1,1 15 colors.
Lewis concludes by noting that Ridgway’s
approach to the color book was much like that
of the amateur ornithologists ol an earlier age. He
eschewed the use of scientific terms, favoring
lyrical names to describe colors. He eschewed the
use of phvsics to identify colors by their numeric
wavelengths. He actively rejected the urging of
Smithsonian Secretary Samuel Langley to use
spectral analysis. Thus, the colors are described
with names as obtuse as ‘elephant's breath or
•Chapman's blue' rather than chromaticity coor¬
dinate 0.3127, 0.3290. The book concludes with a
chronological list of Ridgway’s publications,
scientific and popular.
The book's central premise is repeated across
chapters at length; it becomes tedious. There are
several minor errors. For instance, in describing
the preparation of skins, the anterior orifice is
described as an unus rather than a cloaca. Lewis
identifies the Hirundinidae as a family ot
flycatchers. The more serious problem, however,
is the assertion by Lewis (page 212) that
Ridgway was falling out of step with the trend
in biology to study the living bird, and con¬
founding the value of the knowledge to be gamed
in field studies of living birds with 'popular
ornithology.’ True. Ridgway himself in 1901
famously equated the study of behavior with
‘popular ornithology' in the first volume ol
Bulletin 50. However, integrative biology was
just drawing its first breath at that time and it is
not surprising that a man who devoted all his
energy to systematics would not have taken note
of the increasing scientific rigor ot these other
approaches. In fact, these areas of study were
also coming to acquire the characteristics ot
‘professional science' in the development ol
classification schemes, technical language, and
publication in scientific journals. The first
number of the Auk includes a lengthy treatment
by Bicknell of bird song, who urged that song
832
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 4. December 2012
should be the subject of scientific study. The
Wilson Ornithological Society (whose establish¬
ment only 5 years after the establishment of the
AOU Lewis ignores entirely in the chapter about
American's earliest ornithological organizations)
had established a food and song division. Investi¬
gators were exhorted to examine and record stomach
contents. Song was to be described by periodicity
with weather correlates to show variation between
breeding and migration periods, and more. The
nesting division requested reports on more than two
dozen aspects of nesting behavior. Ridgway indeed
exemplified the transition of bird study to a science
but. by focusing so narrowly on Ridgway and the
AOI r, Lewis erroneously concluded that profession¬
alization of ornithology as a scientific discipline did
not extend to the study of the living bird in its natural
context. Lewis’ lens may have had great clarity, but
it was lacking in field of vision.— ELLEN PAUL,
5107 Sentinel Drive, Bethesda, MD. 20816
USA; e-mail: ellen.paul@verizon.net
AUSTRALIAN HIGH COUNTRY OWLS By
Jerry Olsen. CSIRO Publishing, Collingwood,
Victoria, Australia. 2012: x and 366 pages, 23
color plates, numerous figures and tables. ISBN:
978-0-643-09705-6. AUD 69.95 (paper), — Read
ers and reviewers of this engaging book will
notice immediately that its content provides more
than its title would suggest. The book contains
considerable discussion of species that occur
outside of Australia, and it is not restricted to
owls of the ‘high country*. Olsen reviews a fair
amount of work by other owl researchers, but
much of the book is a personal narrative drawn
from his extensive field experience around
Canberra with repeated emphasis on how Austra¬
lian owls (especially Ninox) differ in behavior and
ecology from those in the Northern Hemisphere,
and how comparatively difficult they are to study.
Indeed, so little i.s known about the country’s
nocturnal raptors that the range maps in Appendix
A for each of the eight species (4 T\to and 4
Nin°x) are labeled ’Possible breeding range
of... in Australia.’ The book clearly is written for
a lay audience but will appeal to anyone with an
interest in owls, including professional biologists,
and it should be especially appreciated by owl
researchers who have not visited Australia
The three chapters in the introduction arc
entitled: What is an Owl? What is a Ninox'/ and
What is a Southern Boobook? The latter question
is not trivial given that Southern Boobooks on the
Australian mainland have been classified under
Ninox boobook with mainland and Tasmanian
birds treated as conspecific: N. novaeseelandiae
with mainland, Tasmanian, and New Zealand
birds as conspecific; and ,V. boobook again, but
with mainland. Tasmanian (N. leucopsis), and
New Zealand (TV. novae se eland uie) birds treated
as lull species. The question remains open, and
Olsen uses N. boobook in his list of Australian
owls on page 14. and N. novaeseelandicie in
Appendix A, although he leans toward splitting
them into three species with mainland birds being
N. boobook.
Five chapters deal with studying owls. The first
is a brief biography of David Flcay. who authored
the classic Nightwatchmen of Bush and Plain in
1968 and was the first person to describe the nest
anil eggs of the Powerful Owl ( Ninox strenua ).
and to breed Southern Boobooks in captivity. The
chapter on surveying owls describes how most of
the Australian species are difficult to study
because they tend to he strictly nocturnal,
typically nest in deep hollows in large trees,
almost never use artificial nest sites, and roost in
dense cover. Consequently, much of what i.s
known about their biology has come from surveys
where birds were heard but not seen.
Ten chapters that deal with diet and hunting
summarize information on Great Homed Owls
(Bubo virgmianus), Northern Hawk Owls ( Sumia
ulu/a). Spotted Owls (Strix occidentalis). Great
Gray Owls (5'. nebulosa). Long-eared Owls (Asio
otus). Southern Boobooks, and Powerful Owls.
Olsen revisits the well-known fact that medium-
anil large-sized North American and Holarctic
species tend to feed on small mammals captured
on the ground, and even larger taxa such as Great
Homed Owl and Great Gray Owl often take many
small prey such as voles ( Microtus ) and deer mice
( Peromyscus ). In contrast. Southern Boobooks
glean spiders and stick insects from tree limbs and
foliage and catch moths and bats in mid-air, in
addition to taking birds and small mammals such
as house mice (Mas musculus). Powerful Owls,
ihc largest owls in Australia, favor medium-sized
arboreal marsupials such as possums (Pseudo-
cheirus peregrinus) and gliders ( Petauroides
volans, Petaurus breviceps), and also eat fruit
hats (Ptempus) and large birds such as cockatoos
(Cacatua, Calyptorhynchus) and Laughing Kook¬
aburras ( Dacelo novae guineae). They seldom
capture prey on the ground and often roost with
ORNITHOLOGICAL LITERATURE
833
large prey items clutched in their talons, a behavior
largely absent in Northern Hemisphere owls. On
average, they take larger prey relative to their body
mass than similarly sized Great Horned Owls.
The section on breeding biology contains 17
chapters, the first six of which focus on the
Southern Boobook, which has received more ol
Olsen's research attention than any other owl.
Where Olsen works. Southern Boobooks are
permanent residents with high site tidelity. They
nest once a year during the austral spring, and
males are highly territorial, detending an area ol
-I km: within which both sexes hunt, female
Southern Boobooks. like females ol several North
American owls, do not provision fledglings, even
when fledglings “sidled up to them along a
branch and begged” (page 197). These chapters
present detailed information on vocalizations,
territorial behavior, courtship, nest provisioning,
and breeding biology before and alter young
boobooks fledge. Information on breeding Pow¬
erful Owls is interspersed with that lor boobooks.
1 found the chapters on breeding Snowy Owls
{Bubo scandiacus) and Tawny Ow ls (St fix aluco)
distracting because they did not offer much in the
way of comparison with Australian species,
Three of the five chapters on conservation also
pertain to non- Australian owls, although they
range in length from only three to live pages. The
last two conservation chapters provide valuable
information on Australasian laxa. Sadly, three
went extinct in the 20th century: Lord Howe
Island Boobook (N. n. atbaria). Norfolk Island
Boobook (N. n. undulata ), and the Laughing Owl
( Scelogtanx albifacies ) of New Zealand. The
extant owl of highest concern in the region is
the endemic Christmas (Island) Boobook ( Ninox
tuitalis). Other threatened taxa include two insular
subspecies of Australian Masked Owl (Tyto
novaehollandiae custanops and I n. melvillensis)-
Timber harvest seems to pose the greatest threat to
conservation on the mainland. Owls arc legally
protected in Australia, but Olsen remarks (pages
255-256) that “There continue to be infringe¬
ments of raptor protection laws' and that
“farmers, developers and governments still break
these laws.” He concludes (page 262) that “At
detail Olsen’s work on Sumba in the Lesser Sunda
Islands of Indonesia. Sumba is east of Wallace s
line but contains birds with Palearctie and
Australasian affinities. Its avitauna is poorly
known and includes two species of Tyto. the
endemic Sumba Boobook (N. rudoljt), and the
Little Sumba Hawk-Owl ( N . sumbaensis). The
latter was a ‘mystery’ species first reported by
ornithologists in the late 1980s and described as a
new species by Olsen and his colleagues after they
visited the island late in 2001. I thoroughly
enjoyed Olsen's account of his work on Sumba,
where his group dodged crocodiles, endured high
humidity and insect swarms, and dealt with locals
who from bad past experiences harbored a strong
distrust of white foreigners. The group persevered,
however, and located several pairs of the new owl,
obtained photographs and sound recordings, and
even examined a fresh specimen that had been
billed by a hunter. Measurements of the intact
carcass, DNA extracted from several leathers
(most of the specimen was left with local
villagers), and vocalizations recorded in the wild
left no doubt that the mystery bird was a new
Species of Ninox.
Non-Australians who are familiar with the
publications of Jerry Olsen might be surprised to
learn that he was born anil raised in Spokane,
Washington, USA, although he’s lived in Aus¬
tralia for so long (40 years) he probably could
pass for a native. North American readers, and
perhaps also those from Europe, may find the
information on Northern Hemisphere species
superfluous, and it certainly makes the book a bit
disjointed. But surely this information was includ¬
ed for Australians, not for Westerners and, in any
case, the latter can detour around those chapters if
they wish and still find plenty of interesting reading
on the Australian and Indonesian species. On
balance, the book is a thought-provoking and
readable account of the status and ecology ol
Australia’s owls, albeit with a focus on the most
widespread strigid Down Under, the Southern
Boobook. I recommend it for anyone with an interest
in owls.— JEFFREY S. MARKS. 4241 SE Liebe
Street, Portland, OR 97206, USA: e-mail: jeff 17_
marks@msn.com
the moment loo little is done about these breaches
of law.” However, it was encouraging to read that
biologists are preparing and implementing reco¬
very plans for owls throughout the country.
The last section contains a brief introductory
chapter about Wallacea and three chapters that
EMERGING AVIAN DISEASE. Edited by
Ellen Paul. University of California Press, Berke¬
ley, California, USA., 2012: 108 pages. ISBN:
978-0-520-27237-8. $39.95 (hardcover).— As a
834 THE WILSON JOURNAL OF ORNITHOLOGY • Vo/. 124. No. 4. December 2012
veterinarian specializing in agricultural animals Impact) continued the same format using research
and wildlife, understanding diseases and how they to help the reader understand various disease jm-
tmpact an animal's health is of utmost impor¬
tance. Moreover, emerging diseases are a constant
struggle to keep up with and understand. Most
disease texts are geared toward domestic animals
with few ‘exotic’ texts available. When one exists,
the diseases mentioned are often limited to the
most common conditions with little known or
written on new and emerging diseases. Having a
guide on emerging avian diseases is an important
addition to the literature due especially to the
global impact of these diseases.
This book begins with a Forward by Robert G.
McLean which sets the tone of the importance of
the text and gives an overview and breakdown of
what to expect. However, as a reader, the title led
me to believe the text was going to be more
descriptive in nature as many books on diseases
are constructed. This book is arranged by sections
that seemingly flow from transmission to popula¬
tion impact to more specific monitoring, detec¬
tion, and research practices. As I started to read
each section. I quickly realized this book is more
than a descriptive etiology, pathophysiology,
diagnosis, and treatment disease text book. Paul
took a unique perspective on the classic disease
text and used current research as examples to
explain each section heading.
By focusing on a few diseases and using current
research. Paul compiled literature to help show the
reader how these diseases etnerged and the impact
they had on a given population. Pan I (Environ¬
mental and Behavioral Aspects of Transmission)
consisted of a series of research projects to help
readers understand disease dynamics within a
population and movement-emergence in different
habitats and locations, and among individuals
within a population. Part II (Population-level
pacts on a given population.
Part III (Monitoring, Detection, and Research
Practices) was much different than I had antici¬
pated. I expected several chapters on different
sampling and laboratory diagnostic tests. Instead.
I found a series of compelling articles that ranged
from theory and disease transmission modeling,
understanding immune function, and a description
of zoonotic diseases.
The final chapter. Zoonotic Diseases, found a
way to tie etiology, pathophysiology, etc., in a
new and interesting W'ay. By taking the approach
to give personnel in the Field knowledge to protect
themselves from zoonoses, this chapter allows the
reader to empower themselves with the know¬
ledge ot disease transmission and symptoms to
enable them to identify conditions where these
diseases can arise. Avian Influenza and West Nile
were highlighted and followed by a section on
other zoonoses. The final summary gave practical
precautions when dealing with all pathogens one
may encounter.
While this text did not meet my initial expecta¬
tions, I found the style to be a refreshing way to
present information. There are times when using
concrete examples help to emphasize a particular
point better than descriptive narratives. In this book.
I learned about diseases and the impact they have
on species and populations in a new and novel
way. I particularly liked the last chapter where it
seemed to empower individuals to protect them¬
selves with knowledge on these diseases.— JACOB
R. WERNER. Attending Veterinarian for Agri¬
cultural Animals and Wildlife, Pennsylvania
State University, 101 Centralized Biological
Laboratory, University Park, PA 16802, USA;
e-mail: jrwl40@psu.edu
The Wilson Journal of Ornithology 1 24(4):835- 846, 2012
PROCEEDINGS OF THE NINETY-THIRD ANNUAL MEETING
JOHN A. SMALLWOOD. SECRETARY
The Ninety-third Annual Meeting ot the
Wilson Ornithological Society was held from
Tuesday, 14 August, through Saturday, 18
August 2012. on the campus of the University
of British Columbia in Vancouver, in joint
session with the American Ornithologists'
Union, the Association of Field Ornithologists,
La Sociedad para Estudio y Conservacidnde las
Aves en Mexico (CIPAMEX). the Cooper
Ornithological Society, the Raptor Research
Foundation, the Society of Canadian Orniihol-
ogists/Soeiete des Ornithologistes du Canada,
and the Waterbird Society, This joint meeting
was the Fifth North American Ornithological
Conference (NAOC-V). Kathy Martin, Envi¬
ronment Canada and University of British
Columbia, served as the NAOC-V Conference
Chair and Chair of the NAOC-V Steering
Committee, which also included Erica Nol
(Latin American Participation, Society of Ca¬
nadian Ornithologists), Peter Davidson (Field
Trips, Bird Studies Canada), Kimberly Cl. Smith
(Finance Committee. American Ornithologists'
Union). Lee H. Robinson (Society Meeting
Requests, Association of Field Ornithologists),
Katherine Renton (Latin American Participa¬
tion. CIPAMEX). Kimberly A. Sullivan (Sci¬
entific Program Liaison, Cooper Ornithological
Society), Elizabeth K. Mojica (Student Affairs,
Raptor Research Foundation). Robert L. Curry
(Student Presentation Awards. Wilson Ornitho¬
logical Society), and Robert W. Elner (Chair.
Local Organizing Committee, Waterbird Soci¬
ety). The Local Organizing Committee also
included Andrea M. S. Norris. David P. L.
Toews, Erin Gendron, Lee II. Robinson. Mark
Drever. Nancy Mahony, Peter Arcese. Peter
Davidson. Shelagh Bueknell. and Wendy
Easton. The following organizations sponsored
(he conference: Environment Canada (Wildlife
Research Division). The University ol British
Columbia (Beaty Biodiversity Museum. Centre
for Applied Conservation Research, Depart¬
ment of Zoology, Forestry, and Office of
Vice-President of Research and International).
Simon Fraser University (Biological Sciences,
Centre for Wildlife Ecology), Commission for
Environmental Cooperation of North America,
and Holohil Systems Ltd.
NAOC-V activities began on Sunday. 12
August, with a workshop on estimating avian
abundance and occupancy with marked and
unmarked individuals. Additional events from
Sunday. 12 August, through Tuesday. 14 August,
included a continuation ol the avian abundance
and occupancy workshop, plus five more work¬
shops on writing and reviewing scientific
papers, communicating research effectively
through the media, using and contributing to
avian collections, loon conservation, and a
workshop conducted by the North American
Ornithological Atlas Committee. Several of the
participating societies also held their council/
board meetings. The Wilson Ornithological
Society had held its annual Council Meeting
previously, from 31 March to 1 April 2012, in
Buffalo, New York. Bridget Stutchbury present¬
ed the lecture “Frequent fliers: tracking song¬
bird migration through the Americas' on
Monday evening and the opening reception
was held on Tuesday evening.
Conference Chair Kathy Martin opened the
scientific program on Wednesday morning with
welcoming remarks, noting the NAOC-V had
attracted >1.500 participants from >25 coun¬
tries. Chairperson Martin subsequently intro¬
duced John L, lnnes. Dean of Forestry, who
welcomed those assembled to the University ol
British Columbia. Dean lnnes. in turn, introduced
the first plenary speaker, Fiona Schmiegelow,
who presented the lecture “An odyssey of boreal
bird research and conservation in Canada. " The
scientific program, conducted over 4 days, con¬
sisted of an astounding 1.167 presentations,
including 643 papers organized into 69 sessions
and 12 symposia, 520 poster presentations
organized into two sessions, and a plenary lecture
to begin each day of the program. On Thursday
morning Irby J. Lovetie presented the plenary
lecture “Historical perspectives on the evolution
of warbler diversity, behavior, and ecology."
Roxanna Torres opened the Friday program with
••Sexual selection from a life history perspec¬
tive: colour communication in a seabird. On
835
836
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124. No. 4. December 2012
Saturday Peter P. Marra delivered the fourth
plenary lecture, “Studying birds in the context of
the annual cycle: carry-over effects and seasonal
interactions.”
The Local Committee hosted field trips each
morning to various bird-watching trails on
campus. Longer trips, from 1 to 3 days, during
and alter the conference included (I) watching
shorebirds on the Fraser Delta, (2) observing
marine birds and mammals of the Salish Sea, (3) a
trip to the Colony Farm Banding Station, (4) a
tour of the Vancouver North Shore Coast and
Mountains. (5) a hike in Manning Provincial Park.
(6) birding in the Okanagan Valley, and (7) a trip
to Bamficld Marine Sciences Centre.
On Saturday evening the conferees gathered at the
UBC Museum of Anthropology for a reception prior
to the annual banquet. The evening events included
an enjoyable dinner accented by live musical
performances. WOS awards (below) were presented
at the banquet, previously during the WOS Awards
ceremony on Thursday, or on the WOS web site.
MARGARET MORSE NICE MEDAL
(for the WOS plenary lecture, to be presented at
the 2013 Annual Meeting)
Peter R. and B. Rosemary Grant.
WILLIAM AND NANCY KLAMM
SERVICE AWARD
(for distinguished service to the Wilson Ornitho¬
logical Society)
Doris J. Watt.
EDWARD’S PRIZE
(for the best major article in Volume 123 of The
Wilson Journal of Ornithology)
Morton L. Isler and Bret M. Whitney, “Species
limits in antbirds (Thamnophilidae): the Scale-
backed Antbird (Willisomis poecilinotus) com¬
plex.”
Kelsey Low, Villanova University, “Plumage
brightness, social dominance, and reproductive
success of male Carolina Chickadees (Poeeile
carol inert sis): implications for hybridization with
Black-capped Chickadees (P. atrieapillus)T'
GEORGE A. HALL/HAROLD F.
MAYFIELD AWARD
Daira Ximena Villagran Chavarro. Fundacion
Conservation Verde Colombia. "Saving the
Cundinamarca Antpitta: assessment and conser¬
vation of the Cundinamarca Antpitta ( Grallaria
kaetsneri), Colombia.”
PAUL A. STEWART AWARDS
Michael Akresh, University of Massachusetts,
“Examining carry-over effects in Prairie War¬
blers using stable-isotope analysis."
Jacob Armiger, Villanova University, “The
genetic mating system and reproductive skew in
the Yucatan Wren (Campylorhynchus yucatmi-
CltS)."
Kristen Covino. University of Southern Mis¬
sissippi, "Hypothalamic-pituitary-gonadal axis ac¬
tivity in Nearctic-neotropieal songbirds throughout
spring migration.”
Rachel Eaton, Michigan Stale University.
“Following frugivores: tracking avian use of
and damage to cherry orchards."
Annette Fayet, University of Oxford. “Migra¬
tory navigation and behaviour of the Atlantic
Puffin."
Landon Jones. University of Louisiana, “Spa¬
tial patterns of seed dispersal by two species of
toucans in a tropical agricultural landscape."
Kristin Kovach. University of Windsor. "The
function ol duelling behavior in Thryothorus
wrens."
Bethany Krebs, University of filinois. Cham-
paign/Urbana, “Impacts of parasitism on avian
immunocompetence, behavior, and movement."
STORRS L. OLSON PRIZE ALEXANDER WILSON PRIZE
(for the best book review in Volume 123 of The and Luis Fubio Silveira
Brown. Mary Bombcrger. Editorial News. 643
Bubo virginianns. 627-628. 780
Bubulcits ibis. 237. 570
Budgerigar. See Melopsittmus undulcitus
Bullfinch. Greater Antillean, see Loxigilla violacea
Lesser Antillean, see Loxigilla noctis
Bunting, Indigo, see Pasxetina cyanea
Lark, see Ctdamospi-a mehnocorys
Snow, see Plectrophenax nivalis
Burger Jr.. L. Wes, see Mitchell. Kristina L, Samuel K.
Riffell. - . and Francisco J. Vilella
burrlish. see Cliiloinyclerus sp.
Bushtil. sec Psallriparux minimus
Butcherbird. Hooded, see Cracticus cassicus
Ha reo albicaudatus. 636-640
jumaicensis, 416. 627-628. 758-766, 783. 786. 818-820
jamuit crisis jumaicensis, 758
lineaius, 764. 783-787
mognirostris, 93. 570, 768
platypterus | platyperus, 624J. 631. 783
platypterm brunnescens, 758. 763
solitarius, 669. 76 1
swainsoni. 636-640
llureogallus anthracinus, 563. 570
meridional is. 636-641 )
urubiringa, 636-640
Buthraupis exirnia, 572-580
montana. 572-580
wetrnnrei, 572-580
Buzzard, Paul, see Liu, Qiang, Feng-Shan Li. - . Fa-
Wen Qian. Fan Zhang. Jian-Lin Zhao. Jun-Xing
Yang, and Xiao-Jun Yang
Buzzetti, Dante, see d'Horta. Fernando Mendonya. Guy M.
Kirwan, and -
C
Cacicus chry sonants, 572-580
sclateri, 23
Caeeilius antillanus, 153
Cain III. James W.. see Smith, Kathryn N., - ,
Michael L. Morrison, and R. Neal Wilkins
Calamospiza melanoeorys, 261
Calcarius plans. 261. 396
Calidris alba. 42-43. 45-46, 367
canurus. 42-43, 45-46. 48
fuscicoULs. 42-43. 45-46. 48
pusilla. 42-43. 47
spp., 414
Callipepla squamata, 27
Caloeiua fortnusa. 6 1 .3
Calomys laitcha, 59 1
miisculinus. 591
spp.. 591-592
Calonectris diomedea. 68-69
Calnthorax lueifer, 641
Calypre anna. 1 10. 347. 413. 641
costae. 347. 641
Camp. Richard J.. see Judge, Seth W.. Jacqueline M.
Gaudioso. P. Marcos Gorresen. and -
Campephilus principalis. 728
Camptostama imberbe. 413
CampyUiptertis curvipennis, 1 1 1
ensipennis, 1 1 I
excellent, 1 1 1
hemileucums, 1 1 1
largipcnnis, 1 1 1
rufus, 106, 111
spp., 106
villaviscensin, 22
Campylorhynchus zonatus, 57 1
INDEX TO VOLUME 124
853
Canastero, Cipo. see Asthenes luizae
Cnnis familiaris, 478. 484. 743
capuchin, lulled, see Cebus appela
Caracara [Carcara), Chimango, see Milvago chimango
Northern Crested. see Caracara die ri way
Southern Crested, see Caracara plancus
Yellow-headed, see Milvago cltimachiina
Camcaru cheriway. 407. 570
plancus, 636-640. 768
Caranx hippos , 70
sp„ 70
Curdellina canadensis. 217-229. 571
pusilla. 217-229. 374. 571
Cardinal. Northern, see Cardinalis cardinalis
Red-crested, see Paroaria coronala
Cardinalis cardinalis. 33, 632. 808-81 1
Carib. Green-throated, see Eulampis holosericeus
Purple-throated, see Eulampis jugularis
Carpodacus mexicanus. 349. 413. 632. 779
purpureas. 217-229
Curridn-Tucuri, Jorge. Regina Berjano. Giovanny Guerrero.
Enrique Figueroa. Alan l ye. and Jesus M. Castillo.
Predation on seeds of invasive Lantana camara by
Darwin's finches in the Galapagos Islands. .338-344
Cassey. Phillip, see Baylis, Shane M., - - and Mark E.
Hauber
Cussin's Auklet. see Ptychoramphus aleuiicus
Castillo, Jesiis M.. see Carridn-Tucuri Jorge. Regina
Berjano, Giovanny Guerrero. Enrique Figueroa.
Alan Tye. and -
cat, domestic, see I'd is cams
Catbird. Black, see Melanoptilu glabri rosins
Gray, see Dumetellu curulinensis
Cuthttrtes aura. 570. 636-640, 758
Cailuirus bicknelli. 396-399
fuscescens. 13, 217-229. 265-269, 396-399. 702
guitatus. 375-379
ivitulutus, 12, 217-229. 345. 348. 350. 369
Cava. Jenna A., Andrew C. Stewart, and Robert N.
Roscnficld, Introduced species dominate the diet
of breeding urban Cooper’s Hawks in British
Columbia. 775-782
Curia aperea. 591-592
Cebus appela. 91
Celeus spectabilis spectabilis, 22
Centmcercus urophasianus. 96
Cepphus grylle, 247
Certhia americana. 177-179. 217-229
americana exiima. 1 77
Chaelura brae Inara. 807
cinereiveniris. 807
meridionalis. 807
pelagica. 802-807
spp.. 156
vauxi, 806
Chaffinch. Common, see Fringilla coelebs
Chalcomitra amethyslina , 348
Chalfoun. Anna D.. see Kramer. Gunnar R. and
Chaoborus crystillimis. 1 59
Cliaradriits collaris. 42-44. 47
falklandicus, 489. 494
melodus, 525
modesties. 42-43. 47
montanus. 390
semipalmatus, 42-44. 46-47
thnracicus. 487
vociferous. 27-28
wilsonia. 494
Chart ier. Allen T„ review. The Crossley ID guide: eastern
birds, by Richard Crossley. 422-426
Chat. Yellow-breasted, see Icteria virens
Chiarello. A. G., see Srbck-Araujo. Ana Carolina. Luis
Fabio Silvcira. and -
Chickadee. Black-capped, see Poecile atricapillus
Boreal, see Poecile hudsanicus
Carolina, see Poecile curolinensis
Chestnut-backed, see Poecile rufescens
Chicken. Domestic, see Callus gallus domestievs | Gallus gallus]
Cllilomycterus sp.. 70
chipmunk. Eastern, see Tamias slriatus
Chlidonias niger. 69. 71
Chloridops kona. 680
spp.. 667
Cliloroclirysa caUiparaea \cal!iparea\. 380-384
niudissima. 380
phoenicotis. 380. 383
Clilnrodrepanis spp., 655
Chlorophonia pyrrhophrys, 572-580
Chlotostilhon spp.. 106
Chohepus spp.. 295
( 'hnndestes grammacus , 24-30
Chondrahieras uncinatus, 636-640
Clwrdeiles minor. 27-28. 113-118. 793-797
Chroieoceplialus philidelphia, 69
ridibundus, 607
Ciconia ciennia. 354-366
maguart, 636-637
Cinclus cinclus. 685
mexicanus. 682. 685
Cinnyris dussumieri. 348
Circus buffoni. 636-640
spp., 670
Ciridops anna. 651-674 (Frontispiece). 680
tenax. 655-656. 660. 669
Cissopis spp., 380
Cislolhorus palustris , 188-190
platensis, 57 1
Clethrionomys gapperi. 203
climate change
affect on protandry in seven passerines in North
America, 208-216
Megascops asio responses to suburban sprawl, warmer
climate, and additional avian food in central
Texas. 630-633
Cnemoscopus rubrirostris, 572—580
coati [coatimundil. South American, see Nasua nasua
white-nosed, see Nasua narica
Coccyzus americanus , 33. 570
Coereba flaveola, 84
Colaptes auratus. 217-229. 389-392, 779
rivolii, 572-580
rubiginosus. 570
854
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 4. December 2012
Colinus virginianus, 27-28. 1 86. 299, 364
Collins, Charles T. and Betsy Trent Thomas. Food habits of
two Fork-tailed Swifts in Venezuela, 152-157
Collocalia esculenla, 153
Coltimba livid. 391. 570, 593, 759, 779
Col umbi na inca. 570
minuta. 570
picui , 593
lulpcicoti, 570, 770
Conebill, Blue-backed, see Conirostrum sitticolor
Conirostnirn sitticolor. 572-580
conservation status
historical and current status of Leucophaeus atricilla
breeding in New York State, 525-530
Contopus cinereus , 570
fiunigatus , 172
nigrescens nigrescent, 23
virens, 217-229
Comtropsis carol inensis, 728
Co rue i as spp„ 336
Coragyps atralus, 570, 636-640
Cormorant. Double-crested, see Phalacrocorax auritus
Great, see Phalacrocorax carbo
Neotropic, see Phalacrocorax brasilianus
Correa, Leandro, see Reinert, Bianca L„ Ricardo Belmonte-
Lopes. Marcos R. Bornschein, Daiane D. Sobotka,
- , Marco R. Pie. and Marco A. Pizo
Con ns brachvrhynchns , 8 1 9
cuurinus. 779
corax. 406
corone. 514-515
hawaiiensis, 680
macrorhynrhox, 514
ruficollis , 406
splendent, 406-408
spp„ 190
Coryphaspiza melanotis. 60
cottontail. Eastern, see Sylvilagus floridanus
Cotumix japonica, 1 89
Courier. Jason R. and Gars Ritehison. Asymmetries in mobbing
behavior among nuclear flockmates, 626-629
Cowhird. Bronzed, see Molothrus aeneus
Brown-headed, see Molothrus ater
Shiny, see Molothrus honatiensis
Cracticus cassicus, 35 1
Crane, Black-nccked. sec Crus nigricoltis
Red-crowned, see Crus japonensis
White-naped, sec Crus vipio
Cranioleuca erythrops , 812-815
Crary. Andrea L.. see Junda, James H„ - , and Peter
Pyle
Crax alec tor, 325-326
blurnenbachii, 32 1-327
daubentoni, 326
fasciola ta. 325-326
glob id osa, 326
rubra, 294, 326
rubra rubra, 326
Creeper. Brown, see Certhla antericana
Crombec, Red-faced, see Sylvietta whytii
Crossbill, Red, see Loxia curvirostra
Croston. Rebecca. Christopher M. Tonra. Sacha K. Heath,
and Mark E. Hauber, Flange color differences of
brood parasitic Brown-headed Cowbirds front nests
of two host species, 139-145
Crotoplmgu am. 342
sulcirostris, 570
Crow. American, see Corvus brachyrhynchos
Carrion, see Con us corone
House, see Con us splendent
Large-billed, see Conus macrorhynchos
Northwestern, see Corvus caurinus
Cryptonanus chacoensis, 592
Crypturellus casiqitiare , 22
duidae , 22
Cuckoo, Common, sec Cuculus canorus
Guira. see Cairo guira
Yellow-billed, see Coccyzus americanus
C iicii I us canorus. 1 42- 143. 51 3-5 1 4
Cuervo, Andrds M.. see Ocampo. David. M. Camila
Estradn-F, Jenny M. Munoz, Laura V. Londono.
Santiago David. Giovanny Valencia. Paula A.
Morales. Jaime A. Garizabal. and -
Cuelo, Gerardo, see Tela. Pablo. Carina Hercolini, and
Curassow. Great, see Cray rubra
Helmeted, see Pauxi pauxi
Red billed, see Crax blurnenbachii
Currie, Dave, see Ewert, David N.. Kimberly R. Hall.
Joseph M. Wunderle Jr., - , Sarah M. Rock¬
well. Scott B. Johnson, and Jennifer D. White
Curry, Robert L.. see LaPergola, Joshua B.. Jesus Gustavo
Marina Hipolito, Juan E. Martinez-Gomez, and
Cyan isles caeruleus , 162-165, 265, 387
Cyanocitta cristata. 217-229
Cyanocorax beecheii. 93
caeruleus. 93-94
c/uysops. 87-95
cristatellus , 93
dickeyi , 93-94
heilprini \helprini. 181. 23
yncas, 93. 171
yucatanicus. 571
Cyanvliseus patagonus, 586
Cyanolyca armillata , 572-580
Cyanomitru olivacca. 348
Cynanthus latirostris , 641
Cyphorinus arada salvin. 23
Cypse /aides niger borealis, 1-8 (Frontispiece). 797-802
niger costaricensis, 1-2
Cypsiurus pun as. 1 53
D
D Angelo, Giulia B.. see Sazima, Ivan and -
d'Horta, Fernando Mendon^a. Guy M. Kirwan. and Dante
Buzzetti, Gaudy juvenile plumages of Cinereous
Mourner (Laniocera hypopyrra) and Brazilian
Laniisoma ( Laniisoma elegans). 429—435
Daigre. Maximiliano. Paulina Arce, and Alejandro Simeone,
Fledgling Peruvian Pelicans ( Pelecanus tluigus)
INDEX TO VOLUME 124
855
attack and consume younger unrelated conspecifics,
603-607
Da Silva. Jose M. C.. see Borges, Sergio H. and -
Duvanyo. Paulo V., Livia M. S. Sou/a. Leonardo S. de
Oliveira, and Mereival R. Francisco, Intraspecific
brood parasitism of the Pale-breasted I hrush
( Titrdus leucomelas), 611-614
David. Santiago, see Ocampo, David. M. Camila Estrada-P.
Jenny M. Munoz. Laura V. Londono, - .
Giovanny Valencia. Paula A. Morales. Jaime A.
Garizabal, and Andres M. Cuervo
Davis Jr.. William E.. review A field guide to the birds of
New Zealand, by Julian Fitter and Don Merton.
647-648
Davis Jr.. William E.. review. The complete guide to
finding the birds of Australia, by Richard Thomas.
Sarah Thomas. David Andrew, and Alan McBride.
195
Decapterus sp.. 70
deer, see Odocoileus spp.
Delichon urbicum , 79 1
Delord. Karine, see Lormee, Herve, - . Bruno
Letoumcl, and Christophe Barbraud
Bellamys kempt. 592
Dendrobaena octaedra, 376
Dendrucopps spp., 336
Deiulrocygita autumnal is. 183-1 85
spp., 240
de Oliveira, Leonardo S., see Davanyo. Paulo V.. Livia M.
S. Souza, - . and Mereival R. Francisco
Deutschl under, Mark E.. John B. Phillips, and Ursula
Munro, Age-dependent orientation to magnetically-
simulated geographic displacements in migratory
Australian Silvercycs (Zost crops I. lateralis). 467-
477
Dickcissel, sec Spi&t anwricana
Oit rttrus adsimilis. 348
Didclphis albiventris. 507. 591-592
marsupialis, 294. 296
spp., 93
diet
food habits of Tuchornis squamaia in Venezuela. 1 52—
157
introduced species dominate the diet of breeding urban
Accipitcr cooper! i in British Columbia. 775-782
items of Harpia harpyja in Belize. 292-297
nestling diet of Stumella magna in east-central Illinois,
399-402
of Spiza americana nestlings in native warm-season
grass field buffers, 298-309
of western North Atlantic seabirds foraging over
Sargassum, 66-72
predation on seeds of invasive Lantana camara by
Darwin's finches in the Galapagos Islands. 338-
344
variation in the diet of Tyto alba along an urban-rural
gradient, 589-596
Oiglossa alhilatera, 572-580
cyanea. 572-580
lafresnayii , 572-580
spp.. 177
Dipper, American, see Cinclus mexicanus
White-throated, see Cinclus cinclus
dispersal
movement and cover-type selection by fledgling Seiurus
uurocapiUa. 620-625
distribution
a new location lor Hvlamanes momotula in Costa Rica,
815-817
first record of a llarpia harpyja nest in Belize. 292-297
historical and current status of Leucophaeus atricilla
breeding in New York State. 525-530
history, structure, evolution, behavior, distribution, and
ecology of the extinct Hawaiian genus Ciridops
(Fringillidae. Carduelini. Drepanidini). 651-674
migration routes and breeding areas of Gras nigricollis,
704-712
winter songs reveal geographic origin of migratory
seedeaters ( Sporophifa spp.) in southern neo¬
tropical grasslands. 688-697
wintering area of Cypseloides niger borealis. 1-8
Diuca spp.. 380
Dives dives. 562, 564. 571
Dixiphia pipru discolor. 23
dog. feral, see Cants familiaris
Dolospmgus fringilloides. 23
dos Anjos. Luiz. see Boesing. Andrea Larissa. Willian
Menq, and -
dos Anjos, Luiz, see Uejima. Angelica Maria Kazue.
Andrea Larissa Boesing, and -
Dove. Laughing, see Streplupelia senegalensis
Mourning, sec Zenaida macroura
Ruddy Ground, sec Columbian talpacoti
White-winged, see Zenaida asiatica
Drepanis pacij'ica, 659
sensu lata. 655
spp., 655, 661
driftfish, see Pscnes sp.
Drongo, Fork-tailed, see Dicrurus adsimilis
Drosophila spp.. 667
Dryocopus Hneatus. 178-179. 570
Dubusia taeniata , 572-580
Duck, American Black, see Anas rubripes
Whistling, see Dendrocygna spp.
Wood, see Aix sponsa
Dumetella carolinensis. 33. 267-268, 571. 702
Dykstra. Cheryl R.. Jeffrey L. Hays, Melinda M. Simon,
and Ann R. Wegman, Protocalliphara (Diptera:
C'alliphoridae) infestations of nestling Red-shoul-
dered Hawks in southern Ohio, 783-787
E
Eagle. Bald, see Haliaeetus \ Hal i news] leucocephalus
Harpy, see Harpia harpyja
earthworm. European, see Lumbricus spp.
Eclectus ro ratus. 393
ecology
aromatic plants in Cyanistes caeruleus nests: the 'Nest
Protection Hypothesis' revisited, 162-165
arthropod abundance and bird use or bottomland forest
gaps. 31-39
brood sex ratio of Amazona finschi , 393-396
856
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124. No. 4. December 2012
composition of mixed-species bird flocks in Alto
Quindto, Colombia, 572-580
ecology and habitat selection of Pluvianellus sorialis ,
487-496
environmental factors affecting nest-site selection and
breeding success of Ciconia ciconia in Western
Turkey, 354-361
grassland bird community response to wildfire, 24-30
history, structure, evolution, behavior, distribution, and
ecology of the extinct Hawaiian genus Ciridops
(Fringillidae, Carduelini. Drepanidini). 651-674
landscape-level forest cover is a predictor of Setuphaga
ceru/ea abundance. 721-727
mating and breeding success decline with elevation for
Troglodytes pacificus in coastal mountain for¬
ests. 270-276
Megascops osio responses to suburban sprawl, warmer
climate, and additional avian food in central
Texas, 630-633
nesting density of Catharus guttatus in a remnant
invasive earthworm-free portion of a Wisconsin
hardwood forest, 375-379
post-fledging ecology of Glaucidium gnoma in the
Rocky Mountains, 199-207
predation on seeds of invasive Lantana comum by
Darwin's finches in the Galapagos Islands, 338
344
sexual selection and mating chronology of Tympanuchus
patlidicinetus, 96- 1 05
species, functional groups, and habitat preferences of
birds in five agroforestry classes in Tabasco,
Mexico, 558-57 1
temporal and spatial patterns in abundance of Glvpho-
rynchus spirurus in lowland Ecuador. 4.36^445
variation in the diet of Tyto alba along an urban-rural
gradient, 589-596
winter microhabitat foraging preferences of sympatric
PoecUe hudsonicus and P. atricapillus in
Michigan's Upper Peninsula, 820-824
Zosterops lateralis song differentiation in an island-
mainland comparison. 454-466
editorial. 848
editorial news, 427. 643
Edwards. Ernesl P.. Award, 1970-201 1, 877
eggs
description for Anthus latest ens. 119-126
description lor Chlorochiysa calliparaea [calliparea],
380-384
description for Cyanocorax clirysops, 87-95
description for Hypopyrrhus pyrohypogaster of the
Colombian Andes. 538-546
description for Myiotlteretes fnmigatus from Ecuador.
169-173
description for Poospiza cinema in southeastern Brazil.
166-169
description for Sporophila melanogaster. 173-176
description lor Stymphtdornis acutiro.xtrix, 286-291
firs, description of the nest and eggs of the island-
endemic Vireo hairdi. 741-749
measurements for Troglodytes aedon chilensis on Chi)o<5
Island, southern Chile, 531-537
Egret, Western Cattle, see Bubulcus ibis
Egretta caerulea, 570
r/iula. 570
Elacnia, White-crested, see Elaenia albiceps
Elaenia albiceps. 6.33
chiriquensis albivertex, 554
cristata. 554
Ela/ioides forjicatus, 768
Elanus lencurus. 570
Elaphe hairdi. 281
clirnacophora, 5 1 4
obsolete /, 732-733
bllis-Eclege. Susan N . review. Trophic interactions:
predators, prey and the changing dynamics of
nature, edited by John Terborgh and James A.
Estes. 646-647
Emberiza ciris, 655
Emberizoides herbicola , 60
Emheniagru longicauda. 57-65
Emerald, White-bellied, see Amazilia Candida
Empidonax albignlaris, 570
alnornm , 2 1 7-229
flaviventris . 217-229. 347. 570
minimus , 217-229, 268. 570
oberholseri. 554
traiUii , 2 1 7-229, 570
virescens, 347
endemism
new area lor Amazonian birds in the Rio Neero Basin.
15-23
Enderson. James I I.. Robert J. Oakleaf, Ralph R. Rogers,
and Jay S. Sumner. Nesting performance of
Peregrine Falcons in Colorado. Montana, and
Wyoming. 2005-2009. 127-132
I-.nilo. Sachiko. Nest-site characteristics affect probability
ol nest predation of Bull headed Shrikes, 513-517
EremophUa alpestris, 24-30. 413
alpestris arricolu, 274-275
Eriophora biapicata, 347. 350
spp., 351
Erithucus rubecula. 364
ermine, see Mustela erminea
Escalante. Patricia, see Pease. Shannon M.. Alejandro
Salinas-Melgo/.a. Katherine Renton, - . and
Timothy F. Wright
Estadcs. Cristian F.. see Quilodran. Claudio. S.. Rodrigo A.
Vdsqucz. and - -
Estrada T. M. Camilu. see Ocampo. David. - . Jenny
M. Munoz, Laura V. Londoiio. Santiago David.
Giovunny Valencia. Paula A. Morales, Jaime A.
Garizahal. and Andrds M. Cuervo
Eudvcimus albas. 606
Eugenia sp„ 744
Ea lam pis Iwlosericeas, 84
jagalaris. 8 1 -86
Eamops bonariensis. 592
Eupetomcna macronra. 106. Ill
Euphagus carolinas. 698-703
Euphonia liirandinacea. 571
laniirostris, 8 1 2-8 1 5
Euphonias, Thick-billed, see Euphonia laniirostris
INDEX TO VOLUME 124
857
Evans. William C, see Bond. Alexander. - . and lan
L. Jones
Ewert. David N„ Kimberly R. Hail. Joseph M. Wundcrle
Jr.. Dave Currie. Sarah M. Rockwell, Scotl B.
Johnson, and Jennifer D. White. Duration and rate
of spring migration of Kirkland's Warblers. 9-14
Excalfacioria chinensis, 519
F
Fainwren. Red-backed, see Mulurus melanocephalus
Superb, see Mulurus cyaneus
Fulco columbarius , 4 1 6
mexieanus. 783
peregrinus. [perigrinus, 127] 127-132. 148
\par\rrius, 753, 758. 791
spp.. 336
linnunculus, 395
Falcon, Peregrine, see Falco peregrinus
Prairie, see Falco mexieanus
Slaty-backed Forest, see Micrastur mirandollei
Fanlail, Rufous, see Rhipidura rufifrons
Fvlis calus. 385, 478. 514, 610. 675, 679. 743
Ferrer-Paris. Jose Rafael, see Rodriguez. Gustavo A., Jon
Paul Rodriguez. - . and Ada Sanchcz-Mereado
Ficedula alhicollis, 387
hpuleuca, 387, 467. 613
Figueroa, Enrique, see Carridn-Tacuri, Jorge. Regina
Berjano. Giovanny Guerrero. - . Alan Tyc,
and Jesus M. Castillo
filefish, see Aluterus sp.. Monucanthus sp.
fringed, see Monacanihus ciliatus
planehead, see Steplwnolepis bispidus
Finch. Black-capped Warbling, see Paospiza melanoleuca
Black-masked, see Corypbaspiza melanotis
Cinereous Warbling, see Paospiza cinerea
House, see Carpodacus mexieanus
Lurgc Ground, see Geospizu niagnirostris
Medium Ground, see Geospizu fords
Plain-tailed Warbling, see Paospiza a In cola
Purple, see Carpodacus purpureas
Ringed Warbling, see Paospiza lon/nura
Rusty-browed Warbling, see Paospiza erythrophrys
Semi, see Embernagra longicauda
Slaty Brush, see Ailapetes schixtaceus
Wedge-tailed Grass, see F.mberiz.oides herbicola
Zebra, see Taeniopygiu guttata
Firefinch. Jameson's, see Lagannsticta rhodopareia
Red-billed, see Lagonostictu scnegala
Fitzgerald, Jane A., see Thompson III. Frank R . Mark B.
Robbins, and -
Flathill, Yellow-olive, see Tohnomyias sulphurcsccns
Flicker. Northern, see C.olaptes auratus
Flowerpiercer. Masked, see Diglossa eyanea
Flycatcher. Acadian, see Empidonax viresccns
Alder, see Empidonax alnorum
Ash-throated, see Myiarehus eineraxcens
Chapada. see Suiriri islerorum
Cinnamon, sec Pyrrhnmyias cinnamomeus
Cliff, see Hinmdinea ferruginea
Collared, see Ficedula alhicollis
European Pied, see Ficedula hypoleuca
Least, see Empidonax minimus
Pale-edged, see Myiarclms cephalotes
Scissor-lailed. see I'yrannus forjicatus
Spotted, see Muscicapa striata
Suiriri, see Suiriri suiriri
Vermilion, see Pyrocepltalus rubinus
Willow, see Empidonax traillii
Yellow-bellied, see Empidonax flaviventris
Foliage-gleaner. Henna-capped, see Hylacryplus rectirostris
Fontana. Carla Suertcgaray. see Rovedder. Cristiano Eidt
and -
Forbes. Scott, see Grieves, Leunne A. and -
fox. arctic, see Alapex lagopus
gray, see Urocyon cinereoargenteus
Fox. James W.. see Beason. Jason P.. Carolyn Gunn. Kim
M. Potter. Robert A. Sparks, and -
Fox. James W.. sec Johnson, James A., Steven M.
Matsuoka. David E. Tessler. Russell Greenberg,
and -
Francisco. Mercival R„ see Davango, Paulo V.. Livia M. S.
Souza, Leonardo S. de Oliveira, and
Francisco. Mercival R.. see Freitas. Maikon S. and
Fratercula arcticu. 246. 250-251
Freeman-Gallant. Corey R- see Taff. Conor C. Katherine
A. Littrell. and -
F regain minor. 600
Freitas. Guilhcrme H. S. and Marcos Rodrigues, Territory
distribution and habitat selection of the Serra Finch
{Embemagru longicauda) in Serra do Cipo, Brazil.
57-65
Freitas. Maikon S. and Mercival R. Francisco. Reproduc¬
tive life history traits of the Yellowish Pipit (Ambus
lutescens ), 119-126
Frigatebird Great, see Fregata minor
Fringilla anna. 653-656
coelebs. 265
spp.. 653-655
Frye, Graham G. and Harry R. Jageman, Post-fledging
ecology of Northern Pygmy-Owls in the Rocky
Mountains. 199-207
Fulmar. Northern, see Fulmanis glacial is
Fulmarus glacialis , 69, 416
Funes. Carlos. Oscar Bolafios. and Oliver Komar. Breeding
of the Brown Creeper ( Certbia americana ) in
Central America, 177-179
Furnarius rufus, 593
G
Galbalcyrhynchus leucotis , 22
Galbula chalcothorax , 22
pastazae, 22
tombacea tombacea. 22
Galictis cuja. 507
Gallus gallus domesticus [Gallus gallus. 294. 521 ]
Gannet. Northern, see Moms bassanus
Gantchoff. Mariela G.. see Segura. Luciano N.. Diego A.
Masson, and -
Garcia. William, see Rotenberg. James A.. Jacob A. Marlin.
Liberato Pop. and - -
Garizabal, Jaime A., see Ocampo. David. M. Camila
Estrada-F, Jenny M. Munoz. Laura V. Londono.
858
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 4. December 2012
Santiago David. Giovanny Valencia, Paula A.
Morales. - . and Andres M. Cuervo
Gaudioso, Jacqueline M.. see Judge. Seth W„ - . p.
Marcos Gorresen, and Richard J. Camp
Gavia irtimer. 73-80
Gayk. Zach G. and Alec R. Lindsay. Winter microhabitat
foraging preferences of sympatric Boreal and
Black-capped chickadees in Michigan's Upper
Peninsula. 820-824
Gehibach, Frederick R.. Eastern Screech-Owl responses to
suburban sprawl, warmer climate, and additional
avian food in central Texas, 630-633
Gelochelidon nilorica , 68
Geococcyx californianus, 283
Geospna /'orris. 338-344
magnirostris. 338-344
spp.. 139
Geot hty pis fonttusa , 33
Philadelphia \philadephia, 229], 208-216
triclm, 33. 208-216, 267, 349, 370-374, 571
Geotrygon costaricensis. 815
Gerwin. John A., see Bishop. Jennifer Thompson, - ,
and Richard A. Lancia
glasseye, sec Heieropriacanihus eruentatus
Glaucidium brusilianum , 200, 204-205, 239, 570
gnonui, 199-207 (Frontispiece), 628
griselceps. 8 1 5
nana. 633-635
passerinum, 204—205
Glyphorynehus spirurus, 436-445
Gnatcatchci. Blue-gray, see Polioptila caerulea
California, see Poliopiila calif arnica
Godwit, lludsonian, see Lunosa haemastica
Goldcrest. see Regains regulus
Golden-Plover (Golden Plover), American, see Pluvial is
dvminica
Goldfinch, American, see Spinas tristis
Lesser, see Spinas psahria
Goose. Canada, see P ran la canadensis
Giant Canada, see U rani a canadensis maxima
Hawaiian (Nene), see Urania sandvicensis
Gorresen, P. Mateos, see Judge. Seth W.. Jacqueline M.
Gaudioso. - , and Richard J. Camp
Goshawk. Northern, see Accipiier gentilis
Gosser, Allen L., see Washburn. Brian E., Martin S.
Lowney. and -
Gow, Elizabeth A. and Karen L. Wiebe. An unusually
synchronous double brooding attempt by a North¬
ern Flicker pair. 389-392
Gowda. Vinita, Ethan J. Temeles. and W. John Kress,
Territorial lidelity to nectar sources by Purple-
throated Caribs. Euhtmpis jugidaris. 81-86
Crackle, Common, see Quiscalus quiscula
Great-tailed, sec Quiscalus mexicanus
Red-bellied, sec Hypopyrr/uis pymhypogasler
Velvet -I ron ted, sec Umipropsar tanagrinus
Grallam dlgnissima | dignissima . 23]
Grallisirix spp.. 669
Grassquit Blue- black, see VolaUnla jacarina
Grebe, Black-necked, see Podiccps nigricollis
C lark’s, see Aechmophorus clarkii
nigricollis
Eared, see Podiceps nigricollis
North American Eared, see Podiceps nigricollis califor-
nicus
Pied-billed, see Podilymbus podiceps
Red-necked, see Podiceps grisegena
Silvery, sec Podiceps occipitalis
Western, sec Aechmophorus occidentals
Greenberg. Russell, see Johnson. James A.. Steven M.
Matsuoka. David F. Tessler, - . and James W.
Fox
Greeney. Harold F„ see Stawarczyk. Tadeusz. Marta
Borowiec. - . and Jose T. Simbana
Greenlaw, Jon S. and William Post, Apparent forced
mating and female control in Saltmarsh Sparrows.
253-264
Grieves. Leanne A. and Scott Forbes. Do Sora nests protect
Red-winged Blackbirds from Marsh Wren preda¬
tion? 188-190
Grisham, Blake A., see Behney, Adam C.. - . Clint
W. Boat. Heather A. Whitlaw. and David A.
Haukos
grison, lesser, see Galictis cuja
Grosbeak. Blue, sec Passerina caerulea
Kona, see Chbridops kona
Rose-breasted, see Pheucticus ludovicianus
Grouse. Chinese, see Telrastes sewerzowi
Red. sec Lagopus lagopus scotica [scoticus]
Ruffed, sec Ronasa umbel I us
Sharp-tailed, see Tyrnpanuchus phasianellus
Grus japonensis. 709
nigricollis. 704-712
spp.. 335
vipio, 709
Gill. Orhan. see Onmu*. Orta?, Yildirtn Agaoglu, and
Guerrero. Giovanny. see Carrion-Tacuri. Jorge. Regina
Berjano, - . Enrique Figueroa. Alan Tye. and
Jesus M. Castillo
Guillemot, Black, see Cepphus grylle
Guinealowl, Helmeted. see Numida meleagris
Guira guira, 507, 509
Gull, Audouin's. see Ichthyaetus audouinii
Black-headed, see Chroicocephalus ridibundus
Bonaparte's, see Chroicocephalus philidelphia
Glaucous-winged, see Lams glaucescens
Great Black-backed, see Lams marinus
Herring, see Larus argeniatus
Kelp, see Lams dominicanus
Laughing, see Leucophaeus a trie ilia
Ring-billed, see Larus delawarensis
Sabine’s, see Xema sabini
Gunn. Carolyn. Kim M. Potter, and Jason P. Beason. Nest
microclimate at Northern Black Swift colonies in
Colorado. New Mexico, and California: tempera¬
ture and relative humidity, 797-802
Gunn. Carolyn, see Beason. Jason P.. - . Kim M.
Potter, Robert A. Sparks, and James W. Fox
Gynmomystax mexicanus. 544
Gymiiopiihys leucaspis casianeus , 23
leucaspis lateralis. 23
INDEX TO VOLUME 124
859
H
habitat
behavioral activities of male Setophaga cerulea in
relation to habitat characteristics. 447-505
ecology and habitat selection of Pluvianellus socialis,
* 487-496
effect of habitat edges on nest survival of Antfuis
spragueii. 310-315
movement and cover-type selection by fledgling Seiuru.s
aurocapilla , 620-625
of Myadestes obscurus in leeward woodland habitat and
their distribution in alpine habitat on Hawai i
Island. 675-681
selection by Lanins colluria breeding in different
landscapes. 51-56
selection of Embernagra longicauda in Serra do Cipd.
Brazil. 57-65
Haliaeerus [Haliceetus, 76) leucocephalus. 160. 407
Hall. Kimberly R., see Ewerl. David N.. - . Joseph M.
Wunderle Jr.. Dave Currie. Sarah M. Rockwell.
Scott B. Johnson, and Jennifer D. White
Halley, Matthew R. and Christopher M. Heckscher,
Multiple male feeders at nests of the Vcery. 396-
399
Hanula, James L.. see Moorman. Christopher F... Liessa 1 .
Bowen. John C. Kilgo. - , Scott Horn, and
Michael D. Ulyshen
Harpagus diodon , 636-640
Harpia harpyja, 292-297
Harrier. Long-winged, see Circus huffoni
Hauber, Mark E.. see Baylis. Shane M.. Phillip Cassey, and
Hauber, Mark E.. see Croston. Rebecca. Christopher M.
Tonra. Sacha K. Heath, and -
Haukos, David A., see Bchney. Adam C.. Blake A.
Grisham. Clint W. Boal. Heather A Whitlaw. and
Hawk. Bicolored, see Accipiicr bicolor
Broad-winged, see Butea plalvplcrus
Chilean, see Accipiicr chilensis
Cooper's, sec Accipiicr cooperii
Great Black, see Buteogallus urubiiingu
Grcv-bellied, see Accipiicr poliogasier
Gundlach's. see Accipiicr gundlachi
Hawaiian, see Uuico solitariu.s
Red-shouldered, see Buieo linealus
Rcd-tailcd, see Buieo jumaicensis
Roadside, see Butea magnirostris
Rufous-thighed, see Accipiicr erythronemius
Savanna, see Buteogallus meridionalis
Sharp-shinned, see Accipiicr striatus
Swainson's. see Buieo .swiiinsoni
White-breasted, see Accipiicr cliionogaslcr
White-tailed, see Buieo albicaudaius
Hawk-Eagle, Ornate, see Spizuctus omalus
Hawkins. Gerard L... Viewpoint. The ‘first basic problem'
revisited: a re-evaluation of Howell et al. (2003).
409-419
Hawk-Ow l. Brown, see Ninox scutulata
Hays, Jeffrey L„ see Dykstra, Cheryl R.. - . Melinda
M. Simon, and Ann R. Wegman
Heath, Sacha K.. see Croston. Rebecca. Christopher M.
Tonra. - . and Mark E. Hauber
Heckscher. Christopher M.. see Halley, Matthew R. and
Hdiodoxa gularis, 22
Helmilheros vennivorum , 33
Hcmignalhus vorpalis. 668
Hcmispingus. Black-headed, see Hemispingus verticalis
Heinispingus atropileus . 572-580
superciliaris, 572-580
verticalis. 572-580
Hemitriccus grunudensis. 572-580
1 lercolini. Carina, see Teta. Pablo. - . and Gerardo Cucto
I lermit. Little, see Pliuelhorni.s longuamireus
Long-billed, see Phaelltomis longtrostris
Long-tailed, see Phaetliornis superciliosus
I lernande/ Daumiis, Salvador, sec van der Wal. Hans. Beatriz
Pena- Alvarez, Stefan L. Arriaga-Weiss, and -
Heron, Black-crowned Night- - - see Nycticorax
nycticorax
Great Blue, see A idea heradias
Hcrpcstcs auropunctatus , 478. 764
Herpetothcres cachinnans. 570
Herpsilochmus dorsimaculatus. 23
dugandi. 23
Hess. Steven C.. Christina R. Leopold. Kathleen Misajon.
Darcy Hu. and John J. Jeffrey, Restoration of
movement patterns of the Hawaiian Goose. 478-486
Heterncercus aurantiivertex. 23
Jlavivertex, 23
Heleropriacanthiis cruenlalus, 70
llimatione san guinea, 483. 651-674
llipolilo. Jesus Gustavo Marina, see LaPergola, Joshua B.,
- , Juan E. Martinez-Gomez, and Robert L.
Curry
Hippocampus sp., 68
Hirundinea ferruginea. 1 72
Hirundo neoxena. 348
hlirundo ruslica , 27-28, 140, 213, 215. 348, 413, 571. 608-
611. 636-637
ruslica erythrogaster, 610
history
of the extinct Hawaiian genus Ciridops (Fringillidae,
Carduclini. Drepanidini), 651-674
Hogle, Joel Lahman, see Belinsky. Kara Loeb, - . and
Kenneth A. Schmidt
Hogna spp.. 399-402
Holochilus brasiliensis. 592
home range
female home-range size during the nestling period of
Junco hyemalis. 614-620
movement patterns of Branta sandvicenxis, 478-486
size for Cyamcvrax chrysops in the Brazilian Atlantic
Forest, 87-95
size of Embernagra longicauda in Serra do Cipo. Brazil.
57-65
spatial dynamics of Buieo jamaicensis in the Luquillo
Mountains of Puerto Rico. 758- 766
Honeyeater. Grey -headed, see Lichennstomus keartlandi
Lewins', see Meliphaga lev in ii
New Holland, see Phylidonyris novaehollandiae
860
THE WILSON JOURNAL OF ORNITHOLOGY • VoL 124. No. 4. December 2012
Hoopoe, Eurasian, see Upupa epops
Hopey, Mark E.. see Vogt. David F., - , G. Rad
Mayfield III. Erie C. Soehren, Laura M. Lewis.
John A. Trent, and Scott A. Rush
Horn. Scott, see Moorman. Christopher E.. Liessa T.
Bowen. John C. Kilgo, James L. Hanula. - ,
and Michael D. Ulvshen
Hu, Darcy, see Hess, Steven C„ Christina R. Leopold,
Kathleen Misajon. - . and John J. Jeffrey
Hubbard. Joanna K. and Audrey L. Tobin. Malicious
motherhood: instance of infanticide by a female
Bam Swallow, 608 61 1
Hummingbird, Allen's, see Selasphorus seisin
Anna's, see Culypte anna
Ant i I lean Crested, sec Onhnrhynchus cristatus
Black-chinned, see Archilochus ctlexandri
Blue-throated, see lumipomis clemenciae
Broad-billed, see Cv mini /his latirostris
Broad-tailed, sec Selasphorus platycercus
Calliope, see Slellula calliope
Copper-rutnpcd, sec Amazilia lobaci
Costa's, see Culypte costae
Lucifer, see Calothornx lucifer
Ruby-throated, see Archilochus colubris
Rufous, see Selasphorus ruj'us
Rufous-tailed, sec Amazilia tz.acatl
Swallow-tailed, see Eupetotncna macroura
Vervain, sec Mellisugu minima
While-cared, see Hylocharis hiucotis
Hydrohates pelagians. 248
Hydroprogne caspia. 68
Hylexetastes stresemanni insignis. 22
[Hylexestastes] stresemanni stresemanni. 18
Hylocharis cyanus, 347
eliciae. 1 1 1
leucotis, 641
HyloCichla mustelina , 5, 12-13, 266-268. 571. 702
Hylocryptus rectirostris. 62
Hylomanes momotula. 8 1 5-8 1 7
Hylopezus fiilviventris fdviventris. 23
Hylophilus brunneiceps. 23
hypoxant Inis fuscicapillus. 23
Hylophylax naevius obscurus, 1 8
Hypocnemis hypoxantha hypoxantha , 23
Hypopyrrhus pyrohypogaster. 538-546
I
Ibis, American White, see Eudacimus albas
Australian White, see Threskiomis moluccus
Ichthyaetus audouinii. 395
Icteria virens, 33, 217-229
Icterus hu/lockii , 28
dominicensis. 57 1
galbtda, 208-229. 57 1
gularis. 571
spurius, 571
Ictinia mississippiensis , 63 1 . 636- 640
plumhea, 636. 768
iguana, green, see Iguana iguana
Iguana iguana , 294
liwi (Tiwi), see Vestiaria coccinea
invasive species
biology of invasive Myiopsitta monachns in south
Florida, 58 1 -588
predation on seeds of invasive Lantana camara by
Darwin's finches in the Galapagos Islands. 338-
344
lodopleura fusca . 432
isabellae, 432
pipra. 432
spp., 432, 434
Ippi, Silvina, Rodrigo A. Vasquez. Juan Moreno. Santiago
Merino, and Camila P. Villavicencio, Breeding
biology of the Southern House W'ren on Chiloe
Island, southern Chile. 531-537
Iridisornis rufivertex , 572-580
Ispidina picta, 347
Ixodes spp., 786
Ixoreus naevius. 779
J
jack, see Cnrunx sp.
crcvalle, see Caron \ hippos
Jaeger, Long-tailed, see Stercnrarius Umgicaudus
Parasitic, see Stercnrarius parasiticus
PoiTiurinc. see Stercnrarius pomarinus
Jagemun, Hurry R„ see Frye, Graham G. and -
James, J, Dale. Jonathan E. Thompson, and Bart M. Ballard.
Evidence of double brooding by Black-bellied
Whistling-Ducks. J 83- 1 85
Jay, Azure, sec Cyanncorux eaeruleus
Blue, see Cyanocitta cristata
Brown, see Psilnrhinus morio
Curl-crested, see Cyanocorax cristatellus
Horida Scrub-, see Aphelocoma coerulescens
Inca, see Cyanocorax vneas
Plush crested, see Cyanocorax day sops
Purplish-backed, see Cyanocorax beecheii
Tulled. see Cyanocorax dickeyi
Jeffrey. John J.. see Hess. Steven C.. Christina R. Leopold.
Kathleen Misajon. Darcy Hu. and -
Johnson. James A.. Steven M. Mutsuoka. David F.
Jesslcr. Russell Greenberg, and James W. Fux.
Identifying migratory pathways used by Rusty
Blackbirds breeding in southcentral Alaska. 698-
703
Johnson. Scott B . sec Ewcrt. David N.. Kimberly R. Hall.
Joseph M. Wunderlc Jr.. Dave Cumc, Sarah M.
Rockwell. - - and Jennifer D. White
Jones, Ian L.. see Bond. zMexandcr. William C. Evans, and
Jones. Stephanie L. and Gar) C. White. The effect of
habitat edges on nest survival of Sprague's Pipits,
310-315
Judge. Seth W„ Jacqueline M. Gaudioso. P. Marcos
Gorresen, and Richard J. Camp. Reoccurrence of
Oma'o in leeward woodland habitat and their
distribution in alpine habitat on Hawai i Island.
675-68 1
Juhanl. Marias A.. Raptor migration at Concepcion. Bolivia,
636-640
Junco. Dark-eyed, see Junco hyemalis
INDEX TO VOLUME 124
861
Junco hyemalis , 274-275, 369. 614-620
hyemalis carolinensis, 6 1 5
Junda, James H„ Andrea L. Crary. and Peter Pyle. Two
modes of primary replacement during prebasic molt
of Rufous Fantails, Rliipidura mjifmns. 682-687
K
Kakapo. see Slrigops habroptila
Kama'o, see Myadestes myadestinus
katydid, greater arid-land, see Neobarreilia spinosa
Kcacher. Kandy L., see Michael L. Avery. Eric A. I illman,
- . John E. Arnett, and Kelli J. Lundy
Kestrel, American, see Falca sparverius
Common, see Falco tinnunculus
Kenerson. Ellen D.. see Reichard. Dustin G. and -
Kilgo, John C., see Moorman, Christopher E.. Licssa T.
Bowen. - , James L. Manilla. Scott Horn, and
Michael D. Ulyshen
Killdeer, see Charadrius vociferous
Kingbird, Eastern, see Tyrannus ty ramus
Tropical, see Tyrannus melancliolicus
Kingfisher. Af rican Pygmy , see Ispidina pictu
Kinglet. Golden-crowned, see Regains satrapa
Ruby-crowned, see Regains calendula
kinkajou, see Polos flavus
Kirwan. Guy M„ sec d'Horta. Fernando Mendonya. -
, and Dante Buzzctti
Kite. Grey-headed, see Leptodon cayanensis
Hook-billed, see Chomlrohierax uncinalus
Mississippi, see leiinia mississippiensis
Plumbeous, see leiinia plumbeu
Rufous-thighed, see Harpagas diodon
Snail, see Rostrhamus sociahilis
Swallow-tailed, see EUuwides forfuaius
Kittiwake, Black-legged, see Rissa tridactvln
Rhus guinwli , 1 1 1
Klamm Service Award, 2007-2012. 878
Klamm Service Award, 2012: Doris J. Watt. 825-826
Knipolegus lopltoles, 61
Knot, Red. see Calidris canal ii s
Koa-Finch. Greater, see Rliodacanlhis palmeri
Lesser, see Rliodacanlhis flav'ueps
Komar. Oliver, see Funes, Carlos. Oscar Bolanos. and -
Konter. Andre. Observations on Aigunruhe in spring
migrating Eared Grebes. 158 161
Konter. Andre. Visual assessment of interbreeding by
Aeehnwphorus grebes, 713-720
Kramer. Gunnar R. and Anna D. Chalfoun. Growth rate and
relocation movements of Common Nighlhawk iChnr-
deiles minor) nestlings in relation to age. 793-797
Kress, W. John, see Gowda. Vinila. Ethan J. Temclcs, and
L
Laciophrys sp„ 70
Lagonosticta rliodopareia , 349-350
senegala. 348
Lagopus lagopus scotica [scolicus, 1 861. 103
Lampornis clemenciae , 64 1
Lampropsar tanagrmus. 544
Lancia. Richard A., see Bishop. Jennifer Thompson. John
A. Gerwin, and -
Laniisoma, Brazilian, see Laniisoma elegans
Laniisoma elegans. 429-435
elegans bucklcyi, 430
elegans elegans. 430-43 1
Laniocera hypnpyrra. 429-435 (Frontispiece)
rufescens. 429. 434
Lanins huceplialus. 513-517
col I urio. 51-56. 516
cri slants, 686
ludovicianus. 516
spp., 686
LaPergola. Joshua B.. Jesus Gustavo Marina Hipolito. Juan
” E. Martine/ Gome/,. and Robert L. Curry, First
description of the nest and eggs of the island-
endemic Cozumel Vireo, Vireo bairdi. 743-749
Lapwing. Southern, see Vcinellus chilensis
Lark. Horned, see Ereniophila alpestris
Laras argentalus. 67. 528
argentatus smithsonianus. 247, 250
delawarensis. 67
dominicanus , 146. 603-604
glaucescens. 148.416
marinus, 67, 247
spp.. 335
Lathroiriccus euleri , 552. 554
Latreutes face rum. 68
Latrodecles sp„ 348, 350
Lee. David S., see Moser. Mary L. and
Leite. Lemuel Olivio. see Anciaes, Marina, That's Maya
Aguilar, - , Renata Dornelas Andrade, and
Miguel Angelo Marini
Leopold. Christina R.. see Hess, Steven C„ — - - •
Kathleen Misajon, Darcy Hu. and John J. Jeffrey
Lepidocolaptes affinis, 1 79
ungustirostris, 507. 509
souleyetii , 1 79
Lepidoirhix corcmata caqueta, 23
coronata coronata. 23
Leplasihenura aegithaloides. 633
Leptodon cayanensis. 768
Lepiopogon amaurocephalus, 552, 554
Leploptilos crumenifer , 358
Leptolila plumheiceps. 570
verreauxi, 570
Lepus europaeus. 591-592
Letoumel. Bruno, see Lormee, Herve. Karine Delord.
- . and Christophe Barbraud
Leucippus chlorocercus, 22
Leucophaeus uiricilla. 69. 525-530
Leucosticte leplirocotis. 148
Lewis, Laura M., sec Vogt, David F„ Mark E. Hopey. G.
Rad Mayfield III. Eric C. Soehren, - , John A.
Trent, and Scott A. Rush
Li. Feng-Shan. see Liu. Qiang. - . Paul Buzzard, Fa-
Wen Qian. Fan Zhang. Jian-Lin Zhao. Jun-Xing
Yang, and Xiao-Jun Yang
Liclienostomus keartlandi. 347
life history
reproductive traits of Ambus luiesccns , 119-126
wing deformities among Sula dactylatra at Clipperton
862
THE WILSON JOURNAL OF ORNITHOLOGY • Vol 124. No. 4. December 2012
Island: life history consequences and insight into
etiology, 597-602
Limnothylpis si vainsonii. 72S-736
Limosa haemastica, 42-43, 47
Lindsay, Alec R.. see Gavk, Zaeh G. and -
Liolaemus spp., 633
Lishman, Carmen and Erica Nol, Ecology and habitat
selection of the Magellanic Plover ( Pluvianellus
socialis)'. a little-known Patagonian shorebird, 487-
496
Litiopa melanostoma , 68
Littrell. Katherine A., see Tuff, Conor C„ - , and
Corey R. Freeman-Gallant
Liu. Qiang. Feng-Shan Li, Paul Buzzard. Fa-Wen Qian. Fan
Zhang. Jian-f.in Zhao, Jun-Xing Yang, and Xiao-
Jun Yang. Migration routes and breeding areas of
Black-necked Cranes. 704-712
Livezey. Dale A., see Butcheldcr, Ned. Gigi Batchelder.
- . and Jeffrey S. Marks
lizard, see Liolaemus spp.
Lizcano. Diego J . see Setina, Victor. - , Daniel M.
Brooks, and Luis l abio Silveira
Lloyd Evans. Trevor I.., sec Baubock, Lisa, Abraham J.
Miller-Rushing. Richard B. Primack, - , and
Fred E. Wasserman
Locusiella lusciniodes , 685 686
Loiselle. Bette A., see Blake, John G., and -
Lonchura castmeothorax , 349
cucullaia , 260
Londono, Gustavo A., see Martinez. Manuel A. Sanchez
and -
Londono. Laura V., see Ocampo, David. M. Camila
Estrada-F. Jenny M. Munoz, - . Santiago
David. Giovanny Valencia. Paula A. Morales.
Jaime A. Garizabal. and Andres M. Cuervo
Longspur. Smith’s, sec Cdlcariux pictus
Loon, Common, see Gavia immer
Lophospingus spp.. 380
Lormee, Herve. Karine Delortl, Bruno Letourncl. and
Christophe Barbruud. Population survey of
Leach's Storm-Petrels breeding at Grand Colomb¬
ia Island. Saint-Pierre and Miquelon Archipelago.
245-252
Loss, Scott R., Nesting density of Hermit Thrushes in a
remnant invasive earthworm- free portion of a
Wisconsin hardwood forest, 375-379
Lowney. Martin S., see Washburn, Brian E., - , and
Allen L. Gosser
Lowther. Peter E.. Does nest-box size impact clutch size of
House Sparrows? 384-389
Loxia cun'lrostra, 85
Loxigilla noctis, 84
violacea, 349
Loxioides spp.. 667
Loxops coccineus , 666-668
spp., 655. 660
virens. 667
Luchesi. Natalia, see Asti*. Andrea and _
Lumbricus spp.. 375-379
Lundy. KdB J ,« Mictau, Aveiy, Eric A. Tillnu
Kandy L. Keacher. John E. Arnett, and _
Luscinia luscinia, 467
megarhynchos. 268, 45 1
Lynx rufus , 283
M
Mager III. John N.. Charles Walcott, and Walter H. Piper.
Male Common Loons signal greater aggressive
motivation by lengthening territorial vodels,
73-80
Magpie, Black-billed, see Pica hudsonia
Magpie-Jay. White-throated, see Culocitta formosa
malaria, avian, sec Plasmodium reliction
Mallard, sec Anas platyrhynchos
Mai unis cyaneus, 347
melanocephahts, 347
Mama Hawaii, sec Drcpanis pacifica
management
capsaicin as a deterrent against introduced mammalian
nest predators. 5 1 8-524
Mannikin, Bronze, see Lonchura cucullaia
Chestnut-breasted, see Lonchura castaneotharax
Margarornis squumiger, 572-580
Marm-Gome/, Oscar IT, see Arbclaez-Cortes. Enrique and
Marini, Miguel Angelo, see Anciacs. Marina. That's Maya
Aguilar. Lemuel Olt'vio Leite, Renata Domelas
Andrade, and -
Marks. Jeffrey S„ review, Australian high country owls, by
Jerry Olsen. 832-833
Marks, Jeffrey S„ see Batchelder, Ned. Gigi Batchelder,
Dale A. Livezey. and -
Marlin. Jacob A,, sec Rotenberg. James A., - •
Liberato Pop, and William Garcia
Marquex-Snntos. Fernando, see Wischhoff, Uschi, - .
and Marcos Rodrigues
Martin, Common House, see Delichon urbicum
Purple, see Prague subis
Martin. Kathy, see Ogden. Lesley J. Evans. Michaela
Martin, and - -
Martin. Michaela, sec Ogden. Lesley J. Evans. - . and
Kathy Martin
Martinez. Manuel A. Sanchez and Gustavo A. Londono,
First nesting information for the Orange-eared
I anager ( Chlorachrysa calliparaea [calliparea]),
380-384
Martinez-Gomez. Juan E., see LaPergola. Joshua B.. Jesus
Gustavo Marina Hipolito, - . and Robert L.
Curry
Masson. Diego A., see Segura. Luciano N., - • and
Mariela G. Gantchoff
Mastophora sp.. 347. 350
Matsuoka, Steven M„ see Johnson. James A.. - . David
F Tessler, Russell Greenberg, and James W. Fox
Mayfield III. G. Rad. see Vogt. David F.. Mark E. Hopev.
- . Eric C. Soehren. Laura M. Lewis. John A.
Trent, and Scott A. Rush
McDermott, Molly E.. see Slager. David L.. - -, and
Amanda D. Rodewald
McGovern. Patrick G.. see Millican, David M„ - . and
Mark T. Stanback
INDEX TO VOLUME 124
863
McNew, Lance B. and William J. While, First case of
renesting after brood loss by a Greater Prairie-
Chicken, 185-187
Meadowlark, Eastern, see Stumella magna
Western, see Stumella neglecta
Slecocerculus leucophrvs, 572-580
stiaopterus. 572-580
meetings, annual of The Wilson Ornithological Society,
649
Megaceryle lorquata, 570
Megaptera novaeangliae, 463
Meganm hus pitongua, 570
Megascops asio , 627-628, 630-633, 750-757
Melamprosops phaeosonui, 655, 661, 668
spp.. 660
Melanerpes aurifrons , 178-179, 562, 564. 570
earolinus. 267
erythrocephalus, 390
fbmiicivorus, 570
uropygialis, 390
MelanoptUa glabrirostris, 743, 748
Mekagris galltipavo, 1 86
Meliphaga lewinii , 347
Metlisuga minima, 346-347. 350
Metopsiltucus undulatus, 265
Mi’lospiza georgiana, 217-229
lincolnii, 217-229
melodla , 139-145. 180
memorium: Pershing Benard “Jack” Hofslund (191 8—
2012), 827-828
Mcnq. Willian, see Bocsing, Andrea Larissa, - , and
Luiz dos Anjos
Mercocerculus stictopterus , 572-580
Merino, Santiago, see Ippi, Silvina, Rodrigo A. Vasquez,
Juan Moreno, - , and Camila P. Villaviccncio
Merlin, sec Falco columbarius
Mesocr ii eltis uuratus, 592
methods
for trapping Chaetura pelagica and other birds that nest
in vertical hollows, 802-807
nation-wide standardized bird survey scheme for Vene¬
zuela. 230-244
survey of Oceanoclrunui leurorhaa breeding at Grand
Colombier Island, Saint-Pierre and Miquelon
Archipelago, 245-252
Michael L. Avery, Eric A. Tillman, Kandy L. Keacher.
John E. Arnett, and Kelli J. Lundy, Biology ol
invasive Monk Parakeets in south Florida. 581-588
Micrastur mirandollei, 767. 773
spp.. 764. 815
Microbates cinereiventris hormotus , 23
Microcerculus bambla alhigularis, 23
Micratus arvalis, 354
midge, phantom, see Chaoboms crystillinus
migration
age-dependent orientation to magnetically-simulated
geographic displacements in migratory Zoster-
ops I. lateralis, 467—477
climate change and protandry in seven passerines in
North America, 208-216
duration and rate for Setophaga kirtlandii, 9-14
migrant songbird stopover ecology on two islands in the
Gulf of Maine, 217-229
pathways used by Euphagus earolinus breeding in
southcentral Alaska. 698-703
patterns and timing of Cxpsetoides niger borealis, 1-8
raptor migration at Concepcion. Bolivia. 636-640
routes and breeding areas of Crus nigricollis, 704-712
stopover site fidelity by Oreotldypis peregrina at a
southern Appalachian high-elevation site. 366-
370
Miller-Rushing. Abraham J., see Baubock, Lisa. - ,
Richard B. Primack. Trevor L. Lloyd Evans, and
Fred E. Wasserman
Millican. David M.. Patrick G. McGovern, and Mark T.
Stanback, Effects of conspecifics on feeder choice
by Northern Cardinals, 808-811
Milvaga chimachima, 93. 636-640. 768-769
chimangn , 507. 509
Mimas gilvus, 237. 571
pan ulus. 342
poly g lottos. 786. 819
salurninus, 593
Mionectes ruftventris. 552, 554
Misajon, Kathleen, see Hess, Steven C.. Christina R.
Leopold. - . Darcy Hu. and John J. Jeffrey
Mitchell, Kristina L. Samuel K. Riffell. L. Wes Burger Jr.,
and Francisco J. Vilella. Provisioning of nestling
Dickcissels in native warm-season grass field
buffers. 298-309
Mitu salvini, 22
tomentosum (tomentosa), 22, 325
lube rasa, 325
Mniotiltu varict, 208-229. 57 1
Mockingbird, Galapagos, see Mimus pan-ulus
Northern, see Mimus polyglottos
Tropical, see Mimus gilvus
Mohoua albicilla , 665
ochrocephala, 651. 665
spp., 665
Molossus rnolossus, 592
Molothrus acne us. 281
ater. 27-28. 139-145, 179-183, 189. 277-285, 723,
728-736, 748. 791
hanariensis, 133-134. 139, 166-169. 748
Momotus momota, 570
Monacanthus ciliatus . 70
sp.. 68, 70
mongoose. Indian, see Herpestes auropunctatus
monkey. Central American spider, see Aides geoffroyi
Yucatan black howler, see Alouatta pigra
Moorman. Christopher E., Liessa T. Bowen. John C. Kilgo.
James L. Hanuia. Scott Horn, and Michael D.
Ulyshen, Arthropod abundance and seasonal bird
use of bottomland forest harvest gaps, 31-39
Morales, Paula A., sec Ocampo, David. M. Camila Estrada-
F. Jenny M. Munoz. Laura V. Londono, Santiago
David. Giovunny Valencia, - . Jaime A.
Garizabal. and Andres M Cuervo
Morelli, Federico. Plasticity of habitat selection by Red-
backed Shrikes (Lanius collnrio) breeding in
different landscapes. 51-56
864
THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 124. No. 4. December 2012
Moreno, Juan, see Ippi, Silvina, Rodrigo A. Vasquez,
- . Santiago Merino, and Camila P. Villavi-
cencio
morphology
descriptive anatomy of the pelvic appendage myology of
Tetmstes sewerzowi, 328—337
growth rate and relocation movements of Chordeiles
minor nestlings, 793-797
history. Structure, evolution, behavior, distribution, and
ecology of the extinct Hawaiian genus Ciridops
(Fringillidae. Carduelini, Drcpanidini). 651-674
measurements for Cyunocorax chrysops nestlings. 87-95
of nestling Troglodytes cieilon chilcnsis on Chiloe Island,
southern Chile. 531-537
wing deformities among Sulci clactylaira at Clipperton
Island: life history consequences and insight into
etiology, 597-602
Morris. Sara R„ see Suomala, Rebecca W„ - . and
Kimberly J. Babbitt
Morrison, Michael L„ see Smith, Kathryn N„ James W.
Cain III, - , and R. Neal Wilkins
mortality and injury
birds caught in spider webs: a synthesis of patterns, 345-
353
mortality associated with volcanic gas seep at Kiska
Island, Aleutian Islands, Alaska, 146-15 1
Moms bassanns , 67
Moser. Mary L. and David S. Lee, Foraging over
Sargossum by western North Atlantic seabirds,
66-72
Mot mot. Tody, see Hylnmanes momotula
Mountain-Tanager, Scarlet-bellied, see Anisognathus igni-
ventris
Mourner. Cinereous, see Laniocera hypopyrra
Speckled, see Laniocera rufescens
mouse, see Apodemus spp.
deer, see Peromy.scus nianiculaius
house, see Mus tmisculus
Munoz. Jenny M.. sec Ocampo. David. M. Camila Estrada-
F. - . Laura V. l.ondono. Santiago David,
Giovanny Valencia. Paula A. Morales, Jaime A.
Garizabal, and Andres M. Cuervo
Munoz- Pedreros. Andres, see Norambuena, Heraldo V. and
Munro. Ursula, see Deutschlander. Mark E., John B
Phillips, and -
Murre. Common, see Uriel aulge
Mus muse ulus. 521. 591-592
Muscicupa siriaiu. 348, 401, 682
Mus tela erminea , 518, 521
it at si. 514
Myadestes lunaiensis. 675
myadestinus. 675
obscurus. 675-68 1
pa/meri, 675, 679
woahensis , 675
Myiarchus eephalotes. 1 7 1
cinerascens. 387
striaticollis. 1 72
t ubercu lifer, 570
tyrann u I us, 570
Myiobius, Black-tailed, sec Myiobius atricaudus
Myiobius atricaudus. 432
spp., 432
Myioborus ornatus, 572 580
Myiodynasies rnaculcllus , 570
Myiophobus ciyproxanrhiis, 23
Myiopsitta monachus | Myopsitta monacha, 593], 581-588
monachus luchsi, 5 85
monachus monachus. 585
Myiollwretes fumigants, 1 69- 1 73. 572-580
funiigatus cajumarcae, 1 69
rufipennis. 1 72
Myinthlypis luieoviridis. 572-580
Myiozetetes similis, 570
Myrmecizxi disjuncta, 23
elzelni, IS
melanoceps. 23
pelzelni, 23
Myrntoborus luguhris siictopterus, 1 8
myotherinus, 1 8
myothcrinus ardesiacus, 15-23
myotherinus elegans, 1 8
Mynnothenda ambigua (ambigua, 23)
cherriei, 23
ignotu. 18
ignotci obscura. 23
longicauda soderstromi, 23
sunensis sunensLs, 23
N
Niisiui narica, 294. 296
nasiui, 93
natural history
Mega scops asio responses to suburban sprawl, warmer
climate, and additional avian food in central
Texas, 630-633
of Crax blumcnhachii, 321-327
of invasive Myiopsitta monachus in south Florida. 581—
588
Neobarrettia spinosa, 28 1 . 283
Neoctantcs niger, 22
Ncomorphus pucheranii puclieranii. 22
Neoscomi hentzii, 347. 350
Neothraupis fasciata, 62
spp., 380
Nephila [Nephilia], clavipes, 347-350
inaurata. 350
maculuta, 350-35 I
spp. 347, 351
Nephilengys cruentata, 347. 349-350
nest
aromatic plants in Cyanistes caendeus nests: the ’Nest
Protection Hypothesis’ revisited. 162-165
description lor Certhia americana in Central America,
177-179
description lor Chlorochrvsa calliparea [calliparaea].
380-384
description for Cyunocorax chrysops, 87-95
description lor Myiotheretes funiigatus from Ecuador,
169-173
INDEX TO VOLUME 124
865
description for Poospiza cinerea in southeastern Brazil.
166-169
description for Sporophila metanogaslcr, 173-176
description for Stymphalornis aculirostris. 2X6-29 1
description of Anihus lutescens, 1 19-126
first description of the nest and eggs of the island-
endemic Vireo baircli. 743-749
first description of the reproductive biology of Accipiter
poliogaster, 767-774
microclimate at Cypseloides niger borealis colonies.
797-802
microhabitat nest cover effect on nest survival ot
Paroaria coronata , 506- 5 1 2
nesting biology of Tolmomyias sulphurescens in Atlantic
Forest fragments. 547-557
nest-site characteristics affect probability ol nest preda¬
tion of Lanius bucephalus, 5 1 3-5 1 7
nest-site characteristics of Chordeiles minor in a Pine
Barrens grassland. 113-118
nest-site habitat description for Lanius collurio, 51-56
nest-site selection and breeding success of Ciconia
dconia in Western Turkey. 354—361
site description for Umnolhylpix swairtsonii in a South
Carolina bottomland forest. 728 736
nesting
biology of Tolmomyias siilphurescens in Atlantic Forest
fragments, 547-557
density of Catharus gallants in a remnant invasive
earthworm-free portion of a Wisconsin hard¬
wood forest. 375—379
ecology of Limnothylpis swainsonii in a South Carolina
bottomland forest, 728-736
ecology of Vireo alricapilla in southwest Texas. 277-285
of Aphrastura spinicauda in a pine plantation in
southcentral Chile, 737-742
nestling
description and provisioning behavior of Accipiter
poliogaster, 767-774
description and provisioning for Myiotheretes fumigatus
from Ecuador, 169 173
description for Hypopyrrhus pyrohypoguster of the
Colombian Andes. 538-546
description for Limnothylpis swainsonii in a South
Carolina bottomland forest, 728-736
description of Chlorochrysa caUiparuea \callip