ENT
A5SEF

HARVARD UNIVERSITY

nase)

Ernst Mayr Library

of the Museum of

Comparative Zoology

MCZ
LIBRARY
JUL 24 2012

of
<P
> i
i>
$3

a

_

7845

on
—
™
_—
Z.
DN
DN
_—
nee
=
sO
Z-
—e)

ENTOMOLOGICAL

SOCIET

/

Y

Volume
One Hundred and Forty One

2010

Published November 2010

: | ISSN 1713-7845
JOURNAL ¥ . oe
ofthe : vad
ENTOMOLOGICAL SOCIETY
me : : ; .
ONTARIO | .
Volume One Hundred and Forty One =
2010 ¥
THE ENTOMOLOGICAL SOCIETY OF ONTARIO
OFFICERS AND GOVERNORS
2009-2010 .
President: G. UMPHREY ESO Regional Rep to ESC: H. DOUGLAS
Department of Mathematics and Statistics Canadian Food Inspection Agency :
University of Guelph, Guelph, ON N1G 2W1 960 Carling Ave., Ottawa ON K1A 06C
umphrey@uoguelph.ca douglash@inspection.ge.ca
Librarian: J. BRETT

President-Elect: H. FRASER

Ontario Ministry of Agriculture, Food and Rural Affairs
4890 Victoria Ave. North, P.O. Box 8000

Vineland, ON LOR 2E0

hannah. fraser@ontario.ca

Past President: C. SCOTT-DUPREE

Dept. of Environmental Biology

University of Guelph, Guelph, ON NIG 2W1
cscottdu@uoguelph.ca

Secretary: N. MCKENZIE

Vista Centre, 1830 Bank Street, P.O. Box 83025
Ottawa, ON K1V 1A3

nicole_mckenzie@hc-sc.ge.ca

Treasurer: S. LI

Natural Resources Canada, Pest Management Centre
Building 57, 960 Carling Ave.
Ottawa, ON K1A 0C6
shiyou@nrcan.ge.ca
Directors:

H. DOUGLAS

Canadian Food Inspection Agency
960 Carling Ave., Ottawa ON K1A 06C
hume.douglas@inspection.ge.ca

S. KULLIK
Department of Environmental Biology

(2008-2010)

(2009-2011)

University of Guelph, Guelph, ON N1G 2W1
kullik.sigrun@gmail.com
S. LACHANCE

(2010-2012)
University de Guelph - Campus D’ Alfred
31 St. Paul Street, Alfred, ON KOB 1A0
slachance@alfredc.uoguelph.ca
K. RYALL (2009-2011)
Canadian Forest Service, Great Lakes Forestry Centre, Natural
Resources Canada, 1219 Queen Street East,
Sault Ste. Marie, ON P6A 2E5

kryall@nrcan.gc.ca

K. RYAN

Faculty of Forestry, University of Toronto
Toronto, ON MS5S 3B3

kathleen.ryan@utoronto.ca

1. SCOTT

Agriculture and Agri-Food Canada
1391 Stanford Street, London, ON NSV 4T3
ian.scott@agr.gc.ca

(2008-2010)

(2010-2012)

FELLOWS OF THE ENTOMOLOGICAL SOCIETY OF ONTARIO

W. W. BILL JUDD

C. RON HARRIS
GLENN WIGGINS
BERNARD PHILOGENE
FREEMAN MCEWEN

Library, University of Guelph

Guelph, ON NIG 2W1

jimbrett@uoguelph.ca

Newsletter Editor: J. ALLEN

Ontario Ministry of Agriculture, Food and Rural Affairs
1 Stone Road West, Guelph, ON NIG 4Y2
jennifer.allen@ontario.ca

Student Representative: J. GIBSON
Department of Biology, Carleton University
1125 Colonel By Drive, Ottawa, ON K1S 5B6
jgibsonS@connect.carleton.ca

Website: M. JACKSON

School of Environmental Science

University of Guelph, Guelph, ON NIG 2W1
jackson@uoguelph.ca

JESO Editor: M. RICHARDS

Dept. of Biological Sciences, Brock University
St. Catharines, ON L2S 3A1
miriam.richards@brocku.ca

Technical Editor: J. VICKRUCK
Dept. of Biological Sciences, Brock University
St. Catharines, ON L2S 3A1
jess.vickruck@brocku.ca

Associate Editors:

A. BENNETT

Agriculture and Agri-Food Canada

960 Carling Ave., Ottawa ON K1A 06C

N. CARTER

Engage Agro Corporation

1030 Gordon St., Guelph, ON, N1G 4X5
neilcarter@engageagro.com

C. SCOTT-DUPREE

Dept. of Environmental Biology

University of Guelph, Guelph, Ontario NIG 2W1
cscottdu@uoguelph.ca

J. SKEVINGTON

Agriculture and Agri-Food Canada

Eastern Cereal and Oilseed Research Centre
960 Carling Ave., Ottawa, ON K1A 0C6

2002
2003
2006
2010
2010

MCZ
JESO Volume 14 lAR Y

JOURNAL \AN -
of the

NN

ENTOMOLOGICAL SOCIETY OF ONTARIO) v="

VOLUME 141 2010

In my previous Editor’s message, I commented that in an age where entomologists
are becoming a rare species, an adaptive response is to broaden our perspective on
entomology to include all science focused on insects. When I first joined the ESO and
attended my first ESO conference, Yves Prevost, the previous JESO Editor, asked me in a
very friendly manner, whether I had just moved to Ontario. I replied that no, I had been
at Brock for five or six years. Yves asked why I had not been at previous meetings, and |
replied that I wasn’t really sure that I was an entomologist. Yves looked really puzzled, and
inquired if I studied insects. When I told him that I studied bees, he responded ‘Well, then,
you are an entomologist!” I have always treasured that conversation, because it represented
to me such a broad and welcoming perspective in defining entomology. This perspective
has also guided me as Editor of JESO — all sorts of insect science are welcome at ESO and
JESO.

[have been Editor of JESO for about 5 years, starting with Volume 135 (2005) which
I co-edited with Yves. I am very pleased that we have managed to accomplish so much in
that time. The Journal is back to a regular, annual publication cycle and is now distributed
electronically from the ESO website, as well as being published in the more classical paper
format. An exciting development is a plan to include JESO in a large electronic journal
listing service which will lead to a quantum leap in journal visibility. Although final details
are not yet settled, I anticipate that this listing will begin with the current volume. Another
exciting development is a plan to have all back issues made available electronically in the
near future.

With these developments, JESO will have successfully accomplished the mission
that I set out when I first became Editor. I sincerely thank Yves, all the Associate Editors,
and the ESO Board for entrusting JESO to me, in the process convincing me, that yes, I
am an entomologist. I am very proud of our accomplishments and very gratified that I
can pass the baton to a new Editor, knowing that JESO is thriving. I will be co-editing
Volume 142 (2011) with a new Editor, who I am sure will guide the Journal through its next
developmental phase.

Happy reading!

Miriam H. Richards
Editor

a ia : } ‘ a
|

Aerial foraging in burying beetles JESO Volume 141, 2010

AERIAL FORAGING AND SEXUAL DIMORPHISM IN BURYING
BEETLES (SILPHIDAE: COLEOPTERA) IN A CENTRAL
ONTARIO FOREST

D. L. LEGROS AND D. V. BERESFORD!
Department of Biology, Trent University, 1600 West Bank Drive,
Peterborough, ON, Canada K9J 7B8
email: davidberesford@trentu.ca

Abstract J. ent. Soc. Ont. 141: 3-10

Burying beetles (Coleoptera: Silphidae) are commonly sampled on the
ground using pitfall traps. Recent work has shown that these beetles also
respond to aerial traps baited with carrion. In this study, we sampled the
Silphidae of Algonquin Park using traps baited with mouse and bird carrion,
and set at 2, 4, and 6 m heights. The most abundant species caught was
Nicrophorus tomentosus, followed by (in order) N. defodiens, N. sayi,
Oiceoptoma noveboracense, N. pustulatus, Necrophila americana, and
Necrodes surinamensis. Only N. tomentosus showed bait preference, with
higher than expected catches at traps baited with mice. Catches differed
based on trap height for two species, with most N. defodiens being caught
in the lower traps (2 m), and all N. pustulatus caught at the high traps (6
m). Nicrophorus tomentosus males caught in the 6 m traps were significantly
larger than males caught in the lower traps, and females caught at all heights.
Possible reasons are discussed.

Published November 2010

Introduction

The carrion beetles (Family Silphidae) have long been a favourite group with
collectors and naturalists in North America. There are 30 species of these in North America,
and individual species specialize in carrion types based on size and source, ranging from
large carcasses such as black bears (Watson and Carlton 2003) (e.g. subfamily Silphinae),
to small rodent sized carcasses such as mice and song birds (subfamily Nicrophorinae, the
burying beetles; Anderson and Peck 1985). Burying beetles use olfactory cues to locate
carcasses, and are able to locate fresh squirrel carcasses several metres distant in a few
minutes (Dethier 1947).

' Author to whom all correspondence should be addressed.

LeGros and Beresford a el ‘JESO Volume 141, 2010

In spite of the attention that this group has attracted in the past, basic life history
and niche information is still lacking. For example Nicrophorus pustulatus Herchel was
only recently determined to be a parasitoid on snake eggs (Blouin-Demers and Weatherhead
2000; Keller and Heske 2001). Regional surveys of extant Nicrophorus species do report
catching N. pustulatus in low numbers (e.g., Anderson 1982; Shubeck et al. 1981), and
outside of the range of the black rat snake (Smith et al. 2007). It appears that N. pustulatus
must utilize some other unknown source of carrion.

What this is may be consistent with the recently observed vertical distribution of N.
pustulatus in Georgia, where N. pustulatus were almost exclusively caught several metres
above ground (Ulyshen and Hanula 2007a) in the forest canopy. The canopy habitat includes
tree cavities, and these could offer a specialized niche of carrion such as dead nestlings, e.g.
squirrels, birds, or bats. Any species differences in how this habitat is exploited should be
reflected in catches obtained using carrion baited traps placed at various heights.

In this study, we report on the species composition of Silphidae caught in carrion
baited traps placed at three different heights above the ground in Algonquin Park, a large
forested region of central Ontario. We also compared trap catches at traps with avian and
mammalian baits.

For burying beetles, there are reproductive advantages to size, with larger species
and individuals winning fights over carcasses (Otronen 1988; Trumbo 1990). Body size is
also related to flight capability. During flight, beetles lose heat due to convection (Merrick
and Smith 2004), so that conserving heat would enable longer flights, for example, flight
associated with searching or localized dispersal. Such flights would take place at higher
levels (Taylor 1974), so we would expect elevated traps to catch these individuals. For the
most numerous species caught, NV. tomentosus, we tested for differences in the size of males
and females at each height, reasoning that such size differences might indicate sex biased
flight capability associated with dispersal from natal sites.

Materials and Methods

Silphid beetles were collected during August 2008, in Algonquin Provincial Park,
Ontario, Canada. The study site was located along Highway 60, at kilometre 20, Found
Lake, Peck Township on the Canadian Shield. The forest was composed of mature trees:
maple (predominantly Acer saccharum Marsh.), beech (Fagus grandifolia Ehrh.), hemlock
(Tsuga canadensis (L.) Carr.), and birch (Betula papyrifera Marsh and Betula allegheniensis
Britton). The understory was shaded, was easily accessible by foot, and composed mainly
of bracken (Pteridium aquilinum (L.) Kuhn) with some low density shrubs.

Twenty-four traps were deployed for seven day periods beginning 1, 7, and 14
August 2008, for a total of 72 samples. During sampling, many traps were destroyed by
wildlife (bears and raccoons) and wind. If damage occurred early in the sampling week,
traps were re-installed for later collection, so that the length of a trapping period varied for
some traps. Fourteen ruined traps could not be replaced. For each sampling week, traps
were positioned in a grid or block comprised of three rows of eight traps per row. The rows

Aerial foraging in burying beetles JESO Volume 141, 2010

were spaced 15 m apart, with traps in each row spaced 10 m. Traps were placed at 2, 4, and
6 m above ground, with 6 m traps placed in the upper trunk zones but just below the canopy
level. Trap height and bait type were randomized over the 24 possible locations in each
block (there were eight possible X and three possible Y coordinates), so that there were
four traps for each bait type at each height in the block.

Traps were constructed from 2 L plastic soda pop bottles with a 6 cm diameter
hole cut into the middle of one side to allow beetles to enter the traps. Bait was wrapped in
cheese cloth and hung in each bottle by a piece of wire pushed through the lid. The bottom
of each trap had a 1.5 cm deep layer of killing solution consisting of 5% dish soap and water
(Larsen 2005). A sling shot was used to send a weighted rope over a tree branch to raise
and lower traps.

Half the traps were baited with chicken wings and the other half with mice. Frozen
domestic mice (Mus musculus) were obtained from a reptile feed supply store. The mean
weight per mouse was ~ 25 g. Frozen chicken wings were obtained in bulk from the grocery
store (mean weight ~ 30 g). Baits were frozen until placed in traps without any prior aging
or ripening.

Trapped beetles were preserved in 70% isopropyl alcohol. A sub-sample of 320
Nicrophorus tomentosus, about 100 specimens from each height, were sexed and measured
for total body length.

Because of the missing data, ANOVA could not be used to test the effects of bait
type and trap height on trap catches. Instead, we used a chi-square test (Sokal and Rohlf
1995) to compare the observed to expected total catch frequencies of each species for
bait type and trap height. The expected frequencies were determined from the number of
trapping days for each category. For example, if 140 individuals of a species were caught
over 50 trapping days at traps baited with mice, and 220 were caught over 100 trapping days
at traps baited with birds, then the expected frequencies would be (140+220) x (50/150)
=120 for mouse traps and (140+220) x (100/150) = 240 for bird traps. Because several
comparisons were performed for each test, the critical values of chi-square at a significance
level of a = 0.05 were adjusted using the Bonferroni method by which a’ = a/k (Sokal and
Rohlf 1995). For the bait tests and the trap height tests we used k = 7 (number of species
tested). Our adjusted critical values for chi-square were 9.94 for 2 degrees of freedom
(three trap heights), and 7.33 for 1 degree of freedom (two bait types).

We tested whether there were differences in body length of N. tomentosus
between males and females at each height using a 2-way ANOVA with trap height and sex
as treatments. Statistical tests were done using an Excel spreadsheet and STATISTICA 7
(Statsoft Inc. 2004).

Results

We caught 2388 Silphidae from 7 species in the traps (Table 1). The most abundant
species was Nicrophorus tomentosus, accounting for 81% of the total catch. The rarest
species was Necrodes surinamensis, of which only a single individual was caught, this
at 4 m. Members of each species were more abundant in the 2 m traps except for N.

LeGros and Beresford JESO Volume 141, 2010

TABLE 1. Number of each species of Silphidae captured in carrion baited aerial traps at
three different heights in Algonquin Park, Ontario, in August 2008.

Trap height
Species . 2m 4m 6m Total
Nicrophorus tomentosus 863 497 585 1945
Nicrophorus defodiens 19] 76 42 309
Nicrophorus sayi 43 22 25 90
Oiceoptoma noveboracense 21 7 5 33
Nicrophorus pustulatus 0 0 6 6
Necrophila americana * 0 0 -
Necrodes surinamensis 0 l 0 l
Total 1122 603 663 2388

pustulatus, which was only found in 6 m traps (Table 1). MN. tomentosus was the only
species for which trap catches differed by bait types, with slightly more caught at mouse
baited traps than expected (observed = 856, expected = 791.9; Table 2).

More N. defodiens were caught in the lowest traps and more N. pustulatus in the
higher traps (Table 2). For the other species, observed trap catches at the three heights did
not differ from the expected proportions.

The biggest male N. tomentosus were caught in the 6 m traps; these were
significantly larger than females caught at all heights (Duncan’s Multiple Range post-hoc
test, 2 metres: p=0.003; 4 metres: p=0.024; 6 metres, p=0.025) and males at 2 metres (2
metres: p=0.012; 4 metres, p=0.07) (Table 3, Fig. 1).

20
15
10

female

male
a=_,
Oo

rs)

number per size class
N
—)

0

2 metres 4 metres 6 metres

length mm
FIGURE 1. Frequency distribution of body lengths of female and male N. tomentosus at 2,

4, and 6 metre traps.

JESO Volume 141, 2010

Aerial foraging in burying beetles

ee CEC SS eS eee ee
Lv (79°) p8°61

Ly-—APT TC) OC TZ wg

ES (€6'1) 96°61 Sr C512) uc 07 Wp

OL (ELI) IL'6I 6S (00°7) SZ'0Z wz

SEG ee eee es oy. SSlts Los ee een oo ee See oes
SS © Par a ee ee ee

Se me EE LE Ds A ee ee ee ee

‘8007 Isnsny ut

‘OLIRIUO “‘yled umnbuos;y ul s]ystoy JUDIOFJIP IoIY} 7e sdey [Bllov poyleq UOLLUe9 UI jysneo SNSOJUIUO] *N' JO (uwruL) sy}sud] uevoW “€ A IGAVL

“Wys1oy dey 10} Gp Z) p6"6 pur adAy Weq Joy GP 1) Eg'L = "orenbs-1yo ‘cQ"Q = 0 1 ueoyrUaIS,

(S0°EO) ¢ 0 0 OI ‘e're) sss (ZS) SZ 4(6L°0 F'0)9 (67 ‘FZ ZH LI (8Z1) wg
(8:0 ‘r'0) L (er 10) I O WLI for O77") cz 0 (Tr‘s'h) 94 OT (OTT) Wp
(pI “6'0) IZ 0 (O0‘7O)r (78h ‘9 LE) €98 (S°7 ‘6'1) Eb Ox(SL ‘p'8) 161 €% (9LT) WZ
(60 ‘€0) L 0 C070) x(S'sp TLE) 968 OZ 6D (Z0‘T0)Z (LS ‘L'S)O€1 €Z CLI) asnow
(ZI “8°0) 92 (Z'0 “€0'0) I 0 (69€ ‘O'EE) 6801 (FZ ‘P19 (SSO‘TO)b (€'9 P'S) OLI EE (6bz) psig

ISUIIDAOGIAOU ‘O SISUIUDULANS *\J- DUDI1AAUD ‘N SNHSOJUIUO] ‘NJ 1ADS ‘N

snpjnisnd ‘nN suaipofap ‘NN (skeq) A10801e9

sa1oeds Aq (QS ‘uRayAy) yoIe9 [RIO],

SS ee eS ee Be ee eS Eo IS

‘(skeq)
A1039}e9 yord Joy skep Suiddey yo wins oy) uo paseq o1am sainuonbay payoodxg “o poysn{pe ruoueyuog ev uo pasegq onyea [onto ou}

YIM 3S} oreNbs-1y9 v BUISN pojso} DOM sJUDUNRAIL, “gNOZ IsN3ny Ul “OWRIUCO “yeg uINbuos;y ul “(Wg “Wp ‘W Z) 1YySIOY den pue
‘(osnoul pur pig) 9dAj y1eq Aq ‘poinjdeo oeprydyis jo sorsads Yovd JOJ “SUONRIASp plepurys puv suvow dey Jod ‘sye}o) [euOseaS “7 FTAVL

LeGros and Beresford JESO Volume 141, 2010

Discussion

Nicrophorus tomentosus and N. defodiens were the most common species captured
in this study. Work done in North Carolina has shown that these species are frequently
encountered late in the warm season (Trumbo 1990). In southern Ontario, N. tomentosus
breeds from mid to late summer (Anderson and Peck 1985), with trap catches peaking in
late August (Anderson 1982); N. defodiens is active from May to early September and has
been trapped at similar levels during this period (Anderson 1982). Nicrophorus sayi, a
spring breeder in Ontario (Anderson 1982) was the third most common species captured,
consistent with a previously reported peak in early and late August of teneral adults
(Anderson 1982).

Only N. tomentosus showed any bait preference, with a minor preference for traps
with mice. For the Nicrophorus spp., small carrion would include dead fledglings as well
as dead rodents. In terms of possible tree hole exploitation, both types of carrion would be
present. Generally, Silphinae are attracted to larger carrion (Anderson and Peck 1985).

Height Preference

Nicrophorus were caught at all heights except N. pustulatus and N. defodiens.
Nicrophorus defodiens is a small species, and it compensates for this competitive
disadvantage by being able to locate carcasses quicker than its larger competitors, such as
N. orbicollis Say (Trumbo and Bloch 2002). That it was caught less often in the higher traps
may reflect a possible decreased flight height due to its smaller size rather than its inability
to find the bait. |

Our results support our initial reasoning that carrion in the forest canopy might be a
suitable specialized niche for exploitation for N. pustulatus. Our low catch of 6 individuals
is similar to low catches reported in previous studies (Anderson 1982; Robertson 1992).
Nicrophorus pustulatus does not appear to respond to traps baited with fresh carcasses
(Trumbo 1990). However, it has been caught in pitfall traps baited with well-rotted carrion
(Trumbo 1990; Anderson 1982).

Catching N. pustulatus at elevated traps is consistent with earlier work (Ulyshen
and Hanula 2007b). In Ontario, Robertson (1992) caught N. pustulatus at 1m to 2m. Low
catches of N. pustulatus at ground level could be due to this species specializing in canopy
or nest-cavity habitats rather than specific carrion sources; N. pustulatus will breed on dead
rodents in lab settings (Robertson 1992).

Nevertheless, black rat snake eggs are the only known wild breeding medium
(Smith et al. 2007; Blouin-Demers and Weatherhead 2000), which may explain the generally
low numbers caught using mammalian or avian baits. Because of this, the presence of N.
pustulatus is relevant to the conservation of regionally rare or endangered snake species
(Smith et al. 2007) e.g. the black rat snake Elaphe obsoleta (Say) in Ontario, a species not
found in Algonquin Park (Logier 1970). Our results suggest that surveying for NV. pustulatus
should include aerial traps.

Sex and Size Dimorphism in Nicrophorus tomentosus
For N. tomentosus, because males and females both remain with their brood after

8

Aerial foraging in burying beetles JESO Volume 141, 2010

covering a carcass, it is unlikely that there is a size advantage for one sex or the other in
terms of contests over carcasses. However, there may be a size advantage in terms of flight
capability. During flight, beetles lose heat due to convection (Merrick and Smith 2004), so
that conserving heat would enable longer flights, for example flight associated with local
dispersal. Nicrophorus tomentosus is a bumble bee mimic (Fisher and Tuckerman 1986),
and is covered in yellow hairs (Milne and Milne 1944), which can contribute to conserving
heat and regulating body temperature in Nicrophorus spp. (Merrick and Smith 2004).

The female Nicrophorus tomentosus we caught were the same size at all trap
heights, whereas males caught on 6 m traps were significantly larger than both females and
males from lower traps (Table 3). Trumbo (1990), found no difference in the size of male
and female Nicrophorus tomentosus, nor did we in our lower traps. The larger males were
largely present in 6 m traps only (Fig. 1). Sampling at the higher traps would over-represent
this group.

Acknowledgments

The authors thank Dr. James Sutcliffe of Trent University, Algonquin Provincial
Park biologist B. Steinberg, as well as Peter Mills, Nathan G. Miller, and Natalie Earl for
their assistance.

References

Anderson, R. S. 1982. Resource partitioning in the carrion beetle (Coleoptera: Silphidae)
fauna of southern Ontario: Ecological and evolutionary considerations. Canadian
Journal of Zoology 60: 1314-1325.

Anderson, R. S. and S. B. Peck. 1985. The Carrion Beetles of Canada and Alaska. Coleoptera:
Silphidae and Agyrtidae. The Insects and Arachnids of Canada, Part 13. 121 pp.

Blouin-Demers, G. and P. J. Weatherhead. 2000. A novel association between a beetle and
a snake: parasitism of Elaphe obsoleta by Nicrophorus pustulatus. Ecoscience 7:
395-456.

Dethier, V. G. 1947. The role of the antennae in the orientation of carrion beetles to odors.
Journal of the New York Entomological Society 55: 285-293.

Fisher, R. M. and R. D. Tuckerman. 1986. Mimicry of bumble bees and cuckoo bumble bees
by carrion beetles (Coleoptera: Sylphidae). Journal of the Kansas Entomological
Society 59: 20-25.

Keller, W. L. and E. J. Heske. 2001. An observation of parasitism of black rat snake (Elaphe
obsoleta) eggs by a beetle (Nicrophorus pustulatus) in Illinois. Transactions of the
Illinois State Academy of Science 94: 167-169.

Larsen, T. 2005.:Trap spacing and transect design for dung beetle biodiversity studies.
Biotropica 37: 322-325.

Logier, E. B. S. 1970. The snakes of Ontario. University of Toronto Press, Toronto. 94 pp.

LeGros and Beresford . JESO Volume 141, 2010

Merrick, M. J.and R .J. Smith. 2004. Temperature regulation in burying beetles (Nicrophorus
ssp. Coleoptera: Silphidae): effects of body size, morphology and environmental
temperature. The Journal of Experimental Biology 207: 723-733.

Milne, L. J. and M. J. Milne. 1944. Notes on the behavior of burying beetles (Nicrophorus
spp.). Journal ofthe New York Entomological Society 52: 311-327.

Otronen, M. 1988. The effect of body size on the outcome of fights in burying beetles
(Nicrophorus). Annales Zoologici Fennici. 25:191-201.

Robertson, I. C. 1992. Relative abundance of Nicrophorus pustulatus (Coleoptera: Silphidae)
in a burying beetle community, with notes on its reproductive behavior. Psyche 99:
189-198.

Shubeck, P. P., N. M. Downie, R. L. Wenzel and S. B. Peck. 1981. Species composition and
seasonal abundance of carrion beetles in an oak-beech forest in the Great Swamp
National Wildlife Refuge (N.J.). Entomological News 92: 7-16.

Smith, G., S. T. Trumbo, D. S. Sikes, M. P. Scott and R. L. Smith. 2007. Host shift by
the burying beetle, Nicrophorus pustulatus, a parasitoid of snake eggs. Journal of
Evolutionary Biology 20: 2389-2399.

Sokal, R. R. and F. J. Rohlf. 1995. Biometry. W. H. Freeman and Company, New York.

StatSoft Inc. 2004. STATISTICA (data analysis software system), version 7. http://www.
statsoft.com.

Taylor, L. R. 1974. Insect migration, flight periodicity and the boundary layer. Journal of
Animal Ecology 43: 225-238.

Trumbo, S. 1990. Reproductive success, phenology and biogeography of burying beetles
(Silphidae, Nicrophorus). The American Midland Naturalist 124: 1-11.

Trumbo, S. and P. L. Bloch. 2002. Competition between Nicrophorus orbicollis and N.
defodiens: resource locating efficiency and temporal partitioning. Northeastern
Naturalist 9: 13-26.

Ulyshen, M. D. and J. L. Hanula. 2007a. Burying beetles (Coleoptera: Silphidae) in the
canopy: The unusual case of Nicrophorus pustulatus Herschel. The Coleopterists
Bulletin 61: 121-132.

Ulyshen, M. D. and J. L. Hanula. 2007b. A comparison of the beetle (Coleoptera) fauna
captured at two heights above the ground in a North American temperate deciduous
forest. American Midland Naturalist 158: 260-278.

Watson, E. J. and C. E. Carlton. 2003. Spring succession of necrophilous insects on wildlife
carcasses in Louisiana. Journal of Medical Entomology 40: 338-347.

10

Natural enemies of Ceratina in the Niagara Region JESO Volume 141, 2010

:
: NATURAL ENEMIES OF THE BEE GENUS CERATINA

! (HYMENOPTERA: APIDAE) IN THE NIAGARA REGION,
: ONTARIO, CANADA

J. L. VICKRUCK’, J.T. HUBER? AND M. H. RICHARDS

Department of Biological Sciences, Brock University,
St. Catharines, ON, Canada L2S 3A1
email: jess.vickruck@brocku.ca

Abstract J. ent. Soc. Ont. 141: 11-26

Ceratina dupla and C. calcarata (Hymenoptera: Apidae) are abundant bees
in southern Ontario, commonly nesting in staghorn sumac (Rhus typhina),
wild raspberry (Rubus strigosus) and teasel (Dipsacus fullonum). Ceratina
nests were collected from April-September 2008 and parasitized individuals
were reared to adulthood in the laboratory. Pyemotes sp. (Pyemotidae) and
Baryscapus americana (Eulophidae) were the most common natural enemies,
followed by Baryscapus sp., Axima zabriskiei, and Hoplocryptus zoesmairi.
Eupelmus vesicularis, Coelopencyrtus sp. and Eurytoma sp. near apiculae
were rarely collected. This is the first record of E. vesicularis (Eupelmidae)
as a primary host on any member of the family Apidae. New host records are
also reported for H. zoesmairi (Ichneumonidae), two different Baryscapus
spp. (Eulophidae), Eurytoma sp. near apiculae (Eurytomidae) and Pyemotes
sp. (Pyemotidae) on C. calcarata and C. dupla. Detailed descriptions of
immature development of the parasitoids, and their preferences for host bee
species and host plant species are provided.

Published November 2010

Introduction

Parasite—host relationships have been studied for numerous species in a laboratory
setting (Harri et al. 2008; Jervis et al. 2008; Traynor and Mayhew 2005). These studies are
vital to help understand the dynamics of host—parasite interactions, however they often only
involve the most common one or two parasitoids associated with the host under study. Ina

' Author to whom all correspondence should be addressed
* Canadian National Collection of Insects, Arachnids and Nematodes, Ottawa, ON,
K1A 0C6

11

Vickruck et al. . JESO Volume 141, 2010

natural setting, hosts may be parasitized by a number of species af varying frequencies, each
using different parasitism and developmental strategies at different times. By describing
the life history, development and preferences of numerous parasite species attacking one
host, a more complete understanding of these interactions is gained.

Bees of the genus Ceratina Latreille (often referred to as dwarf carpenter bees),
are cosmopolitan, with the subgenus Zadontomerus Ashmead being found exclusively in
the Western Hemisphere (Michener 2007). The life history of Ceratina offers an excellent
opportunity to study the development and interactions of parasites with their hosts. All
offspring from eggs laid by a single female can be collected together in a nest, thus allowing
for observation of how the parasites interact with an individual host, as well as how nest
substrate, position in the nest, and interactions with other parasites and the foundress bee
occur.

The Niagara Region, Ontario, Canada, is home to two common species of Ceratina
(Zadontomerus): C. dupla Say and C. calcarata Robertson. Their nests are commonly
collected from staghorn sumac (Rhus typhina L.), wild raspberry (Rubus strigosus Michaux)
and teasel (Dipsacus fullonum L.; J. Vickruck, unp. data). Both sumac and wild raspberry
are native to the region whereas teasel is an obsolete crop plant introduced from Europe,
whose flower heads (when the seeds are mature) were once used to raise the knap on
wool (Rector et al. 2006). Sumac and raspberry are both perennial plants found at wood
margins, differing from teasel which is a biennial weed found in open, generally abandoned
agricultural fields.

Ceratina in the Niagara region are solitary and-univoltine, producing one brood
per year and overwintering as newly emerged, unmated adults (J. Vickruck, unpublished
data). Emergence and mating typically take place in mid-April, and new nests are founded
in May. Nests are not reused from year to year and can only be initiated in twigs with
exposed pith. After digging a linear tunnel females begin to forage, forming pollen and
nectar provisions into rounded masses upon which a single egg is laid (Grothaus 1962;
Johnson 1988; Kislow 1976). Each provision mass and egg is separated from its neighbours
by a cell septum formed by the foundress. Once finished provisioning, females sit and
guard the nest entrance until the eclosion of their offspring. The newly eclosed adults can
either overwinter in their natal nest or disperse to found new hibernacula for the winter
(Grothaus 1962; Kislow 1976).

Ceratina immatures can be classified into 18 developmental stages which were
originally described by Daly (1966) for C. dallatoreana. The first eight stages rank the
pupa in relation to the size of the pollen ball, after which the immature passes through a
pre—pupal stage followed by metamorphosis. The eyes of the pupa then pass from white
through to black (five stages), followed by darkening of the body (four stages). In the final
stage the black bodied pupa emerges as an adult with milky wings.

Natural enemies of Ceratina in the Niagara region include predators, parasites,
and parasitoids. Predators consume more than one prey individual in order to complete
development. Parasites feed on the host contents but do not consume the entire host
before completing development (Godfray 1994). Parasitoids consume a single host in
order to complete development (Godfray 1994). Parasitoids were classified as idiobionts
or koinobionts, endoparasitoids or ectoparasitoids, and gregarious or solitary. Idiobionts
prevent the larva from developing further after initial parasitisation (Askew and Shaw 1986).

12

Natural enemies of Ceratina in the Niagara Region JESO Volume 141, 2010

Koinobionts do not kill the host until it has reached a certain point in its development,
as the parasitoid benefits from the continued life of the host (Askew and Shaw 1986).
Ectoparasitoids develop outside the host (although they are often attached to it), while
endoparasitoids consume the host internally. In solitary species the parasitoid to host ratio
is 1:1, whereas in gregarious parasites multiple individuals develop in one host.

The objectives of this study were to identify and describe the development of
the natural enemies of Ceratina in the Niagara Region as well as quantify their host and
substrate preferences.

Materials and Methods

Host nest collections

All parasites were reared from a total of 107 nests of C. calcarata and C. dupla
collected from 14 April to 30 September 2008. Each week at least 15 Ceratina nests were
collected so that sampling effort was consistent over the season. Supplementary nest
collections also took place in June 2009 to aid with final parasite identifications only. The
2009 data are not included in the statistical analysis. All collections took place at the Brock
University campus (43.1197, —79.2492), the Glenridge Quarry Naturalization Site (43.1223,
—79.2375) and an abandoned old field site near the Welland Canal (43.1479, —79.1811).
Nests were collected from sumac, raspberry, and teasel and brought back to the laboratory
in early morning to ensure that all occupants were present inside. After being chilled, twigs
were carefully split open longitudinally to identify nest contents. Bee species, plant nest
substrate, position of any parasitized cells in the nest, and developmental stages of bees
and parasites were recorded on the day of collection. Dissected nests were then inserted in
transparent PVC tubing slightly larger than the diameter of the nest (ranging from '2—1 inch
depending on twig diameter) for protection and to allow for easy visual observation of nest
contents. This also allowed for behavioural observations of host—parasite interactions in
the laboratory.

Ceratina species were identified using the key of Rehan and Richards (2008).
Parasite identifications were made by JTH and Dr. Gary Gibson at the Canadian National
Collection of Insects, Arachnids and Nematodes (CNC), Dr. Michael Gates at the National
Musuem of Natural History (NMNH) in Washington, DC, as well as JV. Dr. Andrew
Bennett (CNC) verified identity and nomenclature of Hoplocryptus zoesmairi Dalla Torre.
Voucher specimens of Baryscapus sp. and americana, Eupelmus vesicularis (Retzius),
Coelopencyrtus sp., Axima zabriskiei Howard and Eurytoma sp. near apiculae, were
deposited in the CNC. Baryscapus sp., Coelopencyrtus sp., Eupelmus vesicularis and
Eurytoma sp. near apiculae are labelled as CNC Ident. lot # 2008-341, and Baryscapus sp.,
Axima zabriskiei and H. zoesmairi as 2009-188.

Parasite development and classification

Hosts were observed on a daily basis to detect parasitoid presence. Position in
the nest, stage parasitized, and parasitoid species were recorded as soon as they became
apparent. Developmental milestones such as defecation, pupation, pigmentation of the
exoskeleton as well as emergence dates were recorded for parasites whenever possible.

13

Vickruck et al. JESO Volume 141, 2010

Once parasitoids had pupated they were transferred to their own individual 0.2 mL
microcentrofuge tubes prior to eclosion. Upon emergence parasitoids were placed in 70%
ethanol for later identification.

Data Analysis

All data were analyzed using SAS 9.1.. Parasite prevalence is defined as the
number of individuals affected by a particular parasite species divided by the number
of hosts examined (Margolis et al. 1982). Parasite frequency is defined as whether that
particular species is present in the nest, regardless how many individuals in the nest were
parasitized. G-tests for goodness of fit were used when sample sizes were large, Fisher’s
exact tests were used when expected values were small (<5). Hoplocryptus zoesmairi has
not been included in statistics as it is a predator.

Results

Host parasitism

Eight species of arthropod parasites representing two classes (Insecta, Arachnida),
two orders (Hymenoptera and Trombidiformes), and seven families were reared from a
total of 107 C. dupla and C. calcarata nests containing 850 brood cells. Characteristics
of these eight species are compared in Table 1. Of the 107 nests collected, 64 were
teasel, 36 raspberry, and 7 sumac. Twenty-nine percent (243/850) of all brood cells were
parasitized, and 68% (73/107) of nests contained at least one parasite. Ceratina calcarata
had a significantly higher proportion of cells parasitized than C. dup/a but the proportion
of nests parasitized between host species did not differ significantly (Table 2). Parasitism
for each Ceratina species also varied by substrate, with significantly higher proportion of
cells and nests parasitized in raspberry compared to teasel (Table 2). Ceratina calcarata
was parasitized more often than C. dupla when nesting in raspberry (G=20.05, d.f.=1,
P<0.0001), however no difference was seen between species in teasel (G=0.04, d.f=1, n.s.)
Sumac nests were not included in substrate comparisons due to small sample size. Ceratina
dupla nesting in raspberry was the least parasitized with 15% of available cells affected
(Table 2, Fig. 1). Only seven sumac nests were found, all C. calcarata, in which 16/33
(48%) of immatures had been parasitized (Fig. 1).

Parasite and predator development

The frequency and prevalence, i.e., proportion of hosts affected, of all parasites
and predators in Ceratina nests is presented in Table 3 for affected cells and Table 4 for
affected nests. Detailed observations for each species are given below.

Predators
Hoplocryptus zoesmairi (Dalla Torre) (Hymenoptera: Ichneumonidae)
This species has previously been associated with C. dupla (as Habrocryptus

graenicheri Viereck; Viereck 1904). Hoplocryptus Thomson has until recently been
considered a junior synonym of Aritranis (Férster) (Yu and Horstmann 1997), but Yu et

14

JESO Volume 141, 2010

Natural enemies of Ceratina in the Niagara Region

‘pupaidaup sndvasdavg uo proysesediadAy ev aq Avyy (9
‘OBAIL] UMOIS [[NJ SB INJUIMIDAO SplozseIeg (q
BAIL] UO JO JUDWIOJIAODP dU} UI PoUNsUOd oIe soINyeULUT BUNeIDD sjdniny (e

so1seds sosvys jednd Auaqdsey pjpspajp2 “ys aytseredoyoq
YIOg IO} P1ODII JSOY MON pure [eAle] [[Y snouesoin ‘[asealL ‘pidnp ‘9d [eInudyH (sepnowsd,) ‘ds sajowadgy
(8761 ney ‘0961 usIquiory SnoLesoiH
‘9L6[ MOSES) DIDADIIVI “Dd oednd pata dVUING YIDADIIVI ‘Dd ploysesedojoq (oepru0yAing )
pue vjdnp > uo poyioday -a11yM ‘oedndaig 30 Areyjog = ‘Aueqdsey = ‘vyjdnp ‘5 JUOIQOIP] 101YSIAGDZ DUIIXP
DIDADIIDI
‘) pl10da1 JSOY MON “(996 proysesedojoq (oepruoyAing )
d0qsng) vuljp1ay) UO poyioday BAIR] ISIC] Arey]OsS [aseay, DIDADIIVI ‘Dd JUOIQOIP] avjnaidp resu ‘ds puojduny
soy | Sev oepidy plozisesedojoq (ovprujodnq)
A[ Ue} 1OJ p1OIOI soy MoNoednd poXo-azTy A AreyI]OS joseay, §8=,o7dnp ‘a JUOIQOIP] SLADINIISAA Snujadny
(L961 Aled) eipavajp9 (0Z<) proyiseredopug (oepidoug)
‘) uo poyiodal zanjdy ‘Ds ORAIe] WINIpayy snoliesa1H ovuINg YIDADIIVI “Dy JUOIQOUIOY ‘ds snjadouadojaoy
aaoge | ‘ds sndpostung q oednd podo (r1-8) ovuins ployiseredopuyq (oeprydojng)
JO} Sp1O99I JSOY SNOIASId sag —oyYM ‘ovdndaig snowessn ‘Auaqdsey vyp1pIj1v9 ‘9D JUOIQOUIOY ‘ds sndposduvg
pidnp ‘D pi0se1 ysoy Mou ‘(9/6] sednd pata ayy (I<)
MOIST “87H NY) BIDADIIVDI A|jeuoiseo00 Auoqdsey pjpspojp2 ‘yD ptoysesedopugq (aeprydojng)
‘) Wolf poyiodal snupoiaup “g ‘oedndaig snoresain ‘[asealL ‘pidnp ‘9D JUOIQOUIOY puvoaidaup sndpasduvg
DIDADIIDI “7 PlODAI JSOY
MOU “(SG JOYSIUSBID ‘POG Alloqdsey pjp41p2]09 “D (oepruounsuyoy)
YIOI9IA_) Djdnp ‘Dd uo payioday svVAIVT JOJepold ‘aseoy ‘ojdnp ‘a lowepag luipuisaoz snjddusojdoyy
ysoy aod
poyoee SIIWIIUI = =—_- OJV.AYSQNs sa1eds
P10III JSOY SNOTAIAG SISBIS JSOH [BAnjVN] SUTQSIU JSOHY }SOH ASOOIg IOJVPIAg /IISVIV

"SOULOJIPIQUIOI], 0} SSuUOTOq YoIyM ‘ds sajowady daoxo viaydouswiAP |e oe satoads
YJ, “UOISOY BIeSeIN Oy) Ul YJDUDI/DI ‘D pue Yjdnp DUlJYAa_D JO SoIWdUd [BANeU JO SOT|SLIDJOKIeYO [eyUOWIdOJOAOp JuRVOdW] *| ATAVL

15

Vickruck et al. JESO Volume 141, 2010

TABLE 2. Prevalence of natural enemies associated with Ceratina dupla and C. calcarata
in each substrate. Due to low sample sizes sumac was excluded from statistical analysis of
parasitism amongst substrates.

Prevalence (“%)

6 t
se ea lyfe Brood cells Nests
C. dupla Teasel 107/426 27/49
Raspberry 15/97 9/10
Total 122/523 36/59
C. calcarata Teasel 25/96 8/15
Raspberry 80/198 25/26
Sumac 16/33 4/7
Total 121/327 37/48
Grand Total 243/850 73/107
C. dupla vs. C. calcarata G=18.42, d.f.=1, P<0.0001 G=3.21, d.f.=1, P=0.07
Teasel vs. Raspberry G=4.44, d.f=1, P=0.04 G=20.21, d.f.=1, P<0.0001
0.60
no]
N 0.50
8
o
@ 0.40
7)
rm OBs.1
S = 8 Col
: 0.20 MEV.
= VILLETTE: Eyt.
a 0.10 - m@ Axm.
a gm Pym.
0.00 -
C. dupla C. dupla C. calcarata C. calcarata C. calcarata
Raspberry Teasel Teasel Raspberry Sumac

Host species and substrate

FIGURE 1. The proportion of available cells parasitized for Ceratina dupla and C. calcarata
in each substrate. Values associated with each bar indicate the number of available cells
for each species in each substrate. Abbreviations: Bs. 1.=Baryscapus americana, Bs.
2=Baryscapus sp., Col.= Coelopencyrtus sp., E.v.= Eupelmus vesicularis, Eyt.= Eurytoma
sp. near apiculae, Axm.=Axima zabriskiei, Pym.= Pyemotes sp.

16

Natural enemies of Ceratina in the Niagara Region

JESO Volume 141, 2010

TABLE 3. Prevalence of parasites on each Ceratina host by affected brood cells. Prevalence
is the proportion of brood parasitized in each host species in each nesting substrate.
Significance testing was conducted using G tests unless indicated by * where Fisher’s Exact

tests were used.

Parasite

Baryscapus americana
(Eulophidae)

Baryscapus sp.
(Eulophidae)

Coelopencyrtus sp.
(Encyrtidae)

Eupelmus vesicularis
(Eupelmidae)

Eurytoma sp. near apiculae
(Eurytomidae)

Axima zabriskiei
(Eurytomidae)

Pyemotes sp.
(Pyemotidae)

Host

C. dupla

C. calcarata

C. calcarata

C. calcarata

C. dupla

C. calcarata

C. dupla

C. calcarata

C. dupla

C. calcarata

Substrate

Teasel
Raspberry
Total
Teasel
Raspberry
Sumac
Total
Teasel
Raspberry
Sumac
Total
Teasel
Raspberry
Sumac
Total
Teasel
Raspberry
Total
Teasel
Raspberry
Sumac
Total
Teasel
Raspberry
Total
Teasel
Raspberry
Sumac
Total
Teasel
Raspberry
Total
Teasel
Raspberry
Sumac
Total

Prevalence cells
available

55/426
2/97
57/523
9/96
0/198
0/33
9/327
0/96
51/198
13/33
64/327
0/96
0/198
1/33
1/327
1/426)
0/97
1/523
1/96
0/198
0/33
1/327
0/426
8/97
8/523
0/96
14/198
2/33
16/327
51/426
5/97
56/523
15/96
15/198
0/33
30/327

Statistics

Species:
G= 21.42, d.f.=1,
P<0.0001

Substrate:
G=46.68 ,d.f=1,
P<0.0001

Substrate
G= 2.49, d.f.=1,
N.S.

Species:
G= 8.02, d.f.=1,
P=0.005

Substrate:
*X7= 0.08, d.f.=1,
n.s.

Species:
G=0.53, d.f.=1, n.s.

Substrate:

G= 7.56 d.f.=1,
P=0.006

al. (2005) consider Hoplocryptus a valid genus. This is the first time this species has been

recorded with C. calcarata.

This natural enemy is considered a predator as it always consumed multiple

17

Vickruck et al.

JESO Volume 141, 2010

TABLE 4. Infection rate of nests of Ceratina spp. by substrate type and species of natural
enemy. Nests were scored as infected if at least one individual of the eight natural enemies
were present in a nest. Significance testing was conducted using G tests unless indicated
by * where Fisher’s Exact tests were used.

Natural Enemy

Baryscapus americana
(Eulophidae)

Baryscapus sp.
(Eulophidae)

Coelopencyrtus sp.
(Encyrtidae)

Eupelmus vesicularis

(Eupelmidae)

Eurytoma sp. near apiculae
(Eurytomidae)

Axima zabriskiei
(Eurytomidae)

Pyemotes sp.
(Pyemotidae)

Host

C. dupla

C. calcarata

C. calcarata

C. calcarata

C. dupla

C. calcarata

C. dupla

C. calcarata

C. dupla

C. calcarata

Substrate

Teasel
Raspberry
Total
Teasel
Raspberry
Sumac
Total
Teasel
Raspberry
Sumac
Total
Teasel
Raspberry
Sumac
Total
Teasel
Raspberry
Total
Teasel
Raspberry
Sumac
Total
Teasel
Raspberry
Total
Teasel
Raspberry
Sumac
Total
Teasel
Raspberry
Total
Teasel
Raspberry
Sumac
Total

ests wit
at least one
natural enemy/
Total nests

13/49
2/10

15/59
2/15
0/26

0/7
2/48
0/15

16/26

2/7

18/48
0/15
0/26

1/7
1/ 48

1/49 |

0/10
1/59
1/15
0/26
0/7
1/48
0/49
4/10
4/59
0/15
7/26
1/7
8/48
13/49
3/10
16/59
5/15
2/26
0/7
7/48

Statistics

Species:
G= 10.16, d.f.=1,
P=0.001

Substrate:
G= 6.03, d.f.=1, P=0.01

Substrate:
*X*= 2.45, d.f.=1, nus.

Species:
G= 2.60, d.f=1, n.s.

Substrate:
*X?= 0.87, d.f.=1, n.s.

Species:
G= 2.53, d.f.=1, n.s.

Substrate:
G= 2.80, d.f.=1, n.s.

Ceratina immatures before completing development. The predator egg was always laid
in the innermost cell of the nest. After the egg hatched, the larva attached to the small
Ceratina larva, but did not kill it immediately. Rather, the H. zoesmairi larva waited until the

18

Natural enemies of Ceratina in the Niagara Region JESO Volume 141, 2010

Ceratina larva was at least half as large as its pollen mass, at which point it consumed
the immature Ceratina and the remainder of its provisions. Once the entire contents of
the cell had been consumed the larva broke down the cell septum and consumed the next
larva and its pollen mass. This process was repeated, with individual H. zoesmairi larvae
devouring anywhere from two to five Ceratina immatures and pollen masses, then spinning
silken cocoons. Each H. zoesmairi larva then defecated and pupated inside its cocoon before
emerging as an adult. Development from time of hatching to adulthood took 27-48 days,
with emergence dates ranging from 28 July to 14 August 2008. There were four occurrences
of this predator, two in C. dupla nests (one in teasel and one in raspberry), one in a C.
calcarata nest (raspberry), and one in a Ceratina nest that contained no adult female and no
surviving offspring.

Parasitoids

Baryscapus americana (Ashmead) (Hymenoptera: Eulophidae)

Baryscapus americana was previously known to parasitize C. calcarata in
Georgia (Kislow 1976) and Missouri (Rau 1928). The species was transferred from the
genus Aprostocetus Westwood by Lasalle (1994). This is the first record of any member of
the genus Baryscapus Forster parasitizing C. dupla.

Baryscapus americana is a gregarious, koinobiont endoparasitoid of Ceratina
immatures. Their presence was undetectable until they began to consume their hosts (Fig.
2a), but the larvae grew to approximately half the length of their Ceratina host by the time its
contents had been entirely consumed. At this point the parasitoids migrated to the anterior
or posterior ends of the pre-pupal skin (Fig. 2b). The parasitoids then emerged in three
ways: either all individuals in the Ceratina larval skin pupated and emerged that summer
(Fig. 2c), or all of the individuals remained as prepupae to overwinter together and emerge
the following spring, or several individuals occupying a single host would pupate while
the rest would overwinter. The aforementioned strategies were also observed by Kislow
(1976). Of the 66 immature Ceratina parasitized, 20 (30%) showed total emergence, 35
(53%) overwintered as a group together, and 11 (17%) showed partial emergence, with
some individuals emerging that summer and some overwintering as prepupae. Average
development time was 21.6 + 2.3 days (range 11—37) once B. americana larvae had begun
to consume Ceratina immatures. Emergence was highly synchronized for non-diapausing
larvae, with all newly eclosed adults emerging from the host within 24 hours.

Baryscapus americana was the most common parasitoid species observed,
infecting 8% (66/850) of all cells, and 16% (17/107) of all nests. This parasitoid was
found in nests collected from 14 July through 1 August 2008. They were most often found
parasitizing nests in teasel, with low levels of infection in raspberry, and none in sumac
(Tables 3, 4). On average they infected 39% of available brood in an affected nest, ranging
from one immature to the entire nest. This parasitoid predominantly affected the prepupal
stage (8/9 C. calcarata and 53/56 C. dupla) and occasionally white eyed pupae. Individuals
of Baryscapus sp. 1 were often found in nests with other associated species (7/17, 41%),
including Eurytoma sp. near apiculae, Axima zabriskiei, Eupelmus vesicularis and Pyemotes

sp.

19

Vickruck et al. JESO Volume 141, 2010

FIGURE 2. Development of Baryscapus americana a) Parasitoid larvae consume the
contents of the Ceratina immature, leaving the larval skin intact. b) Full grown larvae move
to the anterior and posterior ends of the host. c) Thereafter, pupation and development
continue to eclosion or individuals overwinter as prepupae.

Baryscapus sp. (Eulophidae)

This parasitoid which is morphologically very similar to B. americana, but
mummifies its host, overwintered as prepupae in the larval or pupal skin of Ceratina
calcarata only. All individuals of this gregarious, koinobiont endoparasitoid that emerged
as adults were male. It infected 20% (64/327) of the total C. calcarata cells available and
17% (18/48) of all C. calcarata nests. It was found most commonly in raspberry (51 of
64 cells), occasionally in sumac (13 of 64 cells), and never in teasel. On average 3.8 + 0.6
cells per affected nest were parasitized, representing 51% of infected C. calcarata nests on
average. Other associated species were present in 8 of the 17 infected nests (47%); these
were always Pyemotes or Axima. Prepupae were the most commonly affected host stage
(43/64), but white-eyed pupae (21/64) were also susceptible to parasitism.

Parasitism went unnoticed until these internal parasitoids began to consume the
host. Infection became evident when the larval skin of the C. calcarata changed dramatically
in colour and consistency. The larval skin of living Ceratina is somewhat transparent and
the gut is often visible. Parasitism caused the larval skin of the Ceratina to become a rusty
red-brown colour; it also became much more brittle with the consistency of paper mache.
The parasitoids overwintered as full grown larvae in the host, and the tough pupal casing
of the larval or pupal skin may provide protection to the diapausing larvae (Legrand et al.
2004). Only males of this species emerged as adults from Ceratina immatures, in constrast
with Baryscapus americana where both sexes emerged. These parasites were collected
from Ceratina nests from 22 July through 21 August 2008.

Coelopencyrtus sp. (Hymenoptera: Encyrtidae)
A single C. calcarata larva in a sumac nest was affected by this gregarious,

20

Natural enemies of Ceratina in the Niagara Region JESO Volume 141, 2010

endoparasitic koinobiont. The only other observation of C. calcarata being attacked
by Coelopencyrtus Timberlake is by R.W. Matthews (reported by Daly et al. 1967),
who reported C. hylaei Burks parasitism on six consecutive cells in a nest collected in
Connecticut. Coelopencyrtus have also been reported to parasitize members of the twig-
nesting, bee genus Hylaeus Fabricius (Burks 1958).

The C. calcarata nest was collected on 7 July 2008 and parasitism became evident
on 10 July 2008 when more than 20 Coelopencyrtus larvae could be seen consuming the
bee larva, which was in the second innermost cell in a nest with six other immatures. Once
the entire contents of the Ceratina larva had been consumed, development of the parasitoids
continued inside the transparent larval skin. Eyes of the parasitoids began to darken on 4
August with their exoskeletons gaining pigmentation by 7 August. Synchronized emergence
took place on 13 August, when all of the new Coelopencyrtus adults emerged, except for
one individual that had died during development.

Eupelmus vesicularis Retzius (Hymenoptera: Eupelmidae)

One Eupelmus vesicularis specimen was reared from a C. dupla nest in teasel.
While this is the first host record of E. vesicularis parasitizing C. dupla, members of the
genus Eupelmus are well known for parasitizing a large number of different hosts (Burks
1979a; Gibson 1990). Eupelmus vesicularis has a Holarctic distribution, but may have been
introduced to North America from Europe in straw (Burks 1979a). Its first record in North
America was from Pennsylvania in 1915 (Burks 1979a).

Usually a primary parasitoid, E. vesicularis has been occasionally reported as a
secondary parasitoid (Burks 1979a). The wasp collected here had actually parasitized a
white-eyed bee pupa that had also been parasitized by Baryscapus americana. The E.
vesicularis egg had already been laid when the nest was collected on 15 July 2008. The
parasitoid hatched and began feeding externally on the bee larva on 20 July 2008. A day later
it became apparent that the bee larva had also been parasitized internally by B. americana.
Eupelmus vesicularis consumed the bee larva, followed by the B. americana parasitoids,
and pupated on | August. Body sclerotization was quite rapid, beginning 4 August and
finishing 2 days later. The adult E. vesicularis emerged on 8 August 2008, 19 days after
first hatching. This is the first record of the family Eupelmidae associated with a parasitoid
developing in bees.

Eurytoma sp. near apiculae Bugbee (Hymenoptera: Eurytomidae)

This is the first record of Eurytoma Illiger parasitizing C. calcarata. Eurytoma
apiculae and E. nodularis Boheman have been reported as parasitoids on C. callosa
Fabricius, C. dallatoreana Friese, C. nanua Cockerell, and C. punctigena Cockerell (Bugbee
1966; Burks 1979b; Daly 1966), and an unknown Eurytoma species has been observed as a
parasitoid of C. australensis Perkins in Queensland, Australia (S. Rehan, pers. comm.).

An external parasitoid of C. calcarata, only one E. sp. near apiculae individual
was collected which was parasitizing a larva that had almost finished eating its pollen ball
in a nest constructed in teasel. The E. sp. near apiculae egg was laid in the innermost brood
cell and by 16 July, 2008, had begun to feed on the host Ceratina larva. Over the course of
the next week the parasitoid finished consuming the host, after which it defecated and then

21

Vickruck et al. JESO Volume 141, 2010

pupated. The eyes of the E. sp. near apiculae began to darken on 27 July and the integument
was fully pigmented by | August. The teneral adult emerged on 3 August, 2008.

Axima zabriskiei Howard (Eurytomidae)

Axima zabriskiei has been reported as a parasitoid of both C. dupla and C.
calcarata (Kislow 1976; Krombein 1960; Rau 1928). An ectoparasitic idiobiont, 1—7
Axima individuals could be seen consuming a single Ceratina immature, always a pre-pupa
or white-eyed pupa, most often attached between the head and thorax and/or near the wing
buds of white eyed pupae (Fig 3b). The parasitoids consumed the hosts’ contents rapidly
(usually in 24 — 48 hours), leaving the skin intact. It was at this point that most lab-reared
parasitoids died, but two did pupate in the laboratory in 2008 (Fig. 3c). None of these
chalcid parasitoids were successfully reared to adulthood in the lab in 2008 but one was
reared to adulthood during 2009 collections.

Axima zabriskiei parasitoids infected 3% (24/850) of all available cells and 11%
(12/107) of available nests. Twenty-two of the infected cells were found in raspberry (11
nests) and two cells were in sumac (one nest), for an average of 1.9 + 0.3 cells per infected
nest, with a maximum of four infected Ceratina immatures but never representing more
than 50% of the total brood in a nest. Axima zabriskiei was found with other parasites

FIGURE 3. Axima zabriskiei wasp development. a) Newly hatched larvae pierce the soft
exoskeleton of the pupa and rapidly ingest the contents (a, circle), usually within 24-48
hours. Often multiple parasitoids will attack a single Ceratina immature (b). Once finished
feeding larvae pupate (c) before emerging as an adults (d).

22

Natural enemies of Ceratina in the Niagara Region JESO Volume 141, 2010

in 7/12 (58%) affected nests, most often in conjunction with Baryscapus sp.. The first
Ceratina nest containing Axima zabriskiei was collected on 14 July, with the last parasitized
nest collected on 21 August 2008.

Parasites (other than parasitoids)

Pyemotes sp. (Acari: Actinedida: Pyemotidae)

Pyemotes sp. were the most common natural enemy found on Ceratina immatures,
infecting 10% (86/850) of all available brood cells and 21% (23/107) of all available nests.
This is the first record of Pyemotes mites infecting C. dupla and C. calcarata, although
they have been reported on C. dallatorreana (Friese) in California (Daly 1966). They were
more common in teasel nests (66 of 86 infected brood) than in raspberry (20 of 86 infected
brood), and were not found in sumac (Table 3). On average Pyemotes sp. affected 3.7 + 0.7
immatures per nest, representing 28% of the total brood in affected nests. Pyemotes sp. was
present in nest collections from 25 June to 25 July 2008.

This external parasite was found to infect all immature stages, from small larvae
to fully pigmented pupae. Multiple individuals often infected a single larva or pupa, but a
single mite was effective in paralyzing and killing the host. Pyemotes seemed to monopolize
parasitism in a nest, being found with other parasitoids only 22% of the time (5/23 nests).
Pyemotes mites were also observed feeding on two A. zabriskiei larvae which subsequently
died. Other members of the genus Pyemotes have been known to decimate nests of the
bee Melipona colimana Ayala and the stem-nesting wasp, Psenulus interstitalis Cameron
(Macias-Macias and Otero-Colina 2004; Matthews 2000).

Discussion

Many parasitoids were more prevalent in one substrate than in another. Baryscapus
americana for example, was collected significantly more often from teasel nests, with only
two cells parasitized in raspberry (Table 3). While not statistically significant, Axima
zabriskiei was collected more in raspberry than sumac (Table 3). Pyemotes mites did not
parasitize one species more than another, but were significantly more common in teasel nests
then they were in raspberry (Tables 3 and 4). While Baryscapus sp. was found parasitizing
64 individuals in 18 nests, it was only ever a parasite of C. calcarata in raspberry and
sumac, never in teasel.

The parasitoid preferences seen for specific host substrates may be due to a number
of factors such as the structure or biology of the host plant itself. The following discussion
pertains mainly to raspberry and teasel, because so few sumac nests were collected. One
possible reason for higher parasitism rates in raspberry than in teasel may be the structure of
the plant species used for Ceratina nests. Teasel nests can only contain one nest per plant, in
the straight stalk that grows perpendicular to the ground. Shrubs like raspberry (and sumac)
have multiple branches in each plant and thus multiple possible nest substrates. These
shrubs also tend to grow in aggregations, with multiple plants in very close proximity to one
another. This can lead to higher nest densities in raspberry than in teasel. As Ceratina dupla
and C. calcarata females guard only their own nests, the high density of nests in shrubs may

23

Vickruck et al. JESO Volume 141, 2010

lead to increased rates of parasitism, as an individual parasitoid may be able to efficiently
locate and infect several nests in close proximity. When comparing parasitism rates for
a number of non-social hymenopteran species that nest solitarily and in aggregations,
Rosenheim (1990) found that aggregated nests had higher parasitism rates in most cases. —

Higher parasitism rates in raspberry may also relate to the habitat and biology of
the plants in which Ceratina nest. Teasel is an invasive plant found in large open fields,
almost always in full sunlight, while. raspberry and sumac are both native plants located
in shaded wood margins. In other words, Ceratina are nesting in different microclimates,
in substrates with different biology, and with different possible chemical signatures.
Numerous experiments have shown that many parasitoids are attracted to chemical cues
of the flora where their host species are commonly found (Drost et al. 1986; Elzen et al.
1986; Godfray 1994; Vet 1983). If parasitoids use the microclimate and/or chemical cues
emitted by the native substrates, then this might explain why the nests in native shrubs
had higher parasitisation. Members of the genus Eupelmus parasitize a very wide range
of host species (Gibson 1990). Gibson (1990) hypothesized that Eupelmus searched for
hosts in specific microclimates, with the microclimate being of more importance than the
host species. Searching for hosts by their preferred substrate may also be more effective
in temperate regions due to the relatively short and synchronized phenology of foraging
insects and nest substrates (Wcislo 1987).

Acknowledgements

The authors wish to thank Dr. Gary Gibson and Dr. Andrew Bennett at the Canadian
National Collection of Insects and Arachnids, and Dr. Michael Gates at the United States
National Museum for identification and confirmation of natural enemies. The comments of
Dr. Jeff Skevington as well as three anonymous reviewers also greatly helped to improve the
manuscript. This research was funded by a Brock University Deans Graduate Fellowship to
JLV and an NSERC discovery grant to MHR.

References

Askew, R. R. and M. R. Shaw. 1986. Parasitoid communities: their size, structure and
development. pp. 225-264 in J. Waage and D. Greathead (Eds), Insect parasitoids.
Academic Press. London UK. 398 pp.

Bugbee, R. E. 1966. A new species of the genus Eurytoma Illiger parasitic on bees of the
genus Ceratina Latreille. The Pan-Pacific Entomologist 42: 210-211.

Burks, B. D. 1958. A recharacterization of the genus Coelopencyrtus, with descriptions of
two new species (Hymenoptera: Encyrtidae). Journal of the Washington Academy
of Sciences 48: 22-26.

Burks, B. D. 1979a. Family Eupelmidae. pp. 878-889 in K. V. Krombein, P. D. Hurd, D.
R. Smith and B. D. Burks (eds), Catalogue of Hymenoptera in America north of
Mexico. Smithsonian Institution Press. Washington D.C.

Burks, B. D. 1979b. Family Eurytomidae. pp. 835-859 in K. V. Krombein, P. D. Hurd, D.

24

Natural enemies of Ceratina in the Niagara Region JESO Volume 141, 2010

R. Smith and B. D. Burks (eds), Catalogue of Hymenoptera in America north of
Mexico. Smithsonian Institution Press. Washington D.C.

Daly, H. V. 1966. Biological studies on Ceratina dallatorreana, an alien bee in California
which reproduces by parthenogenesis. Annals of the Entomological Society of
America 59: 1138-1154.

Daly, H. V., G. I. Stage and T. Brown. 1967. Natural enemies of bees of the genus Ceratina
(Hymenoptera: Apoidea). Annals Entomological Society of America 60: 1273-
1282.

Drost, Y. C., W. J. Lewis, P. O. Zanen and M. A. Keller. 1986. Beneficial arthropod
behaviour mediated by airborne semiochemicals. 1. Flight behaviour and influence
of preflight handling of Microplitis croceipes (Cresson). Journal of Chemical
Ecology 12: 1247-1262.

Elzen, G. W., H. J. Williams and S. B. Vinson. 1986. Wind tunnel flight responses by
hymenopterous parasitoid Campoletis sonorensis to cotton cultivars and lines.
Entomologia Experimentalis et Applicata 42: 285-289.

Gibson, G. A. P. 1990. Revsion of the genus Macroneura Walker in America north of Mexico
(Hymenoptera: Eupelmidae). The Canadian Entomologist 122: 837-873.

Godfray, H. J. C. 1994. Parasitoids. Princeton University Press, Princeton, New Jersey. 488

Graenicher, S. 1905. On the habits of two Ichneumonid parasites of the bee Ceratina dupla
Say. Entomological News 16: 43-49.

Grothaus, H. G. 1962. The biology of the species of Ceratina (Hymenoptera, Xylocopidae)
in Indiana. MSc Thesis Purdue University. West Lafayette, Indiana.

Harri, S. A., J. Krauss and C. B. Muller. 2008. Natural enemies act faster than endophytic
fungi in population control of cereal aphids. Journal of Animal Ecology 77: 605-
611.

Jervis, M. A., J. Ellers and J. A. Harvey. 2008. Resource acquisition, allocation, and
utilization in parasitoid reproductive strategies. Annual Review of Entomology
53: 361-385.

Johnson, M. D. 1988. The relationship of provision weight to adult weight and sex ratio in
the solitary bee, Ceratina calcarata. Ecological Entomology 13: 165-170.

Kislow, C. J. 1976. The comparative biology of two species of small carpenter bee, Ceratina
strenua F. Smith and C. calcarata Robertson (Hymenoptera: Xylocopinae) PhD
Thesis University of Georgia, Athens, Georgia.

Krombein, K. V. 1960. Biological notes on some Hymenoptera that nest in sumach pith.
Entomological News 71: 29-36.

LaSalle, J. 1994. North American genera of Tetrastichinae (Hymenoptera, Eulophidae).
Journal of Natural History 28: 109-236.

Legrand, M. A., C. Salin, A. Langer and T. Hance. 2004. Are mummy characteristics
reliable indicators of diapause and cold tolerance in the parasitoid wasp Aphidius
rhopalosiphi (Braconidae, Aphidiinae)? Cryoletters 25: 161-166.

Macias-Macias, J. O. and G. Otero-Colina. 2004. Infestation of Pyemotes tritici (Acari:
Pyemotidae) on Melipona colimana (Hymenoptera: Apidae: Meliponinae): a case
study. Agrociencia 38: 525-528.

25

Vickruck et al. | JESO Volume 141, 2010

Margolis, L., G. W. Esch, J. C. Holmes, A. M. Kuris and G. A. Schad. 1982. The use of
ecological terms in parasitology (Report of an ad hoc committee of the American
Society of Parasitologists). The Journal of Parasitology 68: 131-133.

Matthews, R. W. 2000. Nesting biology of the stem-nesting wasp Psenulus interstitialis
Cameron (Hymenoptera: Crabronidae: Pemphredoninae) on Magnetic Island,
Queensland. Australian Journal of Entomology 39: 25-28.

Michener, C. D. 2007. The bees of the world. Johns Hopkins University Press, Baltimore,
Maryland.

Rau, P. 1928. The nesting habits of the little carpenter bee, Ceratina calcarata. Annals of
the Entomological Society of America 21: 380-396.

Rector, B. G., V. Harizanova, R. Sforza, T. Widmer and R. N. Wiedenmann. 2006. Prospects
for biological control of teasels, Dipsacus spp., a new target in the United States.
Biological Control 36: 1-14.

Rehan, S. M. and M. H. Richards. 2008. Morphological and DNA sequence delineation of
two problematic species of Ceratina (Hymenoptera: Apidae) from Eastern Canada.
Journal of the Entomological Society of Ontario 139: 59-67.

Rosenheim, J. A. 1990. Density-dependent parasitism and the evolution of aggregated
nesting in the solitary Hymenoptera. Annals of the Entomological Society of
America 83: 277-286.

Traynor, R. E. and P. J. Mayhew. 2005. Host range in solitary versus gregarious parasitoids:
a laboratory experiment. Entomologia Experimentalis et Applicata 117: 41-49.

Vet, L. E. M. 1983. Host—habitat location through olfactory cues by Leptopilina clavipes
(Hartig)(Hym, Eucoilidae), a parasitoid of fungivorous Drosophila: the influence
of conditioning. Netherlands Journal of Zoology 33: 225-248.

Viereck, H. L. 1904. A new cryptine from the nest of Ceratina dupla. Entomological News
15: 333-335.

Weislo, W. T. 1987. The roles of seasonality, host synchrony, and behaviour in the evolution
and distributions of nest parasites in Hymenoptera (Insecta), with special reference
to bees (Apoidea). Biological Reviews of the Cambridge Philosophical Society 62:
515-543.

Yu, D. S. and K. Horstmann. 1997. A catalogue of world Ichneumonidae (Hymenoptera).
Memoirs of the American Entomological Institute 58:1-1558.

Yu, D. S., C. van Achterberg and K. Horstmann. 2005. World Ichneumonoidea 2004.
Taxonomy, biology, morphology and distribution Taxapad, Vancouver (CD-ROM
available at http://www.taxapad.com).

26

Biodiversity in burned and unburned alvar woodland JESO Volume 141, 2010

ORTHOPTERANS (ORTHOPTERA), GROUND BEETLES
(COLEOPTERA: CARABIDAE), AND SPIDERS (ARANEAE)
IN BURNED AND UNBURNED ALVAR WOODLANDS — THE

IMPORTANCE OF POSTFIRE SUCCESSION TO INSECT

DIVERSITY

P. M. CATLING', H. GOULET’, R. BENNETT? AND B. KOSTIUK?

Agriculture and Agri-Food Canada, Environmental Health, Biodiversity,
Wm. Saunders Building, Central Experimental Farm, Ottawa, ON, Canada K1A 0C6
email: paul.catling@agr.gc.ca

Abstract J. ent. Soc Ont. 141: 27-37

To contribute to understanding the importance of successional habitat to insect
diversity and assist biodiversity management in globally imperilled alvar
ecosystems, we surveyed three groups of arthropods in an Ottawa Valley,
Ontario, alvar landscape. Using pitfall traps and sweeping, we compared
grasshopper (Orthoptera), ground beetle (Coleoptera: Carabidae), and
spider (Araneae) diversity in two sites on the same successional gradient: an
unburned climax alvar woodland and a corresponding burned woodland that
had developed into alvar shrubland nine years after fire. Between-site species
similarity was 47.4% for orthopterans (9 species), 6.9% for ground beetles (2
species), and 40.9% for spiders (10 species). Both sites included regionally
rare orthopterans and ground beetles. For all three groups species richness and
density was higher on the burned site. The value of Brillouin’s biodiversity
index was higher for both orthopterans and ground beetles in the burned site
but higher for spiders in the unburned alvar woodland. These results provide
evidence for: (1) the importance of successional habitat to insect diversity, (2)
the value of alvar shrublands to overall alvar landscape biodiversity, and (3)
the potential value of fire in maintaining alvar biodiversity.

Published November 2010

‘Author to whom all correspondence should be addressed

?Agriculture and Agri-Food Canada, Environmental Health, Biodiversity, K.W. Neatby
Building., Central Experimental Farm, Ottawa, ON, Canada K1A 0C6

email: henri.goulet@agr.gc.ca, brenda.kostiuk@agr.ge.ca

British Columbia Ministry of Forests, Saanichton, BC, email: rbennett@esc-sec.ca

27

Catling et al. JESO Volume 141, 2010

Introduction

Fire was a major ecological factor in much of southeastern Canada during pre-
settlement times (Day 1953; Wein & MacLaren 1983), maintaining a variety of seral stages
across the landscape. In the absence of fire, much of the landscape is now dominated by
woodlands. Since biodiversity is considered to be higher during middle and later stages
of vegetational succession in general (Bormann and Likens 1979; Brown 1984) and
specifically for insects (Brown 1984; Strong et al. 1984; Kayna & Giirkan 2007), the loss
of middle and late stages may be contributing to the decline in insect diversity. We chose
an imperilled alvar ecosystem to investigate this hypothesis and to improve understanding
of the importance of successional habitat to insect diversity. Specifically, the objective of
our work was to clarify the importance of fire and subsequent succession to insect diversity
through a comparative study. This involved three groups of arthropods, orthopterans
(Orthoptera), ground beetles (Coleoptera: Carabidae), and spiders (Araneae) in two different
habitats representing different temporal positions on the same successional gradient: an
early successional alvar shrubland (“burned woodland”, nine years post-fire) and a nearby
climax alvar woodland (“unburned woodland”).

Materials and Methods

The study area

The Burnt Lands, approximately 40 km SW of Ottawa in the Ottawa Valley of
eastern Ontario, is one of the richest (in terms of species number and rare species) and
most extensive alvar landscapes in the Great Lakes region. Alvars are globally imperilled
ecosystems with a fragmented distribution in North America (Catling and Brownell 1995,
1999; Reschke et al. 1999; Brownell and Riley 2000). Evidence of past fire is common
in alvars (Catling and Brownell 1998; Jones and Reschke 2005) and, considering the high
plant diversity in successional alvar habitats, large scale biomass removal may significantly
contribute to biodiversity protection (e.g. Catling et al. 2001, 2002; Catling and Sinclair
2002). The insect fauna of alvars is distinctive and significant (Bouchard 1997a, b, 1998;
Bouchard et al. 1998, 2001, 2005), making information on the importance of alvar succession
to insects particularly relevant.

The climax woodland study site included four hectares centered at 45.2569,
—76.1437. The burned woodland study site, also 4 hectares in size, is centered at 45.2507,
—76.1437, 0.5 km southeast of the climax site. Both sites are located in Burnt Lands
Provincial Park, Lanark County, Ontario, and are part of the Burnt Lands Alvar landscape
(Brunton 1986). Based on personal observations (annually 1985 to 1995) and examination
of aerial photographs obtained from the National Air Photo Library of Natural Resources
Canada (e.g., number A 16525-105, 29 May 1959), both of these study sites were semi-
open, mixed boreal forest until 23 June 1999 when a fire burned 152 hectares, including
the burned woodlands study site. The forest (Figure 1a) was dominated by Abies balsamea
(L.) P. Mill., Picea glauca (Moench) Voss, Pinus strobus L., Thuja occidentalis L., and
Populus tremuloides Michx. with an understory of mosses including Pleurozium schreberi
(Brid.) Mitt., and Dicranum polysetum Sw., and occasional depauperate shrubs including

28

Biodiversity in burned and unburned alvar woodland JESO Volume 141, 2010

FIGURE 1. Burned (a) and unburned (b) alvar woodland on the Burnt Land Alvar west of
Ottawa. a)Fallen and dead standing trees are Abies balsamea, Picea glauca, Pinus strobus,
and Thuja occidentalis, regrowth on upper left is Populus tremuloides and Arctostaphylos
uva-ursi can be seen flowering in the foreground. b)The forest is dominated by Abies
balsamea, Picea glauca, Pinus banksiana, Pinus strobus, Populus tremuloides and Thuja
occidentalis. Shrubs of Juniperus communis are present in the foreground. (a) Area burned
on 23 June 1999 was taken at 45.2507, —76.1437. The right photo was taken at 45.2569,
—76.1437 in late May. Both photograps by P. M. Catling.

he = Nee .
ayo. - te \ a.)
“\ . ; x a
~ Be r - xX o
Lad — ~~ >
— ’ a _§
> _ = “M4 : a =
> Ue Qoaime 3 F- 3 } Fai
> <4 . e
; { 24
= -

at

Juniperus communis L. var. depressa Pursh. Nine years after the fire, the burned area had
developed into a species-rich, open grassy shrubland dominated by graminoid plants such
as Danthonia spicata (L.) Beauv. ex Roemer & J. A. Schultes and Carex richardsonii R.
Br., herbs such as Packera (Senecio) paupercula (Michx.) A. & D. Love, and Solidago
nemoralis Ait. var. nemoralis, and shrubs such as Amelanchier alnifolia (Nutt.) Nutt. ex M.
Roemer var. compacta (Nielsen) McKay and Prunus virginiana L. Additional information
on the vegetation of the two study sites is in Catling (in press).

The Burnt Lands area is subject to fire because of its shallow soils and location on
an elevated plateau of porous limestone rock. It was named by settlers in 1870 following
an extensive fire. Additional background information on the Burnt Lands Alvar is in White
(1979), Brunton (1986), and Catling et al. (2001, 2002).

Collection and identification of insects

(1) Traps: Ten pitfall traps (15 cm x 10 cm x 5 cm deep) were buried 10 m apart
in east-west transects in each of the burned and unburned alvar woodlands. The traps
were buried so that the tops were flush with the ground surface and there were no nearby
obstructions. Each trap was filled with antifreeze and a drop of soap to half depth. Five days

29

Catling et al. | JESO Volume 141, 2010

after setting, the traps were checked. The survey continued from spring through summer to
fall with several gaps. The dates of checking the traps were 16 May; 1, 9 June; 1, 5, 12 July;
16, 21, 26 August; and 8, 13 September 2008. These traps, set out and checked by PMC
and BK, provided the entire basis for a comparison of Coleoptera and Araneae and most of
the information on Orthoptera.

(2) Sweeping: To additionally sample Orthoptera, at each site on each visit, 15
minutes was spent sweeping vegetation less than 1.5 m tall. Sweeping was always done on
vegetation selected randomly along the same 100 m transect.

Orthopterans were identified by PMC using Vickery and Kevan (1985). Ground
beetles were identified by HG (1961, 1963, 1966, 1968, 1969a, 1969b), Bousquet and
Larochelle (1993), and Goulet & Bousquet (2004). Spiders were identified by RB using
primary taxonomic literature and available regional keys (e.g., Dondale and Redner 1978,
1982, 1990; Paquin and Dupérré 2003; Platnick and Dondale 1992). Ninety-one juvenile
spiders and 52 juvenile orthopterans, unidentifiable to species, were excluded from the
analysis. Voucher specimens were deposited in the Canadian National Collection of Insects
at Agriculture and Agri-Food Canada (CNCI) in Ottawa.

Comparing biodiversity

Biodiversity was compared with respect to: (1) total number of species and
numbers of individuals within’species, (2) the presence of regionally rare species (confined
to alvars or known from less than four locations in the Ottawa valley), (3) the extent of
distinctive composition, and (4) by applying Brillouin’s Index which includes consideration
of heterogeneity (species richness and evenness), is relatively sensitive to the abundance of
rare species, and assumes a finite sample and collection of that sample without replacement
of individuals (Krebs 1999, 2008). Replacement in this case is expected to have been the
same in both habitats, would not likely have been from substantial distances (1.e., over 100
m) for these ground dwelling species, and would not have involved second generations
since most of these species have a single generation in a year.

Results

Overall, 19 species of orthopterans, 29 species of ground beetles, and 42 species of
spiders were recorded (Tables 1—3). Species composition differed between the burned and
unburned sites. The sites shared 9, 2, and 10 grasshopper, ground beetle, and spider species,
respectively (Tables 1—3), or 47.4 %, 6.9 %, and 40.9 % of all collected grasshopper, ground
beetle, and spider species. For species in common, the number of individuals was generally
highest in the burned woodland for orthopterans and ground beetles but not for spiders. At
each site certain unique species were common, e.g., the grasshopper Jefrix ornata (Say),
the spider Schizocosa avida Walckenaer in the burned site, and the ground beetle Synuchus
impunctatus (Say) in the unburned site.

Four regionally rare grasshopper species were present at each site (Table 1).
Of these, Melanoplus keeleri luridus (Dodge), Spharagemon bolli bolli Scudder, and
Encoptolophus sordidus (Burmeister) were found only in the burned site and Melanoplus

30

Biodiversity in burned and unburned alvar woodland JESO Volume 141, 2010

TABLE 1. Species and number of individuals of orthopterans (Orthoptera) recorded in
burned and unburned woodland on the Burnt Lands. Species marked with an asterisk (*)
are regionally rare.

Species Burned Unburned
Acrididae

Chloealtis conspersa Harris*

Chortophaga viridifasciata (De Geer)

Encoptolophus sordidus (Burmeister) *

Melanoplus bivitattus (Say)

M. dawsoni (Scudder) *

M. fasciatus (F. Walker)*

M. keeleri luridus (Dodge)*

M. punctulatus (Scudder) *

M. sanguinipes (Fabricius)

Spharagemon bolli bolli Scudder*
Gryllidae

Allonemobius fasciatus (De Geer) 19 2

Gryllus pennsylvanicus Burmeister 32 8

G. veletis (Alexander & Bigelow) 22 6
Oecanthidae

Oecanthus quadripunctatus (Beutenmiiller) 3 2
Phaneropteridae

Scudderia curvicauda (De Geer) | 1

S. furcata furcata Brunner von Wattenwy1 l |
Rhaphidophoridae

Ceuthophilus cf. maculata (Harris) - 7
Tetrigidae

Nomotettix cristatus cristatus (Scudder) 3 ]

Tetrix ornata ornata (Say) 23 -
Totals 178 44

5

—

eS)
ONWi Wes WOw ,

—

dawsoni (Scudder), M. punctulatus (Scudder), and Chloealtis conspersa Harris only in the
unburned site. Similarly, of the 6 regionally rare ground beetle species collected during the
study, Harpalus indigens Casey, Selenophorus gagatinus Dejean, S. opalinus (LeConte),
and the southern Calathus opaculus LeConte were found only in the burned woodland,
while the boreal species Harpalus fulvilabris Mannerheim and the alvar-restricted species
Pterostichus novus Straneo were found only in the unburned woodland. All collected
spiders were members of wide-ranging and relatively common species.

Species richness was greater in the burned woodland for all three groups. With
respect to orthopterans, the burned woodland had 15 species and unburned woodland had
13 species (Table 1, Figure 2). For spiders, the difference was greater with 31 species
in the burned compared to 22 species in the unburned site (Table 3, Figure 2). Ground
beetles provided the greatest contrast in species richness, with 21 species in the burned area
compared to 9 species in the unburned area (Table 2, Figure 2).

In all three groups there were more individuals in the burned area (Table 3). This
was most pronounced in the case of orthopterans with 3.55 times as many in the burned
woodland, and least for spiders with 1.69 times as many in the burned woodland.

3]

Catling et al. | JESO Volume 141, 2010

TABLE 2. Number of various species of ground beetles (Coleoptera: Carabidae) in 10 pitfall
traps in each of a burned and unburned alvar woodland. Species marked with an asterisk (*)
are regionally rare.

Species Burned Unburned

Agonum cupripenne (Say)

Amara pennsylvanica Hayward

Anisodactylus rusticus (Say)

Calathus gregarius (Say)

C. opaculus LeConte*

Calosoma calidum Fabricius

Carabus nemoralis O.F. Miller 3
Chlaenius emarginatus Say

Cicindela punctulata Olivier

C. purpurea Olivier

C. sexguttata Fabricius

Diplocheila obtusa (LeConte)

Harpalus faunus Say 3
H. fulvilabris Mannerheim*

H. indigens Casey*

H. laevipes Zetterstedt

H. laticeps LeConte °

H. opacipennis (Haldeman)

H. pensylvanicus (De Geer)

Notiophilus aeneus (Herbst)

Poecilus lucublandus (Say)

Pterostichus novus Straneo*

P. mutus (Say)

P. pensylvanicus LeConte

Selenophorus gagatinus Dejean*

S. opalinus (LeConte)*

Sphaeroderus stenostomus lecontei Dejean
Synuchus impunctatus (Say) ‘ 34

Totals 124 66

The value of Brillouin’s biodiversity index was higher for both orthopterans and
ground beetles in the burned site but higher for spiders in the unburned woodland (Figure
2).

es
ORF OR W, BRR WRK MRS MN NUN NY
'

1 ns —OO— 1

i — i —s

Discussion

In some cases the much greater presence of a species in either habitat is to be
expected on the basis of known ecological associations of a general or specific nature. For
example, the orthopterans found only in woodland (Chloealtis conspersa and Melanoplus
punctulatus) are known to require wood for oviposition, and the latter species is found
mostly on tree trunks (Vickery and Kevan 1985). The ground beetles present are mostly
normal to one site or the other (Lindroth 1961). The large number of Carabus nemoralis
in the open areas may be a result of greater abundance of earthworms in the more mineral
substrates of the open area as compared to the more acidic needle litter of the woodland.
Harpalus faunus, which collects small seeds, may be more abundant in the burned area as a

32

Biodiversity in burned and unburned alvar woodland JESO Volume 141, 2010

TABLE 3. Numbers of various species of spiders (Araneae) in 10 pitfall traps in each of a
burned and unburned alvar woodland.

Species Burned Unburned
Agelenidae
Agelenopsis potteri (Blackwall) ) 6
Agelenopsis utahana (Chamberlin & Ivie) l -
Clubionidae
Clubiona mixta Emerton 1 -
Elaver excepta (L. Koch) - Zz
Corinnidae
Castianeira longipalpa (Hentz) 3 -
Gnaphosidae
Callilepis pluto Banks l
Drassodes neglectus (Keyserling)
Drassylus depressus (Emerton) ]
D. niger (Banks) -
D. socius Chamberlin -
Haplodrassus bicornis (Emerton) -
H. signifer (C.L. Koch) 8
Herpyllus ecclesiasticus Hentz -
Gnaphosa muscorum (L. Koch) 24
Micaria laticeps Emerton 1
2
7

—
oS)
1

Z. fratris Chamberlin

Z. hentzi Barrows
Hahniidae

Neoantistea magna (Keyserling)
Liocranidae

Agroeca ornata Banks - 4

A. pratensis Emerton 1 6
Lycosidae

Alopecosa aculeata (Clerck) 2

Hogna frondicola (Emerton) -

P. distincta (Blackwall) 9 16

P. moesta Banks -

Schizocosa avida (Walckenaer) 76 -

S. crassipalpata Roewer 10 -

S. saltatrix (Hentz) 14 6

Trochosa ruricola (De Geer) 3 -

T. terricola Thorell 3 23
Oxyopidae

Oxyopes scalaris Hentz - ]
Philodromidae

Thanatus formicinus (Clerck) z l
Salticidae

Evarcha hoyi (Peckham & Peckham)

Habronattus viridipes (Hentz)

Phidippus purpuratus Keyserling
Thomisidae

Xysticus alboniger Turnbull et al.

X. ampullatus Turnbull et al.

X. canadensis Gertsch

X. elegans Keyserling

X. luctuosus (Blackwall)

X. pellax O. P.-Cambridge

X. punctatus Keyserling

X. triguttatus Keyserling -
Totals Zoe 140

yar a ee,

— ae
SR i NR it NNR

!
Nn

NCO 1
1

—
NOR ne WHOM

33

Catling et al. JESO Volume 141, 2010
Fal Unburned Woodland
(EG Burned Woodland

S
oO

31

te)
oO

21

No
oO

Number of Species
o

oO

Number of Individuals

Brillouin’s Index Value

& o
& S
‘ $

O O

FIGURE 2. Number of species, number of individuals, and the value of Brillouin’s Index
for three arthropod groups in burned and unburned alvar woodland.

result of greater numbers of herbs with small seeds in that area. The abundance of Synuchus
impunctatus in the unburned woodland and its absence from the burned area is anticipated
on the basis of its association with deep litter (Lindroth 1961), which was removed by fire
from the burn. Likewise with respect to the spiders, some of the major differences were
anticipated based on known species and habitat associations, such as the relationship of
many Schizocosa and Xysticus species with dry, open habitats.

Our results suggest that the relatively long lasting successional shrubland that
follows burning of alvar woodland differs from the original woodland in species composition,
higher species richness and density, and higher biodiversity index values for some arthropod
groups. The fact that the Brilluoin Index has a slightly lower value for spiders in the burned
area than in the unburned is a consequence of less evenness in the number of individuals
of different species in that site, despite higher diversity and species number. Other studies
similarly found highest insect diversity in middle successional stages (e.g., Brown 1984;
Kayna & Giirkan 2007) and qualitative differences between burned and unburned sites
(e.g., Burger et al. 2005). The importance of succession and differing species compositions
in different seral stages is not surprising considering that opposite ends of the sere are
characterized by organisms with different life history strategies (Brown 1984).

34

Biodiversity in burned and unburned alvar woodland JESO Volume 141, 2010

The tendency for insect diversity to track plant diversity (e.g. Knops et al. 1999)
may help to explain the generally higher insect diversity in the burned woodland, which had
higher vascular plant diversity than the unburned alvar woodland (Catling in press). With
regard to herbivorous insect diversity, which is tracked by predator and parasite diversity
(e.g., Knops et al. 1999), other explanatory factors associated with high plant diversity may
include increased insect richness per plant host and higher average plant host specificity
(Lewinsohn et al. 2005), as well as increased structural diversity of plant hosts (Southwood
et al. 1979).

The evidence presented here for the importance of succession to ground-dwelling
insects on alvars is based on a single location and a rather limited sampling procedure.
However, the relationship seems to hold for other alvar sites in the Ottawa valley based
on general comparative surveys (Catling, unpublished data). Although management of
alvar vegetation with succession-initiating fire seems appropriate, it may also have negative
impacts (Siemann et al. 1996), especially if it does not allow survival of some species in
unburned patches that serve as refugia. Fire or any form of biomass removal should be
part of a broad, long-term landscape management plan that takes many species and species
groups into account.

Acknowledgements

The CanaColl Foundation (http://www.canacoll.org) provided financial support
for identification and processing of the spider collection. Useful reviews were provided by
P. Bouchard and J. Miskelly.

References

Bormann, F. H. and G. F. Likens. 1979. Pattern and process in a forested ecosystem.
Springer, New York. 253 pp.

Bouchard, P. 1997a. Insect diversity in alvar habitats, Manitoulin Island, Ontario. The
Nature Conservancy and the Ontario Natural Heritage Information Centre. 28 pp.
+ appendices.

Bouchard, P. 1997b. Insect diversity of four alvar sites on Manitoulin Island, Ontario. M.Sc.
thesis, McGill University. 93 pp.

Bouchard, P. 1998. Insect diversity in alvars of southern Ontario. Federation of Ontario
Naturalists. 87 pp.

Bouchard, P., H. Goulet and T. A. Wheeler. 1998. Phenology and habitat preference of three
species of ground beetles (Coleoptera: Carabidae) associated with alvar habitats
in southern Ontario. Proceedings of the Entomological Society of Ontario 129:
19-29.

Bouchard, P., K. G. A. Hamilton and T. A. Wheeler. 2001. Diversity and conservation status
of prairie endemic Auchenorrhyncha (Homoptera) in alvars of the Great Lakes
region. Proceedings of the Entomological Society of Ontario 132: 39-56.

Bouchard, P., T. A. Wheeler and H. Goulet. 2005. Ground beetles (Coleoptera: C arabidae)
from alvar habitats in Ontario. Journal of the Entomological Society of Ontario
136: 3-23.

35

Catling et al. | | JESO Volume 141, 2010

Bousquet, Y. and A. Larochelle. 1993. Catalogue of the Geadephaga (Coleoptera:
Trachypachydae, Rhysodidae, Carabidae including Cicindelini) of America North
of Mexico. Memoirs of the Entomological Society of Canada No. 167. 397 pp.

Brown, V. K. 1984. Secondary succession: insect-plant relationships. Bioscience 34: 710-
716.

Brownell, V. R. and J. L. Riley. 2000. The alvars of Ontario, significant alvar natural areas in
the Great Lakes region. Federation of Ontario Naturalists, Toronto. 270 pp.

Brunton, D. F. 1986. A life science inventory of the Burnt Lands. Ministry of Natural
Resources. 118 pp + 3 maps.

Burger, J. C., M. A. Patten, J. T. Rotenbury and R. A. Redak. 2005. Patterns and processes
of arthropod community succession after a fire. pp. 249-251 in B. E. Kus and
J. L. Beyers (tech. coord.) Planning for Biodiversity: Bringing Researcha and
Management Together USDA Forest Service General Technical Report, PSW-
GTR-195, Pacific Southwest Research Station, Albany, CA. 274 pp.

Catling, P. M. In press. Vascular plant biodiversity in burned and unburned alvar woodland:
more evidence of the importance of disturbance to biodiversity and conservation.
Canadian Field-Naturalist. (in press)

Catling, P. M. and V. R. Brownell. 1995. A review of the alvars of the Great Lakes region:
distribution, floristic composition, phytogeography and protection. Canadian
Field-Naturalist 109: 143-171.

Catling, P. M. and V. R. Brownell. 1998. Importance of fire in alvar ecosystems — evidence
from the Burnt Lands, Eastern Ontario. Canadian Field-Naturalist 112: 661-667.

Catling, P. M. and V.R. Brownell. 1999. The alvars of the Great Lakes region. Pp. 375-391
in R.C. Anderson, J.S. Fralish and J.M. Baskin, eds. Savanna, barren and rock
outcrop communities of North America. Cambridge University Press, Cambridge,
U.K. 470 pp.

Catling, P. M. and A. Sinclair. 2002. Initial beneficial effects of fire and bulldozing on
Neglected Milkvetch, Astragalus neglectus, in an eastern Ontario Alvar Woodland.
Canadian Field-Naturalist 116: 640-642.

Catling, P. M., A. Sinclair and D. Cuddy. 2001. Vascular plants of a successional alvar burn
100 days after a severe fire and their mechanisms of re-establishment. Canadian
Field-Naturalist 115: 214-222.

Catling, P. M., A. Sinclair and D. Cuddy. 2002. Plant community composition and
relationships of disturbed and undisturbed alvar woodland. Canadian Field-
Naturalist 116: 571-579.

Day, G. W. 1953. The Indian as an ecological factor in the northeastern forest. Ecology 34:
239-346.

Dondale, C. D. and J. H. Redner. 1978. The crab spiders of Canada and Alaska (Araneae:
Philodromidae and Thomisidae). The Insects and Arachnids of Canada and Alaska.
Part 5. Agriculture Canada, Ottawa. Publication 1663. 255 pp.

Dondale, C. D. and J. H. Redner. 1982. The sac spiders of Canada and Alaska (Araneae:
Clubionidae and Anyphaenidae). The Insects and Arachnids of Canada and Alaska.
Part 9. Agriculture Canada, Ottawa. Publication 1724, 194 pp.

Dondale, C. D. and J. H. Redner. 1990. The wolf spiders, nurseryweb spiders and lynx
spiders of Canada and Alaska (Araneae: Lycosidae, Pisauridae, Oxyopidae). The

36

Biodiversity in burned and unburned alvar woodland JESO Volume 141, 2010

Insects and Arachnids of Canada and Alaska. Part 17. Agriculture Canada, Ottawa.
Publication 1856. 383 pp.

Goulet, H. and Y. Bousquet. 2004. The ground beetles of Canada. Canadian Biodiversity
Information Facility. http://www.cbif.gc.ca/spp_pages/carabids/phps/index_e.php
(accessed 9 February 2010).

Jones, J. and C. Reschke. 2005. The role of fire in Great Lakes alvar landscapes. Michigan
Botanist 44: 13-27.

Kayna, B. Y. and B. Giirkan. 2007. Species diversity of butterflies in Turkish Pinus brutia
forest ecosystems after fire. Entomological News 118: 31-39.

Knops, J. M. H., D. Tilman, N. M. Haddad, S. Naeem, C. E. Mitchell, J. Haarstad, M. E.
Ritchie, K. M. Howe, P. B. Reich, E. Siemann and J. Groth. 1999. Effects of plant
species richness on invasion dynamics, disease outbreaks, insect abundances and
diversity. Ecology Letters 2: 286-293.

Krebs, C. 1999. Ecological Methodology, 2" edition. Addison, Wesley Longman Inc., New
York. 620 pp.

Krebs, C. 2008. Ecological Methodology, Programs for Ecological Methodology, 2™ edition.
Exeter Software, Setauket, New York.

Lewinsohn, T. W., V. Novotny and Y. Basset. 2005. Insects on plants: diversity of herbivore
assemblages revisited. Annual Review of Ecology and Systematics 36: 597-620.

Lindroth, C. H. 1961, 1963, 1966, 1968, 1969a, 1969b. The ground-beetles (Carabidae, excl.
Cicindelinae) of Canada and Alaska, Part 2. Opuscala Entomologica Supplement
20: 1-200; 24: 201-408; 29: 409-648; 33: 649-944; 34: 945-1192; 35: I-XLVIII.

Paquin, P. and N. Dupérré. 2003. Guide d’ identification des araignées (Araneae) du Québec.
Fabreries, Supplément 11: 1-251.

Platnick, N. I. and C. D. Dondale. 1992. The ground spiders of Canada and Alaska
(Araneae: Gnaphosidae). The Insects and Arachnids of Canada and Alaska. Part
19. Agriculture Canada, Ottawa. Publication 1875. 297 pp.

Reschke, C., R. Reid, J. Jones, T. Feeney and H. Potter. 1999. Conserving Great Lakes
alvars. The Nature Conservancy, Chicago. http://www.epa.gov/ecopage/shore/
alvars/ (accessed 9 February 2010).

Siemann, E., J. Haarstad and D. Tilman, D. 1996. Short term and long term effects of burning
on Oak savanna arthropods. American Midland Naturalist 137: 349-361.
Southwood, T. R. E., V. K. Brown and P. M. Reader. 1979. The relationship of plant and
insect diversities in succession. Biological Journal of the Linnaean Society 12:

327-348.

Strong, D. R. Jr., J. H. Lawton and T. R. E. Southwood. 1984. Insects on plants: community
patterns and mechanisms. Blackwell Science, Oxford. 313 pp.

Vickery, V. R. and D. K. M. Kevan. 1985. The Grasshoppers, Crickets and related insects
of Canada and adjacent regions , Ulonata: Dermaptera, Cheleutoptera, Notoptera,
Dictuoptera, Grylloptera and Orthoptera. The Insects and Arachnids of Canada,
Part 14. Agriculture Canada. Publication 1777. 918 pp.

Wein, R. W. and D..A. MacLean. 1983. An overview of fire in northern ecosystems. Pp. 1-18
in R. W. Wein and D. A. MacLean, eds., the role of fire in northern circumpolar
ecosystems. John Wiley & sons, Toronto. 322 pp.

White, D. J. 1979. Burnt Lands Alvar. Trail and Landscape 13: 34-38.

aH

GAD ot dmuloV-O2Ar ~

a - gee - AC are 7

a ae ae. ai)
‘pompant (2 natn anustuslit Rh RELA aa aaNet pt
‘ractwpachydae, Riveshtidee, Catabhe as : rcbach |
tae ofthe si.2 ugborad 1b eshesod \ 1s at ‘
Adie 7 vies ete lieresa larg ig penta aM es 10s sat
for ht wee used Te oe aka ote ako a A
veraticgen a Chet Toa aia tuaed )
heate ie wh itihien sot cee. STOOL LombtiOMeh bey Ye roa
; rx’ Cxge omornisi oft its an mev2009 phere ="

rraune alba bald civh i/f hin TRG od abd phgege at. ™

yreatent AT arte ss must. Lé Ary thE os

cocnkay 2 unheed o leo ngose

SRO ARE SS toate yi detect die

f yet Digan md, Renter? S Woks beatae eee

he orecd ana ee

dint (eeneinocd tet resi > dcp TR ities oe

Hy poem’ oot Suet sawhtod

Wit Mile ee eee iy. bap) COMA~ peee® | W Caner cre ole —

Bf} wort? bucoronieee ae mica tieviared op on -
: wd Sito adT CAP! alan! ener Enel, ae! He - bait

formuithh xf 19S rind abe deinen hasmer) ae

| Satie ed Rb OOD IG) RS Ore OO LTE G tiees

' ‘edt eeepud dobar ober tts oie FPO expt bee ia

hl eobeeSiey gan ye Se

Cl n.Gern biteesh, 2

epizin nenk DROME
a J Sine

wetic. / é; a ‘pow A ne d

tf | rwish odT 2i6vie
Loemanran 3 haul
vote ie MO isd

«4 ‘ 354i]

-
2s 1 7]
gs
'
=
mpi f al
pv as os &

‘ ; % =r aot SaiT) Die 27S
wd ae ee dl

7 .
e,) -— 4

retical cho ome arsotpbad band 4 rh ‘7.

-
nb ot scrah pari) Dae S srmyplet Lise cunsntlt .
7 >
— FS] Beutacatrigit- rebate & ou han ae

; , es soe aati sh wee aes noiven ter esl Oe A ‘Pi Gh

" rigeis wut to zhos, efit cakes Qed ps at Woh ~
qy) LEM) cldere Tata aie gel irmatigtes .
(04.2% «peep aaceliyos =

Bombus of southern Ontario JESO Volume 141, 2010

THE BUMBLE BEES OF SOUTHERN ONTARIO: NOTES ON
NATURAL HISTORY AND DISTRIBUTION

S. R. COLLA' AND S. DUMESH?

Department of Biology, York University,
4700 Keele Street, Toronto, ON, Canada M3J 1P3
email: scolla@yorku.ca

Abstract J. ent. Soc. Ont. 141: 39-68

Although North American bumble bees are common and easily recognizable
insects in many habitats, details of their natural history are poorly known.
This study presents basic ecological information based on a literature review,
databased insect collections and recent survey work performed throughout
southern Ontario. As a result of this review, phenology, food plants,
distribution and habitat associations are summarized for each species of this
important group of pollinators.

Published November 2010

Introduction

The plight of native pollinators has recently gained the interest of scientists and
naturalists alike. Globally, bees have been documented as declining throughout their native
ranges (Berenbaum et al. 2007; Biesmeijer et al. 2006). Conservation plans are highly
dependent upon basic natural information, which is lacking for almost all North American
bee species. Southern Ontario is an important region to consider as it has relatively high
biodiversity and many potential threats to these native organisms (Allen et al. 1990). Habitat
loss and fragmentation due to high population density and agricultural production are major
threats to wild pollinators in this region (eg. Taki et al. 2007; Findlay and Houlahan 1997).
Understanding basic natural history aspects of native bees in southern Ontario is important
to conserve these pollinators and their associated native flowering plants.

Bumble bees are eusocial organisms with an annual colony cycle. Queens emerge
in the spring, find nest sites, build honey pots and lay eggs. Hatched workers then take over
foraging and nest tending duties, while the queen focuses on reproduction. Towards the end
of the colony cycle, males and new queens are produced. These reproductive individuals
leave the nest and mate. Newly mated queens overwinter in rotting logs, mulch or dirt
while the rest of the colony perishes with the onset of cold weather. Cuckoo bumble bees
(subgenus Psithyrus) are exceptions, as they do not produce a worker caste, but usurp the
colonies of other species and the host workers collect resources for the cuckoo’s offspring

‘Author to whom all correspondence should be addressed
7 email: sdumesh@yorku.ca

39

Colla and Dumesh | JESO Volume 141, 2010

instead. The timing of queen emergence, worker production and colony decline for each
species varies with latitude, elevation and weather variation from year to year (Benton 2006).
Here, using historical and'recent records of bumble bees in southern Ontario, information is
provided on distribution, phenology, habitat and forage for each of the 18 species found in
this region.

Materials and Methods

Phenology graphs were produced using bumble bee records from collections and
recent surveys. Bumble bee specimens from southern Ontario insect collections (University
of Guelph, Royal Ontario Museum, Canadian Museum of Nature, PCYU York University,
Algonquin Provincial Park) were databased with species identifications being determined
or verified by SR Colla. Surveys were made throughout southern Ontario during the
summers of 2005-2009 (Colla and Packer 2008; Colla.et al. 2006; Colla, unpublished).
Bees were collected using hand nets and were either identified and released or collected
for identification. Plant records were accumulated from specimen labels, surveys, the
literature (Macfarlane 1974; Robertson 1929). In Robertson (1929), plant records were not
determined in southern Ontario but were included if the taxon occurs naturally in the region.
Habitat notes were collected from Macfarlane (1974) and field surveys.

Results

A total of 9052 bumble bee records representing 18 species spanning the years
1876-2009 were accumulated from insect collections (n=6506) and field surveys (n=2546).
Laverty and Harder (1988) note the presence of B. frigidus Smith in southern Ontario, but
specimens for this species were not found during this study. Ecological information is
presented below for each species. Introduced plant species are marked with an asterisk (*).
Figures presenting the phenology and collection locations for each species are presented at
the end of the paper.

Bombus impatiens Cresson: the common eastern bumble bee
Phenology and Distribution: This species exhibits early spring emergence (earliest

record April 23) with a long colony cycle extending into autumn and has a widespread
distribution (Fig. 1).

Floral Records: Robertson (1929): Actinomeris, Agastache, Amphicarpaea, Arabis,
Asclepias, Blephilia, Camassia, Campanula, Caulophyllum, Cercis, Cicuta, Claytonia,
Clematis, Collinsia, Coreopsis, Crataegus, Delphinium, Dentaria, Desmodium,
Dasistoma, Dicentra, Fragaria, Gaura, Geranium, Gerardia, Gleditzia, Gymnocladus,
Helenium, Helianthus, Helianthus divaricatus, Heliopsis, Hydrophyllum, Impatiens,
Lactuca, Liatris, Lithospermum, Lobelia, Lonicera, Lycopus, Lythrum, Monarda,
Nelumbo, Osmorhiza, Penstemon, Petalostemum, Phlox, Podophyllum, Polemonium,
Prenanthes, Prunella, Prunus, Pycnanthemum, Pyrus, Ribes, Rudbeckia, Salix,

40

Bombus of southern Ontario JESO Volume 141, 2010

Scrophularia, Scutellaria, Sicyos, Silphium, Sium, Smilax, Stachys, Staphylea,
Symphoricarpos, Symphyotrichum, Teucrium, Tradescantia, Verbena, Viola, Zizia.
Macfarlane (1974): Acer ginnala*, Aesculus hippocataneum*, Althaea rosea*, Antirrhinum
majus*, Arctium minus*, Berberis thunbergii*, Caragana arborescens*, Carduus nutans *,
Cotoneaster adpressa*, Daucus carota*, Dipsacus sylvestris*, Echium vulgare*, Epilodium
angustifolium, Euthamia graminifolia, Helianthus annuus*, Hesperis matronalis*,
Hydrophyllum virginianum, Hypericum perforatum*, Impatiens capensis, Kalmia latifolia,
Kolkwitzia amabilis*, Ligustrum vulgare*, Lonicera caerulea, Lonicera periclymenum*,
Lonicera tatarica*, Medicago sativa*, Melilotus alba*, Nepeta cataria*, Oenthera biennis,
Phaseolus coccineus*, Philadelphus coronarius*, Potentilla, Prunus cerasus*, Prunus
tomentosa*, Pyrus malus*, Rhododendron, Ribes grossularia*, Ribes nigrum*, Ribes
rubrum*, Robinia fertilis*, Rubus, Salix, Salvia sylvestris*, Silene vulgaris*, Solanum
dulcamara*, Solidago canadensis, Solidago flexicaulis, Solidago rugosa, Stachys palustris *,
Symphyotrichum (Aster) ericoides, Symphyotrichum (Aster) lateriflorum, Symphyotrichum
novae-angliae, Symphytum officinale*, Syringa vulgaris*, Taraxacum officinale*, Tilia
platyphyllos*, Trifolium pratense*, Trifolium repens*, Vicia cracca*, Weigelia florida*.
Field and Museum Records: Amelanchier alnifolia, Ceanothus americanus, Centaurea
macrocephala, Cephalanthus, Cephalanthus occidentalis, Chelone glabra, Clinopodium
vulgare, Echinacea, Erythronium, Eupatorium fistulosum, Eupatorium maculatum, Justicia,
Lespedeza intermedia, Linum, Lupinus, Mentha, Onopordum acanthium*, Pediomelum,
Pontederia cordata, Prunus virginiana, Rhexia virginica, Rhus, Rubus idaeus, Rubus
occidentalis, Rudbeckia hirta, Solidago altissima, Solidago bicolor, Solidago caesia,
Solidago sempervirens, Spiraea, Spiraea alba, Uvularia, Vaccinium angustifolium,
Vaccinium vacillans.

Habitats: Close to or within wooded areas, open fields, urban parks and gardens,
wetlands.

Bombus bimaculatus Cresson: the two-spotted bumble bee
Phenology and Distribution: This species exhibits early spring emergence (earliest record

April 13) and has a widespread distribution (Fig. 2).

Floral Records: Robertson (1929): Amelanchier, Blephilia, Collinsia, Cephalanthus,
Dentaria, Dicentra, Geranium, Helianthus, Hydrophyllum, Mertensia, Monarda, Phlox,
Polemonium, Ribes, Triosteum, Uvularia, Verbena.

Macfarlane (1974): Ajuga genevensis*, Ajuga reptans*, Aesculus hippocataneum*,
Camassia scilloides, Carduus nutans*, Cotoneaster adpressa*, Cynoglossum officinale*,
Deutzia gracilis*, Dipsacus sylvestris*, Echium vulgare*, Hydrophyllum virginianum,
Hypericum perforatum*, Lamium amplexicaule*, Leonurus cardiaca*, Linaria vulgaris *,
Lonicera caerulea, Lonicera periclymenum*, Lonicera tatarica*, Mahonia aquifolium,
Melilotus alba*, Medicago sativa*, Monarda didyma, Onopordum acanthium*, Prunella
vulgaris*, Prunus tomentosa*, Pyrus malus*, Ribes grossularia*, Ribes nigrum*, Robinia
fertilis*, Salix, Solanum dulcamara*, Solidago canadensis, Solidago flexicaulis, Solidago
graminifolia, Symphytum officinale*, Syringa vulgaris*, Taraxacum officinale*, Trifolium
pratense*, Trifolium repens*, Vicia cracca*, Weigelia florida*.

Field and Museum Records: Arabis, Asclepias, Campanula, Campanula rotundifolia,
Caulophyllum, Ceanothus americanus, Centaureamacrocephala, Cephalanthus occidentalis,

4]

Colla and Dumesh | JESO Volume 141, 2010

Claytonia, Clinopodium vulgare, Dasistoma, Desmodium, Dicentra cucullaria, Echinacea,
Erythronium albidum, Euthamia graminifolia, Gaylussacia, Hypericum prolificum, Kalmia
polifolia, Lonicera, Lotus corniculatus*, Lupinus, Lythrum alatum, Mentha, Pontederia
cordata, Rhexia virginica, Rhus glabra, Rubus odoratus, Spiraea, Spiraea alba, Tilia
americana, Vaccinium angustifolium, Vaccinium corymbosum, Vaccinium myrtilloides,
Vaccinium vacillans, Viola.

Habitats: Close to or within wooded areas, urban parks and gardens.

Bombus terricola Kirby: the yellow-banded bumble bee
Phenology and Distribution: This species exhibits early spring emergence (earliest record

April 24) and has historically a widespread distribution (except extreme southwestern
Ontario) with fewer recent records (Fig. 3).

Floral Records: Macfarlane (1974): Berberis thunbergii*, Caragana arborescens*,
Carduus nutans*, Centaurea jacea*, Cirsium arvense*, Cotoneaster adpressa*, Echium
vulgare*, Hydrophyllum virginianum, Hypericum perforatum*, Impatiens capensis, Lactuca
canadensis, Lonicera caerulea, Lonicera tatarica*, Melilotus alba*, Medicago sativa*,
Philadelphus coronarius*, Prunus cerasus*, Prunus tomentosa*, Pyrus malus*, Rhus
typhina, Ribes grossularia*, Ribes nigrum*, Robinia fertilis*, Salix, Solanum dulcamara’*,
Solidago canadensis, Solidago flexicaulis, Solidago hispida, Solidago juncea, Sonchus
oleraceus*, Sorbus americana, Spiraea, Symphyotrichum (Aster) ericoides, Symphyotrichum
(Aster) lateriflorum, Symphyotrichum novae-anglia, Symphytum officinale*, Syringa
vulgaris*, Taraxacum officinale*, Tilia platyphyllos*, Trifolium pratense*, Trifolium
repens *, Vicia cracca*, Weigelia florida*.

Field and Museum Records: Anaphalis margaritacea, Aquilegia canadensis, Aralia,
Arctostaphylos uva-ursi, Asclepias, Asclepias incarnata, Asclepias syriaca, Astragalus,
Baptisia tinctoria, Diervilla lonicera, Epigaea repens, Erigeron philadelphicus,
Epilodium angustifolium, Eupatorium fistulosum, Eupatorium maculatum, Eurybia
macrophylla, Euthamia graminifolia, Gaylussacia, Heracleum lanatum, Kalmia, Kalmia
augustifolia, Ledum groenlandicum, Linaria vulgaris*, Lupinus, Mertensia, Monarda
fistulosa, Onopordum acanthium*, Pontederia cordata, Prunus, Prunus pensylvanica,
Rhexia virginica, Rhus, Senecio, Solidago, Spiraea latifolia, Thalictrum pubescens, Tilia
americana, Trifolium hybridum*, Urticularia cornuta, Vaccinium angustifolium, Vaccinium
corymbosum.

Habitats: Close to or within wooded areas.

Bombus vagans Smith: the half-black bumble bee
Phenology and Distribution: This species exhibits early spring emergence (earliest record

April 21) with a long colony cycle extending into the fall and has a widespread distribution
(Fig. 4).

Floral Records: Robertson (1929): Blephilia, Cercis, Claytonia, Clematis, Delphinium,
Dicentra, Ellisia, Erigenia, Geranium, Hydrophyllum, Hypericum, Ipomoea, Liatris,
Lobelia, Mertensia, Mimulus, Monarda, Phlox, Physostegia, Polygonatum, Polemonium,
Prunella, Ribes, Scrophularia, Scutellaria, Stachys, Staphylea, Symphoricarpos, Teucrium,
Tradescantia, Triosteum, Verbascum, Verbena, Veronica, Viola, Zizia.

Macfarlane (1974): Aesculus hippocataneum*, Althaea rosea*, Arctium minus*, Berberis

42

Bombus of southern Ontario JESO Volume 141, 2010

thunbergii*, Carduus nutans*, Centaurea jacea*, Cichorium intybus*, Cirsium arvense*,
Crataegus, Dipsacus sylvestris*, Daucus carota*, Echium vulgare*, Erica cinerea*,
Helianthus annuus*, Hesperis matronalis*, Hydrophyllum_ virginianum, Hypericum
perforatum*, Impatiens capensis, Kolkwitzia amabilis*, Leonurus cardiaca*, Linaria
vulgaris*, Lonicera periclymenum*, Lonicera tatarica*, Lotus corniculatus*, Melilotus
alba*, Medicago sativa*, Nepeta cataria*, Onobrychis viciifolia*, Prunella vulgaris*,
Prunus cerasus*, Pyrus malus*, Ribes nigrum*, Rubus, Silene vulgaris*, Solanum
dulcamara*, Sonchus oleraceus*, Symphyotrichum (Aster) lateriflorum, Symphyotrichum
novae-angliae, Symphytum officinale*, Syringa vulgaris*, Tamarix gallica*, Taraxacum
officinale*, Trifolium pratense*, Trifolium repens*, Verbena hastata, Vicia cracca*,
Weigelia florida*.

Field and Museum Records: Amphicarpaea, Anaphalis margaritacea, Apocynum, Aquilegia
canadensis, Aralia, Aralia hispida, Asclepias incarnata, Asclepias syriaca, Astragalus
canadensis, Chelone glabra, Clinopodium vulgare, Collinsonia canadensis, Cornus,
Dasistoma, Decodon, Desmodium, Diervilla lonicera, Erythronium albidum, Eupatorium
fistulosum, Eupatorium maculatum, Eurybia macrophylla, Euthamia graminifolia, Gerardia
pedicularia, Hypericum prolificum, Lactuca canadensis, Ledum groenlandicum, Lonicera,
Lupinus, Mentha, Monarda fistulosa, Nymphaea odorata, Onopordum acanthium*,
Pontederia cordata, Prunus, Pyrus, Rhexia virginica, Rhododendron, Rubus idaeus, Rubus
odoratus, Sarracenia purpurea, Scutellaria lateriflora, Solidago altissima, Solidago
canadensis, Solidago flexicaulis, Solidago hispida, Solidago juncea, Solidago sempervirens,
Spiraea alba, Tilia americana, Vaccinium angustifolium.

Habitats: Close to or within wooded areas, urban parks and gardens.

Bombus perplexus Cresson: the confusing bumble bee
Phenology and Distribution: This species exhibits early spring emergence (earliest record

April 16) and has a widespread distribution (Fig. 5).

Floral Records: Macfarlane (1974): Althaea rosea*, Asclepias incarnata, Asclepias syriaca,
Berberis thunbergii*, Campanula rapunculoides*, Carduus nutans*, Cirsium arvense*,
Cotoneaster adpressa*, Dipsacus sylvestris*, Echium vulgare*, Helianthus annuus*,
Hesperis matronalis*, Hydrophyllum virginianum, Lonicera caerulea, Lonicera tatarica*,
Onopordum acanthium*, Philadelphus coronarius*, Prunus americana, Prunus cerasus*,
Pyrus malus*, Ribes grossularia*, Ribes nigrum*, Robinia fertilis*, Salix, Solidago,
Solidago altissima, Solidago canadensis, Solidago flexicaulis, Symphytum officinale*,
Taraxacum officinale*, Tilia americana, Tilia platyphyllos*, Trifolium pratense*, Weigelia
florida*.

Field and Museum Records: Aralia, Arctostaphylos uva-ursi, Astragalus canadensis,
Campanula rotundifolia, Cephalanthus, Collinsonia canadensis, Desmodium, Echinacea,
Erythronium albidum, Eupatorium, Eupatorium fistulosum, Eupatorium maculatum,
Euthamia graminifolia, Fragaria, Helianthus, Hypericum perforatum*, Hypericum
prolificum, Kalmia latifolia, Lonicera, Lotus corniculatus*, Lysimachia ciliata, Medicago
sativa*, Mentha, Monarda, Nymphaea odorata, Penstemon, Pontederia cordata, Prunus,
Rhexia virginica, Rubus odoratus, Rudbeckia hirta, Spiranthes lacera, Spiranthes
romanzoffiana, Spiraea, Spiraea alba, Spiraea latifolia, Symphyotrichum, Syringa
vulgaris*, Tamarix gallica*, Vaccinium angustifolium, Vaccinium corymbosum, Vaccinium

43

Colla and Dumesh JESO Volume 141, 2010

myrtilloides, Vaccinium vacillans, Viola.
Habitats: Close to or within wooded areas, urban parks and gardens, wetlands.

Bombus griseocollis DeGeer: the brown-belted bumble bee
Phenology and Distribution: This species exhibits late spring emergence (earliest record

May 11) and has a widespread distribution (Fig. 6).

Floral Records: Robertson (1929): Actinomeris, Agastache, Amorpha, Arabis, Astragalus,
Baptisia, Bidens, Blephilia, Camassia, Campanula, Caulophyllum, Cephalanthus,
Cercis, Collinsia, Cornus, Crataegus, Delphinium, Dentaria, Desmodium, Dicentra,
Eupatorium, Frasera, Gerardia, Geranium, Gleditzia, Hibiscus, Houstonia, Hydrophyllum,
Ipomoea, Iris, Justicia, Krigia, Liatris, Lobelia, Lythrum, Mertensia, Monarda, Nelumbo,
Penstemon, Petalostemon, Phlox, Podophyllum, Polemonium, Prunella, Prunus,
Pediomelum, Pycnanthemum, Pyrus, Rudbeckia, Salix, Scutellaria, Sisyrinchium, Spiraea,
Symphoricarpos, Symphyotrichum, Teucrium, Tradescantia, Triodanis, Verbena, Vernonia,
Viburnum, Viola, Vitis, Uvularia, Zizia.

Macfarlane (1974): Aesculus hippocataneum*, Carduus nutans*, Echium vulgare*,
Helianthus annuus*, Hesperis matronalis*, Hydrophyllum_ virginianum, Hypericum
perforatum*, Linaria vulgaris*, Lonicera tatarica*, Melilotus alba*, Medicago sativa*,
Pyrus malus*, Robinia fertilis*, Solanum dulcamara*, Solidago canadensis, Solidago
sempervirens, Symphyotrichum novae-angliae, Symphytum officinale*, Syringa vulgaris*,
Taraxacum officinale*, Trifolium pratense*, Vicia cracca*.

Field and Museum Records: Aesculus glabra, Asclepias incarnata, Asclepias syriaca,
Asclepias tuberosa, Clinopodium vulgare, Echinacea, Eupatorium dubium, Eupatorium
perfoliatum, Heliopsis helianthoides, Hypericum prolificum, Lactuca canadensis,
Onopordum acanthium*, Pontederia cordata, Rudbeckia hirta, Vaccinium angustifolium,
Vaccinium corymbosum, Vaccinium myrtilloides, Urticularia vulgaris.

Habitats: Open farmland and fields, urban parks and gardens, wetlands.

Bombus fervidus Fabricius: the yellow bumble bee

Phenology and Distribution: This species exhibits mostly late spring emergence with a
long colony cycle extending into autumn and has a widespread distribution (Fig. 7). The
accumulated database contained only one single queen record in April with an unknown
date. The majority of queen records were from May and June.

Floral Records: Macfarlane (1974): Ajuga genevensis*, Ajuga reptans*, Aesculus
hippocataneum*, Caragana arborescens*, Carduus nutans*, Centaurea jacea*, Cichorium
intybus*, Cirsium arvense*, Delphinium, Dipsacus sylvestris*, Echium vulgare*,
Gleditzia, Hydrophyllum virginianum, Iris, Kalmia latifolia, Kolkwitzia amabilis*, Lactuca
canadensis, Lathyrus latifolius*, Linaria vulgaris*, Lonicera caerulea, Lonicera tatarica*,
Lotus corniculatus*, Malus, Melilotus alba*, Medicago sativa*, Monarda didyma, Nepeta
cataria*, Onobrychis viciifolia*, Onopordum acanthium*, Potentilla, Prunella vulgaris*,
Pyrus malus*, Ribes odoratum, Robinia fertilis*, Salix, Solanum dulcamara*, Solidago
canadensis, Solidago graminifolia, Symphyotrichum novae-angliae, Symphytum officinale*,
Syringa vulgaris*, Taraxacum officinale*, Trifolium pratense*, Tulipa*, Vicia cracca*,
Weigelia florida*.

Field and Museum Records: Centaurea maculosa*, Erigeron, Euthamia graminifolia, Inula

44

Bombus of southern Ontario JESO Volume 141, 2010

helenium*, Lobelia cardinalis, Lonicera, Lythrum salicaria*, Melilotus alba*, Penstemon
digitalis, Pontederia cordata, Securigera varia*, Solidago, Sonchus oleraceus*, Spiranthes,
Urticularia vulgaris.

Habitats: Open farmland and fields.

Bombus ternarius Say: the tri-coloured bumble bee
Phenology and Distribution: This species exhibits early spring emergence (earliest record

April 15) and has a widespread distribution except in extreme southwestern Ontario (Fig.
8).

Floral Records: Macfarlane (1974): Salix discolor.

Field and Museum Records: Aralia, Aralia hispida, Aralianudicaulis, Astragalus canadensis,
Chamaedaphne_ calyculata, Cirsium vulgare*, Claytonia caroliniana, Cynoglossum
officinale*, Echium vulgare*, Epilodium angustifolium, Erythronium albidum, Eupatorium
fistulosum, Eupatorium maculatum, Eurybia macrophylla, Euthamia_ graminifolia,
Hypericum perforatum*, Impatiens capensis, Ledum groenlandicum, Medicago sativa*,
Melilotus alba*, Mentha, Monarda, Pilosella aurantiaca*, Prunus pensylvanica, Rhexia
virginica, Securigera varia*, Solidago altissima, Solidago canadensis, Solidago juncea,
Spiraea, Spiraea alba, Symphyotrichum novae-angliae, Symphyotrichum puniceum,
Syringa vulgaris*, Tanacetum vulgare*, Taraxacum officinale*, Tilia americana, Trifolium
hybridum*, Trifolium pratense*, Trillium grandiflorum, Urticularia vulgaris, Vaccinium
angustifolium, Verbascum thapsus*, Verbena hastata, Vicia cracca*.

Habitats: Close to or within wooded areas.

Bombus rufocinctus Cresson: the red-belted bumble bee

Phenology and Distribution: This species exhibits late spring emergence (earliest record
May 28) and has a widespread distribution with more records in the Greater Golden
Horseshoe region (Fig. 9).

Floral Records: Macfarlane (1974): Lactuca canadensis, Potentilla, Symphyotrichum
(Aster) lateriflorum.Field and Museum Records: Apocynum androsaemifolium, Arctium
minus*, Campanula, Centaurea maculosa*, Cichorium intybus*, Cirsium arvense*,
Daucus carota*, Echium vulgare*, Eupatorium, Eupatorium fistulosum, Eupatorium
maculatum, Geranium, Helianthus, Heracleum lanatum, Hypericum prolificum, Inula
helenium*, Lupinus, Medicago sativa*, Melilotus alba*, Mentha, Monarda /fistulosa,
Prunella vulgaris*, Rubus, Securigera varia*, Solidago, Solidago altissima, Solidago
bicolor, Syringa vulgaris*, Trifolium pratense*, Trifolium repens*, Verbena hastata, Vicia
cracca*.

Habitats: Close to or within wooded areas, urban parks and gardens.

Bombus affinis Cresson: the rusty-patched bumble bee

Phenology and Distribution: This species exhibits early spring emergence (earliest record
April 20) with a long colony cycle extending into the autumn and has a southern distribution
with fewer recent records (Fig. 10).

Floral Records: Macfarlane (1974): Arctium minus*, Asclepias syriaca, Berberis
thunbergii*, Carduus nutans*, Centaurea cyanus*, Cotoneaster adpressa*, Crataegus,
Cucumis melo*, Deutzia gracilis*, Echium vulgare*, Hydrophyllum_ virginianum,

45

Colla and Dumesh JESO Volume 141, 2010

Hypericum perforatum*, Impatiens campensis, Kalmia latifolia, Linaria vulgaris*,
Lonicera caerulea, Lonicera periclymenum*, Lonicera tatarica*, Lotus corniculatus*,
Melilotus alba*, Medicago sativa*, Nepeta cataria*, Prunus americana, Prunus cerasus*,
Prunus tomentosa*, Pyrus malus*, Rhododendron, Ribes grossularia*, Ribes nigrum*,
Ribes rubrum*, Robinia fertilis*, Rubus, Salix, Silene dichotoma*, Solanum dulcamara*,
Solidago canadensis, Solidago fiexicaulis, Sonchus oleraceus*, Stachys palustris*,
Symphyotrichum (Aster) ericoides, Symphyotrichum (Aster) lateriflorum, Symphyotrichum
novae-angliae, Symphytum officinale*, Syringa vulgaris*, Taraxacum officinale*, Trifolium
pratense*, Trifolium repens*, Vicia cracca*, Vinca minor*, Weigelia florida*.

Field and Museum Records: Eupatorium maculatum, Eupatorium perfoliatum, Eupatorium
rugosum, Euthamia graminifolia, Helianthus decapetalus, Helianthus divaricatus, Kalmia,
Onopordum acanthium*, Rhexia virginica, Rhus, Spiraea, Vaccinium angustifolium,
Vaccinium vacillans.

Habitats: Close to or within wooded areas, open fields, urban parks and gardens.

Bombus citrinus Smith: the lemon cuckoo bumble bee

Phenology and Distribution: Males and females of this species are found from early spring
until late autumn and this species has a widespread distribution (Fig. 11). The earliest spring
record is a female collected on April 26.

Floral Records: Robertson (1929): Blephilia, Verbena.

Field and Museum Records: Centaurea jacea*, Cephalanthus occidentalis, Cirsium
vulgare*, Daucus carota*, Epilobium, Eupatorium fistulosum, Eupatorium maculatum,
Eupatorium perfoliatum, Euthamia graminifolia, Helianthus, Melilotus alba*, Prunella
vulgaris*, Solidago, Solidago altissima, Solidago bicolor, Symphyotrichum (Aster)
ericoides, Trifolium pratense*, Verbena hastata, Vicia cracca™.

Habitats: Close to or within wooded areas.

Bombus ashtoni Cresson: Ashton’s cuckoo bumble bee

Phenology and Distribution: Males and females of this species are found from early spring
until late autumn (Fig. 12). Recent occurrences of this species in Ontario are scarce. The
earliest spring record is a female collected on April 21.

Floral Records: Field and Museum Records: Allium, Aralia, Cephalanthus, Eupatorium,
Inula helenium*, Melilotus alba*, Penstemon, Pilosella aurantiaca*, Rubus, Solidago,
Solidago canadensis, Symphyotrichum novae-angliae, Syringa vulgaris*, Taraxacum
officinale*, Trifolium hybridum*, Trifolium pratense*, Vaccinium angustifolium, Vaccinium
corymbosum.

Habitats: Close to wooded areas.

Bombus borealis Kirby: the northern amber bumble bee
Phenology and Distribution: This species exhibits late spring emergence (earliest record

May 14) and is sparsely distributed across southern Ontario (Fig. 13).

Floral Records: Field and Museum Records: Astragalus canadensis, Cirsium vulgare*,
Echium vulgare*, Eupatorium fistulosum, Inula helenium*, Medicago sativa*, Melilotus
alba*, Onopordum acanthium*, Rubus, Solidago, Symphyotrichum novae-angliae, Trifolium
pratense*, Vicia cracca*.

46

Bombus of southern Ontario JESO Volume 141, 2010
Habitats: Close to or within wooded areas.

Bombus pensylvanicus DeGeer: the American bumble bee
Phenology and Distribution: This species exhibits late spring emergence (earliest record

May 15) and is mostly distributed in southernmost regions where it is at the northern edge
of its range (Fig. 14).

Floral Records: Robertson (1929): Amelanchier, Amorpha, Antennaria, Asclepias,
Astragalus, Baptisia, Blephilia, Campanula, Cephalanthus, Cerastium, Cercis, Circaea,
Claytonia, Clematis, Collinsia, Coreopsis, Cornus, Crataegus, Delphinium, Desmodium,
Dentaria, Dicentra, Frasera, Gaura, Gentiana, Geranium, Gerardia, Gymnocladus,
Helenium, Helianthus, Heliopsis, Heuchera, Hibiscus, Hydrophyllum, Impatiens, Ipomoea,
Tris, Krigia, Lespedeza, Lithospermum, Lobelia, Ludwigia, Lycopus, Mertensia, Mimulus,
Monarda, Nelumbo, Oenothera, Orobanche, Oxalis, Petalostemum, Penstemon, Phlox,
Physostegia, Plantago, Podophyllum, Polemonium, Polygonatum, Polygonum, Polytaenia,
Potentilla, Prenanthes, Prunella, Prunus, Pycnanthemum, Rhamnus, Ribes, Rubus,
Rudbeckia, Ruellia, Sagittaria, Salix, Scutellaria, Sida, Silene, Silphium, Sium, Solidago,
Stachys, Staphylea, Strophostyles, Symphoricarpos, Teucrium, Tilia, Tradescantia,
Triosteum, Uvularia, Verbascum, Verbesina, Verbena, Vernonia, Veronica, Viburnum, Viola,
Zizia.

Macfarlane (1974): Althaea rosea*, Carduus nutans*, Dipsacus sylvestris*, Echium
vulgare*, Erigeron philadelphicus, Symphyotrichum novae-angliae, Hesperis matronalis*,
Hydrophyllum virginianum, Kalmia latifolia, Lonicera tatarica*, Medicago sativa*, Pyrus
malus*, Robinia fertilis*, Solidago flexicaulis, Solidago graminifolia, Sonchus oleraceus*,
Symphytum officinale*, Syringa vulgaris*, Trifolium pratense*, Vaccinium angustifolium,
Vicia cracca*, Weigelia florida*.

Field and Museum Records: Astragalus canadensis, Campsis, Decodon, Dasistoma,
Echinacea, Euthamia graminifolia, Justicia, Lupinus, Pontederia cordata, Pediomelum,
Rubus idaeus, Symphyotrichum, Triodanis.

Habitats: Open farmland and fields.

Bombus insularis Smith: indiscriminate cuckoo bumble bee

Phenology and Distribution: Males and females of this species are found from late spring
until early autumn (Fig. 15). Records of this species are across southern Ontario but are
scarce. The earliest spring record is for a female collected on May 30.

Floral Records Field and Museum Records: Centaurea maculosa*, Eupatorium maculatum,
Melilotus alba*, Rubus, Solidago, Trifolium pratense*, Trifolium repens*, Vaccinium
angustifolium, Vicia cracca*.

Habitats: Unknown.

Bombus auricomus Robertson: the black and gold bumble bee
Phenology and Distribution: This species exhibits mid-spring emergence (earliest record

May 5) and has mostly a southwestern distribution (Fig. 16).

Floral Records Field and Museum Records: Dipsacus fullonum*, Eupatorium perfoliatum,
Hypericum, Malus, Monarda, Penstemon, Rubus occidentalis, Solanum dulcamara*,
Trifolium pratense*.

47

Colla and Dumesh JESO Volume 141, 2010

Habitats: Open farmland and fields.

Bombus sandersoni Franklin: Sanderson’s bumble bee

Phenology and Distribution: Few records exist for this species, consequently little is
known on its distribution and phenology (Fig. 17). The earliest spring record for this species
is June 2 in southern Ontario, indicating it may be a later emerging species.

Floral Records: Field and Museum Records: Epilobium, Gaylussacia, Kalmia angustifolia,
Kalmia polifolia, Lonicera, Malus, Monarda, Penstemon, Rhododendron, Rubus, Salix,
Sarracenia purpurea, Scutellaria lateriflora

Habitats: Unknown.

Bombus fernaldae Franklin: Fernald’s cuckoo bumble bee

Phenology and Distribution: Very few records exist for this species in the region,
consequently little is known on its distribution and phenology (Fig. 18). The earliest spring
record for this species is May 27 in southern Ontario.

Floral Records: Field and Museum Records: Asclepias, Aster, Helianthus, Pilosella
aurantiaca*, Potentilla, Rubus, Solidago, Solidago hispida, Taraxacum officinale*,
Trifolium repens*, Vaccinium angustifolium.

Habitats: Unknown.

Discussion

The bumble bees of southern Ontario differ in phenology, food plant choice,
abundance and habitat selection. Unlike some invertebrate pollinators, bumble bees in
southern Ontario are food generalists, foraging on a variety of native plant genera. For
example, B. impatiens, the most common species in the region (Fig. 1), has been found
visiting over 100 native plant genera throughout its range. This is likely due to their long
colony life-cycles which span the flowering cycles of more than one plant species. Broad
diet tolerances allows for behavioural flexibility in highly competitive situations where
nectar is often a limiting resource (Fontaine et al. 2008). Differences in food choice are a
major factor in niche partitioning among bumble bees in Ontario (Harder 1985).

This review indicates species in southern Ontario are often associated with particular
habitat types and associated phenologies. Interestingly, the earliest emerging species (i.e.
B. bimaculatus, B. ternarius, B. perplexus, B. affinis, B. vagans, B. impatiens, B terricola)
are all associated with wooded habitats (Figs. 1-5, 8, 10). These species likely have co-
evolutionary relationships with woodland spring ephemerals. Species associated with open
fields tend to be later emerging species (i.e. B. auricomus, B. griseocollis, B. pensylvanicus,
and B.fervidus) and are likely more reliant on later blooming field flowers (Figs. 6, 7, 14,
16). It has been suggested that later emerging species may be more vulnerable to stressors
such as habitat loss (Williams et al. 2009).

Although this study focuses on natural history, some comments can also be made
on species abundances. These data presented are consistent with previous findings that B.
impatiens and B. bimaculatus are the most abundant species in southern Ontario (Colla
and Packer 2008). Whether this was historically the situation or the consequence of their

48

Bombus of southern Ontario JESO Volume 141, 2010

tolerance of urbanized habitats remains to be determined. In contrast, many species have
few records and are both historically and recently uncommon. For some rarer taxa this
may be because they are at the northern edge of their native ranges in southern Ontario
(e.g. B. auricomus and B. pensylvanicus; Figs. 14, 16). Additionally, very few records
exist for most of the socially parasitic species (i.e. B. ashtoni, B. fernaldae, B. insularis),
which have likely been always rare and dependent on host abundances. Basic information
on distribution, ecological requirements and phenology are still required for the rare and
uncommon species to aid in the conservation of these potentially at-risk species (COSEWIC
2010). Additionally, to better understand this important group of bees, further study is
needed on nesting requirements, queen overwintering requirements, mating behaviours and
dietary breadth for all Bombus species in southern Ontario. Additional studies on changes
in distribution and abundance over time will also better our understanding of the ecological
needs of these native pollinators.

Acknowledgements

This study would not have been possible without the use of valuable historical
specimens from the following collections: Canadian Museum of Nature, University of
Guelph Insect Collection, Royal Ontario Museum and Algonquin Provincial Park. Thanks
to Laurence Packer, Paul Williams, Paul Catling, James Thomson and Cory Sheffield for
valuable discussion. This is contribution No. 8 from the Canadian Pollination Initiative
(NSERC-CANPOLIN)

References

Allen, G. M.., P. F. J. Eagles and S.D. Price. 1990. Conserving Carolinian Canada. University
of Waterloo Press, Waterloo, ON. 346 pp.

Benton, T. 2006. Bumblebees. Collins New Naturalist Series, London, UK. 592 pp.

Berenbaum, M., P. Bernhardt, S. Buchmann, N. W. Calderone, P. Goldstein, D. W. Inouye,
P. G. Kevan, C. Kremen, R. A. Medellin, T. Ricketts, G.E. Robinson, A. A. Snow,
S. M. Swinton, L. B. Thien and F. C. Thompson. 2007. Status of pollinators in
North America. The National Academies Press, Washington, DC. 312 pp.

Biesmeijer, J. C., S. P. Roberts, M. Reemer, R. Ohlemueller, M. Edwards, T. Peeters, A.
Schaffers, S. G. Potts, R. Kleukers, C. D. Thomas, J. Settele, and W. E Kunin.
2006. Parallel declines in pollinators and insect-pollinated plants in Britain and the
Netherlands. Science 313: 351-354.

Colla, S. R., M. C. Otterstatter, R. J. Gegear, and J. D. Thomson. 2006. Plight of the
bumble bee: Pathogen spillover from commercial to wild populations. Biological
Conservation 129: 461-467.

Colla, S. R. and L. Packer. 2008. Evidence for decline in eastern North American bumblebees
(Hymenoptera: Apidae), with special focus on Bombus affinis Cresson. Biodiversity
and Conservation 17: 1379-1391.

COSEWIC. 2010. Assessment and status report on the rusty-patched bumble bee (Bombus

49

Colla and Dumesh JESO Volume 141, 2010

affinis). 40 pp.

Findlay, C. S. and J. Houlahan. 1997. Anthropogenic correlates of species richness in
southeastern Ontario wetlands. Conservation Biology 11: 1000—1009.

Fontaine, C., C. L. Collin and I. Dajoz. 2008. Generalist foraging of pollinators: diet
expansion at high density. Journal of Ecology 96: 1002-1010.

Harder, L. D. 1985. Morphology as a predictor of flower choice by bumble bees. Ecology
66: 198-210.

Laverty, T. M. and L. D. Harder. 1988. The Bumble Bees of Eastern Canada. The Canadian
Entomologist 120: 965-987.

Macfarlane, R. P. 1974. Ecology of Bombinae (tbymenopterst Apidae) of Southern Ontario,
with emphasis on their natural enemies and relationships with flowers. PhD Thesis.
University of Guelph, Guelph, ON. 210 pp.

Mitchell, T. B. 1962. Bees of the eastern United States. II. Technical bulletin (North Carolina
Agricultural Experiment Station)*152: 1-557.

Robertson, C. 1929. Flowers and insects. Lists of visitors to four hundred and fifty-three
flowers. Science Press Printing Company, Lancaster, PA. 221 pp.

Taki, H., P. G. Kevan and J. S. Ascher. 2007. Landscape effects of forest loss in a pollination
system. Landscape Ecology 22: 1575-1587.

Williams, P., S. R. Colla and Z. Xie. 2009. Bumblebee vulnerability: common correlates of
winners and losers across three continents. Conservation Biology 23: 931-940.

50

Bombus of southern Ontario JESO Volume 141, 2010

—e— Queens
i Workers

Frequency

—t— Males

APR MAY JUNE JULY AUG SEPT OCT

Legend
a Before 1950

a 1950-1979

FIGURE 1. Phenology and distribution for Bombus impatiens in southern Ontario
(n=3017).

ae

Colla and Dumesh JESO Volume 141, 2010

—e— Queens
—&— Workers

Frequency

—#— Males

APR MAY JUNE JULY AUG SEPT OCT

FIGURE 2. Phenology and distribution for Bombus bimaculatus in southern Ontario
(n=1316).

52

Bombus of southern Ontario JESO Volume 141, 2010

—e— Queens
—@— Workers

Frequency

—t— Males

JUNE JULY AUG SEPT OCT

FIGURE 3. Phenology and distribution for Bombus terricola in southern Ontario (n=996).

53

Colla and Dumesh JESO Volume 141, 2010

—e— Queens
= Workers

Frequency

—t— Males

APR MAY JUNE JULY AUG SEPT OCT

FIGURE 4. Phenology and distribution for Bombus vagans in southern Ontario (n=914).

54

Bombus of southern Ontario JESO Volume 141, 2010

—e— Queens
fi Workers

Frequency

—#te— Males

APR MAY JUNE JULY AUG SEPT OCT

Legend
A Before 1950
a 1950-1979

e 1980-2010

[] mca

FIGURE 5. Phenology and distribution for Bombus perplexus in southern Ontario
(n=646).

55

Colla and Dumesh JESO Volume 141, 2010

—e Queens
—®— Workers

Frequency

—*— Males

APR MAY JUNE JULY AUG SEPT OCT

FIGURE 6. Phenology and distribution for Bombus griseocollis in southern Ontario
(n=611).

56

Bombus of southern Ontario JESO Volume 141, 2010

—e— Queens
—f— Workers

Frequency

—*— Males

APR MAY JUNE JULY AUG SEPT OCT

FIGURE 7. Phenology and distribution for Bombus fervidus in southern Ontario (n=585).

57

Colla and Dumesh JESO Volume 141, 2010

Frequency

APR MAY JUNE JULY AUG SEPT OCT

Legend
a Before 1950
1950-1979

FIGURE 8. Phenology and distribution for Bombus ternarius in southern Ontario (n=534).

58

Bombus of southern Ontario JESO Volume 141, 2010

—@— Queens
—i— Workers

Frequency

—k— Males

MAY JUNE JULY AUG SEPT OCT

FIGURE 9. Phenology and distribution for Bombus rufocinctus in southern Ontario
(n=527).

59

Colla and Dumesh JESO Volume 141, 2010

Frequency

APR MAY JUNE JULY AUG SEPT

FIGURE 10. Phenology and distribution for Bombus affinis in southern Ontario (n=310).

60

Bombus of southern Ontario JESO Volume 141, 2010

—e— Queens
(ii Workers

Frequency

—t— Males

APR MAY JUNE JULY AUG SEPT

FIGURE 11. Phenology and distribution for Bombus citrinus in southern Ontario (n=285).

61

Colla and Dumesh JESO Volume 141, 2010

—e— Queens
—i— Workers

Frequency

—t— Males

APR MAY JUNE JULY AUG SEPT OCT

FIGURE 12. Phenology and distribution for Bombus ashtoni in southern Ontario
(n= 275).

62

Bombus of southern Ontario JESO Volume 141, 2010

—e— Queens
ii Workers

Frequency

—t— Males

APR MAY JUNE JULY AUG SEPT OCT

FIGURE 13. Phenology and distribution for Bombus borealis in southern Ontario
(n= 191).

63

Colla and Dumesh JESO Volume 141, 2010

Frequency

MAY JUNE JULY AUG SEPT OCT

FIGURE 14. Phenology and distribution for Bombus pensylvanicus in southern Ontario
(n=135).

Bombus of southern Ontario JESO Volume 141, 2010

—e— Queens
=i Workers

Frequency

—t— Males

APR MAY JUNE JULY AUG SEPT OCT

FIGURE 15. Phenology and distribution for Bombus insularis in southern Ontario (n=54).

65

Colla and Dumesh -JESO Volume 141, 2010

—e— Queens
—@— Workers

Frequency

—t— Males

APR MAY JUNE JULY AUG SEPT

FIGURE 16. Phenology and distribution for Bombus auricomus in southern Ontario
(n=43).

66

Bombus of southern Ontario JESO Volume 141, 2010

—e— Queens
i Workers

Frequency

—t— Males

MAY JUNE JULY AUG SEPT OCT

FIGURE 17. Phenology and distribution for Bombus sandersoni in southern Ontario
(n=40).

67

Colla and Dumesh JESO Volume 141, 2010

—e— Queens
—&— Workers

Frequency

—*— Males

MAY JUNE JULY AUG SEPT OCT

FIGURE 18. Phenology and distribution for Bombus fernaldae in southern Ontario
(n= 19).

68

Weevil communities in hardwood forests JESO Volume 141, 2010

GROUND-DWELLING WEEVIL
(COLEOPTERA: CURCULIONIDAE) COMMUNITIES IN
FRAGMENTED AND CONTINUOUS HARDWOOD FORESTS
IN SOUTH-CENTRAL ONTARIO

E. PROCTOR’, R. S. ANDERSON’, E. NOL’,
J. M. GIRARD* AND S. RICHMOND*

Department of Environmental and Life Sciences, Trent University
1600 West Bank Drive, Peterborough, ON, Canada K9J 7B8

email: eproctor@trentu.ca

Abstract J. ent. Soc Ont. 141: 69- 83

Weevils (Coleoptera: Curculionidae) are the largest family in the animal
kingdom and can be found in any habitat where plants grow. Many species
not native to North America have invaded both anthropogenic and natural
habitats, and the aim of this paper is to determine whether forest landscape
continuity has discouraged introduced species. We compared the ground-
dwelling weevil communities of hardwood forest fragments to those in
hardwood stands in a continuously forested landscape, with the prediction
that the fragments would have more introduced species. Pitfall traps
caught 5090 individuals from 26 species. Both landscapes were dominated
by introduced weevils (96% of all individuals), but forest fragments were
dominated by Barypeithes pellucidus (Boheman), while Sciaphilus asperatus
(Bonsdorff) represented 74% of all weevils caught in the continuous forest.
Sixty-four percent of the introduced species were parthenogenetic, and all
parthenogenetic species were polyphagous and flightless. Fifteen native
species were captured but they accounted for only 4% of total individuals, and
the only numerous native species, Hormorus undulatus (Uhler), was absent
from the continuous forest. Seven native species were each represented by
a single individual, one of which, Sirocalodes sericans (LeConte) is the first
record for Ontario. Ground-dwelling weevil communities in central Ontario’s
forests are composed largely of non-native species, and relatively intact forests
do not provide conservation protection for this group of invertebrates.

Published November 2010

' Author to whom all correspondence should be addressed

? Canadian Museum of Nature, email: randerson@mus-nature.ca

> Biology Department, Trent University, email: enol@trentu.ca

+ Biology Department, Carleton University, email: jphilli8@connect.carleton.ca
> Faculty of Forestry, University of Toronto email: sonya.richmond@utoronto.ca

69

Proctor et al. JESO Volume 141, 2010

Introduction

The family Curculionidae (Coleoptera), hereafter weevils, is the largest family in
the animal kingdom and contains about 51000 species worldwide, in 4600 genera (Anderson
1997; Oberprieler et al. 2007). As larvae and adults, almost all weevils are phytophagous,
although a few species are saprophagous. While most of the phytophagous species are
associated with angiosperms, weevils can be found in association with almost any terrestrial
or freshwater plant species, and any plant part (Anderson 2002; Oberprieler et al. 2007).
The largest subfamily, Entiminae, have larvae that mostly live in the soil and feed on roots.
Both adult and larval entimines are largely polyphagous, feeding on many species of host
plants. The other 17 subfamilies contain species whose larvae tend to live and feed inside
plant parts including stems, leaves, roots and reproductive structures. These subfamilies
also tend to have a more restricted range of host plants (monophagous or oligophagous),
some limited to a single family, genus or species (Anderson 2002).

There are about 600 described weevil species in Canada, many of which are
introduced (McNamara 1991). Most of the introduced species are of European origin
(Langor et al. 2009) and most introductions are attributed to the importation of ornamental
plants and other products, or to dry ballast (rock, soil and sand) dumped by British ships at
North American seaports at the turn of the nineteenth century (Anderson 2002; Majka et al.
2007). Introduced weevils are prevalent in forested habitats. Pinski et al. (2005a) found
66.4% of all adult Curculionidae caught in northern hardwood forests in the Great Lakes
region to be an introduced species (Phyllobius oblongus L.) and Coyle et al. (2008) reported
a suite of nine invasive root-feeding weevils from this same region. Maerz et al. (2005)
found one introduced weevil, Barypeithes pellucidus (Boheman), to be more abundant
than all other beetle taxa combined in mature forest stands in New York and Pennsylvania.
These past studies show the prevalence of introduced weevils in forests, but it is not known
whether any large forest stands in Ontario provide refuge for native species.

Niemela and Mattson (1996) argue that European phytophagous insects are better
at invading North American forests than their North American counterparts are at invading
European forests, especially in disturbed or fragmented landscapes where the plant
communities are partially European in origin (Burke and Nol 1998). Periods of glaciation,
more severe in Europe due to its topography than elsewhere in the world (Huntley 1993),
and the past 6000 years of human habitation and exploitation (Ledig 1992) resulted in a
long history of expansion and contraction of European forests. Through this volatility,
traits having high survival-value in patchy landscapes were selected over those adapted
to expansive forests. Armed with such traits as phenotypic plasticity, high reproductive
potential, and stress-tolerance mechanisms, many introduced species have become the
dominant phytophagous insects in their invaded niches (Niemela and Mattson 1996).

Our objective is to compare the ground-dwelling weevil assemblages among forest
fragments in an agricultural landscape and continuous forest in central Ontario, Canada.
We predicted that forest fragments would have a greater proportion and higher abundances
of introduced weevil species than stands found in a continuously forested landscape. We
discuss the life history attributes of the weevils in light of their ability to become established
in continuously forested landscapes.

70

Weevil communities in hardwood forests JESO Volume 141, 2010

Materials and Methods

Study Sites

Forest Fragments —Twenty-two mature deciduous woodlots in the southern portion
of Peterborough County (44° 17’ N, 78° 20’ W) in central Ontario, Canada were selected
as part of a broader study on forest-breeding birds. The region is part of the Great Lakes-
St. Lawrence lowlands, at the southern edge of the Canadian Shield, in the Mixedwood
Plains Ecozone of the Ecological Land Classification of Canada (AAFC 2010). The region
experiences an average of 124 frost-free days a year, and 84 cm of precipitation (Environment
Canada 2008). Elevation ranges from 75 to 408 m with an average of 305 m (Wickware
and Rubec 1989). Though the soils in this region are variable in composition, all woodlots
were located in well-drained loam or sandy-loam soils with layers of organic material 8-10
cm thick (Webber et al. 1946; Gillespie and Acton 1981). The landscape is composed
of agriculture and forest fragments, interspersed with farms, housing developments, and
wetlands (Phillips et al. 2005). On average, intensive agriculture (row-crops) accounted
for 28% of the landscape within 2 km of the woodlots, less-intensive agriculture (hay, old
fields, and pastures) accounted for 30%, and forest cover accounted for 24% (Richmond
2006). All 22 woodlots were dominated by Acer saccharum (Aceraceae), with Fraxinus
americana (Oleaceae), Ostrya virginiana (Betulaceae), Thuja occidentalis (Cupressaceae),
Fagus grandifolia (Fagaceae) and Tilia americana (Tiliaceae) all occurring as frequent
canopy species. The woodlots ranged from 6.7 to 280.4 ha, with a mean of 37.1 ha. None
of the woodlots had been recently exposed to grazing, logging, fire or construction (Phillips
et al. 2005, Richmond 2006). The understory plant communities at the sampling points in
forest fragments were largely native (S. Richmond, pers. obs.).

Continuous Forest — Nine mature hardwood stands in the southern portion of
Algonquin Provincial Park (45° 35’ N, 78° 29’ W) in central Ontario, Canada were selected
as part of a larger study on sustainable forest management. Algonquin Park lies in a
transition zone between the boreal forest to the north and the Great Lakes-St. Lawrence
lowlands to the south (Rowe 1972), in the Boreal Shield Ecozone of the Ecological Land
Classification of Canada (AAFC 2010). The park covers an area of 7700km/’, the western
two-thirds of which (about 4600km7) consists of tolerant hardwood forests over rugged
terrain, interspersed with numerous lakes (Quinn 2004). Mean elevation is 396m, with
the western portion of the park experiencing an average of 84 frost-free days a year, and
100cm of precipitation (Strickland 2006). Soils characteristic of the hardwood forests are
fresh to moist, medium to coarse loams, with an average organic matter layer of 10cm
(Chambers et al. 1997). All nine stands were characterized by canopies dominated by Acer
saccharum, with lesser amounts of Fagus grandifolia, Betula alleghaniensis (Betulaceae),
Prunus serotina (Rosaceae), and Tsuga canadensis (Pinaceae). Sites ranged from 14.4 to
54.8ha, with a mean of 35.8ha. Few non-native plant species occurred in these stands (E.
Proctor, pers. obs.).

Insect Sampling

Ground-dwelling invertebrates were sampled in all sites using pitfall traps, which
consisted of 500ml containers dug into the ground so that the lips of the containers were

71

Proctor et al. JESO Volume 141, 2010

flush with the soil. The containers were filled halfway with water, a pinch of salt (as a
preservative) and a few drops of dish soap(to disrupt surface tension). Each trap was covered
with a wire grate to reduce small mammal and amphibian by-catch, and to discourage larger
mammals from disturbing them.

Sampling in Peterborough County took place in the spring and summer of 2001,
2003 and 2004, and the number-and layout of pitfall traps varied from year to year. In
2001, one trap was placed every 20m along a 100m transect that extended from the edge of
the woodlot into the interior, for a total of six pitfalls per site. Traps were active from mid
May until mid August, for a total of approximately 8800 trap-days. In 2003 and 2004, the
transect was 50m long, with one trap placed every 5m from 0 to 20m, and then every 10m
from 20 to 50m, for a total of eight traps per site. In 2003, sampling went continuously
from late-May to late-July, for a total of approximately 8500 trap-days. In 2004, trapping
began in June and continued until August, and traps were left inactive for six to seven days
following each collection. This resulted in approximately 3600 trap-days. Thus, in the
fragmented forest we had a sampling effort of 20,900 trap-days.

Sampling in Algonquin Provincial Park took place in the spring and summer of
2006 and 2007. Each of the nine stands had 12 pitfalls, placed in a three-by-four grid, with
10m between traps. Pitfalls were located in the centre of each stand and were active for
two seven-day periods: once in late May and again in mid June, for a total of approximately
1500 trap-days per year for a total of 3000.

All invertebrates were rinsed and preserved in 70% ethanol upon collection.
Weevils were later separated from the rest of the samples and identified to species. Voucher
specimens were deposited at Trent University and the Canadian Museum of Nature. We
characterized dominant species as those that represented 5% or more of the total number of
specimens for a region.

Analysis

To determine whether parthenogenesis or flightlessness were more prevalent in the
introduced weevil species than in the native species caught in this study, we used Fisher’s
exact tests. When comparing communities, problems arise if sample sizes differ because
larger samples are expected to contain a greater number of species. The Peterborough
County sites were sampled more intensively than those in Algonquin Park, with sampling
taking place throughout the growing season as compared to a week each in late-May and
mid-June. We used rarefaction to standardize all samples to a common sample size by
estimating the number of species expected in a random sample of individuals taken from
a collection (Krebs 1999). We used EcoSim (Gotelli and Enstminger 2009) to estimate
the number of species expected in Peterborough County had we caught 1000 weevils
there during the same time periods as those in Algonquin and to compare species richness
between the two regions.

Results

In total, 5090 weevil specimens were collected from 10 subfamilies, 21 genera, and
26 species. The fragmented forest sites yielded 24 species, 11 of which were introduced,

72

Weevil communities in hardwood forests JESO Volume 141, 2010

and the continuous forest sites yielded five species, 3 of which were introduced.

More than 4000 individuals were captured in the Peterborough County pitfall traps
(Table 1). Most individuals collected were of introduced species (95.1%) even though
fewer than half the species were introduced (11 out of 24). The three dominant species were
Barypeithes pellucidus Boheman (63.7% of total), Otiorhynchus raucus Fabricius (17.7%),
and Phyllobius oblongus L. (6.1%). Of the 13 native species, Hormorus undulatus Uhler
was the most abundant (3.2%). All other native species represented 0.6% of the specimens,
or less. Five natives (Anametis granulata Say, Rhyncolus brunneus Mannerheim, Grypus
equiseti Fabricius, Listronotus sparsus Say, and Listronotus oregonensis LeConte) were
each represented by a single individual.

One thousand weevils from five species were caught in the Algonquin Park pitfall
traps (Table 1). The three dominant species were all introduced and accounted for 99.8%
of the total: Sciaphilus asperatus Bonsdorff (74%), P. oblongus (20%), and Otiorhynchus
ovatus L. (5.8%). The two native species, Nemocestes horni Van Dyke and Sirocalodes
sericans LeConte, were each represented by a single individual, and were not caught in
the forest fragments. Otiorhynchus ovatus, P. oblongus, and S. asperatus were found in
both forest types, and were collected every year. Five species (H. undulatus, O. raucus, B.
pellucidus, Polydrusus sericeus Schaller, and Trachyphloeus bifoveolatus Beck) were only
caught in the forest fragments, but were caught in all three years.

More than half of the species (57.7%) and 98.7% of the individuals caught in
this study were from the subfamily Entiminae. Of these, 13 were flightless (86.7%) and
nine were parthenogenetic (60%). All but one of the introduced species was from this
subfamily. Seven out of 11 introduced entimines (63.6%) were parthenogenetic and
flightless, three were bisexual and capable of flight (27.3%), and one was bisexual and
flightless. The proportion of parthenogenetic introduced species was significantly greater
than the proportion of parthenogenetic native species [7 out of 11 (63.6%) parthenogenetic
introduced; 2 out of 15 (13.3%) parthenogenetic native; Fisher’s exact test, P= 0.01]. The
proportion of flightless introduced species was not significantly greater than the proportion
of flightless native species [8 out of 11 (72.7%) flightless introduced; 6 out of 15 (40%)
flightless native; Fisher’s exact test, P = 0.10].

Peterborough County sites caught 2016 weevils from 18 species during the
weeklong periods in late-May and mid-June that corresponded to Algonquin’s sampling.
Using the rarefaction method, in a random sample of 1000 weevils from this subsample of
Peterborough County, we would expect to see between 13 and 18 species (95% confidence).
The Peterborough County sites therefore have higher species richness than the Algonquin
sites (1000 individuals from five species).

Discussion

Contrary to our prediction, introduced weevils overwhelmingly dominated both
the fragmented and continuously forested landscapes of central Ontario but the assemblages
of the two regions were distinct and species richness was higher in the fragmented sites.
Most of the weevils in both regions were flightless, but introduced species were more likely
to be parthenogenetic.

73

Proctor et al. . JESO Volume 141, 2010

TABLE 1. Subfamilies, status in North.America (native or introduced), flight capability,
mode of reproduction in North America, and known host plants of weevils (Coleoptera:
Curculionidae) captured in pitfall traps in 22 hardwood forest fragments in Peterborough
County, Ontario and 9 hardwood stands in Algonquin Provincial Park, Ontario.
Peterborough Algonquin

sehaoaly Species 2001 2003 2004 2006 2007. /°t!
Dryophthorinae Sphenophorus minimus Hart 19 5 24
S. parvulus Gyllenhal 10 ; 10
Erirhininae Grypus equiseti Fabricius l ]
Curculioninae Tychius picirostris Germar l l 2
Baridinae Stethobaris ovata LeConte 3 ] 4
Ceutorhynchinae Sirocalodes sericans LeConte l ]
Cossoninae Rhyncolus brunneus Mannerheim l ]
Cryptorhynchinae Acalles carinatus LeConte 15 o 18
Cyclominae Listronotus oregonensis LeConte l l
L. sparsus Say l ]
Entiminae Hormorus undulatus Uhler 55 51 25 131
Otiorhynchus ovatus L. 12 38 14 5 53 122
O. raucus Fabricius FO? 256" YSIS 724
O. rugosostriatus Goeze l l
O. singularis L. 2 2
Nemocestes horni Van Dyke l l
Phyllobius oblongus L. 90 = 124 =F ela ET 67 45]
Polydrusus sericeus Schaller 4 l 4 9
Barypeithes pellucidus Boheman 295 1799 “312 2606
Sciaphilus asperatus Bonsdorff 39 71 67 118 622 917
Sitona lineelus Bonsdorff 2 i
Cathormiocerus aristatus Gyllenhal* 30 16 46
Trachyphloeus bifoveolatus Beck 3 3 p 8
Anametis granulata Say l ]
Phyxelis rigidus Say I 3 4
Molytinae Conotrachelus posticatus Boheman 2 2
TOTAL 594 2430 1066 256 744 5090

74

Weevil communities in hardwood forests JESO Volume 141, 2010

TABLE 1. continued...

Known Host

Species Status’ Flight Reproduction Plants Sources
S. minimus Native Yes Sexual Poaceae, — Vaurie 1951
Cyperaceae
S. parvulus Native Yes Sexual Poaceae, —_- Vaurie 1951
Cyperaceae
G. equiseti Native Yes Sexual Equisetaceae Cawthra 1957; Anderson 2002
T. picirostris Introduced Yes Sexual Fabaceae Anderson and Howden 1994
(Trifolium)
S. ovata Native Yes Sexual Orchidaceae _ Blatchley and Leng 1916; Howden 1988
S. sericans Native Yes Sexual Papaveraceae, Anderson 2002; Korotyaev 2008
Fumariaceae
R. brunneus Native Yes Sexual Downed woody Anderson 1997; Anderson 2002
debris
A. carinatus Native No Sexual Downed woody Anderson 2002; LaChowska et al. 2009
debris
L. oregonensis Native Yes Sexual Apiaceae Campbell et al. 1989
L. sparsus Native Yes Sexual Asteraceae, Boivin 1999; Anderson 2002
Chenopodiaceae
H. undulatus Native No Sexual Liliaceae — Blatchley and Leng 1916; Champlain
and Null 1921
O. ovatus Introduced No Asexual Polyphagous Takenouchi 1965; Anderson 2002
O. raucus Introduced No Asexual Polyphagous Anderson 2002
O. rugosostriatus Introduced No Asexual Polyphagous Wheeler 1999; Anderson 2002
O. singularis Introduced No Asexual Polyphagous Campbell et al. 1989
N. horni Native No Asexual Polyphagous Anderson 2002
P. oblongus Introduced Yes Sexual Polyphagous _ Pinski et al. 2005a
P. sericeus Introduced Yes Sexual Polyphagous _ Pinski et al. 2005a
B. pellucidus Introduced No Sexual Polyphagous Takenouchi 1965; Galford 1987
S. asperatus Introduced No Asexual Polyphagous Pinski et al. 2005a
S. lineelus Native No Sexual Polyphagous Loan 1963
C. aristatus® Introduced No Asexual Polyphagous Piper et al. 2001
T. bifoveolatus Introduced No Asexual Polyphagous Brown 1965; Piper et al. 2001
A. granulata Native No Sexual Polyphagous Campbell et al. 1989; McLain 1998
P. rigidus Native No Asexual’ —_ Brassicaceae, Levesque and Levesque 1994; Shellhorn
Rosaceae and Sork 1997
C. posticatus Native Yes Sexual Fagaceae = Anderson 2002
(Quercus)
TOTAL

a) Subfamily classification based on Anderson 2002

b) Sources: McNamara 1991; Anderson 1997

c) Formerly Trachyphloeus

d) No males in Canadian Museum of Nature or Royal Ontario Museum collections

75

Proctor et al. | JESO Volume 141, 2010

Barypeithes pellucidus dominated the forest fragments in Peterborough County
while S. asperatus dominated the continuously forested sites in Algonquin Park. Both of
these entimine weevils are flightless and polyphagous as larvae and adults (Witter and Fields
1977; Galford 1987; Anderson 2002) but B. pellucidus reproduces sexually (Takenouchi
1965), while S. asperatus reproduces through apomictic parthenogenesis (Suomalainen et
al. 1987). Many parthenogenetic organisms are successful colonizers due to their abilities
to continually propagate even at low population numbers, and to rapidly adapt because
of more frequent random mutations (Ledig 1992; Langor et al. 2009). With asexual
reproduction and a preference for Acer saccharum and other deciduous trees (Witter and
Fields 1977), S. asperatus has been able to colonize not only the continuous hardwood
forests of Algonquin Park, but also those in Michigan and Wisconsin (Werner and Raffa
2000; Pinski et al. 2005a; Coyle et al. 2008). It is a widespread species (McNamara 1991;
Bright and Bouchard 2008) and has been found as far north as Iroquois Falls, Ontario (48°
45’ N, 80° 41° W), and Edmonton, Alberta (53° 32’ N, 113° 29’ W; Bright and Bouchard
2008).

Barypeithes pellucidus, with a preferred diet that includes Quercus rubra
(Fagaceae), Aster spp. (Asteraceae), Medicago spp. (Fabaceae), Trifolium spp. (Fabaceae),
and weedy herbaceous plants (Galford 1987; Campbell et al. 1989) is the dominant species
in the forest fragments in this study and in New York and Pennsylvania (Maerz et al. 2005).
High numbers have been found in agricultural sites such as vineyards (Bouchard et al.
2005), berry plantations (Bomford and Vernon 2005), residential areas (Balsbaugh 1988)
and continuous forests of Wisconsin and Michigan (Werner and Raffa 2000).

We suggest several explanations for why this adaptable colonizing species was
absent from the Algonquin Park samples. Weevil abundance can vary considerably
seasonally, from year to year, and from place to place (Balsbaugh 1988; Bouchard et al. 2005)
and it is possible that B. pe/lucidus is established in the sites in Algonquin Park but the small
sampling effort failed to detect them. In Quebec, Bouchard et al. (2005) caught over 1000
individuals of B. pellucidus in one vineyard but caught only 19 in another vineyard 30km
away. They hypothesized that the high clay-content soils of the depauperate vineyard were
less favourable to this species’ pupation, but none of the soils in our study contained much
clay (Webber et al. 1946; Gillespie and Acton 1981; Chambers et al. 1997). Barypeithes
pellucidus are univoltine (Campbell et al. 1989). Adults usually emerge early in spring and
disappear by mid-summer (Galford 1987; Maerz et al. 2005), and have only been found in
the milder parts of Canada, such as southern British Columbia, around the Great Lakes, and
in the Maritimes (Bright and Bouchard 2008). Specimens have been collected from as far
north as Sault Sainte Marie, Ontario (46° 30’ N, 84° 20’ W; Takenouchi 1965) and Montreal,
Quebec (45° 32’ N, 73° 38’ W; Bright and Bouchard 2008) but the frost-free periods in
both these locations (120d and 140d, respectively), and in Peterborough County (124d), are
much longer than in Algonquin (84d; Marsan 1990; Strickland 2006; Environment Canada
2008; MRCC 2009). The short frost-free period in Algonquin may be insufficient for one
generation to find mates, lay eggs, and for the larvae of the next generation to hatch and
grow to a sufficient size to survive the winter. If B. pe//ucidus is present in Algonquin Park,
the combination of its flightlessness, sexual reproduction, and the short frost-free period, all
likely contribute to limiting its numbers there.

Otiorhynchus raucus, like B. pellucidus, was abundant in Peterborough County,

76

Weevil communities in hardwood forests JESO Volume 141, 2010

but absent from the Algonquin Park samples. This species is flightless, polyphagous, and
parthenogenetic in North America (Mazur 1992; Bright and Bouchard 2008), and has been
found as far north as Calgary, Alberta (51° 07’ N, 114° 19’ W; Bright and Bouchard 2008).
It was first reported in North America in 1936 at a nursery in Fonthill, Ontario (Hicks 1947),
and the larvae are serious pests of garden vegetables, while adults feed on the foliage and
shoots of fruit trees (Campbell et al. 1989). According to Mazur (1992), in Europe O.
raucus is acommon component in anthropogenic habitats such as urban parks, gardens, and
roadsides, and it is probably absent from Algonquin Park due to the lack of cultivated plants
on which it prefers to feed in both its native and introduced range.

Phyllobius oblongus was a dominant species in both landscapes. Unlike the
aforementioned species, P. oblongus is capable of flight, and thus is a good disperser. It is
established in continuous hardwood forests in the Great Lakes Region (Pinski et al. 2005a;
Coyle et al. 2008) and in Nova Scotia (McCorquodale et al. 2005). Host plants include
a wide variety of trees and shrubs, especially Acer saccharum (Witter and Fields 1977)
and Ostrya virginiana (Pinski et al. 2005b). These tree species were common in both
landscapes.

Otiorhynchus ovatus was present in both regions and in all five years, and was
a dominant species in Algonquin. Commonly known as the strawberry root weevil, it is
abundant, widely distributed, and can be found wherever plants occur (Bright and Bouchard
2008). It is flightless, parthenogenetic, extremely fecund, and has a very broad range of
hosts, including conifers (Warner and Negley 1976; Campbell et al. 1989). This broad
niche and the capability of overwintering as adults or larvae (Campbell et al. 1989), have
likely facilitated O. ovatus’ ability to colonize as far north as Fairbanks, Alaska (64° 50° N,
147° 38’ W; Bright and Bouchard 2008). Why it was collected less frequently in the forest
fragments than its congener O. raucus is unknown. Otiorhynchus raucus (5.5 to 7.5 mm) is
larger than O. ovatus (4 to 5.5 mm; Bright and Bouchard 2008) and since pitfalls select for
larger, more active individuals (Baars 1979), the high catches of O. raucus may not reflect
the true proportions of these two species.

The only introduced weevil species caught in this study not in the subfamily
Entiminae was Tychius picirostris Fabricius (subfamily Curculioninae). Commonly known
as the clover-seed weevil, its larvae feed inside the reproductive structures of naturalized and
cultivated clovers (Trifolium spp.; Anderson and Howden 1994; Anderson 2002). Though
there are a few species of clover native to Ontario (e.g. T: reflexum), most are introduced
from Europe (e.g. 7. repens and T. pratens), and have been spread throughout the continent
for their use as forage and in crop rotation (Taylor 1985; Voss 1985). Majka et al. (2007)
suggest 7. picirostris was introduced to North America in dry ballast, and with the ability to
fly and the widespread distribution of its host plants (i.e. introduced clovers), it has become
established throughout the continent (Anderson and Howden 1994).

Hormorus undulatus was the only abundant native weevil species captured in this
study, and it was only caught in the Peterborough sites. Little is known of this entimine
species beyond that it reproduces sexually, is flightless, and has been found on members of the
Liliaceae family (Convallaria, Maianthemum and Polygonatum; Blatchley and Leng 1916:
Champlain and Knull 1921). In Canada, it has been recorded as far north as Wawa, Ontario
(47° 59’ N, 84° 46’ W; Bright and Bouchard 2008), and three were collected from raspberry
(Rubus idaeus) in a Quebec plantation (Levesque and Levesque 1994). A few individuals

77

Proctor et al. JESO Volume 141, 2010

were collected in continuous hardwood forests in the Great Lakes Region compared to
the thousands of introduced specimens (Coyle et al. 2008). Though sampling was not as
intensive in Algonquin Park as it was in Peterborough County, the absence of H. undulatus
from the Park’s samples indicates that it is not an abundant species there. If it ever had been
a significant component of the weevil community in this forest and those elsewhere, it is
possible that the competitive abilities of the invasive European species already mentioned
have displaced them. The short growing season may also have prevented H. undulatus from
establishing in Algonquin Park and may explain the substantially lower species richness of
the weevil communities of the park as compared to the more southerly forest fragments.

All parthenogenetic species caught in this study were flightless and polyphagous.
With parthenogenetic reproduction and a polyphagous diet, these weevils do not need to
find mates nor travel far to find food. The high proportion of introduced species that were
parthenogenetic (63.6%) emphasizes the superior colonizing ability of these flightless
weevils over flightless sexual species like B. pellucidus. The proportion of flightless
introduced species (72.7%), however, was not significantly greater than the proportion of
flightless native species (40%), which suggests that flightlessness alone does not affect
colonizing ability. Therefore the polyphagous diets of entimines, in combination with
either parthenogenetic reproduction or the ability to fly, have made these introduced weevils
dominate the forested sites of this study.

Species richness was lower in the continuous forest sites than in the forest
fragments. We found only five species in 1000 individuals in Algonquin, whereas we would
expect 13 to 18 species in a same-sized sample from Peterborough County for the same
time period. With three common species in Peterborough County (B. pellucidus, O. raucus,
and H. undulatus) all seeming to be absent from Algonquin Park, it is likely that the shorter
frost-free period, as well as the lack of agricultural and anthropogenic habitats are limiting
others species as well.

This is the first report of Sirocalodes sericans for Ontario. Though it is generally
distributed in the western and southern regions of the United States, in Canada it has only
been documented in Manitoba (McNamara 1991; Anderson 2002). Other Sirocalodes
species are associated with Papaveraceae and Fumariaceae, with larvae mining the stems
or crowns of the host plants (Anderson 2002). Dicentra cucullaria (Fumariaceae) is a
common spring ephemeral in northern hardwood forests (Walton and Hufford 1994), and
is a possible host for this weevil. Further targeted sampling around this plant might help to
elucidate more of this species’ biology.

Pitfall traps are useful in assessing relative abundance of invertebrates active at
the ground level, and are the most efficient method to assess ground-dwelling invertebrate
communities (Prasifka et al. 2007). Further research on the weevil communities in these
areas would benefit from additional sampling techniques such as flight-intercept traps,
emergence traps, and sweep-netting.

The life histories and effects of invasive weevils are thoroughly studied in
agricultural systems (e.g. Otiorhynchus sulcatus Fabricius; Moorhouse et al. 1992) because
of the economic damage they can cause, but forest-invaders are poorly understood. We
lack information on native weevil assemblages in forests prior to the invasions (Pinski et
al. 2005a) and studying the tolerances and below-ground herbivory of introduced larval
entimines is difficult (Coyle et al. 2008). There is ample scope for further study of the

78

Weevil communities in hardwood forests JESO Volume 141, 2010

functional role of these adaptable insects in our forested ecosystems.

Acknowledgements

We thank the many field and lab assistants, D. R. Coyle, D. Beresford, and two
anonymous reviewers for their helpful comments. Funding for this work was provided by
the National Science and Engineering Research Council, the Forestry Futures Trust Grant,
the Ontario Ministry of Natural Resources, Environment Canada and Trent University.

References

Agriculture and Agri-Food Canada (AAFC). 2010. National Ecological Framework for
Canada. http://atlas.agr.gc.ca/agmaf/index_eng.html. Viewed 5 October 2010.

Anderson, R. S. and A. T. Howden. 1994. Tychius meliloti Stephens new to Canada with
a brief review of the species of Zychius Germar introduced into North America
(Coleoptera: Curculionidae). The Canadian Entomologist 126: 1363-1368.

Anderson, R. S. 1997. Weevils (Coleoptera: Curculionoidea, excluding Scolytinae and
Platypodinae) of the Yukon. pp. 523-562 in H. V. Danks and J. A. Downes (eds.),
Insects of the Yukon. Biological Survey of Canada (Terrestrial Arthropods),
Ottawa, Ontario.

Anderson, R. S. 2002. Curculionidae Latreille 1802. pp. 722-815 in R. H. J. Arnette et
al. (eds.), American Beetles, Volume 2: Polyphaga: Scarabaeoidea through
Curculionoidea. CRC Press, Boca Raton, Florida.

Baars, M. A. 1979. Catches in pitfall traps in relation to mean densities of carabid beetles.
Oecologia 41: 25-46.

Balsbaugh Jr., E. U. 1988. Distributions for two holarctic weevils which are new household
pests (Coleoptera: Curculionidae). Entomological News 99: 102-104.

Blatchley, W. S. and C. W. Leng. 1916. Rhynchophora or Weevils of North Eastern America.
The Nature Publishing Company. Indianapolis, Indiana. 682 pp.

Boivin, G. 1999. Integrated management for carrot weevil. Integrated Pest Management
Reviews 4: 21-37.

Bomford, M. K. and R. S. Vernon. 2005. Root weevil (Coleoptera: Curculionidae) and
ground beetle (Coleoptera: Carabidae) immigration into strawberry plots protected
by fence or portable trench barriers. Environmental Entomology 34: 844-849.

Bouchard, P., L. Lesage, H. Goulet, N. J. Bostanian, C. Vincent, A. Zmudzinska and J.
Lasnier. 2005. Weevil (Coleoptera: Curculionoidea) diversity and abundance in
two Quebec vineyards. Annals of the Entomological Society of America 98: 565-
574.

Bright, D. E. and P. Bouchard. 2008. Coleoptera, Curculionidae, Entiminae. The Insects
and Arachnids of Canada. Part 25. NRC Research Press, Ottawa, Ontario. 327 pp.

Brown, W. J. 1965. Trachyphloeus Germar (Coleoptera: Curculionidae) in North America.
The Canadian Entomologist 97: 189-192.

Burke, D. M. and E. Nol. 1998. Edge and fragment size effects on the vegetation of deciduous

79

Proctor et al. JESO Volume 141, 2010

forests in Ontario, Canada. Natural Areas Journal 18: 45-53.

Campbell, J. M., M. J. Sarazin and D. B. Lyons. 1989. Canadian beetles (Coleoptera)
injurious to crops, ornamentals, stored products, and buildings. Agriculture
Canada, Ottawa, Ontario. Publication 1826. 491 pp.

Cawthra, E. M. 1957. Some notes on Grypidius equiseti F. (Col.: Curculionidae) with a
description of its larva. Proceedings of the Royal Entomological Society of London
32: 96-106. aif

Chambers, B. A., B. J. Naylor, J. Nieppola, B. Merchant and P. Uhlig. 1997. Field guide
to the forest ecosystems of central Ontario. Queen’s Printer for Ontario. Ottawa,
Ontario. 200 pp.

Champlain, A. B. and J. N. Knull. 1921. Notes on Coleoptera in Pennsylvania, New York
and Connecticut. Ecological News 32: 270-273.

Coyle, D. R., W. J. Mattson and K. F. Raffa. 2008. Invasive root-feeding insects in natural
forest ecosystems of North America. pp. 134-149 in S. N. Johnson and P. J. Murray
(eds.), Root Feeders: An Ecosystem Perspective. CABI Press. London, UK.

Environment Canada. 2008. National climate data and information archive: Canadian climate
normals, Peterborough, Ontario (1971-2000). http://www.climate.weatheroffice.
gc.ca/climate_normals/index_e.html. Viewed January 2010.

Galford, J. R. 1987. Feeding habits of the weevil Barypeithes pellucidus (Coleoptera:
Curculionidae). Entomological News 98: 163-164.

Gillespie, J. E. and C. J. Acton. 1981. Soils of Peterborough County, Report no. 45. Ontario
Institute of Pedology and Agriculture Canada. Ottawa, Ontario. 61 pp.

Gotelli, N. J. and G. L. Entsminger. 2009. EcoSim: null models software for ecology, version
7. Acquired Intelligence Inc. and Kesey-Bear. Jericho, Vermont.

Hicks, S. D. 1947. Brachyrhinus raucus (Fab.), a European weevil new to North America.
The Canadian Entomologist 79: 171.

Howden, A. T. 1988. Structures related to oviposition in Curculionoidea. Memoirs of the
Entomological Society of Washington 14: 53-100.

Huntley, B. 1993. Species-richness in north-temperate zone forests. Journal of Biogeography
20: 163-180.

Korotyaev, B. A. 2008. Distribution of the weevil subfamily Ceutorhynchinae (Coleoptera,
Curculionidae). Entomological News 88: 928-947.

Krebs, C. J. 1999. Ecological Methodology, 2"? edition. Addison-Wesley Educational
Publishers, Inc. Menlo Park, California. 678 pp.

LaChowska, D., M. Rozek and M. Holecova. 2009. Chromosome similarities and
differences among three sibling species of the Acalles echinatus group (Coleoptera,
Curculionidae, Cryptorhynchinae). Zootaxa 1985: 63-68.

Langor, D. W., L. J. DeHaas and R. G. Foottit. 2009. Diversity of non-native terrestrial
arthropods on woody plants in Canada. Biological Invasions 11: 5-19.

Ledig, F. T. 1992. Human impacts on genetic diversity in forest ecosystems. Oikos 63: 87-
108.

Levesque, C. and G.-Y. Levesque. 1994. Abundance and seasonal activity of weevils
(Coleoptera: Curculionidae) in a raspberry plantation and adjacent sites in southern
Quebec (Canada). The Great Lakes Entomologist 27: 23-37.

Loan, C. C. 1963. The bionomics of Sitona scissifrons (Coleoptera: Curculionidae) and

80

Weevil communities in hardwood forests JESO Volume 141, 2010

its parasite Microctonus sitonae (Hymenoptera: Braconidae). Annals of the
Entomological Society of America 56: 600-612.

Maerz, J. C., J. M. Karuzas, D. M. Madison and B. Blossey. 2005. Introduced invertebrates
are important prey for a generalist predator. Diversity and Distributions 11: 83-
90.

Majka, C. G., R. S. Anderson and D. B. McCorquodale. 2007. The weevils (Coleoptera:
Curculionoidea) of the Maritime provinces of Canada, I]: New records from
Nova Scotia and Prince Edward Island and regional zoogeography. The Canadian
Entomologist 139: 397-442.

Marsan, J.-C., 1990. Montreal in Evolution: Historical Analysis of the Development of
Montreal’s Architecture and Urban Environment. McGill-Queen’s Press. Montreal,
Quebec. 456 pp.

Mazur, M. 1992. Description of male of Otiorhynchus raucus (Fabricius, 1777) with some
remarks on the geographical origin of the species (Coleoptera: Curculionidae).
Genus 14: 241-248.

McLain, D. K., 1998. Sexual selection and community structure: an island biogeographic
analysis with beetles. Oikos 82: 271-281.

McNamara, J. 1991. Family Curculionidae: snout beetles or weevils. pp. 329-56 in Y.
Bousquet (ed.), Checklist of Beetles of Canada and Alaska. Agriculture Canada
Publication 1861/E. Ottawa, Ontario.

McCorquodale, D. B., B. L. Musgrave, S. Atkins, C. Majka and R. S. Anderson. 2005. New
records of native and introduced weevils (Coleoptera: Curculionidae) for Nova
Scotia from Cape Breton Island. The Coleopterists Bulletin 59: 27-34.

Midwest Regional Climate Center (MRCC). 2009. Historical Climate Data: Growing
Season Summary, Sault Sainte Marie, Michigan. http://climate.geo.msu.edu/
stations/7366/gss.txt. Viewed 10 January 2010.

Moorhouse, E. R., A. K. Charnley and A. T. Gillespie. 1992. A review of the biology and
control of the vine weevil Otiorhynchus sulcatus (Coleoptera, Curculionidae).
Annals of Applied Biology 121: 431-454.

Niemela, P. and W. J. Mattson. 1996. Invasion of North American forests by European
phytophagous insects. BioScience 46: 741-753.

Oberprieler, R. G., A. E. Marvaldi and R. S. Anderson. 2007. Weevils, weevils, weevils
everywhere. pp. 491-520 in Z.-Q. Zhang and W. A. Shear (eds.), Linnaeus
Tercentenary: Progress in Invertebrate Taxonomy. Magnolia Press. Auckland,
NZ.

Phillips, J., E. Nol, D. Burke and W. Dunford. 2005. Impacts of housing developments on
wood thrush nesting success in hardwood forest fragments. The Condor 107: 97-
106.

Pinski, R. A., W. J. Mattson and K. F. Raffa. 2005a. Composition and seasonal phenology
of a nonindigenous root-feeding weevil (Coleoptera: Curculionidae) complex in
northern hardwood forests in the Great Lakes Region. Environmental Entomology
34: 298-307.

Pinski, R. A., W. J. Mattson and K. F. Raffa. 2005b. Host breadth and ovipositional behavior
of adult Polydrusus sericeus and Phyllobius oblongus (Coleoptera: Curculionidae),
nonindigenous inhabitants of northern hardwood forests. Environmental

81

Proctor et al. . . JESO Volume 141, 2010

Entomology 34: 148-157.
Piper, R. W., S. G. Compton, J.-Y. Rasplus and S. Piry. 2001. The species status of
Cathormiocerus britannicus, an endemic, endangered British weevil. Biological
Conservation 101: 9-13.
Prasifka, J. R., M. D. Lopez, R. L. Hellmich, L. C. Lewis and G. P. Dively. 2007. Comparison
of pitfall traps and litter bags for sampling ground-dwelling arthropods. Journal of
Applied Entomology 131: 115-120.
Quinn, N. W. S. 2004. The pre-settlement hardwood forests and wildlife of Algonquin
Provincial Park: a synthesis of historic evidence and recent research. The Forestry
Chronicle 80: 705-717.
Richmond, S. 2006. The importance of local versus landscape scale features in the
demography of three forest breeding songbirds. M.Sc. Thesis. Trent University,
Peterborough, Ontario. 76 pp.
Rowe, J. S. 1972. Forest regions of Canada. Canadian Forestry Service. Publication 1300.
Ottawa, Ontario, 172 pp.
Schellhorn, N. A. and V. L. Sork. 1997. The impact of weed diversity on insect population
dynamics and crop yields in collards, Brassica oleraceae (Brassicaceae). Oecologia
111: 233-240.

Strickland, D. 2006. Trees of Algonquin Provincial Park. The Friends of Algonquin Park.
Whitney, Ontario. 40 pp.

Suomalainen, E., A. Saura and J. Lokki. 1987. Cytology and Evolution in Parthenogenesis.
CRC Press. Boca Raton, Florida. 216 pp.

Takenouchi, Y. 1965. Chromosome survey in thirty-four species of bisexual and
parthenogenetic weevils of Canada. Canadian Journal of Genetics and Cytology
7: 663-687.

Taylor, N. L. 1985. Clovers around the world. pp. 1-6 in E. N. Taylor (ed.), Clover Science
and Technology. The American Society of Agronomy. Madison, Wisconsin.

Vaurie, P. 1951. Revision of genus Calendra (formerly Sphenophorus) in the United States
and Mexico (Coleoptera: Curculionidae). Bulletin of the American Museum of
Natural History 98: 33-186.

Voss, E. G. 1985. Michigan flora: part II, dicots (Saururaceae-Cornaceae). Regents of the
University of Michigan. Ann Arbor, Michigan. 744 pp.

Walton, G. B. and L. Hufford. 1994. Shoot architecture and evolution of Dicentra cucullaria
(Papavaraceae, Fumarioidea). International Journal of Plant Sciences 155: 553-
568.

Warner, R. E. and F. B. Negley. 1976. The genus Otiorhynchus in America north of Mexico
(Coleoptera: Curculionidae). Proceedings of the Entomological Society of
Washington 78: 240-262.

Webber, L. R., F. F. Morwick and N. R. Richards. 1946. Soil survey of Durham County.
Report no. 9, Ontario Soil Survey. Ontario Agricultural College. Guelph, Ontario.
68 pp.

Werner, S. M. and K. F. Raffa. 2000. Effects of forest management practices on the diversity
of ground-occurring beetles in mixed northern hardwood forests of the Great Lakes
Region. Forest Ecology and Management 139: 135-155.

Wheeler Jr, A. G. 1999. Otiorhynchus ovatus, O. rugosostriatus, and O. sulcatus

82

Weevil communities in hardwood forests JESO Volume 141, 2010

(Coleoptera: Curculionidae): exotic weevils in natural communities, mainly mid-
Appalachian shale barrens and outcrops. Proceedings of the Entomological Society
of Washington 101: 689-692.

Wickware, G. M. and C. D. Rubec. 1989. Ecoregions of Ontario. Ecological lands
classification series no. 26. Sustainable Development Branch, Environment
Canada. Toronto, Ontario. 34 pp.

Witter, J. A. and R. D. Fields. 1977. Phyllobius oblongus and Sciaphilus asperatus associated
with sugar maple reproduction in northern Michigan. Environmental Entomology
6: 150-154.

83

Yrmod ly Rygolorrtta Ee

aa iyirws x

ioesthaudi

{ ’
4 . 2 he oe mr Ed x let wrod
|i
| if
i
* ri - |
’ b
‘ » i ‘
' <-> Hebi
a
’ ¢ ub) bee
i 7
, ¢
fd
r¢
7)
_
i]
o@
’
’ Al = at af?
arin he
¢ cw Coll ‘
if A i, 1a Ju

~bim ‘sla toi hh

rus iaekuaed
zbas! letioohe ah ued Fol Sackgnibas ee
‘eto 8 parr aerne Ne ie
ior ean paige
: tase alba re} See A

286 ntsdrtondy noditsoxqurethaaniatifin,

t bietaue

1000. Effects af foteal management ta - He on the
cites in mbeed northern hardwood Bwests 6
ry arad Matingty' wert 139: Faso 55 -*me v
jt le thant 0. tuyetarians:

~~

mis, Sica aera me ‘

, Vuniaty

forte cvidener ahd facet! repeeReIne Tat
: thas
Le e :
; wortu were 2 scat Ze +3 Mt
nu snmenaw ‘Se Chesce Foor. € jaive
-
nied Foncery Service Publie

: 1 ae

shingeeet al wee iv eanity’ om is
ee oe
winctal- Parke al anes
! ot tS
hind’ Ey debate :
fe rery *. a

? Harte ies Dpotion 6

iouenal at Genet

“. Teylon (elie
nv, Nisizice, Whee ae
Horne) mcthets

he American ss

‘ PACS So}
1 tid
{ e
rn? ais

_
cout nm Ameticn nor aa
| lomblogue > PCIe

7 i Sa
wit. 37 ¢ 1} iEeey < on, 4 BE rr

ove] ula Cae ah
mar ia

eyo

Megachile ericetorum in Ontario, Canada JESO Volume 141, 2010

DISCOVERY OF THE WESTERN PALEARCTIC BEE,
MEGACHILE (PSEUDOMEGACHILE) ERICETORUM
(HYMENOPTERA: MEGACHILIDAE), INONTARIO, CANADA

C. S. SHEFFIELD', T. GRISWOLD? AND M. H. RICHARDS?
Department of Biology, York University,
4700 Keele St., Toronto, ON, Canada M3J 1P3
email: corys@yorku.ca

Scientific Note J. ent. Soc. Ont. 141: 85-92

The indigenous bee fauna of North America north of Mexico contains approximately
3500 described species (Ascher and Pickering 2010), but nearly 30 exotic species of Old
World origin are published as established (Cane 2003; Committee on the Status of Pollinators
in North America 2007). A few of these introduced species have a long history in North
America. The first was the honey bee, Apis mellifera L., brought with European settlers in
the 1620’s (Crane 1999; Horn 2005) for honey and wax production, roles now overshadowed
in importance by pollination services (Free 1993; Delaplane and Mayer 2000). Other, albeit
very few, bee species have been purposely introduced into North America for evaluation as
crop pollinators (e.g., Torchio and Asensio 1985; Batra 2003), though none of these species
are used commercially. Most bee introductions have been accidental. Brown (1950) and
Lindroth (1957) theorized that many introduced insect species may have arrived in the
New World through the importation of dry ballast (e.g., rock, sand, soil). The earliest bee
introductions likely included the ground-nesting species Andrena wilkella (Kirby), which
has been in eastern North America since the 1800’s (Malloch 1918), and Lasioglossum
leucozonium (Schrank). Lasioglossum leucozonium was only recently determined to be an
introduced species (Giles and Ascher 2006; Zayed et al. 2007), and not naturally Holarctic
in distribution as previously assumed (McGinley 1986). The North American population(s)
may have established from a single mated female (Zayed et al. 2007). These and the few
other introduced ground-nesting bee species may have been introduced via ballast from
ships in eastern North America (Giles and Ascher 2006).

Most successful introductions of bees (ca. 80%) have involved cavity-nesting
species (Cane 2003; Committee on the Status of Pollinators in North America 2007), those
nesting in pre-existing or easily excavated cavities, such as in hollow or pithy plant stems or
beetle burrows in wood (Michener 2007). The alfalfa leafcutter bee, Megachile rotundata

Published November 2010

' Author to whom all correspondence should be addressed.

2 USDA-ARS Bee Biology and Systematics Laboratory, 5310 Old Main Hill, Logan, UT,
USA 84322-5310

3 Department of Biological Sciences, Brock University, St. Catharines, ON, Canada

L2S 3Al

85

Sheffield et al. JESO Volume 141, 2010

(F.), has been in North America since at least the 1930’s (Cane 2003) and is now widespread
across the United States and southern Canada, as far east as Nova Scotia (Sheffield et al.
2008), and two additional species of the subgenus Eutricharaea Thomson are also widely
established. Three additional cavity-nesting megachilid bees, Megachile sculpturalis
Smith, Anthidium manicatum L.,, and A. oblongatum (Illiger) are rapidly spreading in North
America (Paiero and Buck 2004; Hinojosa-Diaz 2008; Zavortink and Shanks 2008; Gibbs
and Sheffield 2009; Tonietto and Ascher 2009). Several species only recently detected in
North America, such as M. scu/pturalis (Magnum and Brooks 1997) and Hylaeus hyalinatus
Smith (Ascher 2001), are now widely distributed and locally abundant members of the North
American fauna. Many introduced cavity-nesting species do very well in urban settings
(Matteson et al. 2008). For example, Chelostoma campanularum (Kirby), a recent arrival
in Canada (Buck et al. 2006), is now relatively common in Ontario in the cities of Guelph,
St. Catharines, and Toronto. Urban settings can support introduced bee species due to the
presence of introduced plant species including floral hosts also visited in their native ranges
(Hanley and Goulson 2003; Matteson et al. 2008; Gibbs and Sheffield 2009).

Invasive species are one of the biggest threats to regional biodiversity (Wilson
1999: Chivian and Bernstein 2008). Although introduced bee species account for less
than 1% of the species in North America, they often constitute much larger proportions
of surveyed faunas (calculations exclude Apis): 15% in Grixti and Packer (2006); 29% in
Sheffield (2006); 27% in Matteson et al. (2008); and 8% in Tuell et al. (2009). Additionally,
a recent survey in Guelph, ON found 12.5% ofall bees captured in pan traps to be introduced
species (M. Horn, unpublished data).

Considering that some introduced bee species are thought to disrupt local
indigenous bee populations, and potentially pollination, through competition for floral (e.g.
Paini 2004; Paini and Roberts 2005) and/or nesting resources (Barthell et al. 1998), it is
especially important to note their presence and monitor their establishment (Cane 2003).
It is also important to establish patterns of floral use, since many introduced species share
floral resources with native species, especially in urban settings (Matteson et al. 2008) and
agricultural settings that may have limited native floral resources.

The purpose of this note is to report the discovery in southern Ontario of Megachile
ericetorum Lepeletier, a Western Palearctic bee species new to the Western Hemisphere. Its
biology and diagnostic characters are briefly summarized, and methods for monitoring its
potential establishment are discussed.

Megachile (Pseudomegachile) ericetorum Lepeletier, 1841

Megachile ericetorum is wide-ranging in the Old World, occurring throughout
most of Europe (excluding western Scandinavia), Asia Minor, the Caucasus, Central Asia,
western North A frica, and Syria (Westrich 1989; Ozbek and van der Zanden 1994; Banaszak
and Romasenko 1998). Like many members of the genus Megachile Latreille, this species
nests in pre-existing cavities in canes or wood (Westrich 1989; Banaszak and Romasenko
1998). Females lack beveled cutting edges in the interspaces of the mandibular teeth (Fig.
1), as Pseudomegachile Friese and other members of Chalicodoma sensu lato (Megachile
Group 2, as per Michener 2007) do not cut leaf sections for nest construction but instead use
other materials such as plant resins, sand, and pebbles to construct nest partitions (Mitchell
1980; Westrich 1989; Snelling 1990; Banaszak and Romasenko 1998; Michener 2007).

86

Megachile ericetorum in Ontario, Canada JESO Volume 141, 2010

FIGURE 1. Face of specimen of female Megachile ericetorum Lepeletier collected in St.
Catharines, ON, Canada, showing 4-dentate mandibles without cutting edges.

Westrich (1989) indicates that this species is oligolectic on Fabaceae, mainly Lotus and
Lathyrus; males have been collected on Stachys.

Although the subgenus Pseudomegachile is indigenous to the Old World, another
introduced species, M. (Pseudomegachile) lanata (F.), is commonly collected in Florida
(Leavenwood and Serrano 2005) and the West Indies (Genaro 1997). Sheffield et al. (in
press) provide keys and full descriptions to distinguish M. ericetorum from other leafcutter
bees in Canada, although at this time, evidence is lacking as to whether this species has
established successfully. The female of M ericetorum can be distinguished from most
Megachile in Canada by the lack of cutting edges between the mandibular teeth (Fig. 1),
excluding M. sculpturalis which is much larger (> 20mm) with much orange pubescence,
and M. angelarum Cockerell and M. campanulae (Robertson), which are both slightly
smaller than M. ericetorum and lack the single median apical tubercle on the clypeus of M.
ericetorum (Fig. 1). Although the male has not yet been observed in Canada, males of M.
ericetorum are distinguishable from all other Megachile in Canada, except M. coguilletti
Cockerell, by the unmodified yellowish front tarsomeres; it differs from that species by
lacking a lower triangular process on the mandible (Sheffield et al. in press).

Megachile ericetorum is currently only known in North America from a single
female specimen (Fig. 2) collected on the Niagara Escarpment in St. Catharines, Ontario in
2003 (14.vii.2003; coll. Amy Rutgers) in a former farm field east of, and contiguous with,
the Glenridge Quarry Naturalization Site (43.124, —79.237; elev. 170m), and bordered on
the west by Highway 406. The Naturalization Site was formerly a limestone quarry and
then a landfill, which was closed in 2001 and completely replanted by 2003, whereas the
field in which the specimen was found belongs to Brock University and has remained more
or less undisturbed for almost 50 years. Westrich (1989) indicated similar habitat use (.e.,
calcareous grasslands) by this species in Europe. The habitat in which the specimen was

87

Sheffield etal. ~ JESO Volume 141, 2010

FIGURE 2. Female Megachile ericetorum Lepeletier, A) lateral and B) dorsal view.
Specimen collected in St. Catharines, ON, Canada.

found and the method by which it was collected (pan-trapping) suggest that this species may
have had the opportunity to establish in the area because the site is directly adjacent to a
former landfill. This bee species could have been transported to the area in discarded lumber,
for instance in wooden skids commonly used in international shipping. St. Catharines is
part of the major shipping route for international materials arriving into Canada and the
United States, and is < 20 km north of the United States border. Major seaports offer many
opportunities for introduced species (Majka and LeSage 2006), and this region has a long
history of commercial sea traffic. Several cavity-nesting species have been intercepted at

88

Megachile ericetorum in Ontario, Canada JESO Volume 141, 2010

such ports of entry (Cane 2003), although they may not always have the opportunity to
establish.

Since M. ericetorum has been in Canada at least since 2003, monitoring its
establishment and spread should be done (Cane 2003). Ultimately, modeling its potential
range in North America based on habitat suitability (e.g., Hinojosa-Diaz et al. 2005) may
indicate if it has the ability to become widespread across many ecozones, as in its native
range. Trap-nest surveys (e.g., Fye 1965; Krombein 1967; Sheffield et al. 2008) would
provide a means of monitoring the establishment of this species in North America, as well as
the possible displacement of native species (Barthell et al. 1998). Males of M. ericetorum,
like those of the introduced Anthidium manicatum (Severinghaus et al. 1981; Wirtz et al.
1988), aggressively defend territories (Hass 1960). This behaviour should make the species
stand out among the native Megachile species, potentially assisting in documenting its
spread.

Acknowledgements

We appreciate the assistance of John Ascher (American Museum of Natural History,
New York, NY) who provided the initial identification of this specimen, as well as many
useful comments on the manuscript, Matthias Buck (Royal Alberta Museum, Edmonton,
AB) for reviewing the manuscript and providing additional useful comments, as well as an
anonymous reviewer.

References

Ascher, J. S. 2001. Hylaeus hyalinatus Smith, a European bee new to North America,
with notes on other adventive bees (Hymenoptera: Apoidea). Proceedings of the
Entomological Society of Washington 103: 184-190.

Ascher, J. S. and J. Pickering. 2010. Bee species guide (Hymenoptera: Apoidea: Anthophora).
http://www.discoverlife.org/mp/20q?guide=A poidea_species

Banaszak, J. and L. Romasenko. 1998. Megachild Bees of Europe (Hymenoptera, Apoidea,
Megachilidae). Pedagogical University of Bydgoszcz, Poland. 239 pp.

Barthell, J. F., G. W. Frankie, and R. W. Thorp. 1998. Invader effects in a community of
cavity nesting megachilid bees (Hymenoptera: Megachilidae). Environmental
Entomology 27: 240-247.

Batra, S. W. T. 2003. Bee introductions to pollinate our crops. pp. 85-98 in K. Strickler and
J. H. Cane (eds.). For Nonnative Crops, Whence Pollinators of the Future? Thomas
Say Publications in Entomology: Proceedings, Entomological Society of America,
Lanham, MD. 204 pp.

Brown, W. J. 1950. The extralimital distribution of some species of Coleoptera. The
Canadian Entomologist 82: 197-205.

Buck, M., S. M. Paiero and S. A. Marshall. 2006. New records of native and introduced
aculeate Hymenoptera from Ontario, with keys to eastern Canadian species of

89

Sheffield et al. - JESO Volume 141, 2010

Cerceris (Crabronidae) and eastern Nearctic species of Chelostoma (Megachilidae).
Journal of the Entomological Society of Ontario 136: 37-52.

Cane, J. H. 2003. Exotic*nonsocial bees (Hymenoptera: Apiformes) in North America:
ecological implications. pp. 113-126 in K: Strickler and J. H. Cane (eds.). For
Nonnative Crops, Whence Pollinators of the Future? Thomas Say Publications in
Entomology: Proceedings, Entomological Society of America, Lanham, MD. 204

Pp.

Chivian, E. and A. Bernstein (eds). 2008. Sustaining Life. How Human Health Depends on
Biodiversity. Oxford University Press, New York, NY. 542 pp.

Committee on the Status of Pollinators in North America. 2007. Status of Pollinators in
North America. The National Academies Press, Washington, DC. 322 pp.

Crane, E. 1999. The World History of Beekeeping and Honey Hunting. Duckworth, London,
UK. 682 pp.

Delaplane, K. S. and D. F. Mayer. 2000. Crop Pollination by Bees. CABI Publishing, New
York, NY. 344 pp.

Free, J. B. 1993. Insect Pollination of Crops. Second Edition. Academic Press, Inc. San
Diego, CA. 768 pp.

Fye, R. E. 1965. Biology of Apoidea taken in trap nests in northwestern Ontario
(Hymenoptera). The Canadian Entomologist 97: 863-877.

Genaro, J. A. 1997. Key to the genus Megachile, Chalicodoma group (Hymenoptera:
Megachilidae) in Cuba. Revista de Biologia Tropical 44/45: 193-198.

Gibbs, J., and C. S. Sheffield. 2009. Rapid range expansion of the Wool-Carder Bee,
Anthidium manicatum (Linnaeus) (Hymenoptera: Megachilidae), in North
America. Journal of the Kansas Entomological Society 82: 21-29.

Giles, V. and J. S. Ascher. 2006. A survey of the bees of the Black Rock Forest Preserve,
New York (Hymenoptera: Apoidea). Journal of Hymenoptera Research 15: 208-
Zo.

Grixti, J.C. and L. Packer. 2006. Changes in the bee fauna (Hymenoptera: Apoidea) of an old
field site in southern Ontario, revisited after 34 years. The Canadian Entomologist
138: 147-164.

Hanley, M. E. and D. Goulson. 2003. Introduced weeds pollinated by introduced bees:
cause or effect? Weed Biology and Management 3: 204-212.

Hass, A. 1960. Vergleichende Verhaltensstudien zum Paarungsschwarm solitaérer Apiden.
Zeitschrift fiir Tierpsychologie 17: 402-416.

Hinojosa-Diaz, I. A. 2008. The giant resin bee making its way west: first record in Kansas
(Hymenoptera: Megachilidae). ZooKeys 1: 67-71.

Hinojosa-Diaz, I. A., O. Yafiez-Ordofiez, G. Chen, A. T. Peterson, and M. S. Engel. 2005.
The North American invasion of the giant resin bee (Hymenoptera: Megachilidae).
Journal of Hymenoptera Research 14: 69-77.

Horn, T. 2005. Bees in America. How the Honey Bee Shaped a Nation. University Press of
Kentucky. 333 pp.

Krombein, K. V. 1967. Trap-nesting Wasps and Bees: Life Histories, Nests, and Associates.
Smithsonian Press, Washington, DC. 570 pp.

Leavenwood, J. M., Jr. and D. Serrano. 2005. A distributional checklist of the leaf-cutting
bees (Hymenoptera: Megachilidae) of Florida. Insecta Mundi 19: 173-176.

90

Megachile ericetorum in Ontario, Canada JESO Volume 141, 2010

Lindroth, C. H. 1957. The faunal connections between Europe and North America. Almqvist
and Wiksell, Stockholm, Sweden. 344 pp.

Magnum, W. A. and R. W. Brooks. 1997. First records of Megachile (Callomegachile)
sculpturalis Smith (Hymenoptera: Megachilidae) in the continental United States.
Journal of the Kansas Entomological Society 70: 146-148.

Majka, C. G. and L. LeSage. 2006. Introduced leaf beetles of the Maritime Provinces, 1.
Sphaeroderma testaceum (Fabricius) (Coleoptera: Chrysomelidae). Proceedings
of the Entomological Society of Washington 108: 243-247.

Malloch, J. R. 1918. Occurence of a European solitary bee (Andrena wilkella Kirby) in the
eastern United States. Proceedings of the Biological Society of Washington 31:
61-64.

Matteson, K. C., J. S. Ascher and G. A. Langellotto. 2008. Bee richness and abundance in
New York City urban gardens. Annals of the Entomological Society of America
101: 140-150.

McGinley, R. J. 1986. Studies of Halictinae (Apoidea: Halictidae), I: Revision of New
World Lasioglossum Curtis. Smithsonian Contributions to Zoology 429: 1-294.

Michener, C. D. 2007. The Bees of the World. 2" Ed. Johns Hopkins University Press,
Baltimore, MD. 953 pp.

Mitchell, T. B. 1980. A Generic Revision of the Megachiline Bees of the Western
Hemisphere. Contribution from the Department of Entomology, North Carolina
State University, Raleigh, NC. 95 pp.

Ozbek, H. and G. van der Zanden. 1994. A preliminary review of the Megachilidae of Turkey
Part IV. Megachilini and Lithurgini (Hymeoptera: Apoidea). Turkiye Entomoloji
Dergisi 18: 157-174.

Paiero, S. M. and M. Buck. 2004. The giant resin bee, Megachile sculpturalis Smith, and
other newly introduced and newly recorded native Megachilidae and Andrenidae
(Apoidea) from Ontario. Journal of the Entomological Society of Ontario 134:
141-143.

Paini, D. R. 2004. Impact of the introduced honey bee (Apis mellifera) (Hymenoptera:
Apidae) on native bees: a review. Austral Ecology 29: 399-407.

Paini, D. R., and J. D. Roberts. 2005. Commercial honey bees (Apis mellifera) reduce the
fecundity of an Australian native bee (Hylaeus alcyoneus). Biological Conservation
123: 103-112.

Severinghaus, L. L., B. H. Kurtak and G. C. Eickwort. 1981. The reproductive behavior of
Anthidium manicatum (Hymenoptera: Megachilidae) and the significance of size
for territorial males. Behavioral Ecology and Sociobiology 9: 51-58.

Sheffield, C. S. 2006. Diversity and Management of Bees for the Pollination of Apple in
the Annapolis Valley of Nova Scotia. PhD Thesis, University of Guelph, Guelph,
ON.

Sheffield, C. S., P. G. Kevan, S. M. Westby, and R. F. Smith. 2008. Diversity of cavity-
nesting bees (Hymenoptera: Apoidea) within apple orchards and wild habitats in
the Annapolis Valley, Nova Scotia, Canada. The Canadian Entomologist 140: 235-
249.

Sheffield, C. S., C. Ratti, L. Packer and T. Griswold. In press. Leafcutter and mason bees
of the genus Megachile Latreille (Hymenoptera: Megachilidae) in Canada and

1

Sheffield etal. 7 JESO Volume 141, 2010

Alaska. Canadian Journal of Arthropod Identification (in press).

Snelling, R. R. 1990. A review of the native North American bees of the genus Chalicodoma
(Hymenoptera: Megachilidae). Contributions in Science, Natural History Museum
of Los Angeles County 421: 1-39.

Tonietto, R. K. and J. S. Ascher. 2009. Occurrence of the Old World bee species Hylaeus
hyalinatus, Anthidium manicatum, A. oblongatum, and Megachile sculpturalis, and
the native species Coelioxys banksi, Lasioglossum michiganense, and L. zophops
in Illinois (Hymenoptera: Apoidea: Colletidae, Halictidae, Megachilidae). The
Great Lakes Entomologist 41: 200-203.

Torchio, P. F. and E. Asensio. 1985. The introduction of the European bee, Osmia cornuta
Latr., into the U.S. as a potential pollinator of orchard crops, and a comparison
of its manageability with Osmia lignaria propinqua Cresson (Hymenoptera:
Megachilidae). Journal of the Kansas Entomological Society 58: 42-52.

Tuell, J. K., J. S. Ascher and R. Isaacs. 2009. Wild bees (Hymenoptera: Apoidea: Anthophila)
of the Michigan highbush blueberry agroecosystem. Annals of the Entomological
Society of America 102: 275-287.

Westrich, P. 1989. Die Wildbienen Baden-Wurttembergs: Allgemeiner Teil, pp. 1-431;
Spezieller Teil: Die Gattungen Und Arten, pp. 437-972. Stuttgart: Eugene Ulmer.

Wilson, E. O. 1999. The Diversity of Life. New Edition. W.W. Norton and Company, New
York, NY. 424 pp.

Wirtz, P., M. Szabados, H. Pethig and J. Plant. 1988. An extreme case of interspecific
territoriality: male Anthidium manicatum (Hymenoptera: Megachilidae) wound
and kill intruders. Ethology 78: 159-167.

Zavortink, T. J. and S. S. Shanks. 2008. Anthidium manicatum (Linnaeus) (Hymenoptera:
Megachilidae) in California. Pan-Pacific Entomologist 84: 238-241.

Zayed, A., S. A. Constantin and L. Packer. 2007. Successful biological invasion despite a
severe genetic load. PLoS One 2(9): e868. doi: 10.1371/journal.pone.0000868.

92

JESO Volume 141, 2010

ERRATUM

L. Timms. 2009. Growing pains: How the birth of the Entomological Society of Canada
affected the identity of the Entomological Society of Ontario. The Journal of the
Entomological Society of Ontario 140: 49-56.

The page numbers published for this manuscript in JESO 140 were incorrect. The correct
reference is:

L. Timms. 2009. Growing pains: How the birth of the Entomological Society of Canada
affected the identity of the Entomological Society of Ontario. The Journal of the
Entomological Society of Ontario 140: 46-53.

Below is how the title should appear. The editor apologizes for this error.

GROWING PAINS: HOW THE BIRTH OF THE
ENTOMOLOGICAL SOCIETY OF CANADA AFFECTED THE
IDENTITY OF THE ENTOMOLOGICAL SOCIETY OF ONTARIO

L. TIMMS
Faculty of Forestry, University of Toronto
33 Willcocks Street, Toronto, Ontario, Canada M5S 3B3
email: laura.timms@utoronto.ca

Special Contribution J. ent. Soc. Ont. 140: 46-53

93

JESO Volume 141, 2010

THE ENTOMOLOGICAL SOCIETY OF ONTARIO
OFFICERS AND GOVERNORS
2010-2011 ©

President: H. FRASER

Ontario Ministry of Agriculture, Food and Rural Affairs

4890 Victoria Ave. North, P.O. Box 8000
Vineland, ON LOR 2E0

hannah. fraser@ontario.ca
President-Elect: B. GILL

Entomology Unit, Ontario Plant Laboratories, Canadian

Food Inspection Agency. Building 18 C.E.F.
960 Carling Ave., Ottawa, ON K1A 0C6
bruce.gill@inspection.ge.ca

Past-President: G. UMPHREY
Department of Mathematics and Statistics
University of Guelph, Guelph, ON N1G 2W1
umphrey(@uoguelph.ca

Secretary: N. MCKENZIE

Vista Centre, 1830 Bank Street, P.O. Box 83025
Ottawa, ON K1V 1A3

nicole _mckenzie@hc-sc.gc.ca

S. LI

Pest Management Centre, Building 57
Agriculture and Agri-Food Canada
960 Carling Ave., Ottawa, ON KIA 0C6
Dr.Shiyou.Li@nrcan.ge.ca

Directors:

R. BUITENHUIS (2011-2013)
Vineland Research and Innovation Centre

4890 Victoria Ave. North, P.O. Box 4000
Vineland, ON LOR 2E0
rose.buitenhuis@vinelandresearch.com

S. LACHANCE (2010-2011)
Université de Guelph - Campus d’ Alfred

31 St. Paul Street, Alfred, ON KOB 1A0
Slachance@alfredc.uoguelph.ca

S. KULLIK

Department of Environmental Biology
University of Guelph, Guelph, ON NIG 2W1
sigrun.kullik@sympatico.ca

J. MCNEIL

Department of Biology, BGS 3066
University of Western Ontario,
London, ON N6A 5B7
jmcneil2@uwo.ca

K. RYALL

(2009-2011)

(2011-2013)

(2009-2011)

Canadian Forest Service, Great Lakes Forestry Centre,

Natural Resources Canada, 1219 Queen Street East,
Sault Ste. Marie, ON P6A 2E5

krista.ryall@NRCan-RNCan.ge.ca

94

I. SCOTT
Agriculture and Agri-Food Canada
1391 Sandford Street, London, ON NS5V 4T3
lan.Scott@agr.gc.ca
ESO Regional Rep to ESC: H. DOUGLAS

Canadian Food Inspection Agency

960 Carling Ave., Ottawa ON K1A 06C
douglash@inspection.ge.ca

Librarian: J. BRETT

Library, University of Guelph

Guelph, ON NIG 2W1
jimbrett@uoguelph.ca

Newsletter Editor: A. GRADISH

School of Environmental Science
University of Guelph, Guelph ON NIG 4Y2
agradish@uoguelph.ca

Student Representative: M. LOCKE
Agriculture and Agri-Food Canada

960 Carling Avenue, K.W. Neatby Building
Ottawa, ON, K1A 0C6
michelle.locke@agr.gc.ca

Website: M. JACKSON

School of Environmental Science
University of Guelph, Guelph, ON NIG 2W1
jackson@uoguelph.ca

(2010-2011)

JESO Editor: M. RICHARDS

Dept. of Biological Sciences, Brock University
St. Catharines, ON L2S 3A1
miriam.richards@brocku.ca

Technical Editor: J. VICKRUCK

Dept. of Biological Sciences, Brock University
St. Catharines, ON L2S 3A1
jess.vickruck@brocku.ca

Associate Editors:

A. BENNETT

Agriculture and Agri-Food Canada

960 Carling Ave., Ottawa ON K1A 06C

N. CARTER

Engage Agro Corporation

1030 Gordon St., Guelph, ON, NIG 4X5
neilcarter@engageagro.com

J. SKEVINGTON

Agriculture and Agri-Food Canada

Eastern Cereal and Oilseed Research Centre
960 Carling Ave., Ottawa, ON K1A 0C6

rete ExTOMOLOGICAL 1
OUTICERS AND Gt
2010-2014 |

; Bers
she
t

‘
, a |
. veh. aati
3) : 9 ats ater aoe,
La len Bie ee ro 7

Asi) Régianal Rep
dia ood nape in Aa

Carlie Aven OMS

“ att
| ; RKTT
‘ x tp be Yau
oip Lae MGT Wie.
kes ret ss eae AE vi
% Weare enti +i
(ay i cman

be *

inate reese,

A atpars Ob Ags

960) Carling A
we

‘ ‘
ut ( och

Kipnoyre;: M4, FO CUSON- :
- a Lowen Sot >
eee yh. si, % '

sath ts ao 7H

. ’

. =o
ha Mi RICHARDS

Science's, Drag

IAT. 1s

i SF ,

; VE ERICK

‘ ot Poesd Cab e aM
ee Cie» ON KIA ORE
oo lore

(i Garden St, Cadaiipl,

ee

i« xe" , Ent 1 CRY —_

Ay recta Chae ares Agi-Pond

suern Cs cual tgs OW

dai het ah ie ras

: oe ee ’
; — =

ay i
te a ;

Devils:

_ =

ENTOMOLOGICAL SOCIETY OF ONTARIO

The Society founded in 1863, is the second oldest Entomological Society in North America
and among the nine oldest, existing entomological societies in the world. It serves as an
association of persons interested in entomology and is dedicated to the furtherance of
the science by holding meetings and publication of the Journal of the Entomological
Society of Ontario. The Journal publishes fully refereed scientific papers, and has a
world-wide circulation. The Society headquarters are at the University of Guelph. The
Society’s library is housed in the McLaughlin Library of the University and is available
to all members.

An annual fee of $30 provides membership in the Society, and the right to publish in the
Journal, and receive the Newsletter and the Journal. Students, amateurs and retired
entomologists within Canada can join free of charge but do not receive the Journal.

A World Wide Web home page for the Society is available at the following URL:
http://www.entsocont.ca

APPLICATION FOR MEMBERSHIP

Please send your name, address (including postal code) and email address to:
Nicole McKenzie, Secretary, Entomological Society of Ontario
c/o Vista Centre, 1830 Bank Street, P.O. Box 83025 Ottawa, ON K1V 1A3
email: nicole_mckenzie@hc-sc.gc.ca

NOTICE TO CONTRIBUTORS

Please refer to the Society web site (http://www.entsocont.ca) for current instructions to
authors. Please submit manuscripts electronically to the Scientific Editor
(miriam.richards@brocku.ca).

CONTENTS

T. FROM THE EDUT OR oceceosioseseininscsovccseintoninniansescasttebaaalaias ane sistas
I. ARTICLES

D. L. LEGROS and D. V. BERESFORD — Aerial foraging and sexual dimorphism in bu
beetles (Silphidae: Coleoptera) in a central Ontario forest............csscscsssssssscssssssessesssssseeeees 3-10

J. L. VICKRUCK, J. T. HUBER and M. H. RICHARDS — Natural enemies of the bee gen 1s”
Ceratina (Hymenoptera: Apidae) in the Niagara Region, Ontario, Canada..............s0+0-+.1 1-26

P.M. CATLING, H. GOULET, R. BENNETT and B. KOSTIUK — Orthopterans (Orthoptera),
ground beetles (Coleoptera: Carabidae), and spiders (Araneae) in burned and unburned alvar

/

woodlands — the importance of postfire succession to insect iversity...........ssssescssseseees 27-37

S. C. COLLA and S. DUMESH — The bumble bees of southern Ontario: Notes on natu al ;
history and distribution...............:cesccessvoshesenecsiibietaamitishiianemnmnapeanaaan 5
E. PROCTER, R. S. ANDERSON, E. NOL, J. M. GIRARD and S. RICHMOND — Groun d-
dwelling weevil (Coleoptera: Curculionidae) communities in fragmented and continuous
hardwood forests in south-central Ontari0............scecssseesesserseseesesseeesseseeseeseeesneenenseneenenees 69-83,

;
i

Ill. NOTE

C. S. SHEFFIELD, T. GRISWOLD and M. H. RICHARDS — Discovery of the Weste a
Palearctic bee Megachile (Pseudomegachile) ericetorum (Hymenoptera: Megachilidae), in

Ontario, Canada.... SOSOSSSSSSSSSSHESSSSOSEOSOSSEESSESSE EEO E OEE ESOS OS EEEEEEEEEEEEEEEEESEEEEESESSSESEESESESSEESEEEEEEEESS

IV. ERRATUM

L. TIMMS. 2009. Growing pains: How the birth of the Entomological Society of Canada
affected the identity of the Entomological Society of Ontario. The Journal of the Entomologiell
Society of Ontario 140: 49-56.......cccc.ccssccesescscessesssoesseersesssnasenstesaccnsessensnsnnienansieiessintinasedsnataaE a

V. ESO OFFICERS AND GOVERNORS 2010-201 1........scssssssssssssnsossssssssessnssssesssnscssnscenseeensess 000.94
VI. ESO OFFICERS AND GOVERNORS 2009-2010........ssssesssssessessesnesneeses ..inside front cover

VIL. FELLOWS OF THE ESO .o...conc:ccssccscecsansssensciasspennioserentetacmomnensatasnnanettd inside front cover

VIII. APPLICATION FOR MEMBERSHIP.............0cccescccsescossssenssssossetenesnsaseees inside back cover

Ld

IX. NOTICE TO CONTRIBUTORS i-csnsccsehecccenc shee inside back cover

. = F:. . ao Guns 7 “46
’ 4 ae | 2
_~P-
- S by
a a
-
]
:
: a |
,
.
J

inp 's a. 5¢ es” . f7A9 »

.]
# a . i iv. ”. pete GA ued
ov
y é
“e amy
ey
®
é
=
wilt
a Wels
16 #5
ad ;
aT, a a ey
‘ , / :
6
lL,
rut -<
Pop"
se ry
Vo Int
7
se
a oi
ae o
ns :
a ety i bP De

WWCTANLNULNMYL
3 2044 118 666 171