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THE TEXAS JOURNAL OF SCIENCE
Volume 6 1 , No. 1 FEBRUARY, 2009
CONTENTS
The Effects of All-Terrain Vehicle Use on the Herpetofauna of an East Texas Floodplain.
By T imothy R. Hunkapiller, Neil B. Ford and Kevin Herriman ............................ 3
Selection of Desert Bighorn Sheep {Ovis canadensis) Transplant Sites in Sierra Maderas del Carmen and Sierra San Marcos y del Pino,
Coahuila, Mexico.
By Alejandro Espinosa-T, Armando J. Contreras-Balderas,
Andrew V. Sandoval and Mario A. Garcia~A ..................................................... 15
Geographic Distribution Records for Select Fishes of Central and Southern Arkansas.
By Chris T, McAllister, Renn Tumlison and Henry W. Robison.......................... 31
Comparison of Total Lipid and Fatty Acid Compositions of Whole-Body and Body Segments of Lertha extensa Adults (Neuroptera: Nemopteridae).
By Ozlem Cakmak, Mehmet Bashan and Ali Satar . . . . . ........45
General Notes
Myxidium serotinum (Protista: Myxozoa) from a Jefferson Salamander {Ambystoma jeffersonianum), in Illinois.
By Chris T. McAllister, John A. Crawford and Andrew R. Kuhns ................ 61
Records of the Porcupine (Erethizon dorsatum) from the Eastern Margins of the Edwards Plateau of Texas.
By Amy B. Baird, Gregory B. Pauly, David W. Hal and
Travis J. Laduc .............................................................................................. 65
First Record of Cymbovula acicularis (Gastropoda: Prosobranchia: Ovulidae) from the Coast of Tamaulipas, Mexico.
By Alfonso Correa-Sandoval and Ned E. Strenth. .................................. ....... 67
Author Instructions ..............................................................................................73
Membership Application
80
THE TEXAS JOURNAL OF SCIENCE EDITORIAL STAFF
Managing Editor:
Ned E. Strenth, Angelo State University Manuscript Editor:
Frederick B. Stangl, Jr., Midwestern State University Associate Editor for Botany:
Janis K. Bush, The University of Texas at San Antonio Associate Editor for Chemistry:
John R. Villarreal, The University of Texas-Pan American Associate Editor for Computer Science:
Nelson Passos, Midwestern State University Associate Editor for Environmental Science:
Thomas LaPoint, University of North Texas Associate Editor for Geology:
Ernest L. Lundelius, University of Texas at Austin Associate Editor for Mathematics and Statistics:
E. Donice McCune, Stephen F. Austin State University Associate Editor for Physics:
Charles W. Myles, Texas Tech University
Manuscripts intended for publication in the Journal should be submitted in TRIPLICATE to:
Dr. Frederick B. Stangl, Jr.
TJS Manuscript Editor Department of Biology Midwestern State University Wichita Falls, Texas 76308 frederick.stangl@mwsu.edu
Scholarly papers reporting original research results in any field of science, technology or science education will be considered for publication in The Texas Journal of Science. Instructions to authors are published one or more times each year in the Journal on a space-available basis, and also are available on the Academy's homepage at:
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AFFILIATED ORGANIZATIONS American Association for the Advancement of Science,
Texas Council of Elementary Science Texas Section, American Association of Physics Teachers Texas Section, Mathematical Association of America Texas Section, National Association of Geology Teachers Texas Society of Mammalogists
TEXAS I OF SCI61(1):344
FEBRUARY, 2009
THE EFFECTS OF ALL^TER^IN VEHICLE USE ON THE HERPETOFAUNA OF AN EAST TEXAS FLOODPLAIN
Timothy R. Hunkapiller, Neil B* Ford and Kevin Herriman
Department of Ecology and Evolutionary Biology University of Tennessee, Knoxville, Tennessee 37996 Department of Biology, University of Texas at Tyler,
Tyler, Texas 75799 and Texas Parks and Wildlife Department Lindale, Texas 75771
Abstract “Recreational all-terrain vehicle (ATV) use is known to cause extensive environmental damage in xeric habitats, however their impact has been poorly studied in floodplain ecosystems. Floodplains are complex and important wetland habitats due to their high primary productivity and biodiversity. In this study, amphibians and reptiles are used as indicators of environmental stress from ATV use in a floodplain at the Old Sabine Bottom Wildlife Management Area (OSBWMA), Smith County, Texas. The herpetofauna were surveyed using cover board arrays (wood and tin) placed at nine sites: three within a forest, three along trails open to ATV traffic, and three along trails closed to ATV traffic. No significant differences were observed in abundance, richness, evenness, or diversity of amphibians and reptiles found among these three treatments (P>0.05). The apparent lack of effect could be due to restricted use and the recent opening of the OSBWMA to ATVs, and/or the natural resilience of floodplain ecosystems to disturbance. Additionally, the impact of ATV use may have been masked by the relatively short time period of the study (14 months) and low rainfall during the investigation.
Off-road vehicle use has increased greatly since the 1970s, from approximately 5 to 35 million annual users (Wisdom et al. 2004; USDA 2004). Minimal research has been conducted on the impact of off-road vehicle trails on ecosystems (Phillips & Alldredge 2000; Gaines et al. 2003). Additionally, only xeric regions have been widely examined in studies of the effects of off-road vehicles on ecosystems (Iverson et al 1981; Adams et ah 1982; Webb & Wilshire 1983).
Recreational all-terrain vehicle (ATV) use can affect wildlife by direct injury or death, by noise pollution, through fragmentation of habitat, and by creating migration barriers (e.g., Webb & Wilshire 1983; Reijnen et al. 1996; Forman & Alexander 1998; Bonnet et ah 1999). Such effects are known to cause changes both in the
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THE TEXAS JOURNAL OF SCIENCE-VOL. 61, NO. 1, 2009
abundance and diversity of organisms in biological communities (Pearson et aL 1999; Findlay & Bourdages 2000; Trombulak & Frissell 2000). Habitat fragmentation and associated edge effects are considered to have detrimental effects on community composition by specifically impacting interior species (Wilcox & Murphy 1985; Robinson & Quinn 1992; Spellerberg 1998). Even less conspicuous effects of ATV use may harm community structure. Palis & Fischer (1997) found that off-road vehicle use disrupts pond floor microtopography by breaking the hardpan that lies below the pond and causing a shorter hydroperiod, thus decreasing the availability of ephemeral ponds for breeding amphibians. Furthermore, a variety of chemicals derived from gasoline additives can be introduced into a habitat leading to direct toxic effects and indirect disruption of food webs (Trombulak & Frissell 2000; Forman et al. 2003).
Floodplains are a complex and important wetland ecosystem because their high productivity leads to increased biodiversity (Reice 1994; Bayley 1995). The flood-pulse concept, characterized by the predictable advance and retreat of water on a floodplain, is postulated to maintain diversity in a system (Bayley 1995; Ostfeld & Keesing 2000). The primary productivity is augmented by an influx of nutrients that are washed into temporary pools and the forest floor resulting in an increase in plant and animal abundance due to extra energy availability (Bayley 1995; Sparks 1995). Additionally, temporary pools that form during the recession phase (Junk 1973; Sparks et al. 1998) hold fish and ftinction as breeding sites for many amphibians. Both forest floor and temporary pools provide readily available food sources for many carnivores (Modes et al. 1998; Shiel et al. 1998). Despite their biological importance, floodplain ecosystems are among the most threatened natural areas in the eastern United States and, of all wetland types, floodplains have suffered the greatest losses (Bayley 1991; Graham et al. 1997).
HUNKAPILLER, FORD & HERRIMAN
5
Amphibians and reptiles are often locally abundant, easy to sample, and respond to an assortment of subtle environmental changes, making them good indicators of wetland health (Heyer et ah 1994; Welsh & Ollivier 1998; Christy & Dickman 2002). Alterations of such environmental factors as temperature (Seebacher et al. 2003), precipitation (Heyer et al. 1994), pH (Wyman & Hawksly-Lescault 1987), salinity (Christy & Dickman, 2002), and ultraviolet radiation (Blaustein et al. 1998) have been shown to cause changes in amphibian and reptile abundance and diversity in an area. Because of their importance in ecosystem structure and function, herpetofauna have also been used as indicators of ecosystem integrity (Duellman & Trueb 1994; Petranka 1998; Lips 1999). The amphibian and reptile community in an east Texas floodplain that is partially open to ATV travel was evaluated to assess the impacts of ATV use on floodplain ecosystems.
Methods
Study site-T\iQ Old Sabine Bottom Wildlife Management Area (OSBWMA) is located in northern Smith County, Texas and is bordered along its northern edge by the Sabine River. With 2087 ha of hardwood forest, the OSBWMA is one of the largest contiguous bottomland hardwood forests remaining in Texas. The primary vegetation type is a diverse Water Oak-Elm- Sugarberry Forest. Dominant vegetative overstory is comprised of water oak (Quercus nigra), willow oak (Quercus phellos), overcup oak (Quercus lyrata), pecan and hickory {Cary a sp.), cedar elm (JJlmus crassifolia), water elm (Planera aquatica), ash {Fraxinus sp.), American hornbeam {Carpinus caroliniana), and black willow {Salix nigra). Periodic flooding occurs at the OSBWMA due to heavy rainfall, opening of the floodgates at the Lake Fork Dam, and overflow from the Iron Bridge Spillway on Lake Tawakoni, however, no flooding occurred during this study. Flooding usually occurs in the winter and spring months and results in the filling of both natural ephemeral pools within the forest and the man-made
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THE TEXAS JOURNAL OF SCIENCE-VOL. 61, NO. 1, 2009
soil compacted ephemeral pools formed from tire ruts in the trails (Hampton & Ford 2007).
Several trails through the OSBWMA were created by the use of motorized vehicles prior to Texas Parks and Wildlife Department (TPWD) ownership of the property. Current trail use includes hiking, horseback riding, and beginning in 2004 the restricted use of all-terrain vehicles for public hunting access on two designated trails from October 1 to May 3 1 each year. No recreational riding is allowed. The previous use of motorized vehicles and AT Vs caused deep tire ruts and compaction of the soil on the trails. Over the course of this study, the trails open to ATV use received an average of one to two users per day during the October to December time period, with less use through the end of May. The on-site staff of the OSBWMA traversed all trails on the area conducting routine trail maintenance and management activities by ATV or medium sized tractor on a year round basis. The personnel at the OSBWMA attempted to restrict their use of the trails to drier periods to reduce impacts (Shaun Crook, pers. comm.).
Methods -^\nQ areas were chosen to monitor reptile and amphibian populations: three within the forest (at least 50 m from any edge), three along trails that are open for ATV traffic, and three along trails that are closed to ATV traffic (very limited use since 1996). Each area was divided into five stations, each 50 m apart. Each station consisted of two wooden cover boards (ca. 175 by 80 cm) and two pieces of corrugated tin (ca. 200 by 80 cm). One of each cover type (wood and tin) was placed on each side of the trail at each station. Because there were no trails within the undisturbed forest plots, each station within the forest consisted of one piece of both tin and wood placed approximately two meters from another cover array to emulate the same sampling system as on the trails. The cover items were placed in November 2004 and checked at least once a week from November 2004 to December 2005. In this wetland system cover boards are an effective survey method in a very short time frame (Hampton & Ford 2007). Individual
HUNKAPILLER, FORD & HERRIMAN
7
amphibian and reptiles captured under boards were identified, sexed and marked when possible, and subsequently released. Individual identification marking consisted of scale clipping, toe clipping, or PIT tagging depending on the size and species of the captured individual.
Statistical methods and analyses.-^owQXdX community indices were computed including Simpson’s index of diversity (Krebs 1999), Smith and Wilson’s index of evenness (Smith & Wilson 1996; Krebs 1999), and Morisita’s index of similarity (Morisita 1959; Krebs 1999). These indices of diversity and evenness as well as abundance and richness of herpetofauna species were compared among sites using an analysis of variance (Systat Software Inc. 2004) to determine if there was a significant difference among treatments.
Results
A total of 403 amphibians and reptiles representing 16 species were recorded under cover boards. Totals included two salamander, one anuran, three lizard, and 10 snake species. Of the total animals captured, 31 (7%) were salamanders, 23 (6%) were anurans, 236 (59%) were lizards, and 113 (28%) were snakes (Table 1). Ten species were captured in all of the treatments. Forty-five marked individuals were recaptured during the sampling period. Thirty-one recaptures were lizards.
The ATV trails had the highest species richness. The highest abundance was observed in the forested control areas. However, abundance, richness, evenness, and diversity of amphibians and reptiles were not significantly different among ATV, non-ATV active trails, or control treatments (f=0.04, 1.05, 0.26, 1.61, P>0.05 respectively; Table 2). Based on Morisita’s index of similarity, community structures were extremely similar (Ca.=1.00 for all comparisons).
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THE TEXAS JOURNAL OF SCIENCE-VOL. 61, NO. 1, 2009
Table 1. Numbers of amphibian and reptile species captured on ATV trails, Non-ATV trails, and within forest control plots at the Old Sabine Bottom Wildlife Management Area, Smith County, Texas.
|
Taxon |
ATV |
Non-ATV |
Control |
Total |
|
Class Amphibia Order Caudata |
||||
|
Ambystoma opacum |
1 |
0 |
0 |
1 |
|
Ambystoma texanum |
10 |
13 |
7 |
30 |
|
Order Anura |
||||
|
Rana utricuJaria |
10 |
5 |
8 |
23 |
|
Class Reptilia Order Squamata |
||||
|
Eumeces fasciatus |
26 |
31 |
37 |
94 |
|
Eumeces laticeps |
10 |
4 |
12 |
26 |
|
Scincella lateralis |
42 |
32 |
42 |
116 |
|
Agkistrodon piscivorus |
5 |
5 |
3 |
13 |
|
Agkistrodon contortrix |
3 |
3 |
0 |
6 |
|
Pantherophis obsoleta |
0 |
1 |
0 |
1 |
|
Farancia abacura |
1 |
0 |
0 |
1 |
|
Lampropeltis getula |
1 |
0 |
1 |
2 |
|
Nerodia erythrogaster |
11 |
12 |
10 |
33 |
|
Nerodia fasciata |
2 |
0 |
2 |
4 |
|
Nerodia rhombifer |
0 |
2 |
0 |
2 |
|
Storeria dekayi |
5 |
2 |
3 |
10 |
|
Thamnophis proximus |
11 |
14 |
16 |
41 |
|
Total Individuals |
138 |
124 |
141 |
403 |
|
Total Species |
14 |
12 |
11 |
16 |
Discussion
Habitats in the three areas where cover boards were placed were visibly different. Damage in the area where AT Vs were in current use included destruction of vegetation within and next to trails, packing of soil in some parts of the trail, and loosening of mud in deeper, wet areas creating suspended silt. The ATV restricted trails showed some packing and older ruts from previous vehicle use, but much less vegetation damage. The forested area had natural depressions and damage from tree falls but little or no human impact. The methods used to place boards in each area resulted in some stations being near pools or rutted areas and some stations
HUNKAPILLER, FORD & HERRIMAN
9
Table 2. Abundance, richness, diversity, and evenness for amphibians and reptiles captured on ATV trails, non~ATV trails, and forest control plots at the Old Sabine Bottom Wildlife Management Area, Smith County, Texas.
|
ATV |
Non ATV |
Control |
F |
P |
|
|
Abundance |
138 |
124 |
141 |
0.04 |
0.962 |
|
Richness |
14 |
12 |
11 |
1.05 |
0.406 |
|
Diversity |
0.846 |
0.839 |
0.816 |
0.26 |
0.780 |
|
Evenness |
0.409 |
0.460 |
0.427 |
1.61 |
0.855 |
being near dry parts of the trail A total of 54 captures of only three species of amphibians were recorded. This reflects a much lower abundance than in previous work at the OSBWMA (Hampton 2004; Hampton & Ford 2007). These studies utilized boards in close proximity to ephemeral pools or deep ruts on trails. The lower number of amphibians obtained during the current study may relate to the random placement of cover objects in relationship to pools of water. Additionally, an unusually low amount of precipitation occurred in the second half of 2005. The average rainfall in nearby Dallas, Texas during November and December is 6.12 cm. In 2004 the average precipitation for November and December was 8.50 cm but for 2005 was only 0.60 cm (NOAA 2006) reflecting the very dry second half of the study period. During this study 349 reptiles belonging to 13 species were recorded. These numbers are more typical for the site and reflect that lizard and snake numbers were less influenced by low rainfall.
Species richness, abundance, diversity, and evenness of herpetofauna did not vary among trails open to ATV use, trails closed to ATVs, and the internal forest areas at the OSBWMA (Table 1). This suggests that the changes to the trails by the ATV use did not affect the biodiversity of amphibians and reptiles in this floodplain ecosystem during the study period. This lack of effect contrasts with previous studies of off-road disturbance (e.g., Iverson et al. 1981; Adams et al 1982; Webb & Wilshire 1983; Luckenbach & Bury 1983; Palis & Fischer 1997; Wisdom et al. 2004). Several
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THE TEXAS JOURNAL OF SCIENCE-VOL. 61, NO. 1, 2009
hypotheses are proposed concerning the lack of significant impact of ATV use at OSBWMA.
First, the current study was limited to a 14-month duration. This time period included the first year the OSBWMA was open to ATV traffic since establishment of the wildlife management area in 1996. Although physical and vegetation damage from AT Vs was evident, the number of vehicles on each trail was very low (an average of 1- 2 users per day; Shaun Crook pers. comm.). Direct mortality from AT Vs would have been unlikely and impacts like siltation in ruts where amphibian eggs or larva occurred also may have been limited. Previous researchers have also suggested that time lags of greater than a year can exist between disturbance and ecological responses (Magnuson 1990), and most studies in upland or desert areas have been at least two years in length (Luckenbach & Bury 1983). Additionally, these aforementioned areas were usually open to and extensively used by off-road vehicles for many years prior to data collection, (Luckenbach & Bury 1983; Wisdom et al. 2004). The abundances and diversity of amphibians and reptiles at the OSBWMA may still be affected over time by ATV use.
A second possibility is that floodplain communities are resilient to disturbances that include ATV activity. Previous studies of off¬ road vehicle disturbance have been conducted in upland forest (Palis & Fischer 1997; Wisdom et al. 2004) or xeric desert habitats (Iverson et al. 1981; Adams et al. 1982; Webb & Wilshire 1983; Luckenbach & Bury 1983). One of the main effects of ATV disturbance is habitat fragmentation, which causes migration barriers and leads to decreased mobility and limited prey access (Nour et al. 1998; Cushman 2006). This affect may be less apparent in floodplain ecosystems because the major source of nutrient influx is from flooding. The temporary pools formed by the recession of floods become stocked with fish and create amphibian breeding grounds. As the pools dry the fish and larva are available food sources for many carnivores. Ruts created by AT Vs simulate these pools and may also contain fish and
HUNKAPILLER, FORD & HERRIMAN
11
amphibian larva. The survival of organisms in those ruts, as opposed to natural pools, is not known, but some species associated with floodplains may be adapted to deal with perturbations. However, observations made during this study revealed that siltation in deep ruts appeared to kill some anuran eggs. A secondary aspect of floods would be that they allow for animal dispersal. Though the impact of the trails during flooding is not known, the trails may acts as corridors as the water often is channeled through them.
Frequent disturbances are known to cause complex effects on ecosystems that can either amplify or mask anthropogenic affects (Swetnam & Betancourt 1998; Hobbs & Morton 1999; Sherman 2001). It is possible that the lack of effect from ATV disturbance was confounded by the low amount of rainfall activity during the study, whereas this habitat is normally subjected to multiple flood events each winter. It seems intuitive that AT Vs driving through pools of amphibian egg masses or larva would have a negative impact on those species. Indeed, it is almost certain that the drought lowered amphibian activity during this study. Although these conclusions are that the limited ATV use in this floodplain appeared to have no significant effect on the herpetofauna, the authors caution that fiarther study is needed. It is suggested that these data represent a good baseline for additional studies, particularly with the amphibians of the OSBWMA,
Acknowledgements
We thank Larry LeBeau and Shaun Crook of Texas Parks and Wildlife for access to the study site and information regarding ATV use at the OSBWMA. We thank Dr. Ron Gutberlet, Dr. Darrell Pogue, and Andree Clark for comments on earlier versions of this manuscript. We thank Stephan Lorenz, Jessica Coleman, Paul Hampton, Casey Wieczorek, Robert Hunkapiller, Jr., and Rachel Buerger for field assistance.
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THE TEXAS JOURNAL OF SCIENCE-VOL. 61, NO. 1, 2009
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TRH at: thunkapi@utk.edu
TEXAS I OF SCI. 61(1):15™30
FEBRUARY, 2009
SELECTION OF DESERT BIGHORN SHEEP {OVIS CANADENSIS) TRANSPLANT SITES IN SIERRA MADERAS DEL CARMEN AND SIERRA SAN MARCOS Y DEL PINO, COAHUILA, MEXICO
Alejandro Espmosa-T*^ Armando J. Contreras-Balderas**,
Andrew V* Sandoval, and Mario A. Garcia-A
*Desert Bighorn Sheep Restoration Program, CEMEX, Sustainability Vice-presidency, Av. Independencia 901 Ote. Colonia Cementos, C.P. 64520, Monterrey, N.L Mexico and **Laboratorio de Ornitologia, U.AN.L . Apartado Postal 425
San Nicolas de los Garza, N.L, Mexico 66450
Abstract*-Between January 2004 and November 2006, a Geographic Information System (GIS) based habitat evaluation was conducted on the Sierra Maderas del Carmen (MDC) and Sierra San Marcos y del Pino (SMP). The objective of this study was to identify the most suitable sites for the restoration of desert bighorn sheep {Ovis canadensis) in Coahuila, Mexico. Priority transplant sites were selected based on potential contact with domestic sheep and goats and free ranging aoudads {Ammotragus lervia), amount and juxtaposition of escape terrain, and water availability. Priority transplant sites contain >15 km^ of escape terrain, water, and are spatially segregated from exotic ungulates. A total of 1,159 km^ of MDC was evaluated; 23% (271 km^) was suitable habitat for desert bighorn sheep. Two priority transplant sites consisting of 25 and 34 km^, respectively, were delineated in MDC. In the SMP, a total of 871 km^ was evaluated, and 20% (175 km^) was classified as suitable habitat. One area consisting of 18 km^ was selected in SMP as a priority transplant site.
Resumen*- De enero de 2004 a noviembre del 2006, desarrollamos un Sistema de Informacion Geografica (SIG) para la evaluacion del habitat en las Sierras de Maderas del Carmen (MDC) y San Marcos y del Pino (SMP) en Coahuila, Mexico. El objetivo del estudio file el de identificar los sitios mas adecuados para la restauracion de borrego cimarron (Ovfr canadensis). La seleccion de los sitios prioritarios para el transplante de cimarrones frie basado en el potencial de contacto con borregos domesticos y cabras, y exoticos ferales como los aoudads {Ammotragus lervia), y la cantidad de la conjuncion de terreno de escape y disponibilidad de agua. Los sitios prioritarios para un transplante tienen un area de >15 km^ de terreno de escape, con disponibilidad de agua y estan espacialmente segregados de ungulados exoticos. Se evaluaron 1,159 km^ en MDC; 23% (271 km^) es habitat adecuado para borrego cimarron. Dos sitios prioritarios para transplante de 25 y 34 km^, respectivamente, fiieron identificados en MDC. En SMP, se evaluaron 871 km^, de los cuales el 20% (175 km^) fiie clasificado como habitat adecuado para la especie. Un sitio de 18 km^ fiie seleccionado en SMP como area prioritaria de transplante.
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Desert bighorn sheep (Ovis canadensis) in Mexico are classified as “sensitive”, and a priority species for recovery and restoration (SEMARNAP 2000). Historically, desert bighorn occurred in a wide geographic area in the states of Chihuahua, Coahuila, Nuevo Leon, Sonora, Baja California, and Baja California Sur (Baker 1956; Leopold 1959; Cossio 1974; Tinker 1978; Sandoval 1985). Viable populations are still found in Sonora, Baja California, and Baja California Sur, but the species has apparently been extirpated from Chihuahua, Coahuila, and Nuevo Leon (Krausman et ah 1999; Espinosa et ah 2006).
Translocations into former habitat have been widely used to restore extirpated populations of bighorn sheep (Krausman 2000), and transplants account for >50% of all present-day populations of bighorn sheep (Bailey 1990). However, bighorn sheep restoration programs can be time-consuming, costly, and bureaucratically challenging (Zeigenfuss et al. 2000). The scarcity of sufficient seed stock and the difficulty of rasing desert bighorn in captivity makes it imperative that potential transplant sites be adequately assessed, and limiting factors mitigated. A number of qualitative habitat rating procedures have been developed to evaluate bighorn habitat (Hansen 1980; Holl 1982; Armentrout; Brigham 1988). More recently. Geographic Information System (GIS) and a landscape approach have been used to increase the success of restoration programs (Dunn 1996; Singer et al. 2000; Zeigenfuss et al. 2000; Johnson & Swift 2000; McKinney et al. 2003; Locke et al. 2005; Espinosa et al. 2007).
The application of GIS at the landscape perspective is an effective and efficient means of evaluating large areas of bighorn habitat because: (1) it provides consistent measurements across all study areas, thereby reducing bias towards any one study area, (2) a measurement of the amount and patchiness of bighorn habitat and a final score and ranking can be obtained directly from the values of the habitat components, (3) it provides for the evaluation of a large geographic area with much less effort that if it was evaluated
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directly in the field, and (4) the amount and distribution of bighorn habitat can be displayed graphically (Espinosa et al 2007).
In Coahuila, the initial restoration of desert bighorn sheep took place in 2000 on Sierra Maderas del Carmen (MDC) (Sandoval & Espinosa 2001; McKinney & Delgadillo 2005). Based on habitat suitability indices Espinosa et al. (2007), ranked MDC and Sierra San Marcos y del Pino (SMP) in the top six potential restoration sites in Coahuila. In addition to the availability of suitable habitat, MDC is under federal protection (SEMARNAP 1997), as is a portion of SMP (SEMARNAP 1999). Both areas also have active wildlife conservation and management programs. The objective of this study was to identify sites of minimum of 15 km^ of escape terrain for release areas for desert bighorn sheep within MDC and SMP.
Study Site
Sierra Maderas del Carmen (MDC) are located in extreme northern Coahuila, at a latitude between 28° 42* 18.2849" and 29° 21’ 29.4179" N, and a longitude between 102° 22* 04,5783" and 102° 55* 04.03.6100" W (Figure 1). The Rio Grande (Rio Bravo) separates Maderas del Carmen from Big Bend National Park, Texas, MDC are a northeast-southwest trending mountain range, with surrounding desert basins on the west and east sides, and is part of the Chihuahuan Desert as defined by Brown (1982). It is a tilted sedimentary fault block with a northeast-trending dip-slope along with Tertiary volcanic rocks of both intrusion and extrusive origins (Wood et al 1999). Elevations range from approximately 500 m along the Rio Grande, to 2,720 m on the highest peaks. The terrain varies from desert flats to rugged canyons with numerous vertical cliffs. Most precipitation occurs during summer and early fall, and varies from approximately 100-200 mm in the foothills to 200-300 mm in the higher elevations (SEMARNAP 1997). The annual mean temperature is approximately 22°C, with winter temperatures dropping below 0 °C.
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Fig. 1. Location of Sierra Maderas del Carmen (MDC) and San Marcos y del Pino (SMP) in Coahuila Mexico.
Ungulates inhabiting MDC include mule deer {Odocoileus hemionus), white-tailed deer {Odocoileus virgianus carminis), a reintroduced population of elk {Cervus elaphus) (Gibert et al. 2005), javelina {Pecari tajacu), and a reintroduced population of desert bighorn sheep (McKinney & Delgadillo 2005). Major predators include mountain lion {Puma concolor), black bear {Ursus americanus), bobcat {Lynx rufus), and coyote {Cams latrans).
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The vegetation of MDC is highly diverse, and varies from desert shrublands to high montane forests. The highest elevations (>2,330 m) are characterized by mixed conifer forests, dominated by Coahuila fir {Abies coahuilensis), Douglas fir {Pseudotsuga menziesii), and Arizona pine {Pinus arizonica). Numerous species of oaks {Quercus spp.) are associated with the mixed conifer forests. At mid-elevations (1,400 to 2,500 m), the forests are replaced by woodlands dominated by oak and chaparral species such as pointleaf manzanita (Arctostaphylos pungens), mountain mahogany {Cercocarpus montanus), and desert ash {Fraximus greggi). Vegetation in the lower elevations is typical of the Chihuahuan Desert, consisting of succulent-scrub, stem succulents, and semi-desert grasslands (Wood et al. 1999).
Sierra San Marcos y del Pino (SMP), are located in central Coahuila, at a latitude between 26° 17' 18.5616" and 26° 53' 44.183" N, and a longitude between 101° 19' 12.25" and 102° 09' 14.1859" W (Figure 1). Desert bighorn sheep persisted in this area until ca. 1950's (Espinosa et al. 2006). SMP is situated adjacent to the Cuatro Cienegas Federal Wildlife and Plant Protected Area (SEMARNAP 1999). Land ownership is a mixture of private and ejidos (communal settlements). Of significance is Rancho Pozas Azules from Pronatura (a non-government conservation organization), with active ecological research and conservation programs. Extensive livestock grazing occurs along the foothills, and at higher elevations in the southern portion of the mountain range.
The climate of SMP is arid, characterized by hot summers and cool winters. Most of the precipitation occurs during winter and varies from 100 to 440 mm, depending on elevation. Summer temperatures may exceed 30°C, and during winter may drop below 12°C (SEMARNAP 1999). Permanent springs are found in the northern and southern part of the mountain range. Rainfall dependent tinajas (potholes) occur throughout the area. A significant feature of SMP is an intermittent stream located in
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Rocillo Canyon, which bisects the central part of the mountain range.
Large mammals include populations of white-tailed deer, javelina, black bear, mountain lion, bobcat and coyotes.
Vegetative communities found on SMP vary greatly with increasing elevation and resultant precipitation. Lower elevations are characterized by desert shrubs, succulent-scrub, and stem succulents. Succulent-scrub and stem succulent communities are important to desert bighorn sheep, and are dominated by leaf and stem succulents such as lechuguilla, candelilla, guapilla (Hechtia ramillosa), ocotillo, and sangre de drago (Jatropha dioica). The understory consists of side-oats grama and threeawns {Aristida spp.) (Vela Coiffier 2000). Desert shrublands are replaced by mountain shrubs, oak woodlands, and conifer forests at higher elevations.
Methods and Materjals
The evaluation of habitat and selection of transplant sites for desert bighorn sheep in MDC and SMP was accomplished between January 2004 and November 2006. This analysis used combined remote sensing imagery in the context of a Geographic Information System (GIS), in order to identify and measure habitat components essential to desert bighorn. Also used was the 2004 Institute Nacional de Estadistica Geografia e Informatica (INEGI) digital elevation models (DEM Raster Tiff Format), comprised of 30 by 30 m cells. Portions of DEM’s encompassed by both study areas were extracted and converted to Universal Transverse Mercator (UTM) projection, using Arcview 3.2. Slope was measured with neighborhood analysis (Webster 1988), to obtain a measure of escape terrain (slopes > 60%). Suitable habitat was defined as cells between 20 and 59 % slope gradients situated < 150 m from escape terrain (Espinosa et al. 2007). Satellite imagery (LANDSAT ETM), with a resolution of 30 by 30 m/pixel was utilized to develop
ESPINOSA-T, ET AL.
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a coverage of vegetation types preferred by bighorn sheep using a supervised image classification procedure. Images Path030, Row040 (March 2003) were used for MDC, and images Path029, Row042 and Path0295 Row041 (18 September and 4 October 2000) were used for SMP.
Satellite imagery was utilized to identify vegetation types using the program ERJ3AS IMAGINE. Previous vegetation surveys in MDC and SMP were used as spectral signatures in the classification of the satellite images in developing the coverage of vegetation. In order to delineate open vegetation preferred by desert bighorn sheep, this study used a filtering process to identify only desert succulent-scrub (DSS) and semi-desert grassland (SDG) community types. The filtered vegetation file was intersected with a coverage of slopes > 60% to create a coverage of escape terrain with open vegetation.
Suitable habitat was defined as cells between 20 and 59% slope gradients situated < 150 m from escape terrain, intersected with the coverage of DSS and SDG. A coverage of impacts was digitized from INEGI topographic maps (1:50,000) and included a 3.5 km buffer around residential areas; 2 km buffer around paved roads; and a 500 m buffer around secondary roads. Impacted areas were eliminated from total suitable habitat (Espinosa et al. 2007).
Location of water sources were digitized from INEGI topographic maps and field notes. Water sources located during field work were marked with a Global Positioning System (GPS). Water availability was then defined as the amount of suitable habitat situated <3,5 km from permanent water sources (springs) and tinajas, (temporary water sources available during the summer) situated < 200 m of escape terrain. A coverage of water sources was intersected with a coverage of escape terrain that had been buffered to 200 m to create a coverage of water sources near escape terrain. A 3.5 km buffer was then created around these water
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sources, and this coverage was intersected with the coverage of suitable habitat to measure water availability.
The selection of initial release sites for desert bighorn sheep was based on the amount of escape terrain, water availability, and the absence of exotic ungulates, the data for the absence ore presence of exotic ungulates was obtained trough direct field verification. Release sites should contain a minimum of 15 km^ of escape terrain to support a viable population (McKinney et al. 2003). Several studies have substantiated the affinity to water by desert bighorn sheep (Dolan 2006). Given the above, only those areas containing a minimum of 15 km^ of escape terrain and water sources were considered as initial release sites.
A direct sampling to obtain verification points and to verify GIS results was conduced through ground and aerial verification surveys. The intent was to visually locate steep, broken topography characteristic of escape terrain (slopes > 60), with open vegetation (DSS and SDG). Secondly, it was important to refiite or substantiate the presence of free-ranging exotic ungulates, ground verification surveys were accomplished by vehicle or on foot. A Cessna 182 and Robinson Raven helicopter were used for aerial reconnaissance of the habitat, covering the entire perimeter of the study areas at a mean distance of 100 m from the mountain side. GPS was used to mark verification and photo points; these data was entered in a field notebook. Finally, a review of the reports on habitat use, movements and distribution of the transplanted free- ranging desert bighorn population in Maderas del Carmen was conducted.
Results
Sierra Maderas del Carwe/i. -Between January 2004 and November 2006, GIS was implemented and verified in MDC. It was possible to complete a habitat verification reconnaissance overflight using fixed wing aircraft in April 2004, covering the entire perimeter of the mountain, and obtaining 15 habitat
ESPINOSA-T, ET AL.
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verification points (places where the habitat characteristics were verified). In September 2006, a helicopter survey was conducted covering the western, northern, and a small portion of the east side of the mountain. During 30 days of field surveys, three water sources were located and 26 verification points were registered.
Of the 1,159 kin^ evaluated in MDC, 270 km^ (27%) was found to be potential habitat for desert bighorn sheep (Figure 2 in white). Two initial release sites were delineated containing a total of 59 km^ of habitat (Figure 2 in black). The Site 1 abuts the Rio Grande, and consists of 25 km^. Site 2 covers 34 km^ and contains Tinaja (pothole) los Chivos, intermittent water flow and manmade water sources in San Isidro Canyon. Site 2 actually represents the release area for the free-ranging bighorn population in MDC, during 2004 and 2005 (McKinney & Delgadillo 2005).
Habitat use data on the free-ranging population indicate a core use area within a radius of approximately 4 km of the release site; identified as site 2 during this study (Figure 2). The exception was 3 adult males that dispersed >15 km to the north from the release site within a few months following their release (B. R. McKinney pers, comm.).
Survery did not locate exotic ungulates in the areas selected as initial release sites (Fig 2, no. 1 and 2). However, domestic goats attended by herders were observed in the northwestern and southern part of MDC, approximately 5 km from the proposed bighorn sheep release sites. According to Carlos Sifiientes (pers. comm.) the Director of the Protected Area of MDC, free-ranging aoudad occur in the northern part of MDC, also their presence exist across the Rio Grande in Big Bend National Park, Texas (Skiles pers. comm.), and in the Black Gap Wildlife Management Area, Texas (Foster 2002).
Sierra San Marcos y del Pmo.-Between January 2004 and May 2006, GIS was implemented and verified in SMP. In April 2004, a habitat verification reconnaissance was conducted encompassing
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Fig. 2. Potential bighorn sheep habitat (white) and priority transplant sites 1 and 2 (black) in Sierra Maderas del Carmen.
the entire periphery of the mountain using fixed-wing aircraft, and obtained 24 verification points. During 26 days of ground surveys 30 habitat verification points and six water sources were located.
A total of 871 km^ was evaluated in SMP; 20% (174 km^) was classified as potential bighorn sheep habitat (Figure 3 in white). Within the potential habitat, 1 initial release site consisting of 18 km ^ was delineated (Figure 3 in black). This area contains seasonal tinajas and one permanent spring in Quintero Canyon.
No exotics were observed in the initial release site. However, herds of free-ranging domestic goats were observed in the southern portion of SMP, approximately 60 km from the proposed bighorn sheep release site, and a mixed herd of penned goats and domestic sheep in the village of Antiguos Mineros del Norte situated <10 km from the proposed release site. Free-ranging aoudad have not been
ESPINOSA-T, ETAL.
25
Fig.3. Potential bighorn sheep habitat (white) and priority transplant site (black) for Sierra San Marcos y del Pino.
reported in SMP, however, records do exist for Sierra la Fragua located <2 km northwest of SMP (Espinosa et al. 2006).
Discussion
Desert bighorn sheep habitat evaluation through the use of GIS in the Chihuahuan Desert has been done in New Mexico (Dunn 1996), Texas (Locke et al. 2005), Chihuahua, Coahuila, and Nuevo Leon (Colchero et al. 2003), and Coahuila (Espinosa et al. 2007). The work by Espinosa et al. (2007) is most pertinent to this current study, because they included both MDC and SMP. Espinosa et al. (2007) conducted an evaluation and ranking of potential bighorn sheep habitat in the known historical range of the bighorn sheep in Coahuila. Digital elevation models with a resolution of 30 by 30 m/pixel were used to analysis topography. INEGI land use and vegetation maps with a scale of 1:250,000 were used for vegetation
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analysis, and INEGI topographic maps (1:50,000) to determine water availability, that was defined as the amount of suitable habitat situated <3.5 km from permanent water sources and tinajas, situated < 200 m of escape terrain. The above study identified 299 km^ of potential bighorn habitat and only 8 km^ of water availability in MDC, and 351km^ of potential habitat and 5 km^ of water availability in SMP (Espinosa et al. 2007). The scale of data sources used in GIS habitat evaluation studies influence the final results (Johnson & Swift 2000). This is attested to by the results of the present study, which identified 277 and 174 km^ of potential habitat, respectively, in MDC and SMP. This is less than the amount delineated by Espinosa et al. (2007) for MDC and SMP, using a smaller scale vegetation data source (1:250,000). More precise results can be obtained through the use of higher resolution data sources, in the case of SMP the combination of the complexity of its topography with 30 canyons, and the use of smaller scales for the vegetation analysis (1:250,000), overestimated the results of the potential bighorn habitat in the study of Espinosa et al. (2007).
All permanent and temporary water sources should be identified in the evaluation of potential habitat for desert bighorn sheep (Locke et al. 2005). The use of more precise water sources data in this present study resulted in the identification of a greater amount of water availability, 59 and 18 km^, respectively, for MDC and SMP. Initial release sites can thus be identified and quantified with more precision.
The wide-spread occurrence of goats and domestic sheep may be the major obstacle for restoration of desert bighorn sheep in Coahuila (Espinosa et al. 2007). These exotics have proven detrimental to bighorn sheep due to the transmission of lethal diseases (Sandoval 1988; Gross et al. 2000; Rudolph et al. 2003; Rominger 2006). This study documented the presence of goats and domestic sheep ranging <15 km from sites selected for the initial release of desert bighorn sheep. Bighorn and domestic sheep must be spatially separated a distance of > 13.5 km to minimize the possibility of contact between the 2 species (DBC Technical Staff 1990), this can be to close to avoid contact between the bighorn and the domestics relatives.
ESPINOSA-T, ET AL.
27
maintain separation is imperative. Habitat management guidelines for bighorn sheep and domestic goats are lacking, nonetheless, every effort must be made to avoid contact between the two species to minimize the potential for disease transmission.
To date no records exist of disease transmission between aoudad and bighorn sheep. However, their habitat requirements are very similar and social and resource competitions are possible risks on sympatric range. Texas and New Mexico euthanize aoudads when encountered in desert bighorn sheep habitat, the same procedures need to be applied for Coahuila.
Development of water sources should be considered as a management component to enhance desert bighorn sheep habitat (Dolan 2006). Water sources for desert bighorn sheep should be located <8 km apart and in close proximity to escape terrain (Douglas & Leslie 1999). MDC and SMP contain a large amount of suitable habitat for desert bighorn sheep; a major limiting factor is the lack of available water. Dense thickets of carrizo {Arundo donax) and salt cedar (Tamarix ramosisima), along the northern part of MDC form an effective barrier to the Rio Grande thus making it unavailable as a water source for desert bighorn. In SMP a paved highway presents a potential formidable barrier to bighorn movements and high tourist traffic at Poza de la Becerra (Cuatro Cienegas Protected Area), effectively denies this large spring as a potential source of water. Given the above, the authors believe that development of water sources in MDC and SMP should be considered as part of the bighorn restoration program in Coahuila.
Although this study did not document exotic ungulates in the proposed bighorn sheep release sites identified in MDC and SMP, they do occur <15 km from these sites. Notwithstanding the 13.5 km buffer recommended by the DBC Tech Staff (1990), it is the belief of the authors that this distance is inadequate to prevent intermingling between bighorn sheep and exotics due to the extent and contiguous nature of the habitat in MDC and SMP. Finally, free-ranging goat herds should be prohibited; instead requiring daily herding and
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penned up situations at night. The eradication of aoudad is an on¬ going activity at Black Gap Wildlife Management Area, Texas (Pittman pers. comm.), and is under consideration in Big Bend National Park (Skiles pers. comm.). Given the close proximity of these two areas to MDC, the same effort needs to be applied for MDC.
Acknowledgements
The present work was made possible thanks to financing by the Desert Bighorn Sheep Restoration Program of CEMEX. The support of M. Valdez of Unidos Para La Conservacion AC is appreciated, and S. Lagham of Environmental Flights, in the aerial verifications. For their support in San Marco y del Pino to Pronatura Noreste (Reserva Poza Azules). The valuable support in the field of J. A. Delgadillo- Villalobos, R. Martinez, B. R. McKinney, and B. P. McKinney (CEMEX), is appreciated; as well as the following persons-O. Gonzalez De Leon, M. Gonzalez F, F. Villaneuva. The present work represents partial fulfillment of the requirements for a doctorate degree in Biological Sciences, with a speciality in Wildlife Management and Sustainable Development by the senior author at the Universidad Autonoma of Nuevo Leon.
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Rudolph, K. M., D. L. Hunter, W. J. Foreyt, E. F. Gassier, R. B. Rimler & A. C. S. Ward. 2003. Sharing of Pasteurella spp. between free-ranging bighorn sheep and feral goats. Journal of Wildlife Diseases, 39(4):897-903.
Sandoval, A.V. 1985. Status of bighorn sheep in the republic of Mexico. Pg. 86-94, in M. Hoefs. editor. Wild sheep: Distribution, abundance, management, and conservation of the wild sheep of the world and closely related mountain ungulates. Northern Wild Sheep and Goat Council Special Report. Yukon, Canada.
Sandoval, A. V. 1988. Bighorn sheep die-off following association with domestic sheep:
case history. Desert Bighorn Council Transactions, 32:36-38.
Sandoval. A. V. & A. Espinosa-T. 2001. Status of bighorn sheep management programs in Coahuila, Mexico. Desert Bighorn Council Transactions 45:53-61.
Secretaria de Medio Ambiente, Recursos Naturales y Pesca (SEMARNAP). 1997. Programa de manejo del Area de Proteccion de Flora y Fauna- “Maderas del Carmen”. Institute Nacional de Ecologia. Mexico, D.F., 129 pp.
Secretaria de Medio Ambiente, Recursos Naturales y Pesca (SEMARNAP). 1999. Programa de manejo del Area de Proteccion de Flora y Fauna Cuartocienegas. Institute Nacional de Ecologia. Mexico, D.F., 166 pp.
Secretaria de Medio Ambiente, Recursos Naturales y Pesca (SEMARNAP). 2000. Proyecto para la conservacion, manejo, y aprovechamiento sustentable del borrego Cimarron (Ovis canadensis) en Mexico. Institute Nacional de Ecologia. Mexico, D.F. 91 pp.
Secretaria de Programacion y Presupuesto (SPP). 1981. Sintesis geografica de Coahuila. Mexico, D.F., 163 pp.
Singer, J. F., M. C. Papouchis & K. K. Symonds. 2000. Translocations as a tool for restoring populations of bighorn sheep. Restoration Ecology, (8) 48:6-13.
Smith, T. S. & J. T. Flinders. 1992. Evaluation of mountain sheep habitat in Zion National Park, Utah. Desert Bighorn Council Transactions, 36:4-9.
Tilton, M. E. & E. E. Willard. 1982. Winter habitat selection by mountain sheep.
Journal of Wildlife Management, 46:359-366.
Tinker, B. 1978. Mexican wilderness and wildlife. University of Texas Press. Austin, USA., Pg. 30-46.
Vela-Coiffier, M. P. 2000. Determinacion de la distribucion vegetal en el valle de Cuarto Cienegas, Coahuila, Mexico a traves del analisis multitemporal de imagenes de satelite. Tesis en Maestria en Ciencias. ITESM. Inedita., 159 pp.
Webster, D. 1988. Introduction to geographic information systems and MOSS. TGS Techonology, Inc. Bureau of Land Management Operations, Lakewood, Colorado, 245pp.
Wood, S., G. Harper, E. Muldavin & P. Neville. 1999. Vegetation map of the Sierra del Carmen, U.S.A. and Mexico-Final Report. U.S. Geological Survey, National Park Service and University of New Mexico. CA7029-1-012. 57pp, plus appendices. Zeigenfuss, L. C., F. J. Singer & M. A. Gudorf. 2000. Test of a modified suitability model for bighorn sheep. Restoration Ecology, 8(48):38-46.
AE at: alejandro.espinosa@cemex.com
TEXAS J. OF SCI. 61(1):31=44
FEBRUARY, 2009
GEOGRAPHIC DISTRIBUTION RECORDS FOR SELECT FISHES OF CENTRAL AND SOUTHERN ARKANSAS
Chris T. McAllister, Renn Tumlisoii and Henry W, Robison
RapidWrite, 102 Brown Street Hot Springs National Park, Arkansas 71913 Department of Biology, Henderson State University Arkadeiphia, Arkansas 71999 and Department of Biology, Southern Arkansas University Magnolia, Arkansas 71754
Abstract.-New geographic records are documented for 16 taxa of fishes within nine families (Anguillidae, Atherinopsidae, Catostomidae, Centrarchidae, Cyprinidae, Fundulidae, Hiodontidae, Icturalidae, Percidae) from 20 counties of the southern portion of Arkansas. Of these, 26 new county records for 13 (81%) of the species are presented. Other findings include new records and range extensions for rarely collected species such as the mooneye (Hiodon tergisus), bluehead shiner (Pteronotropis hubbsi), mud darter {Etheostoma asprigene), swamp darter {Etheostoma fusiforme), and the undescribed Ouachita darter (Percina sp,). Most importantly, the brown madtom, Notorus phaeus is reported from Arkansas for only the second time since its original discovery in Columbia County in 1972.
Robison & Buchanan (1988) provided a summation on the geographic distribution of the fishes of Arkansas. Over the last half decade, new geographic records for fishes of the state have been reported (McAllister et ah 2004; 2006; 2007; 2008) to help supplement previously published historical data. The purpose of this report is to update the status of additional fishes of the central and southern portions of the state.
Materials and Methods
Specimens were collected between August 1981 and April 2005 from streams throughout various localities in central and southern Arkansas, including watersheds in 20 counties (Ashley, Bradley, Clark, Columbia, Dallas, Drew, Garland, Hempstead, Hot Spring, Howard, Lafayette, Little River, Miller, Montgomery, Nevada, Ouachita, Phillips, Pike, Saline, and Union). Collections were made with standard nylon seines (1.8 by 0.5 m and 2.7 by 0.5 m of 3.2 mm mesh) or dipnets. Specimens were preserved in 10% formalin and later transferred to 45% isopropanoL Specimens were field identified,
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verified in the laboratory, and vouchers deposited in the collections at Southern Arkansas University, Magnolia, Arkansas (SAU), Henderson State University, Arkadelphia, Arkansas (HSU), and the University of Louisiana-Monroe Museum of Natural History, Monroe, Louisiana (NLU). Detailed data provided on the new sites are as follows: (county, specific locality [township, section, and range when available], date, museum accession number [if known], number of specimens in parentheses, comments). In addition, several unpublished records deposited in the NLU collection but not reported by Robison & Buchanan (1988) are included below.
List of Species
Material examined -ThQ following is a listing of collection localities for fishes collected in southern Arkansas.
ANGUILLIDAE
Anguilla rostrata (Lesueur) {n = 10). CLAUK CO.: SE Arkadelphia at River Park, Ouachita River (Sec. 17, T7S, R19W). 30 April 1987. HSU 1351 (3); County Club pond, Arkadelphia. 30 March 1991. HSU 1353 (1); Ouachita River, 3.2 km S of Arkadelphia (Sec. 28, T7S, R19W). 21 March 2003. HSU 2893 (1). HOT SPRING CO.: Ouachita River (Sec. 31, T3S, R17W). 15 April 1997. HSU 1979, 2099 (2); Remmel Dam at Jones Mill (Sec. 36, T3S, R18W). 13 May 1997. HSU 2674 (1). LITTLE RIVER CO.: Little River, river run E of Dam (Sec. 26, T12S, R28W). 21 April 1991. HSU 1081 (1). OUACHITA CO.: Little Missouri River, 1.6 km N of Reader on unnamed gravel road (Sec. 18, T1 IS, R18W). 19 February 1983. NLU (1). These specimens supplement previous records from the state. American eel populations have experienced a drastic decline in Arkansas due to construction of dams which block migration in large rivers.
HIODONTIDAE
Hiodon tergisus Lesueur (n = 3). OUACHITA CO.: 24.1 km NE of Chidester at confluence of Little Missouri and Ouachita rivers at Tates Bluff Recreation Area (Sec. 1, TllS, R18W). 19 February 1983. NLU (1). UNION CO.: Ouachita River at U.S. 167 (Sec. 10,
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T16S, R14W). 26 May 1997. SAU (1); Ouachita River at U.S. 82 (Sec. 14, T18S, RIOWS). 17 July 1999. SAU (1). This large river species is rarely encountered in Arkansas. These two new county records document significant collections for the lower Ouachita River.
CYPRINIDAE
Notropis maculatus (Hay) {n = 48). BRADLEY CO.: Snake Creek at Broad (Sec. 30, T16S, R9W). 17 June 2002. SAU (3). COLUMBIA CO.: Dorcheat Bayou at co. rd., 4.8 km SW of Philadelphia (Sec. 16, T18S, R22W). 4 September 1993. SAU (1); Dorcheat Bayou at St. Hwy. 160, 6.4 km E of Taylor (Sec. 9, T19S, R22W). 19 May 2004. SAU (2). DREW CO.: Cut-Off Creek at St. Hwy. 35, 1.1 km E of Collins (Sec. 31, TBS, R4W). 13 April 1993. SAU (2). LAFAYETTE CO.: Bodcau Creek at co. rd„ 1.6 km N of Lewisville (Sec. 7, T15S, R23W). 5 July 1992. SAU (1); Bayou Bodcau at U.S. 82 (Sec. 7, T16S, R23W). 11 October 1995. SAU (2). LITTLE RIVER CO.: Cypress Creek at St. Hwy. 234 in Winthrop (Sec. 7, TllS, R31W). 6 June 1989. SAU (1); Little River backwater at U.S. 71, 3,2 km N of Wilton (Sec. 24, TllS, R29W). 5 October 2001. SAU (2). NEVADA CO.: Middle Creek, 14.5 km N of Prescott on St. Hwy. 19 (Sec. 27, T9S, R23W). 19 February 1983. NLU (1); Terre Rouge Creek, 11.3 km SE of Prescott on St. Hwy. 24 (Sec. 3, TBS, R22W). 19 February 1983. NLU (1); Caney Creek, 4.8 km N of Bluff City on St. Hwy. 24 (Sec. 22, TllS, R20W). 19 February 1983. NLU (26). UNION CO.: Smackover Creek at co. rd. 68, 3.2 km N of Norphlet (Sec. 3, TBS, R15W). 20 September 1992. SAU (1); Grand Marais Lake at Felsenthal (Sec. 16, TBS, RlOW). 18 September 1996. SAU (5). Collections of this lowland cyprinid from Lafayette and Nevada counties represent new county records. This shiner was generally collected from quiet, backwater areas devoid of current but often with vegetation.
Notropis texanus (Girard) (n = 6). COLUMBIA CO.: Dorcheat Bayou at St, Hwy. 160, 6.4 km E of Taylor (Sec. 9, TBS, R22W). 19 May 2004. SAU (1). LAFAYETTE CO.: Bayou Bodcau at U.S. 82 (Sec. 7, TBS, R23W). 11 October 1995. SAU (1). UNION CO.: Smackover Creek at Co. Rd. 68, 3.2 km N of Norphlet (Sec. 3, TBS,
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R15W). 20 September 1992. SAU (1); Big Comie Creek at St. Hwy. 15, 25.7 km SW of El Dorado (Sec. 35, T19S, R18W). 5 October 1995. SAU (3). Specimens from Lafayette County document a new county record and represent the southwestemmost locality of N. texanus in the state.
Pteronotropis hubbsi (Bailey & Robison) {n = 24). ASHLEY CO.: Thompson Creek, 11.3 km NW Crossett (Sec. 11, T17S, R9W). 5 July 1996. HSU 1340 (13); slough off Saline River at Stillions, 14.5 km NW Crossett (Sec. 4, T17S, R9W). 5 July 1996. HSU 1319 (1); Ouachita River, 9.7 km W Crossett at U.S. 82 (Sec. 14, T18S, RlOW). 11 April 1997. HSU 2008 (3). NEVADA CO.: Middle Creek, 14.5 km N of Prescott on St. Hwy. 19 (Sec. 27, T9S, R23W). 19 February 1983. NLU (1); Caney Creek, 4.8 km N of Bluff City on St. Hwy. 24 (Sec. 22, TllS, R20W). 19 February 1983. NLU (6). This species was formerly included in the genus Notropis; the subgenus Pteronotropis was elevated to genus rank by May den (1989). The bluehead shiner has a spotty distribution in lowlands of the Red and Ouachita river systems of southern Arkansas and was previously known from only 10 localities in the state, including two disjunct sites in the Little River system (Bailey & Robison 1978; Robison & Buchanan 1988). This shiner was also listed as a species of special concern in Arkansas (Robison & Buchanan 1988; Anonymous 2004) and the Nature Conservancy considers P. hubbsi vulnerable (S3) in the state (NatureServe 2008). This study documents two new county records in tributaries of the Little Missouri and Saline rivers.
Semotilus atromaculatus (Mitchill) {n = 134). ASHLEY CO.: Ouachita River, 10.5 km W Crossett off St. Hwy. 82 (Sec. 14, T18S, RlOW). 11 April 1999. HSU 2009 (1). CLARK CO.: unnamed tributary to Little Deceiper Creek, 8.0 km W Arkadelphia (Sec. 24, T7S, R20W). 8 February 1997. HSU 1681 (3). DALLAS CO.: unnamed tributary to L’Eau Frais Creek (Sec. 8, T7S, R17W). 5 April 1997. HSU 2118 (4). GARLAND CO.: tributary to Pleasant Run Creek, 2.4 km S Lonsdale (Sec. 26, T2S, R17W). 29 March 1991. HSU 286 (2); Cooper Creek, 1.6 km S of jet. St. Hwys. 171 & 290 (Sec. 6, T4S, R18W). 20 August 1993 & 29 July 1995. HSU 99, 1 1 14
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(7, 1); Cooper Creek, 2.4 km S jet. St. Hwy. 171 & 290 (Sec. 8, T4S, R18W). 23 August 1993. HSU 189 (2). HEMPSTEAD CO.: Bois d’Arc Creek, 3.2 km SW jet. St. Hwys. 73 & 195 (Sec. 13, T12S, R26W). 6 April 1991. HSU 1231 (1). HOT SPRING CO.; Prairie Bayou, 3.2 km NW of New DeRoche (Sec. 31, T4S, R19W). 20 August 1993. HSU 103 (1); 9.7 km W of Malvern at Blakely Creek (Sec. 15, T4S, R18W). 20 August 1993. HSU 1312 (1); 8.0 km NW Bismarck at Valley Creek (Sec. 28, T4S, R21W). 27 August 1993. HSU 165 (3); 4.8 km N Bismarck at Big Hill Creek (Sec. 30, T4S, R20W). 27 August 1993. HSU 170 (15); Mt. Carmel Creek, 7.2 km N jet. St. Hwy. 84 & 128 (Sec. 17, T4S, R19W). HSU 181 (6); tributary of Big Hill Creek, 3.2 km N of Lambert (Sec. 1, T5S, R21W). 5 February 1994. HSU 980 (3); uimamed creek, 8.0 km NW of Lambert (Sec. 28, T4S, R21W). 5 February 1994. HSU 984 (2); unnamed creek, 4.8 km NE of jet. St. Hwy. 84 & 128 (Sec. 25, T4S, R19W). 20 March 1994. HSU 1001 (4); Mt. Carmel Creek at St. Hwy. 128 bridge (Sec. 17, T4S, R19W). 21 July 1995. HSU 1193 (1); Curl Creek, 5.2 km W of St. Hwy. 128 on Land Camp Rd (Sec. 36, T4S, R20W). 22 July 1995. HSU 1102 (1); tributary to Prairie Bayou, 4.8 km W St. Hwy. 128 (Sec. 25, T4S, R20W). 22 July 1995. HSU 1127, 1135 (1, 4); tributary to Valley Creek (Sec. 35, T4S, R21W). 28 July 1995. HSU 1155 (1); tributary to Valley Creek (Sec. 26, T4S, R21W). 28 July 1995. HSU 1166 (1); tributary to Blakely Creek, 0.8 km S O’Neal Trail (Sec. 17, T4S, R18W). 29 July 1995. HSU 1 147 (1); Big Hill Creek at Tower Road (Sec. 30, T4S, R20W). 4 August 1995. HSU 1163 (1); Curl Creek (Sec. 27, T4S, R20W). 4 August 1995. HSU 1169, 1172 (4, 4); tributary to Ouachita River (Sec. 7, T4S, R17W). 16 February 1997. HSU 1469 (4); Stone Quarry Creek at U.S. 270 (Sec. 32, T3S, R17W). 1 April 1997. HSU 1593 (1); Dyer Creek at end of Jenney Lane (Sec. 36, T3S, R17W). 7 March 1999. HSU 2531 (4); Curl Creek, 6.4 km NE Bismarck (Sec. 27, T4S, R20W). 15 January 1999. HSU 2533 (2); Tigger Creek, 1.6 km from county line off U.S. 270E (Sec. 31, T4S, R20W). 10 April 1999. HSU 2672 (1). HOWARD CO.: 6.4 km W Dierks at Saline River near Bluff Creek (Sec. 23, T7S, R29W). 2 March 1991. HSU 1230 (1). LITTLE RIVER CO.: Little River at wall of dam (Sec. 26, T12S, R28W). 23 February 1991. HSU 1233 (1). MONTGOMERY CO.: Dry Mazam
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Creek (Sec. 14, T3S, R24W). 4 May 1991. HSU 42 (8); Little Missouri River at Little Missouri Falls (Sec. 6, T4S, R27W). 1 May 1993. HSU 159 (2); Collier Creek at St. Hwy. 8, 2.4 km N Caddo Gap (Sec. 12, T4S, R25W). HSU 261 (3); Lick Creek, tributary to Caddo River (Sec. 24, T3S, R26W). 2 April 1994. HSU 370 (5); tributary of Little Missouri River at dirt rd. (Sec. 27, T4S, R27W). 19 April 1991. HSU 1607 (1); Greasy Branch (Sec. 35, T4S, R27W). 2 May 1997. HSU 2144 (3). NEVADA CO.: Middle Creek, 14.5 km N of Prescott on St. Hwy. 19 (Sec. 27, T9S, R23W). 19 February 1983. NLU (1). PIKE CO.: spring drainage ditch, 7.2 km NE of Murfreesboro at Wayside Park off Co. Rd. 379 (Sec. 35, T7S, R25W). 18 June 1983. NLU (1); Little Missouri River (Sec. 5, T5S, R27W). 16 March 1997. HSU 2023 (1); 1.6 km N of Langley on St. Hwy. 269 at first bridge (Sec. 12, T5S, R27W). 16 March 1997. HSU 1574 (2); Bear Creek (Sec. 34, T5S, R25W). 20 April 1997. HSU 1928 (2); Rock Creek, 1.6 km SE of Salem off St. Hwy. 70 (Sec. 18S, T5S, R24W). 20 April 1997. HSU 1628 (3); Wolf Creek at St. Hwy. 29 bridge, 1.6 km SW Antoine (Sec. 27, T8S, R23W). 17 April 1999. HSU 2628 (1). SALINE CO.: unnamed creek at 1106 West Place in Benton (Sec. 1, T2S, R15W). 13 March 1994. HSU 482 (6); tributary to McNeil Creek, 0.4 km N of 1-30 on Congo Rd. (Sec. 35, TIS, R15W). 13 March 1994. HSU 509 (2); Brushy Creek, 6.4 km NW Exit 106 off I- 30 at Fairplay Rd. (Sec. 34, T2S, R16W). 5 April 1994. HSU 498 (2); Brushy Creek, 4.8 km NW Exit 106 off 1-30 at Fairplay Rd. (Sec. 35, T2S, R16W). 29 April 1994. HSU 811 (1); unnamed creek behind Watson Place in Benton (Sec. 30, TIS, R15W). 29 April 1994. HSU 1053 (1). New county records for this headwater cyprinid are reported for Ashley, Hempstead, Little River, and Nevada counties, and the records from Howard and Pike counties represent the first collections since 1960 (see Robison & Buchanan 1988). The creek chub inhabits the smallest, clearer headwater streams.
CATOSTOMIDAE
Moxostoma poecilurum (Jordan) {n = 13). CLARK CO.: L’Eau Frais Creek at St. Hwy. 7, 8.9 km S Jet. St. Hwy 51 and 7 (Sec. 1, T8S, R18W). 25 March 1994. HSU 543 (1); L’Eau Frais Creek at St. Hwy 128, 0.8 km of Joan (Sec. 22, T7S, R18W). 2 May 1994 and 1
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March 2006, HSU 575, 3164 (1, 3); Tupelo Creek at St Hwy, 7 bridge (Sec. 35, T7S, R19W). 11 March 2005. HSU 2927 (1). COLUMBIA CO.: Smackover Creek at U.S. Hwy 79, 5.6 km NE of McNeil (Sec. 26, T15S, R20W). 25 September 1991. SAU (1); Big Creek at St Hwy. 98, 6.4 km S of Village (Sec. 3, T18S, R19W). 5 November 1993. SAU (1); Sloan Creek at St. Hwy. 57 (Sec. 11, T16S, R19W). 5 November 1993. SAU (1). NEVADA CO.:
Grassy Lake, 9.7 km NE of Prescott off St. Hwy. 67 (Sec. 1, TIOS, R22W). 2 August 1981. NLU (1); Middle Creek, 14.5 km N of Prescott on St. Hwy. 19 (Sec. 27, T9S, R23W). 19 February 1983. NLU (1); Caney Creek, 4.8 km N of Bluff City on St. Hwy. 24 (Sec. 22, TllS, R20W). 19 February 1983. NLU (1). UNION CO.: Big Comie Creek at St. Hwy. 15, 25.7 km SW of El Dorado (Sec. 35, T19S, R18W). 5 October 1995. SAU (1). The blacktail redhorse is generally confined to the southern Coastal Plain streams of the lower Ouachita River system of southcentral Arkansas (Robison & Buchanan 1988). This is the first time M poecilurum has been reported from Union County.
ICTALURJDAE
Noturus phaeus Taylor {n = 1). COLUMBIA CO.: Horsehead Creek at U.S. 19, 12.9 km SW of Magnolia (Sec. 32, T18S, R21W). 21 November 2001. SAU (1). To the authors' knowledge, this madtom had not been collected in the state since 1972 when Robison (1974) reported three specimens from a spring-fed tributary of Horsehead Creek in Columbia County, 3.5 km S Macedonia (Sec, 29, T18S, R21W). Subsequently, it was previously listed as endangered and considered extremely rare by Robison & Buchanan (1988). However, N. phaeus is not currently listed in any category by the Arkansas Game and Fish Commission. Interestingly, the Nature Conservancy lists the species as SH (possibly extirpated) in Arkansas (NatureServe 2008).
FUNDULIDAE
Fundulus dispar (Agassiz) {n = 40), ASHLEY CO.: Thompson Creek, 11.3 km NW Crossett (Sec. 11, T18S, R9W). 5 July 1996. HSU 1347 (6); Ouachita River, 10.5 km W Crossett at St. Hwy 82
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(Sec. 14, T18S, RlOW). 11 April 1997. HSU 2004 (3). BRADLEY CO.: Moro Creek at Moro Bay State Park (Sec. 21, T16S, R12W). 17 October 1998. SAU (1); Snake Creek at Broad (Sec. 30, T16S, R9W). 17 June 2002. SAU (1); L’Aigle Creek at co. rd., 14.5 km South of Hermitage (Sec. 18, T16S, RlOW). 10 June 2005. SAU (2). CLARK CO.: Tupelo Creek (T7S, R19W). 25 February 1997. HSU 2337 (1). HOT SPRING CO.: tributary to Ouachita River under bridge (Sec. 22, T6S, R18W). 2 February 1997. HSU 2237 (1). OUACHITA CO.: Bragg Lake, 2.0 km SE Bragg City at St. Hwy. 24 (Sec. 33, T12S, R18W). 12 April 1997. HSU 2051 (4); Freeo Creek at St. Hwy. 9, 3.2 km S Dallas County line (Sec. 36, TllS, R16W). 7 June 1997. HSU 2178 (4). NEVADA CO.: Caney Creek, 4.8 km N of Bluff City on St. Hwy. 24 (Sec. 22, TllS, R20W). 19 February 1983. NLU (8). UNION CO.: Lapile Creek at North Road, 8.0 km N of Huttig (Sec. 25, T18S, RllW). 16 June 1992. SAU (1); Lapile Creek at Lapile Road (Sec. 31, T18S, RllW). 16 June 1992. SAU (1). Grand Marais Lake at Felsenthal, (Sec. 16, T19S, RlOW). 18 September 1996. SAU (2); Shallow Lake, lower Ouachita River backwater (Sec. 37, T19S, RlOW). 20 January 1999. HSU 2256 (5). This study documents a new county record for this lowland topminnow in Nevada County.
ATHERINOPSIDAE
Menidia audens Hay {n = 47). ASHLEY CO.: Thompson Creek, 11.3 km NW Crossett (Sec. 11, T17S, R9W). 5 June 1996. HSU 894 (1). BRADLEY CO.: Moro Creek at Moro Bay State Park (Sec. 21, T16S, R12W). 17 October 1998. SAU (3). CLARK CO.: Caddo River at St. Hwy 67 bridge, Caddo Valley (Sec. 31, T6S, R20W). 10 & 26 April 1994. HSU 473, 520 (1, 2); DeRoche Creek at St. Hwy 28 bridge (Sec. 7, T6S, R19W). 20 March 1994. HSU 839 (4); Saline Bayou bridge at St. Hwy 7 (Sec. 16, T7S, R19W). 31 August 2005. HSU 3129 (1). DALLAS CO.: unnamed creek at St. Hwy 128, 6.4 km N of Sparkman (Sec. 35, T9S, R17W). 20 January 1997. HSU 1344 (2); Tulip Creek at St. Hwy 8 (Sec. 27, T8S, R16W). 18 February 1999. HSU 2371 (3). HOT SPRING CO.: Lake DeGray at Lenox Marcus crossing. June 1993. HSU 137 (20). LITTLE RIVER CO.: Little River, run E of dam (Sec. 26, T12S, R28W). 16 February
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1991 & 14 April 199L HSU 289, 27 (1, 6); Little River at Millwood Dam (Sec. 26 T12S, R28W). March 1991. HSU 313 (1). PHILLIPS CO.: Old Town Lake, flood gate of St. Hwy. 44 (Sec. 30, T3S, R3E). 23 March 2005. HSU 3002 (2). Suttkus & Thompson (2002) discussed the rediscovery of this silverside in the Pearl River of Louisiana and Mississippi and provided compelling evidence that M audens is a valid species. New county records are reported for Ashley, Bradley, Clark, and Hot Spring counties.
CENTRARCHIDAE
Centrarchus macropterus (Lacepede) {n = 18). ASHLEY CO.: slough off Saline River at Stillions, 14.5 km NW Crossett (Sec. 4, T17S, R9W). 5 July 1996. HSU 1317 (1); tributary to Hanks Creek, 12.1 km E Crossett (Sec. 21, T18S, R7W). 5 July 1996. HSU 1368 (4). CLARK CO.: McNeeley Creek, 6.4 km S Beime off St. Hwy. 51 (Sec. 31, TIOS, R20W). 20 April 1997. HSU 2156 (1); Clear Lake in Joan off St Hwy. 51 (Sec. 23, T7S, R18W). 8 May 1999. HSU 2649 (1); L'Eau Frais Creek at Ouachita River (Sec. 1, T8S, R19W). 11 March 2005. HSU 3038 (1). HEMPSTEAD CO.: Yellow Creek, 0.4 km from railroad on St Hwy. 32 (Sec. 17, T12S, R27W). 23 March 1991. HSU 1235 (1). HOT SPRING CO.: L’Eau Frais Creek at St Hwy. 222 (Sec. 15, T6S, R17W). 9 March 1997. HSU 1884 (1). OUACHITA CO.: Freeo Creek at St. Hwy. 9, 8.9 km S of Dallas County line (Sec, 36, T22S, R16W). 7 June 1997. HSU 2175 (1). NEVADA CO.: Caney Creek, 4.8 km N of Bluff City on St. Hwy, 24 (Sec. 22, TllS, R20W). 19 February 1983. NLU (4); Middle Creek, 14,5 km N of Prescott on St Hwy. 19 (Sec. 27, T9S, R23W). 19 February 1983, NLU (1), UNION CO.: Lapoile Creek, 5.2 km NE Strong (Sec. 18, T18S, R1 1 W). 22 March 1997. HSU 1688 (2), These new records supplement those of McAllister et at (2004); however, Hempstead is a new county record.
Lepomis marginatus (Holbrook) {n = 117). ASHLEY CO.: Thompson Creek, 1 1,3 km NW Crossett (Sec. 11, T17S, R9W). 5 July 1996, HSU 1346 (4); tributary to Hanks Creek, 12.1 km E Crossett (Sec. 21, T18S, R7W), 5 July 1996. HSU 1367 (9); slough off Saline River, 14.5 km NW Crossett at Stillions (Sec. 1, T17S, R9W). 6 July 1996. HSU 1364 (1). BRADLEY CO.: Snake Creek at Broad (Sec.
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30, T16S, R9W). 17 June 2002. SAU (4). CLARK CO.: Tupelo Creek, 6.4 km S Arkadelphia at St. Hwy. 7 bridge (Sec. 35, T7S, R19W). 22 March 1997 & 4 May 1999. HSU 1791, 2349 (2, 2); Beech Creek, 3.2 km SE Gurdon (Sec. 11, TIOS, R20W). 27 March 1997. HSU 1644 (2); McNeeley Creek, 6.4 km S Beime off St. Hwy. 51 (Sec. 31, TIOS, R20W). 20 April 1997. HSU 2162 (3). COLUMBIA CO.: Horsehead Creek at U.S. 19, 12.9 km SW of Magnolia (Sec. 32, T18S, R21W). 21 November 2001. SAU (6). LAFAYETTE CO.: Bayou Bodcau at U.S. 82 (Sec. 7, T16S, R23W). 11 October 1995. SAU (1). MILLER CO.: Millwood Lake at Paraloma Landing at end of St. Hwy. 234 (Sec. 29, TllS, R28W). 18 June 2002. SAU (3). NEVADA CO.: Caney Creek, 4,8 km N of Bluff City on St. Hwy. 24 (Sec. 22, TllS, R20W). 19 February 1983. NLU (54). PIKE CO.: Saline River, 8.0 km W of Delight on St. Hwy. 26 (Sec. 8, T8S, R24W). 19 June 1982. NLU (1). UNION CO.: Big Comie Creek at St. Hwy. 15, 25.7 km SW of El Dorado (Sec. 35, T19S, R18W). 5 October 1995. SAU (1); Grand Marais Lake at Felsenthal (Sec. 16, T19S, RlOW). 18 September 1996. SAU(17);CalionLakeatCalion(Sec. 22, T16S, R14W). 17 May 2003. SAU (7). The dollar sunfish is a widespread species of the Coastal Plain province in Arkansas. The specimen from Pike County represents a new county record.
Lepomis miniatus Jordan {n = 42). CLARK CO.: Little Deceiper Creek on St. Hwy. 51, 1.6 km W of Arkadelphia (Sec. 26, T7S, R20W). June 1992. HSU 128 (1); Caddo River at St. Hwy. 7 bridge in Caddo Valley (Sec. 31, T6S, R20W). 20 March & 17 April 1994, 1 April 1997. HSU 828, 740, 1937 (1, 1, 1); Caddo River, 3.2 km W of 1-30 bridge in Caddo Valley (Sec. 36, T6S, R20W). 4 May 1994. HSU 775 (1); Tupelo Creek, 6.4 km SE of Arkadelphia off St. Hwy. 7 (Sec. 35, T7S, R19W). 24 February 1995, 25 February 1999, & 11 March 2005. HSU 1240, 2345, 2350, 2979 (1, 2, 1, 1); Gentry Creek (boat ditch), 6.4 km N Gurdon off U.S. 67 (Sec. 3, T9S, R20W). 13 January 1996. HSU 1276 (1); Saline Bayou, 1.6 km E Arkadelphia on St. Hwy. 7 (Sec. 16, T7S, R19W). 2 March 1996. HSU 1283 (1); lower dam of Caddo River at Caddo Valley (Sec. 36, T6S, R20W). 25 February & 1 March 2005. HSU 2899, 2909 (1, 1). COLUMBIA CO.: Bayou Dorcheat Creek at St. Hwy. 160, 6.4 km E of Taylor
MCALLISTER, TLMLISON & ROBISON
41
(Sec. 5, T19S, R22W). 6 October 2003. SAU (2); Horsehead Creek at U.S, 19, 12.9 km SW of Magnolia (Sec. 32, T18S, R21W). 21 November 2001. SAU (1). GARLAND CO.: mouth of Hot Springs Creek, Lake Hamilton (T3S, R18W). 30 April 1999. HSU 2279 (1). HOT SPRING CO.: U Eau Frais Creek, 12,1 km E Donaldson (Sec, 1, T6S, R17W). 22 March 1997. HSU 1493 (1); Saline Bayou, 4.0 km S Friendship (Sec. 23, T6S, R19W). HSU 2719 (1). LAFAYETTE CO.: Lake Erling at St Hwy. 160 (Sec. 35, T19S, R23W). 14 June 2002. SAU (5). NEVADA CO.: Middle Creek, 14.5 km N of Prescott on St. Hwy. 19 (Sec. 27, T9S, R23W). 19 February 1983. NLU (2); Caney Creek, 4.8 km N of Bluff City on St. Hwy. 24 (Sec. 22, Ills, R20W). 19 February 1983. NLU (3). OUACHITA CO.: Bragg Lake, 2 km SE Bragg City off St. Hwy. 24 (Sec. 33, T12S, R18W). 12 April 1997. HSU 2053 (1); Freeo Creek at St Hwy. 9, 8.9 km S Dallas County line (Sec. 36, TllS, R16W). 7 June 1997. HSU 2717 (3). UNION CO.: Grand Marais Lake at Felsenthal (Sec. 16, T19S, RlOW). 18 September 1996. SAU (3); Big Comie Creek at St. Hwy. 15, 9.7 km SW of El Dorado (Sec. 35, T19S, R18W). 5
October 1995. SAU (4); Calion Lake at Calion (Sec. 22, T16S, R14W). 17 May 2003. SAU (1). This fish was formerly regarded as a subspecies of Lepomis punctatus. However, Warren (1992) examined morphological variation and considered L. punctatus miniatus a separate species. New county records for the red-spotted sunfish are documented for Garland and Nevada counties.
PERCIDAE
Etheostoma asprigene (Forbes) (n = 9). BRADLEY CO.: More Creek at Moro Bay State Park (Sec. 21, T16S, R12W). 17 October 1998. SAU (1). HEMPSTEAD CO.: Ozan Creek, 1.1 km W of McCaskill on St. Hwy. 24 (Sec. 28, T9S, R26W). 26 Sept. 1983. NLU (2). HOWARD CO.: Muddy Fork Creek, 12.9 km E of Dierks on FAS south of Muddy Fork (Sec. 33, T7S, R27W). 21 Nov. 1981. NLU (1). UNION CO.: Grand Marais Lake at Felsenthal (Sec. 16, T19S, RlOW). 18 September 1996. SAU (5). Hempstead and Howard counties represent significant southwestward range extensions as well as the westernmost distribution for E. asprigene in the state.
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THE TEXAS JOURNAL OF SCIENCE, VOL. 61, NO. 1, 2009
Etheostoma fusiforme (Girard) {n = 15). COLUMBIA CO.: Bayou Dorcheat at co. rd., 6.4 km NE of Bussey (Sec. 16, T18S, R22W). 6 October 2003. SAU (2). NEVADA CO.: Caney Creek, 4.8 km N of Bluff City on St. Hwy. 24 (Sec. 22, TllS, R20W). 19 February 1983. NLU (1). PIKE CO.: spring drainage ditch, 7.2 km NE of Murfreesboro at Wayside Park off co. rd. 379 (Sec. 35, T7S, R25W). 18 June 1983. NLU (6). UNION CO.: Grand Marais Lake at Felsenthal (Sec. 16, T19S, RlOW). 18 September 1996. SAU (2); Norris Creek at NE comer of Strong (Sec. 32, T18S, R12W). 22 March 1997. HSU 2132 (1); Calion Lake at Calion (Sec. 22, T16S, R14W). 17 May 2003. SAU (3). Robison & Buchanan (1988) considered the swamp darter to be a threatened species in the state and the Nature Conservancy (NatureServe 2008) lists it as imperiled (S2). Few previous records exist for E. fusiforme in Arkansas, and new county records for Columbia, Nevada, and Pike counties significantly add to the knowledge of its current distribution in the state.
Percina sp. {n = 3). CLARK CO.: Caddo River, 3.2 km W of 1-30 bridge in Caddo Valley (Sec. 36, T6S, R20W). J. Hardage. 4 May 1994. HSU 767 (1). HOT SPRING CO.: Ouachita River, river road at Friendship (Sec. 12, T6S, R19W). 27 April 2005. HSU 3102 (2). This undescribed species, an endemic of the Ouachita River, is one of special concern (Robison & Buchanan 1988; Robison 1992; Anonymous 2004). The Clark County record suggests that the former lower Caddo River population may not be extirpated by the tailwater effects of DeGray Dam, a suggestion offered by Buchanan (1984) and reiterated by Robison & Buchanan (1988). More recently, Gagen et al. (2002) provided information on habitat and abundance of the Ouachita darter. This percid species is currently being described by HWR and R. C. Cashner.
Results and Summary
This study documents the collection of 530 specimens, representing 16 taxa within nine families. The following noteworthy species were collected: American eel {A. rostrata), mooneye (//. tergisus), bluehead shiner (P. hubbsi), taillight shiner (N. maculatus), weed shiner {N. texanus), creek chub {S. atromaculatus), blacktail
MCALLISTER, TUMLISON & ROBISON
43
redhorse (M poecilurum), brown madtom {N. phaeus), flier (C macropterus), dollar sunfish (L. marginatus), redspotted sunfish (Z. miniatus), northern starhead topminnow (F, dispar), mississippi silverside (M audens), mud darter (Z. asprigene), swamp darter {E. fusiforme), and the undescribed Ouachita darter (Percina sp.).
In summary, this study documents 26 new county records for 13 (81%) of the species collected. Most importantly, this study includes new records and extensions of the known geographic ranges for rarely collected species, including H. tergisus, P. hubbsi, E. asprigene, E. fusiforme, and Percina sp. nov. nr, nasuta, while N. phaeus is reported from Arkansas for only the second time since its original discovery more than 35 years ago.
Acknowledgments
Special thanks to Dr. N. H. Douglas, University of Louisiana- Monroe for use of the collection of fishes housed in the ULM Museum of Natural History, including those collected by R. A. Loe. Also, thanks to previous SAU Vertebrate Natural History classes, and former SAU students J. Rader, C. Brummett, N. Covington, and K. Ball, and HSU ichthyology classes, and former HSU students J. Abernathy, K. Bailey, B. Baker, B. Chancellor, M. Clark, J. & D. Collins, S. Davis, W. Daggett, J. Daniel, A. DeLaughter, R. Dorer, D. Dyer, D. Fendley, R. Fisher, B. Fluker, J. Hardage, S. Henson, B, Hesington, R. Hicks, J. Hooks, C. Horton, T. James, S. Jordan, J. Jumper, R. Long, J. Nix, J. Patterson, C. Petty, J. Pinkerton, A. Rainwater, C. Pope, J. Rigsby, J. Russell, S. Ryders, L. Self, D. & J. Thompson, D. Turner, K. Watt, T. West, and A. Weston for assistance in collecting. We also thank the Arkansas Game and Fish Commission for providing scientific collecting permits to HWR and RT.
Literature Cited
Anonymous. 2004. Arkansas endangered, threatened, and species of special concern.
Arkansas Game & Fish Comm. Rep., January 9, 2004. 6 pp.
Bailey, R. M. & H. W. Robison. 1978. Notropis hubbsi, a new cyprinid from the Mississippi River basin. Occas. Pap. Mus. Zook, Univ. Michigan, 683:1-21.
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Buchanan, T. M. 1984. Status of the Longnose Darter, Percina nasuta (Bailey), in Arkansas. Arkansas Nat. Hist. Comm. Rep., June 1984, 29 pp.
Gagen, C. J., K. R. Moles, L. J. Hlass & R. W. Standage. 2002. Habitat and abundance of the Ouachita Darter {Percina sp. nov.). J. Arkansas Acad. Sci., 56:230-234.
Mayden, R. L. 1989. Phylogenetic studies of North American minnows, with emphasis on the genus Cyprinella (Teleostei: Cypriniformes). Univ. Kansas Mus. Nat. Hist. Misc. Publ., 80:1-189.
McAllister, C. T., S. E. Barclay & H. W. Robison. 2004. Geographic distribution records for the Flier, Centrarchiis macropterus (Perciformes: Centrarchidae), from southwestern Arkansas. J. Arkansas Acad. Sci., 58:131-132.
McAllister, C. T., H. W. Robison & T. M. Buchanan. 2006. Noteworthy geographic distribution records for the Golden Topminnow, Fundulus chrysotus (Cyprinodontiformes: Fundulidae), from Arkansas. J. Arkansas Acad. Sci. 60:185- 188.
McAllister, C. T., H. W. Robison & R. Tumlison. 2007. Additional geographic records for the Goldstripe Darter, Etheostoma parvipinne (Perciformes: Percidae), from Arkansas. J. Arkansas Acad. Sci., 61: 125-127.
McAllister, C. T., R. Tumlison & H. W. Robison. 2008. Distribution of the Bantam Sunfish, Lepomis symmetricus (Perciformes: Centrarchidae), in Arkansas. Texas J. Sci., 60(l):23-32.
NatureServe, 2008. NatureServe Explorer: An online encyclopedia of life [web application]. Version 7.0. NatureServe, Arlington, Virginia. Available http://www.natureserve.org/explorer. (Accessed: June 29, 2008).
Robison, H. W. 1974. First record of the ictalurid catfish, Noturus phaeus, from Arkansas. Southwest. Nat., 18:475.
Robison, H. W. 1992. Distribution and status of the Ouachita River form of the Longnose Darter in the Ouachita National Forest, Arkansas. Final report submitted to U.S.D.A. Forest Service, Ouachita National Forest, Hot Springs, Arkansas, 58 pp.
Robison, H. W. & T. M. Buchanan. 1988. Fishes of Arkansas. Univ. Arkansas Press, Fayetteville, 536 pp.
Suttkus, R. D. & B. A. Thompson. 2002. The rediscovery of the Mississippi Silverside, Menidia audens, in the Pearl River drainage in Mississippi and Louisiana. SE Fishes Coun. Proc., 44:6-10.
Warren, M. L., Jr. 1992. Variation of the spotted sunfish, Lepomis punctatus complex (Centrarchidae): Meristics, morphometries, pigmentation and species limits. Bull. Alabama Mus. Nat. Hist., 12:1-47.
CTM at: drctmcallister@aol.com
TEXAS J. OF SCI. 61(1):45»60
FEBRUARY, 2009
COMPARISON OF TOTAL LIPID AND FATTY ACID COMPOSITIONS OF WHOLE-BODY AND BODY SEGMENTS OF LERTHA EXTENSA ADULTS (NEUROPTERA: NEMOPTERIDAE)
Ozlem Cakmak, Mehmet Bashan and Ali Satar
Department of Biology, Dicle University 21280 Diyarbakir, Turkey
Abstract. — Total lipid and fatty acid compositions of phospholipids and triacylglycerols fractions, prepared from whole body and selected body segments (head, thorax and abdomen) of adults males and females of Lertha extensa Oliver (Neuroptera: Nemopteridae), were analyzed by gas chromatography and gas chromatography-mass spectrometry. The female abdomen has the highest level of total lipid in body segments. Predominant fatty acid components of phospholipid and triacylglycerol fractions in the whole body and three body segments were C16:0, C18:ln-9 and C18:2n-6 acids, comprising more than 80 % of the fatty acid components. Fatty acid profiles of whole body extracts differed by sex only for phospholipid and triacylglycerol fractions. Fatty acid profiles of phospholipids from the head and abdomen were similar to those of the whole body, but considerably different from that of thorax. Several minor fatty acids, comprising < 2% of the total, were noted. Detailed profiles are reported, and are compared to those of other insects.
Fatty acids (FA) assume broad biological significance, with important roles in three general areas. First, lipids serve as energy reserves, generally stored as saturated and monounsaturated fatty acids, are deployed in development, hibernation and locomotion. Second, fatty acids form essential parts of the cellular structure as components of cellular phospholipids (PL), particularly in biomem¬ branes. Third, certain polyunsaturated fatty acids (PUFAs) - specifically C20:3n-6 (eicosatrienoic), C20:4n-6 (arachidonic acid) and C20:5n-3 (eicosapentaenoic acid) - act in regulatory roles, as substrates for the biosynthesis of prostaglandins and other eicosanoids. With respect to insects, studies of the biology and biochemistry of fatty acids have offered new insights, such as the de novo biosynthesis of Cl 8 and C20 PUFAs (Stanley-Samuelson etal. 1988).
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THE TEXAS JOURNAL OF SCIENCE, VOL. 61, NO. 1, 2009
Insects utilize lipids efficiently for development, reproduction and flight. The amount and composition of lipids in an insect vary considerably between developmental stages, selected tissues, nutrition, starvation, sex and hormones (Beenakkers et al. 1985). Physiological studies in adults address reproduction and mobilization of lipids during flight, a period of high metabolic demand (Goldsworthy & Mordue 1989). Lipid and FA compositions of insects have been studied for whole-body preparations (Nikolova et al. 2000) and, to a lesser extent, individual segments of the body.
FA profiles have been documented for a taxonomic array of insects, but changes in FA composition of individual body segments have been addressed for comparatively few species such as Periplaneta americana (Linnaeus) (Blattaria: Blattidae) (Jurenka et al. 1987); Magicicada septendecium (Linnaeus) (Hemiptera: Cicadidae) (Hoback et al. 1999); and Photinus pyralis (Coleoptera: Lampyridae) (Nor Aliza et al. 2000).
The order Neuroptera has received recent interest, due to their promise as biological control agents and a tolerance for several modem insecticides (Canard 1998). However, few studies of the total FA composition of the Neuroptera have been performed (Fast 1970; Zinkler 1975; Lemesle et al. 1997; Nelson et al. 2003). Larvae of the family Nemopteridae are carnivorous, although adults are unique for their long, filamentous or ribbon-like hind wings, and feed exclusively on pollen and nectar with long specialized mouth parts, whilst all larvae are carnivores (Mansell 1992). Lertha extensa is endemic to Turkey (Satar & Ozbay 2004).
There are no previous descriptions of FA composition of PL and triacylglycerol (TG) fractions of any neuropteran except Lertha sheppardi Kirby (Neuroptera: Nemopteridae) (Cakmak et al. 2007). This study provides data concerning fatty acid composition of PL and TG fractions prepared from whole-body and each of the
CAKMAK, BASHAN & SATAR
47
threebody segments (head, thorax and abdomen) of adult specimens
of Lertha extensa.
Materials And Methods
Biological specimens -Lertha extensa adults were collected with nets and light traps from Diyarbakir, Turkey (37° 54’N, 40° 14’E; at an altitude of about 850 m) throughout June and July 2006. Samples were individually isolated into plastic boxes of 10 by 5 by 5 cm and supplied with drops of water, commercially available pollen, and fixed flowers (family Apiaceae = Umbelliferae).
Analysis of insects ' fatty acids -\nsQCts were anesthetized by chilling on ice, and processed for lipid extraction and analysis following the methods of Bling & Dyer (1959). For whole-body insect analyses, three groups of 20 adult males, and 20 adults females were used per sample in 4 mL of chloroform/methanol (2:1, v/v). For analyses of isolated body segments, 96 anesthetized males and females were dissected, and three sets of 32 samples were collected, then processed for extraction. Each group of samples was transfered into 3 mL of chloroform/methanol (2:1, v/v). Autoxidation of unsaturated components was minimized by adding 50 pi of 2% butylated hydroxytoluene in chloroform to each sample during the extraction process. Total lipid measures were conducted using the method of Christie (1982).
Total lipid extracts were dried under a stream of N2, then PL and TG fractions were isolated by thin-layer chromatography (TLC), using Silica Gel G TLC plates (20 X 20 cm, 0.25 mm thick). After applying the total lipid extracts, the TLC plates were developed in petroleum ether:diethyl ether:acetic acid (80:20:1, v/v). Lipid fractions were made visible by spraying the TLC plates with 2\T- dichlorofluorescein (Supelco, Supelco Park, PA, USA), and PL and TG fractions were identified by corresponding standards.
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THE TEXAS JOURNAL OF SCIENCE, VOL. 61, NO. 1, 2009
PL and TG fractions were scraped into reaction vials, and the associated fatty acids were transmethylated by refluxing the fractions in acidified methanol for 90 min at 85^C. The fatty acid methyl esters (FAMEs) were extracted from the reaction vials three times with hexane, and concentrated. Results were expressed as the percentage of each fatty acid with respect to the total fatty acids. Internal standard was not used.
Gas chromatography -ThQ FAMEs were analyzed by gas chromatography using a Ati Unicam 610 gas chromatograph equipped with a SP-2330 capillary column (30 m by 0.25 mm i.d., 0.2 pm film thickness, Supelco), a flame ionization detector and an Unicam 4815 recording integrator. A split injection of 0.5 pi was used. The temperature condition detector was 250°C. The oven temperature was set at 180°C for 5 min then reached to 200°C with a ramp rate of 2 /min, and then held for 15 min. FAMEs were identified by comparisons of retention times with authentic standards (Sigma Chemical Co., St. Louis, MO, USA). Individual FAMEs were identified by comparisons with the chromatographic behaviors of authentic standards.
Gas chromatography-mass spectrometry -C\\Qm\cdX structures of fatty acid methyl esters were confirmed by capillary gas chromatography-mass spectrometry (GC-MS) (HP 5890-E series GC-System, Hewlett-Packard, Palo Alto, CA, USA) with mass- selective detection. An Innowax column (30m by 0.25 mm i.d., 0.25 pm film thickness) was used, and the temperature was programmed from 150 to 230 ®C at a 2 °C/min increase with an initial hold of 6 min. The carrier gas was helium (1 mL/min) and the split ratio was 1:50. The injection port and the detector temperatures were 250°C and 300°C respectively. The mass spectrometer was operated in the electron impact ionization mode (70 eV). Chemical structures of the FAMEs were determined by comparison of the spectra with the Wiley 275 and Nist 98 databank, and by comparing obtained spectra with that of authentic standards.
CAKMAK, BASHAN & SATAR
49
Fig. 1. Total lipid of body segments of Lertha externa as a percentage of total wet weight.
Statistical analys is. -Stsitistical analysis included ANOVA to determine variability, F-tests to identify treatment effects, and least significant difference and student's Mest (Snedecor & Cochran 1967) to identify significant differences between groups (P<0.05).
Results
The percentage of total lipid of body segments of L. extensa are shown in Fig. 1. The abdomen contain highest level of total lipid percentage in all body segments. The female abdomen contain higher total lipid than male {F =656.417; df= 3,8; P<0.001). No significant difference was observed in total lipid of head {F =12A1\ P>0.05) and thorax (F =11.247; P>0.05) between male and female. The fatty acid compositions of PL and TG prepared from whole-body of adult males and females L. extensa are displayed in Table 1. Predominant fatty acid components of whole-body PL and TG were Cl 6:0 (palmitic), C18:0 (stearic acid), C18:ln-9 (oleic) and C18:2n-6 (linoleic) acids, occuping over 85% of the fatty acids, in which C18:ln-9 was most abundant, attaining to ca. 40%. The fatty acid profiles of PL and
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THE TEXAS JOURNAE OF SCIENCE, VOL. 61, NO. 1, 2009
Table 1. Proportion of fatty acids, as percentage of total fatty acids, associated with phospholipids and triacylglycerols prepared from whole-body of Lertha extensa.
|
Fatty acid |
Phospholipids |
Triacylglycerols |
||
|
Female |
Male |
Female |
Male |
|
|
(means*±5'.Z).)# |
(means *±5". D. )# |
(means *±5. D. )# |
(means*^:^./).)# |
|
|
C14:0 |
1.58±0.04a |
0.89±0.03b |
2.28±0.15a |
2.78±0.15a |
|
C15:0 |
0.51±0.02a |
0.32±0.02b |
1.71±0.07a |
0.24±0.02b |
|
C16:0 |
11.50±0.70a |
lL63±2.01a |
26.07±1.23a |
28.61±1.52a |
|
C17:0 |
0.13±0.02a |
0.18±0.02a |
1.16±0.09a |
0.65±0.02b |
|
C18:0 |
12.70±1.15a |
10.87±0.54a |
5.32±0.16a |
5.77±0.41a |
|
ZSFA |
26.42±1.71a |
23.86±2.50a |
36.54±2.13a |
38.05±1.49a |
|
C16:ln-7 |
6.65±0.90a |
5.62±0.53a |
7.04±0.07a |
6.26±0.08a |
|
C18:ln-9 |
38.14±0.89a |
36.57±1.17a |
44.01±2.31a |
41.63±1.38b |
|
C20:ln-9 |
0.20±0.09a |
0.26±0.09a |
0.10±0.09a |
0.14±0.08a |
|
IMUFA |
44.99±1.47a |
42.45±1.65a |
51.16±3.06a |
47.89±2.39a |
|
C18:2n-6 |
22.25±1.03a |
23.68±0.19b |
11.08±1.07a |
8.33±1.09b |
|
C18:3n-3 |
4.30±0.02a |
9.03±0.20b |
1.21±0.02a |
5.63±0.59b |
|
C20;4n-6 |
0.65±0.02a |
0.51±0.02a |
||
|
C20:5n-3 |
0.80±0.02a |
0.43±0.02b |
||
|
ZPUFA |
28.00±2.69a |
33.65±0.21b |
12.29±1.32a |
13.96±1.08a |
* Averages of three replicates using 20 adult males, and 20 adult females per repli¬ cates.
# Means with the same letter do not significantly different between sexes, P>0.05. Each section is separately evaluated.
SEA: Saturated Fatty Acids; MUFA: Monounsaturated Fatty Acid; PUFA: Polyun¬ saturated Fatty Acid.
TG prepared from whole-body were essentilally similar between female and males, although sexual differences in the proportion were found in some components such as 18:3n-3 (linolenic), the content being higher in males than females, in both lipid fractions. Among minor components occuping less than 2% of fatty acids. Cl 5:0 (pentadecanoic acid) and Cl 7:0 (heptadecanoic acid) existed both in PL and TG fractions, but C20:4n-6 and C20:5n-3 were hardly detected in TG. Odd- chain fatty acid and eicosanoid precursor C20 PUFAs were detected by flame ionization gas chromatography only sporadically; they were in low titres. More sensitive analysis by gas chromatography-mass spectrometry confirmed that these components are present in both fractions. Compared with PLs,
CAKMAK, BASHAN & SATAR
51
the FA profiles of TGs prepared from L. extensa had higher proportions of C16:0, C18:ln~9 and lower proportions of two PUFAs, C18:2m6 and C18:3m3.
The fatty acid compositions of PL prepared from the head^ thorax, abdomen were presented in Table 2. The major components are C16:0, C18:ln-9 and C18:2n»6. The profiles of these components varied among the body segments which were analysed. The major component present in lowest proportion, Cl 6:0, comprised about 25% of phospholipid fatty acids in head and abdomen, but made up about 16% in female and 14% in male of thorax. Similarly, C18:2n-6 accounted for about 20% of the phospholipid fatty acids in the male abdomen, and 41% of the female thorax phospholipid fatty acids. Although there are sexual differences in the proportions of several fatty acids of PL prepared from head, they were more prominent in those prepared from thorax and abdomen. Fatty acid profile in PL prepared from head and abdomen was largely similar to that of whole-body (Table 1), but considerably different from that of thorax. In head and abdomen, C18:ln~9 was predominant, attaining to ca. 35% of the fatty acids, and C16:0 and C18:2n“6 respectively occupied 25%, whereas, in thorax, C18:2n-6 was the most abundant component, occuping 40%, followed by C18:ln-9 (25%) and Cl 6:0 (15%). Some differences among body segments were detected in the minor components: Cl 7:0 and C22:ln-9 (docosenoic acid) were specific to abdomen, C20:2n"6 (eicosadienoic acid) not detected in head, while C20:ln-9 (eicosenoic acid), C20:4n”6 and C20:5n-3 were present in all segments and whole body.
The fatty acid profiles of TG fractions prepared from three body segments of adult are presented in Table 3. Fatty acid profiles in TG prepared from head and abdomen were largely similar to that of whole-body (Table 1), but considerably
Table 2. Proportion of fatty acids, as percentage of total fatty acids, associated with phospholipids prepared from body segments of Lertha externa.
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THE TEXAS JOURNAL OF SCIENCE, VOL. 61, NO. 1, 2009
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CAKMAK, BASHAN & SATAR
53
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I:PUFA 16J5±!.40a 15.59±1.20a 25.61±L94a 25=58±!J8a 16.01±L23a !2J8±lJ9b
* Averages of three replicates using 32 adult males, and 32 adult females per replicates.
# Means with the same letter do not significantly different between sexes, P>0.05. Each section is separately evaluated.
SFA: Saturated Fatty Acids; MUFA: Monounsaturated Fatty Acid; PUFA: Polyunsaturated Fatty Acid
54
THE TEXAS JOURNAL OF SCIENCE, VOL. 61, NO. 1, 2009
different from that of head and abdomen, as in the case of PL (Table 2). In head and abdomen, C18:ln-9 was predominant, attaining to ca. 40% of the fatty acids, followed by Cl 6:0 (ca. 30%) and C18:2n-6 (less than 16%), whereas, in thorax, C16:0 was the most abundant component, occuping over 30%, followed by C18:ln-9 (25%) and C18:2n-6 (23%).
For minor components, some differences were observed among body segments: Cl 5:0 was present only in abdomen; Cl 7:0 was not in head; C20:4n-6 and C20:5n-3 was in head and thorax of males, but not of females, whereas C20:ln-9 present in all segments with both sexes.
Discussion
Changes in lipid stores occur due to flight, mating activities, and oviposition (Gilby 1965) in the adult stage. The amount of total lipid was observed to vary among body segments and sexes of L. extensa. Total lipid amount is significantly highest in female abdomen. This difference may depend on accumulation of lipids in the eggs. Abdomen contains the reproduction system, digestive system, and the most of the fat body. Triglycerides, which con-stitute 50 to 70% of the fat of insects throughout their development, are located mostly in their fat bodies and serve as a source of energy for various metabolic purposes. During ovarial develop-ment, lipids synthesized in the fat body are transported to the developing ovary, and stored for use in embryogenesis.
The major fatty acids in the lipids of L. extensa, are Cl 6:0, Cl 8:0, C18:ln-9 and C18:2n-6, as reported for some other Neuroptera and most other insect orders (Stanley-Samuelson et al. 1988; Cakmak 2006; Cakmak et al. 2007). Aside from these major components, many fatty acids were detected at low proportions of the PLs and TGs. The additional components include shorter chain fatty acids, such as C14:0, odd-chain fatty
CAKMAK, BASHAN & SATAR
55
acids, including C15:0, C17:0 and longer chain saturated and unsaturated fatty acids, C20:ln-9, C20:2n”6, C20:4n-6, C20:5n“3, and C22:ln~9,
Fatty acid profiles of PL and TG prepared from whole- body were essantially similar between female and males, although sexual differences in the proportion were found about some components such as C18:3n-3, the content being higher in males than females, in both lipid fractions. High levels of C18:3n--3 could be based on a number of physiological factors. One of the major functions of C18:3n- 3 and PUFAs in general, is that they serve as a structural component of membranes to maintain proper fluidity and permeability. C18:3n-3 is also a precurser to the eicosanoids, including prostaglandins, leuko-trienes, and thromboxanes (Stanley 2006).
Fatty acid compositions are not fixed in insects and can change seasonally to perform special functions that may be critical for survival. Many factors affect the shape of fatty acid profiles, in particular, development (Cakmak et al. 2007), diet (Bozkus 2003; Stanley-Samuelson & Dadd 1981; Stanley- Samuelson et al. 1985), diapause status (Shimizu 1992; Hodkova et al. 1999; Bashan et al 2002; Bashan & Cakmak 2005), and body segments (Nor Aliza et al. 2000) exert strong influences on the shape of fatty acid profiles.
Fatty acid profiles of PL and TG prepared from head and abdomen was largely similar to that of whole-body, but considerably different from that of thorax. The principal storage site for insect lipids is the fat body, and the lipid composition of the whole insect probably reflects the lipid composition of the fat body. This organ consist of aggregates of cells forming lobes or sheets of tissue, which is spread throughout the body and invests the internal organs. Its spatial arrengement in the abdomen,
56
THE TEXAS JOURNAL OF SCIENCE, VOL. 61, NO. 1, 2009
where large fat deposits are found in close association with the gut, facilitates the uptake of dietary nutritions. Therefore, it is not surprising that the fatty acid composition of abdomen and whole-body were similar but some minor differences were detected in both fractions, such as Cl 6:0 and C18:3n-3. In both fractions, proportions of C18:ln-9 were lower in adult in females than males, which seem most likely to be associated with the processes of egg development and oviposition. When neuropterans pupate, larvae dig a small cavity in the soil and spin a loose silken cocoon around themselves. Many holometabolous insects exhibit similar behavior, but neuropterans are unusual because their silk is produced by Malpighian tubules (excretory organs) and spun from the anus. In contrast, most other endopterygote insects produce silk in modified salivary or labial glands and spin it with their mouthparts. Only one other order, the Coleoptera, makes silk in the same manner as Neuroptera. Lipids also occur in the silk (Meyer 2005), and it is possible the fatty acid differences in the abdomen stem from consumption of some fatty acids while making the cocoon.
PL fraction of thorax of P. americana contained the highest linoleic acid (38%) while oleic acids (49%) was found primarily in abdomen (Jurenka et al. 1987). Similarly, high level of linoleic acid was detected in PL extracted fom thorax of M septendecim (45%) (Hoback et al. 1999) and Tenebrio molitor Linnaeus (Coleoptera: Tenebrionidae) (Howard & Stanley- Samuelson 1990). In both sexes of L. extensa, it was detected that the ratio of PUFAs in thorax had the highest level due to linoleic acid in body segments. This result was valid in both fractions of the insect. In order to fly, insects require flight muscles that constitute at least 12 to 16% of their total mass, and flight performance increases as this percentage increases. However, flight muscles are energetically and materially expensive to build and maintain, and investment in flight muscles constrains other aspects of function, particularly female fecundity
CAKMAK, BASHAN & SATAR
57
(Marden 2000). Fatty acid accumulation in the thorax, where flight muscles are located, makes it a convenient, ready-made energy source. Localization of the fatty acid-containing vesicles in the thorax also supports the possibility that lipid energy is required for rapid muscle contractions (Georgia & Mohammed 2002). Since insect flight muscles are among the most active in nature, they have extremely high rates of fiiel supply and flights of insects are lergely fiieled through fatty acid oxidation. The lipid substrate is transported as diacylglycerol in the blood, employing a unique and efficient lipoprotein shuttle system (Horst et ah 1993). These findings indicate that the accumulation and utilization of these FAs differ in body segment of both sexes.
Arachidonic acid typically occurs in very small proportions in PLs of terrestrial insects, ranging from no more than traces to less than 1% of PL fatty acids, while C20:5n"3 is often missing entirely from insect lipids. In this study, the proportions of C20:4n-6 and C20:5n-3 were detected body segment and whole- body of both fractions (less than 1.8%), especially in PL fraction. Contrarily, C20:4n-6 made up approximately 21% of the PL fatty acids prepared from whole-body of males and females of P. pyralis, and from heads and thoraces prepared from males (Nor Aliza et al. 2000). Ogg & Stanley-Samuelson (1992) detected C20:4n“6 approximately 12% of the PL fraction of head of Manduca sexta (Linnaeus) (Lepidoptera: Sphingidae). These insects are peculiar among terrestrial insects with respect to maintaining high proportions of PL C20:4n-6, which might support an unusually high capacity to generate prostaglandins and other eicosanoids in these insects.
Acknowledgment
This study was supported by Dicle University Research Fund. Project number is DUAPK 03 FF- 02.
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THE TEXAS JOURNAL OF SCIENCE, VOL. 61, NO. 1, 2009
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Horst, D. J,, J. M. Doom, P. C. Passier, M. M. York & F. C Glatz. 1993. Role of fatty acid-binding protein in lipid metabolism of insect flight muscle. Mol. Cell. Biochem. 123:145452
Howard, R. W. & D. W. Stanley-Samuelson. 1990. Phospholipid fatty acid composition and arachidonic acid metabolism in selected tissues of adult Tenebrio moiitor. Ann. EntomoL Soc. of Am., 83:975-981.
Jurenka, R. A,, M. Renobales, & G. J. Blomquist. 1987. De novo biosynthesis of polyunsaturated fatty acids in the Cockroach Periplaneta americana. Arch. Insect Biochem. Biophys., 255(1): 184-193.
Lemesle, A., D. Thierry, F. Foussard & M. Canard. 1997. Preliminary study on lipids in Chrysoperla kolthoffi during diapause (Neuroptera, Chrsopidae). Acta Zool. Fenn., 209:141-144.
Maiden, J. M. 2000. Variabilty in the size, composition, and function of insect flight muscles, Ann. Rew. Physiol, 62:157-178.
Mansell, M. 1992. The systematic position of the Nemopteridae (Insecta: Neuroptera: Myrmeleontidae). Pp. 233-241, in: Canard, M., Aspock, H. & Mansell, M. W. (eds) Current Research in Neuropterology. Proceedings of the Fourth International Symposium on Neuropterology, 24-27 June 1991, Toulouse, France, 414 pp.
Meyer, J.R. 2005. Department of Entomology, North Carolina State University [cited May 2006]. Available from:
http://www. cals, ncsii. edu/course/ent425/compendium/neurop-Lhtml
Nelson, D. R,, T. P, Freeman, J. S. Buckner, K. A. Hoelmer, C. G. Jackson & J. R. Hagler. 2003. Characterization of the cuticular surface wax pores and the waxy particles of the dustywing, Semidaiis flinti (Neuroptera:Coniopterygidae). Comp. Biochem. Physiol. B, 136:343-356.
Nikolova, N., T. Rezanka & B. Nikolova-Damyanova. 2000. Fatty acid profiles of main lipid classes in adult Chrysomela vigintipunctata (Scopoli) (Coleoptera: Chrysomelidae). Z. Naturforsch,, 55:661-666.
Nor Aliza, A., J. C. Bedick, R. L. Rana, H. Tunaz, W. W. Hoback & D. W. Stanley-Samuelson. 2000. Arachidonic and eicosapentaenoic acids in tissue of the firefly, Photinus pyralis (Insecta, Coleoptera). Comp. Biochem. Physiol A, 128:251-257.
Ogg, C. L. & D. W. Stanley-Samuelson. 1992. Phospholipid and triacylglycerol fatty acid compositions of the major life stages and selected tissues of the tobacco homworm Manduca sexta. Comp. Biochem. Physiol, 101:345-351.
Satar A. & C. Ozbay. 2004. Eggs, first instar larvae and distribution of the neuropterids Lertha extensa and L. shappardi (Neuroptera: Nemopteridae) in south-eastern Turkey. Zool Middle East. 32:91-96.
Shimizu, I. 1992. Comparison of fatty acid compositions in lipids of diapause and non-diapause eggs of Bombyx mori (Lepidoptera: Bombycidae). Comp. Biochem. Physiol B, 102:713-716.
Snedecor, G. W. & W. G. Cochran. 1967. Statistical Methods, Iowa State University Press, Iowa, U.S.A. pp, 84-127.
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Stanley D, W. 2006. Prostaglandins and other eicosanoids in insects: Biological significance. Ann. Rev. EntomoL, 51:25-44.
Stanley-Samuelson, D. W. & R. H. Dadd. 1981. Arachidonic and other tissue fatty acids of Culex pipiens reared with various concentrations of dietary arachidonic acid. J. Insect Physiol, 27:571-578.
Stanley-Samuelson, D. W., E. W. Rapport & R. H. Dadd. 1985. Effects of dietary polyunsaturated fatty acids on tissue monounsaturate and saturate proportions in two insect species. Comp. Biochem Physiol. B, 81:749-755.
Stanley-Samuelson, D. W., R. A. Jurenka, C. Cripps, G. J. Blomquist & M. de Renobales. 1988. Fatty acids in insect composition, metabolism, and biological significance. Arch. Insect Biochem. Physiol, 9:1-33.
Zinkler, D. 1975. Zum lipidmuster der photorezeptoren von insecten. Verch. Dt Zool Ges., 3:28-32.
OC at: ocakmak@dicle.edu.tr
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GENERAL NOTES
mXIDIUMSEROTINUM(mOTlSTA: MYXOZOA) FROM A JEFFERSON SALAMANDER {AMBYSTOMA JEFFERSONIANUM), IN ILLINOIS
Chris T. McAllister^ John A. Crawford and Andrew R. Kuhns
RapidWrite, 102 Brown Street Hot Springs National Park, Arkansas 71913 Indiana School of Medicine-Terre Haute, 135 Holmstedt Hall Terre Haute, Indiana 47809-9989 and Illinois Natural History Survey, 1816 S. Oak Street Champaign, Illinois 61820
The Jefferson salamander, Ambystoma jeffersonianum (Green, 1827) ranges from southeastern New York through Pennsylvania and eastern and southern Ohio to southern Indiana, and southward to southcentral Kentucky and northern Virginia (Conant & Collins 1998). However, because of extensive hybridization with the blue-spotted salamander {Ambystoma laterale), the precise range of novel populations is uncertain (Bogart & Klemens 1997), In Illinois, the species is listed as imperiled (S2) by the Nature Conservancy (NatureServe 2008) and has been reported from only two counties of the state (Clark and Edgar) (Brodman 2005). As such, A. jeffersonianum is listed as a threatened species in Illinois (Illinois Endangered Species Protection Board 2006).
Little is known about the endoparasites of A. jeffersonianum. Rankin (1945) reported the trematode, Brachycoelium salamandrae in A. jeffersonianum from Massachusetts, Fischthal (1955) noted unidentified immature trematodes and metacercariae from the species in New York, and Anderson (1960) documented the nematode, Cosmocercoides dukae in this salamander from Ontario, Canada. Herein is provided new host and geographic distribution records for an endoparasite of A. jeffersonianum from Illinois,
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An adult female (snout-vent length = 67 mm) A.
jeffersonianum was collected on 2 April 2008 by minnow trap from Zone 16 in Clark County, Illinois (39.1948°N, 87.4724° W). It was returned to the laboratory and euthanized with a dilute chloretone solution. The gall bladder was removed and processed for myxozoans according to methods of McAllister & Trauth (1995). The voucher specimen is deposited in the Arkansas State University Herpetological Museum (ASUMZ), State University, Arkansas as ASUMZ 3 1 144. A parasite voucher was deposited in the United States National Parasite Collection (USNPC), Beltsville, Maryland as USNPC 100988.
This salamander was found to be infected with a myxozoan fitting the description of Myxidium serotinum by Kudo & Sprague (1940). Numerous free spores and spherical to ovoidal trophozoites were found in bile contents. Ovoidal bivalved spores containing two polar capsules were observed as well as finer details of the spore shell that are typical of M serotinum (cf. McAllister et al. 1995).
This parasite has been previously reported from a variety of amphibians, including at least 16 species of frogs and toads within four families and four species of salamanders within two families (McAllister & Trauth 1995; McAllister et al. 2008). Salamander hosts include the spotted salamander (Ambystoma maculatum) from Arkansas and Texas (McAllister et al. 2008), marbled salamander {Ambystoma opacum) from Arkansas (McAllister & Trauth 1995), small-mouthed salamander {Ambystoma texanum) from Texas (McAllister & Upton 1987), and two-lined salamander {Eurycea bislineata) from West Virginia (Clark & Shoemaker 1973). A similar species, Myxidium melleni Jirku, Bolek, Whipps, Janovy, Kent & Modry, 2006 was described from western chorus frogs {Pseudacris triseriata) and Blanchard’s cricket frogs {Acris blanchardi) from Nebraska (Jirku et al. 2006). More recently, M melleni was
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reported in the Cajun chorus frog, Pseudacris fouquettei {^Pseudacris feriarum) from Texas by McAllister et ah (2008).
In summary, this study provides the first report of M serotinum in a threatened salamander species (A. jeffersonianum) from Illinois. For comparative purposes, it is suggested that additional salamanders, including related A. laterale from Illinois be examined for endoparasites. Like A. jeffersonianum, A. laterale has already been reported to harbor some of the same parasites including unidentified metacercariae (Muzzall & Schinderle 1992) and B. salamandrae (Muzzall & Schinderle 1992) in Michigan, and C dukae (Coggins & Sajdak 1982) in Wisconsin, and may share others, including M serotinum.
Acknowledgments
We thank the Illinois Department of Natural Resources for providing funding from contributions to the Illinois Wildlife Preservation Fund. The specimen was collected under an Illinois Threatened and Endangered Species Permit (#05-118) issued to ARK, We also thank P. A. Pilitt (USNPC) and S. E. Trauth (ASUMZ) for curatorial assistance and C. R. Bursey (Penn. State- Shenango) for information on salamander parasites.
Literature Cited
Anderson, R. C. 1960. On the development and transmission of Cosmocercoides dukae of terrestrial molluscs in Ontario. Can. J. ZooL, 38:801-825.
Bogart, J. P. & M. W. Klemens. 1997. Hybrids and genetic interactions of mole salamanders (Ambysioma jeffersonianum and A. laterale) (Amphibia: Caudata) in New York and New England. Amer. Mus. Nov. No. 3218, Amer. Mus. Nat Hist., New York. 78 pp.
Brodman, R, 2005. Ambystoma jeffersonianum (Green, 1827) Jefferson salamander. Pp. 611-613, in Amphibian declines: The conservation status of United States species (M. Lannoo, ed.), Univ. California Press, xxi + 1-1094. Clark, J. G. & J. P. Shoemaker. 1973. Eurycea bislineata (Green), the two-lined salamander, a new host of Myxidium serotinum Kudo & Sprague, 1940 (Myxosporida, Myxidiidae). J. ProtozooL, 20:365-366.
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Coggins, J. R. & R. A. Sajdak. 1982. A survey of helminth parasites in the salamanders and certain anurans from Wisconsin. Proc. HelminthoL Soc, Washington, 49:99-102.
Conant, R. & J. T. Collins. 1998. A Field Guide to Reptiles and Amphibians of Eastern and Central North America, ed. (expanded). Houghton Mifflin, Boston. 616 pp.
Fischthal, J. H. 1955. Ecology of worm parasites in south-central New York. Amer. Midi. Nat, 53:176-183.
Illinois Endangered Species Protection Board, 2006. Endangered and Threatened Species List. One Natural Resources Way. Springfield, Illinois. http://dnr.state.iLus/espb/datelist.htm
Jirku, M., M. G. Bolek, C. M. Whipps, J. Janovy, Jr., M. L. Kent & D. Modry. 2006. A new species of Myxidium (Myxosporea: Myxidiidae), from the western chorus frog, Pseudacris triseriata triseriata, and Blanchard’s cricket frog, Acris crepitans bl anchor di (Hylidae), from eastern Nebraska: Morphology, phylogeny, and critical comments on amphibian Myxidium taxonomy. J. ParasitoL, 92:611-619.
Kudo, R. & V. Sprague. 1940. On Myxidium immersum (Lutz) and M. serotinum n. sp., two myxosporidian parasites of Salientia of South and North America. Rev. Med. Trop. ParasitoL Bacteriol. Clin. Lab., 6:65-73.
McAllister, C. T. & S. E. Trauth. 1995. New host records for Myxidium serotinum (Protozoa: Myxosporea) from North American amphibians. J. ParasitoL, 81:485-488.
McAllister, C. T. & S. J. Upton. 1987. Endoparasites of the smallmouth salamander, Amby stoma texanum (Caudata: Ambystomatidae) from Dallas County, Texas. Proc. HelminthoL Soc. Washington, 54:258-261.
McAllister, C. T., C. R. Bursey & S. E. Trauth. 2008. New host and geographic distribution records for some endoparasites (Myxosporea, Trematoda, Cestoidea, Nematoda) of amphibians and reptiles from Arkansas and Texas, U.S.A. Comp. ParasitoL, 75:241-254.
McAllister, C. T., S. E. Trauth & B. L. J. Delvinquier. 1995. Ultrastmctural observations on Myxidium serotinum (Protozoa: Myxosporea) from Bufo speciosus (Anura: Bufonidae), in Texas. J. HelminthoL Soc. Washington, 62:229-232.
Muzzall, P. M. & D. B. Schinderle. 1992. Helminths of the salamanders Ambystoma t. tigrinum and Ambystoma laterale (Caudata: Ambystomatidae) from southern Michigan. J. HelminthoL Soc, Washington, 59:201-205.
Rankin, J. S., Jr. 1945. An ecological study of the helminth parasites of amphibians and reptiles of western Massachusetts and vicinity. J. ParasitoL, 31:142-150.
CTM at: drctmcallister@aoLcom
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RECORDS OF THE PORCUPINE {ERETHIZON DORSATUM) FROM THE EASTERN MARGINS OF THE EDWARDS PLATEAU OF TEXAS
Amy B. Baird*^ Gregory B* Pauly^ David W* Hall and Travis J. LaDuc
Section of Integrative Biology and Texas Natural Science Center The University of Texas, Austin, Texas 78712 ^Current address:
National Museum of Natural History, P.O. Box 9517,
2300RA Leiden, The Netherlands
During the first half of the 1900s, the porcupine {Erethizon dorsatum) in Texas was restricted to the northernmost Panhandle and parts of the Trans-Pecos (Bailey 1905; Taylor & Davis 1947; Hall & Kelson 1959), By the mid- 1900s, observations suggested that the range was expanding into the southern Panhandle, and onto the western Edwards Plateau (Milstead & Tinkle 1958). Subsequent accumulations of voucher specimens over the past several decades have served to both substantiate these earlier observations and to document the expansion of the porcupine eastward across the southern Rolling Plains (e.g. Tyler & Joles 1997 and Caire et ah 1989 for Oklahoma; Dalquest & Homer 1984 for north-central Texas) and elsewhere across Texas (e.g., Davis 1974; Davis & Schmidly 1994; Use & Hellgren 2001). The species has presently come to occupy most of the western two-thirds of the state (Stangl et al. 1991; Schmidly 2004),
Goetze (1998) documented the occurrence of the porcupine over the western two-thirds of the Edwards Plateau, and the two sight records reported by Milstead & Tinkle (1958) from Mason and Ken- counties remain the southeastemmost records from both the region and the state. This study reports on two specimens that extend the known range of the species to the eastern margin of the Edwards Plateau, a distance of approximately 160 km from the nearest voucher records of Kimble and Concho counties reported by Goetze (1998). Both were salvaged as road-killed animals, and the skulls were retained as vouchers for deposit with the Natural Science
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Research Laboratories of Texas Tech University (TTU). The first specimen (TTU 108417) was taken on 4 January 2003 from Travis County (0.4 mi NE of Hwy. 71 on Southwest Parkway; 30° 16.777’ N, 97° 54.498’ W), and the second (TTU 108416) was taken on 20 January 2007 from Burnet County (1.5 mi E of Llano-Bumet County line on Hwy 71; 30° 30.903’ N, 98° 19.431’ W). Two sightings from as recently as July 2008 on the Brackenridge Field Laboratory, University of Texas campus in Austin, have also been related to the authors by lab personnel as the first evidence of the species locally since the lab’s inception in 1967.
The reported vouchers and recent sight records provide evidence that the porcupine is a viable resident component of the Edwards Plateau. Given the demonstrated ability of E. dorsatum to expand its range in recent decades across the relatively open terrain dominating much of the northwestern parts of Texas, there seems little to impede its eastward progress beyond the Balconian Escarpment, and across the blackland prairies and postoak belt.
We thank David M. Hillis of the University of Texas for assistance in the collection of the Burnet County specimen, and Larry Gilbert, Director of UT Brackenridge Field Laboratory, for providing information and documentation on the porcupine observed there. Specimens were collected under Texas Parks and Wildlife Scientific Permit (SPR-02010-133).
Literature Cited
Bailey, V. 1905. Biological survey of Texas. North American Fauna 25:1-222. Caire, W., J. D. Tyler, B. P. Glass, & M. A. Mares. 1989. Mammals of Oklahoma.
University of Oklahoma Press, Norman, xiii + 567 pp.
Dalquest, W. W., & N. V. Homer. 1984. Mammals of North-Central Texas.
Midwestern State University Press, Wichita Falls, Texas, 254 pp.
Davis, W. B. 1974. The Mammals of Texas. Texas Parks & Wildlife Press, Austin, 294 pp.
Davis, W. B., & D. J. Schmidly. 1994. The Mammals of Texas. Texas Parks & Wildlife Press, Austin, 338 pp.
Goetze, J. R. 1998. The mammals of the Edwards Plateau, Texas. Special Publications, Museum of Texas Tech University, 41:1-263.
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Hall, E. R., & K. R. Kelson. 1959. The Mammals of North America. Ronald Press, New York, 2:viii + 547-1083,
Use, L. M, and E. C. Hellgren. 2001. Demographic and Behavioral Characteristics of North American Porcupines (Erethizon dorsatum) in Pinyon-Juniper Woodlands of Texas. American Midland Naturalist, 146(l):329-338.
Milstead, W. W. and D. W. Tinkle. 1958. Notes on the porcupine {Erethizon dorsatum) in Texas. Southwestern Naturalist, 3(l-4):236-237.
Schmidly, D. J. 2004. The Mammals of Texas, revised edition. University of Texas Press, Austin, 501 pp.
Stangl, Jr., F. B., R. D. Owen, and D. E. Morris-Fuller. 1991. Cranial variation and asymmetry in southern populations of the porcupine, Erethizon dorsatum. Texas Journal of Science, 43 (3): 237-259.
Taylor, W. P., & W. B. Davis. 1947. The mammals of Texas. Texas Game, Fish, and Oyster Commission, Austin, Bull. 27:1-79
Tyler, J. D. & S. Joles. 1997. The Porcupine in Oklahoma. Proceedings, Oklahoma Academy of Science, 77(1): 107-1 10.
ABB at: baird(§nnm.nl
FIRST RECORD OF CYMBOVULA ACICULARIS (GASTROPODA: PROSOBRANCHIA: OVULIDAE) FROM THE COAST OF TAMAULIPAS, MEXICO
Alfonso Correa-Sandoval and Ned E, Strenth
Laboratorio de Zoologia, Instituto Tecnologico de Cd. Victoria,
A.P. 175, C.P. 87010, Cd. Victoria, Tamaulipas, Mexico (ACS) and Department of Biology, Angelo State University,
San Angelo, Texas, 76909
Members of the family Ovulidae are found in warm marine waters as ectoparasites on sea whips and sea fans upon which they feed (Cate 1973; Rosenberg 1989; Redfem 2001). They are largely restricted to the microhabitat provided by their association with the various host species (Abbott & Morris 1995). The shell may be oblong, ftisiform or elongate. The surface is smooth with the aperture extending the length of the shell and it lacks an operculum (Abbott 1974; 1986). Notable among living specimens is the expanded fleshy mantle which covers the shell and exhibits a
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variety of vivid coloration patterns (Keen 1971; Rehder 1981). Species of Ovulidae are known from the American Atlantic coast and exhibit distributions within the Virginian subprovince and Carolinian and Caribbean provinces (Abbott 1974; 1986; Andrews 1992). Five species, Cyphoma gibbosum (Linnaeus), C macgintyi Pilsbry, C allenae (Cate), C intermedium (Sowerby) and Simnialena uniplicata (Sowerby), are currently known from the state of Tamaulipas in Mexico and have been reported from the northern and southern coastal zones (Leal 1978; Fregoso 1986; Perez 1993).
Cymbovula acicularis (Lamarck), has been reported from North Carolina to Brazil, Bermuda and the West Indies (Morris 1975, Warmke & Abbott 1975; Abbott & Morris 1995; Abbott & Dance 1998). Fossil specimens are known from the Pleistocene of South Carolina (Richards 1962). This species is currently known from the western Gulf of Mexico from Texas (Tunnell & Chaney 1970; Ode 1973) south to Veracruz, Yucatan (Vokes & Vokes 1983; Garcia- Cubas & Reguero 2004) and Quintana Roo (Oliva-Rivera & Navarrete 2007). This species, however, has not been previously recorded by prior surveys from the state of Tamaulipas (Fregoso 1986; Perez 1993; Perez-Rodriguez 1997; Rodriguez-Castro et al 2005). This study reports the collection of Cymbovula acicularis from near the village of La Pesca on Barra Soto la Marina (23°42’06'’N and 97°45'00”W) which is located along the central Tamaulipas coast 51 km east of Soto la Marina. This area is approximately 260 km south of the Texas coast, less than 50 km north of the Tropic of Cancer and exhibits a warm-subhumid climate (INEGI 1981). The area exhibits an isotherm with an average annual temperature of 25° C and average salinity of 33.9 ppt (Rodriguez-Castro 2002).
Two specimens of C acicularis were collected during a field trip to the La Pesca area on 9 May 2007. The gastropods were found on specimens of yellow sea whips {Leptogorgia sp.: Gorgoniidae) upon which they are known to both live and feed
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Figure 1. Cymbovula aciciilaris from La Pesca, Tamaulipas, Mexico. Scale = 1 mm.
(Rehder 1981; Britton & Morton 1989). The specimens are deposited in the Malacological Collection of the Institute Tecnologico de Ciudad Victoria (ITCVZ 5021). A second trip to the same site on 6 November, 2007 resulted in the collection of two additional specimens which are also deposited with the Institute Tecnologico de Cd. Victoria collections (ITCVZ 5118).
The four specimens from La Pesca are yellow, elongated, thin and measure 8-17 mm in length (Figure 1). The aperture extends along the total length of the shell; the lip is thin and sharp. Columella with an opaque anterior thickening and with punctuations. Columellar area flattned. Surface brilliant, with spirals growth lines, more or less equidistant, slightly irregular towards the posterior area of the shell. The morphology of these specimens agrees with the descriptions of Redfem (2001) and Garcia-Cubas & Reguero (2004).
This record of C. acicularis from La Pesca brings the total number of marine gastropods reported from the state of Tamaulipas to 165. This is second only to Yucatan in the total number of reported species among those states in Mexico which border the Gulf of Mexico.
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Acknowledgments
We wish to thank Fred G. Thompson for both his response and assistance to our request during this study for an examination of the Collection of Mollusks of the Florida Museum of Natural History, University of Florida, in Gainesville, Florida. Special appreciation is extended to Dr. Martha Reguero of the Universidad Nacional Autonoma de Mexico and Dr. Fabio Moretzsohn of the Harte Research Institute at TAMU-Corpus Christi for suggestions that greatly improved this manuscript. Also to Anabel Gutierrez for her assistance in the preparation of the manuscript and to Gonzalo Guevara for the preparation of figure 1.
Resumen.-El gastropodo marino Cymbovula acicularis es registrado por primera vez para la malacofauna de Tamaulipas, Mexico.
Literature Cited
Abbott, R. T. 1974. American Seashells. Van Nostrand Reinhold. New York, 663 pp.
Abbott, R. T. 1986. Seashells of North America. A Guide to Field Identification. St. Martin’s Press. New York, 280 pp.
Abbott, R. T. & P. A. Morris. 1995. A Field Guide to Shells of the Atlantic and Gulf Coast and the West Indies. Houghton Mifflin. New York, 350 pp.
Abbott, R. T. & S. P. Dance. 1998. Compendium of Seashells. Odyssey Publishing. China, 41 1 pp.
Andrews,!. 1992. A Field Guide to Shells of the Texas Coast. Gulf Publishing Company. Houston, Texas, 176 pp.
Britton, J. C. & B. Morton. 1989. Shore Ecology of the Gulf of Mexico. University of Texas Press. Austin, Texas, 387 pp.
Cate, C. N. 1973. A Systematic Revision of the Recent Cypraeid Family Ovulidae (Mollusca, Gastropoda). The Veliger 15 (Supplement): 1-1 16.
Fregoso, J. A. 1986. Contribucion al conocimiento de la fauna malacoldgica de la costa del Estado de Tamaulipas, Mexico. Tesis Licenciatura. Escuela de Ciencias Bioldgicas. Universidad del Noreste, Tampico, Tamaulipas, 133 pp.
Garcia-Cubas, A. & M. Reguero. 2004. Catalogo ilustrado de moluscos gasteropodos del Golfo de Mexico y Mar Caribe. Instituto de Ciencias del
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Mar y Limnologia. Universidad Nacional Autonoma de Mexico. Mexico, D. F., 171 pp.
INEGI. 1981. Instituto Nacional de Estadistica, Geografia e Informatica. Carta de Climas. Esc. 1:1000,000. Secretaria de Programacion y Presupuesto. Mexico, D.F.
Keen, A. M. 1971. Sea Shells of Tropical West America. Stanford University Press. Stanford, California, 1064 pp.
Leal, L. 1978. Estudio taxonomico de los moluscos marines (Gastropoda- Pelecypoda) representtativos de la region de Soto la Marina, Tamaulipas, Mexico. Tesis Licenciatura. Facultad de Ciencias Biologicas. Universidad Autonoma de Nuevo Leon. San Nicolas de Los Garza, Nuevo Leon, 107 pp,
Morris, P. A. 1975. A Field Guide to Shells of the Atlantic and Gulf Coast and the West Indies. Houghton Mifflin. Boston, Massachusetts, 330 pp.
Oliva-Rivera, J. J. & A. de Navarrete. 2007. Larvas de moluscos gasteropodos del Sur de Quintana Roo, Mexico. Hidrobiologica 17(2):151-158.
Ode, H. 1973. A survey of the molluscan fauna of the northwest Gulf of Mexico - preliminary report (continued). Texas Conchologist 9: 60-72.
Perez, F. A. 1993. Contribucidn al conocimiento de los gasteropodos (Mollusca: Gastropoda) de la costa de Tamaulipas, Mexico. Tesis Licenciatura. Escuela de Biologia. Universidad del Noreste. Tampico, Tamaulipas, 144 pp.
Perez-Rodriguez, R. 1997. Moluscos de la plataforma continental del Atlantico Mexicano. Universidad Autonoma Metropolitana-Xochimilco. Mexico, D. F., 260 pp.
Redfem, C. 2001. Bahamian Seashells. A Thousand Species from Abaco, Bahamas. Bahamianseashells.com. Boca Raton, Florida, 280 pp.
Rehder, H. A. 1981. National Audubon Society Field Guide to North American Seashells. Alfred A. Knopf New York, 894 pp.
Richards, G. H. 1962. Studies on the Marine Pleistocene: The Marine Pleistocene of the Americas and Europe; The Marine Pleistocene Mollusks of Eastern North America. Trans. Am. Phil. Soc., New Series 52(3): 1-141.
Rodriguez-Castro, J. H. 2002. Sistematica y zoogeografia de los gastropodos y bivalvos marinos de la costa del Estado de Tamaulipas, Mexico. Tesis Maestria en Ciencias. Instituto Tecnologico de Cd. Victoria. Cd. Victoria, Tamaulipas, 248 pp.
Rodriguez-Castro, J. H., A. Correa-Sandoval & N. Strenth. 2005. Gastropodos marinos de Tamaulipas: Pp. 88-96, in: Biodiversidad Tamaulipeca Vol. 1. L. Barrientos, A. Correa-Sandoval, J. V. Horta and J. Garcia (Editors). Instituto Tecnologico de Cd. Victoria. Cd. Victoria, Tamaulipas, 272 pp.
Rosenberg, G. 1989. Aposematism evolves by individual selection: evidence from marine gastropods with pelagic larvae. Evolution, 43(8): 1811-1813.
Tunnell, J. W., Jr. & A. H. Chaney. 1970. A checklist of mollusks of Seven and One-Half Fathom Reef, northwest Gulf of Mexico. Contributions in Marine Science, 15: 193-203.
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Yokes, H. E. & E. H. Yokes. 1983. Distribution of Shallow-water Marine Mollusca, Yucatan Peninsula, Mexico. Middle American Research Institute, Publication 54. Tulane University, New Orleans, 183 pp.
Warmke, G. L. & R. T. Abbott. 1962. Caribbean Seashells. Dover Publications. New York, 348 pp.
AC-S at: agutierr@uat.edu.mx
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Manuscripts intended for publication in the Journal should follow these guidelines and be submitted in TRIPLICATE to:
Dr. Frederick B. Stangl, Jr.
TJS Manuscript Editor Department of Biology Midwestern State University Wichita Falls, Texas 76308
www.texasacademyofscience.org
INSTRUCTIONS TO AUTHORS
Scholarly manuscripts reporting original research results in any field of science or technology, including science education, will be considered for publication in The Texas Journal of Science. Prior to acceptance, each manuscript will be reviewed by both knowledgeable peers and the editorial staff Authors are encouraged to suggest the names and addresses of two potential reviewers to the Manuscript Editor at the time of submission of their manuscript. No manuscript submitted to the Journal is to have been published or submitted elsewhere. Excess authorship is discouraged. Manuscripts listing more than four authors will be returned to the corresponding author.
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Except for the corresponding author's address, manuscripts must be double-spaced throughout (including legends and literature cited) and submitted in TRIPLICATE (typed or photocopied) on 8.5 by 11 inch bond paper, with margins of approximately one inch and pages numbered. Scientific names of species should be placed in italics. Computer generated manuscripts must be reproduced as letter quality or laser prints. Do not justify the right margin. Do not break words at the right margin. The text can be subdivided into sections as deemed appropriate by the author(s). Possible examples are: Abstract; Materials and Methods; Results; Discussion; Summary or Conclusions; Acknowledgments; Literature Cited. Major internal headings are centered and capitalized.
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THE TEXAS JOURNAL OF SCIENCE— VOL. 61, NO. 1, 2009
PAGE ONE
Do not use a title page. Type (single space) the following information within the margins of the upper left of the first page:
PLEASE CORRESPOND WITH:
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The centered title of the article (usually 15 words or less) should be followed by the name(s) of the author(s) and institutional or business address(es), including zip-code (all centered).
Titles which include the scientific name(s) of species should contain sufficient information to alert the average reader (or abstracting service) as to what organism is discussed in the paper. The inclusion of only a scientific name is often insufficient. Instead, the author is encouraged to include a common name or the name of a higher taxonomic category (or combination of categories) in conjunction with the scientific name. The author should select names that will be recognizable by a majority of readers of the Journal.
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THE TEXAS JOURNAL OF SCIENCE— VOL. 61, NO. 1, 2009
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INTRODUCTION
Do not use the word “Introduction” as a heading. Introductory information is self evident and thus needs no heading. Instead, place a two- inch bar or line between the end of the abstract and the first sentence of the introductory comments.
REFERENCES
Cite all references in text by author and date in chronological (not alphabetical) order; Jones (1971); Jones (1971; 1975); (Jones 1971); (Jones 1971; 1975); (Jones 1971; Smith 1973; Davis 1975); Jones (1971); Smith (1973); Davis (1975); Smith & Davis (1985); (Smith & Davis 1985). If more than two authors, use Jones et al. (1976) or (Jones et al. 1976). Citations to publications by the same author(s) in the same year should be designated alphabetically (1979a; 1979b).
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Journal abbreviations in the Literature Cited section should follow those listed in BIOSIS Previews ® Database (ISSN: 1044-4297). This volume is present in all libraries receiving Biological Abstracts. Ask your interlibrary loan officer or head librarian. If not available, then use standard recognized abbreviations in the field of study. Be certain that all citations in the text are included in the Literature Cited section and vice versa.
Consecutively-paged journal volumes and other serials should be cited by volume, number and pagination. Serials with more than one number and that are not consecutively paged should be cited by number as well (Smithson. Misc. Coll., 37(3): 1-30). The following are examples of a variety of citations:
JOURNALS & SERIALS.-
Jones, T. L. 1971. Vegetational patterns in the Guadalupe Mountains, Texas. Am. J. Bot., 76(3):266-278.
Smith, J. D. 1973. Geographic variation in the Seminole bat, Lasiurus seminolus. J. Mammal., 54(l):25-38.
Smith, J. D. & G. L. Davis. 1985. Bats of the Yucatan Peninsula. Occas. Pap. Mus., Texas Tech Univ., 97:1-36.
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THE TEXAS JOURNAL OF SCIENCE— VOL. 61, NO. 1, 2009
BOOKS.-
Jones, T. L. 1975. An introduction to the study of plants. John Wiley & Sons, New York, xx+386 pp.
Jones, T. L., A. L. Bain & E. C. Bums. 1976. Grasses of Texas. Pp. 205- 265, in Native grasses of North America (R. R. Dunn, ed.), Univ. Texas Studies, 205 :xx+ 1-630.
UNPUBLISHED.-
Davis, G. L. 1975. The mammals of the Mexican state of Yucatan.
Unpublished Ph.D. dissertation, Texas Tech Univ., Lubbock, 396 pp.
In the text of the manuscript, the above unpublished reference should be cited as Davis (1975) or (Davis 1975). Do not make citations to unpublished material that cannot be obtained nor reviewed by other investigators (such as unpub. or unpub. field notes).
The citation "in press" must be accompanied by the title of the journal, as well as a volume number and year of expected publication; otherwise the reference will be deleted from the manuscript. The citation "in prep." is unacceptable and will be deleted from the manuscript. "Unpublished results" or material should be referenced to the source of the individual as (Jones pers. comm.). The name of the individual and their professional institution should then be given the "Acknowledgments" section of the manuscript.
VOUCHER SPECIMENS
When appropriate, such as new records, noteworthy range extensions, or faunal or floral listings for an area, the author(s) should provide proper information (to include accession numbers) relative to the deposition of voucher specimens. Specimens should be placed with the holdings of a recognized regional or national museum or herbarium. The name(s) and designated initials used by the museum should be given as part of the introduction or methods section. Do not site the deposition of voucher specimens in personal collections.
The Editorial Staff is very aware that many members of the Academy work with organisms that are protected by state or federal regulations. As such, it may not be possible to collect nor deposit these specimens as vouchers. In the interest of maintaining credibility, authors are expected to
THE TEXAS JOURNAL OF SCIENCE— VOL. 61, NO. 1, 2009
77
provide some alternate means of verification such as black and white photographs, list of weights or measurements, etc. The Editorial Staff retains the option to determine the validity of a record or report in the absence of documentation with a voucher specimen.
GENERAL NOTES
A section for noteworthy but short contributions may appear at the end of each issue of the Journal Manuscripts published as “General Notes” normally will not exceed four or five typed pages in final print. The format is the same as for feature articles except no abstract is included and the only subheading in the text is a centered “Literature Cited” unless additional subheadings are deemed necessary. While the decision as to whether a manuscript is best suited for a feature article or a note will be made by the editorial staff, authors are encouraged to indicate their preference at the time the manuscript is submitted to the Manuscript Editor.
GRAPHICS, FIGURES & TABLES
All tables must be included as a computer generated addendum or appendix of the manuscript. Computer generated figures and graphics must be laser quality and camera ready, reduced to 5.5 in. (14 cm) in width and not exceed 8.5 in. (20.5 cm) in height. Shading is unacceptable. Instead, use different and contrasting styles of crosshatching, grids, line tints, dot size, or other suitable matrix to denote differences in graphics or figures. Figures, maps and graphs should be reduced to the above graphic measurements by a photographic method. A high contrast black and white process known as a PMT or Camera Copy Print is recommended. Authors unable to provide reduced PMT's should submit their originals. Figures and graphs which are too wide to be reduced to the above measurements may be positioned sideways. They should then be reduced to 9 in. (23 cm) wide and 5 in. (12.5 cm) in height. Black and white photographs of specimens, study sites, etc. should not exceed 8 in. in width and be mounted on 8.5 by 11 in. paper or backing. Color photographs cannot be processed at this time. Each figure should be marked on the back with the name of the author(s) and figure number. If confiision might result as to arrangement of a figure, label "top". All legends for figures and tables must be typed (double-spaced) on a sheet(s) of paper separate from the text. All figures must be referred to in text as "Figure 3" or "(Fig,3)"; all tables as "Table 3" or "(Table 3)".
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THE TEXAS JOURNAL OF SCIENCE— VOL. 61, NO. 1, 2009
GALLEY PROOFS & REPRINTS
The corresponding author will receive galley proofs in PDF format prior to the final publishing of the manuscript. Corrections in electronic format are to be returned to the Managing Editor within five days; failure to promptly return corrections to the galley proofs may result in delay of publication. The Academy will provide a PDF and a limited number of reprints without charge for each feature article or note published in the Journal. Reprints will be mailed to the corresponding author or other such designated contact person following the publishing of each issue of the Journal. The distribution of reprints among co-authors is the responsibility of the corresponding author.
PAGE CHARGES
Page charges will be waived on manuscripts in which all authors (one to four) are members of the Texas Academy of Science in good standing at the time of the original submission to the Manuscript Editor. These manuscripts will be published with the customary PDF and a limited number of reprints provided to the corresponding author without charge. As in the past - those authors with institutional or grant support are requested to support these page charges in part or whole when possible.
For manuscripts authored by non-members or a combination of members and non-members - authors are required to pay $50 per printed page. Members of the Academy are, however, allowed four published pages per year free of charge on these publications - full payment is required for those pages in excess of four. Non-members of the Academy are required to pay full page charges for all pages. The Academy, upon written request, will subsidize a limited number of contributions per volume. These exceptions are, however, generally limited to students, post docs or foreign authors without financial support. Should a problem arise relative to page charges, please contact Dr. Ned E. Strenth (ned.strenth@angelo.edu) at Angelo State University.
These guidelines have been prepared in an effort to both reduce the amount of editorial revision and to speed the process by which your manuscript is ultimately published. All questions relating to manuscripts cannot possibly be covered in this one set of guidelines. Should questions
THE TEXAS JOURNAL OF SCIENCE— VOL. 61, NO. 1, 2009
79
arise, then please review the most recent issues of the Journal or contact the Editorial Staff. Thank you for considering the Texas Journal of Science.
Dr. Ned E. Strenth TJS Managing Editor Department of Biology Angelo State University San Angelo, Texas 76909
TJS Manuscript Editor Department of Biology
Midwestern State University Wichita Falls, Texas 76308 frederick.stangl@mwsu.edu
ned. strenth@angelo . edu
An expanded version of the above author guidelines (which includes instructions on style, title and abstract preparation, deposition of voucher specimens, and a listing of standardized abbreviations) is available on the Academy's homepage at:
www.texasacademyofscience.org
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THE TEXAS JOURNAL OF SCIENCE— VOL. 61, NO. 1, 2009
THE TEXAS ACADEMY OF SCIENCE
www.texasacademyofscience.org
Membership Information and Application
MEMBERSHIP -Any person or member of any group engaged in scientific work or interested in the promotion of science is eligible for membership in The Texas Academy of Science.
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THE TEXAS ACADEMY OF SCIENCE, 2008-2009
OFFICERS
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DIRECTORS
2006 Herbert D. Grover, Wayland Baptist University Gary P. Garrett, Texas Parks and Wildlife Department
2007 Renard L. Thomas, Texas Southern University Bob Murphy, Texas Parks and Wildlife Department
2008 Christopher M. Ritzi, Sul Ross State University Andrew C. Kasner, Audubon Texas
SECTIONAL CHAIRPERSONS
Anthropology: Raymond Mauldin, University of Texas at San Antonio Biomedical: G. Scott Weston, University of the Incarnate Word Botany: Joan Hudson, Sam Houston State University
Cell and Molecular Biology: Magaly Rincon-Zachary, Midwestern State University
Chemistry and Biochemistry: Benny E. Amey, Jr., Sam Houston State University
Computer Science: James McGuffee, St. Edward’s University
Conservation Ecology: Cathy Early, University of Mary Hardin Baylor
Environmental Science: Kenneth R. Summy, University of Texas-Pan American
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Geosciences: Joseph I. Satterfield, Angelo State University
Marine Sciences: Larry D. McKinney, Harte Research Institute
Mathematics: Elsie M. Campbell, Angelo State University
Physics: David L. Bixler, Angelo State University
Science Education: R. Russell Wilke, Angelo State University
Systematics and Evolutionary Biology: Allan W. Hook, St. Edward’s University
Terrestrial Ecology and Management: Christopher M. Ritzi, Sul Ross State University
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Collegiate Academy: David S. Marsh, Angelo State University Junior Academy: Vince Schielack, Texas A&M University
Raymond C. Mathews, Jr., Texas Water Dev. Board
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Benjamin A. Pierce, Southwestern University
Hudson R. DeYoe, University of Texas-Pan American
Fred Stevens, Schreiner University
Diane B. Hyatt, Texas Water Development Board
Ned E. Strenth, Angelo State University
Frederick B. Stangl, Jr., Midwestern State University
John A. Ward, Brooke Army Medical Center
James W. Westgate, Lamar University
Armando J. Contreras, Universidad Autonoma de N.L.
PERIODICALS
THE TEXAS JOURNAL OF SCIENCE Texas Academy of Science CMB 6252 Schreiner University Kerrville, Texas 78028-5697
r(y
M V|
THE
TEXAS JOURNAL
OF
SCIENCE
GENERAL INFORMATION
MEMBERSHIP -Any person or member of any group engaged in scientific work or interested in the promotion of science is eligible for membership in The Texas Academy of Science. For more informa¬ tion regarding membership, student awards, section chairs and vice¬ chairs, the annual March meeting and author instructions, please ac¬ cess the Academy’s homepage at:
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Dues for regular members are $30.00 annually; supporting mem¬ bers, $60.00; sustaining members, $100.00; patron members, $150.00; associate (student) members, $15.00; family members, $35.00; affili¬ ate members, $5.00; emeritus members, $10.00; corporate members, $250.00 annually. Library subscription rate is $50.00 annually.
The Texas Journal of Science is a quarterly publication of The Texas Academy of Science and is sent to most members and all sub¬ scribers. Payment of dues, changes of address and inquiries regarding missing or back issues should be sent to:
Dr. Fred Stevens, Executive Secretary The Texas Academy of Science CMB 6252 Schreiner University Kerrville, Texas 78028-5697 E-mail: FStevens@schremer.edu
The Texas Journal of Science (ISSN 0040-4403) is published quarterly at Lawrence, Kansas (Allen Press), U.S.A. Periodicals postage paid at San Angelo, Texas and additional mailing offices. POSTMASTER: Send address changes and returned copies to The Texas Journal of Science, Dr. Fred Stevens, CMB 6252, Schreiner University, Kerrville, Texas 78028-5697, U.S.A. The known office of publication for The Texas Journal of Science is the Department of Biology, Angelo State University, San Angelo, Texas 76909; Dr. Ned E. Strenth, Managing Editor.
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THE TEXAS JOURNAL OF SCIENCE
Volume 61, No. 2 May, 2009
CONTENTS
Vegetation of South Padre Island, Texas: Freshwater and Brackish Wetlands.
By Frank W. Judd and Robert 1. Lonard. . . . . . . . 83
Seasonal Trophic Ecology of the White- Ankled Mouse, Peromyscus pectoralis (Rodentia: Muridae) in Central Texas.
By John T. Baccus, John M. Hardwick, David G. Huffman
and Mark A. Kainer . . . . . 97
Changes In Vegetation Patterns and their Effect on Texas Kangaroo Rats (Dipodomys el at or).
By Allan D. Nelson, Jim R. Goetze, Elizabeth Watson
and Mark Nelson . . 119
Breeding Biology of the Bam Swallow (Hirundo rustic a) in Northeast Texas with Temporal and Geographic Comparisons to other North American Studies.
By K. T. Turner and J. G. Kopachena . . . . 131
General Notes
Reproductive Cycle of the Central American Mabuya,
Mabiiya unimarginata (Squamata: Scincidae) from Costa Rica.
By Stephen R. Goldberg . . . . . 147
New Geographic Distribution Records for Parajulid Millipeds (Diplopoda: Julida), in Arkansas and Texas.
By Chris T. McAllister and Henry W. Robison . . . . 151
Noteworthy Records of Dragonflies (Odonata: Anisoptera) From Jones and Taylor counties of Central Texas.
By Thomas E. Lee, Jr., Amisha J. Patel, Benjamin W. Johnson and Roy C. Vogtsberger
157
THE TEXAS JOURNAL OF SCIENCE EDITORIAL STAFF
Managing Editor:
Ned E. Strenth, Angelo State University Manuscript Editor:
Frederick B. Stangl, Jr., Midwestern State University Associate Editors:
Allan D. Nelson, Tarleton State University Jim R. Goetze, Laredo Community College Associate Editor for Botany:
Janis K. Bush, The University of Texas at San Antonio Associate Editor for Chemistry:
John R. Villarreal, The University of Texas-Pan American Associate Editor for Computer Science:
Nelson Passos, Midwestern State University Associate Editor for Geology:
Ernest L. Lundelius, University of Texas at Austin Associate Editor for Mathematics and Statistics:
E. Donice McCune, Stephen F. Austin State University
Manuscripts intended for publication in the Journal should be submitted in TRIPLICATE to:
Dr. Allan D. Nelson Department of Biological Sciences Tarleton State University Box T-OlOO
Stephenville, Texas 76402 nelson@tarleton.edu
Scholarly papers reporting original research results in any field of science, technology or science education will be considered for publication in The Texas Journal of Science. Instructions to authors are published one or more times each year in the Journal on a space-available basis, and also are available on the Academy's homepage at:
www.texasacademyofscience.org
AFFILIATED ORGANIZATIONS American Association for the Advancement of Science,
Texas Council of Elementary Science Texas Section, American Association of Physics Teachers Texas Section, Mathematical Association of America Texas Section, National Association of Geology Teachers Texas Society of Mammalogists
TEXAS J. OF SCI. 61(2):83-96
MAY, 2009
VEGETATION OF SOUTH PADRE ISLAND, TEXAS: FRESHWATER AND BRACKISH WETLANDS
Frank W. Judd and Robert 1. Lonard
Department of Biology, University of Texas- Pan American Edinburg, Texas 78541
Abstract -Species composition and importance, species richness, species diver¬ sity, and evenness were compared among 14 freshwater and brackish wetlands in the secondary dunes and vegetated flats topographic zone of South Padre Island, Texas. Twenty-four different species were found among the sites, but the greatest species richness at a site was only 14. Mean species diversity was 0.855 and mean evenness was 0.797. Both parameters showed little variability among sites. South Padre Island wetlands had significantly lower species richness and species diversity than freshwater and brackish marshes of the adjacent Texas mainland. Conversely, evenness was similar among island and mainland wetlands. Most of the island wetlands shared 62% to 67% of their species and similarity in species composition was significantly greater for island wetlands than mainland wetlands. Bulrush (Schoenoplectus pungens) was the dominant species at nine wetlands. Umbrella grass (Fiiirena simplex) and marshhay cordgrass {Spartina patens) each were dominant in two wetlands. Bushy bluestem {Andropogon glomeratus) was dominant in one wetland. Bie meager data currently available suggests that species richness of wetland communities is similar on northern and southern portions of Padre Island, but similarity in species composition is modest. Species importance in wetland communities varies markedly between northern and southern areas of Padre Island.
The most conspicuous physiographic feature along the Gulf of Mexico coastline of Texas is a series of five barrier islands that enclose several shallow bays. The flora and vegetation of South Padre Island are relatively well known compared to other areas of the barrier island chain (Dahl et al. 1974; Judd et al. 1977; Lonard et al. 1978; Lonard & Judd 1980; Lonard & Judd 1981; Judd & Sides 1983; Judd & Lonard 1985; Judd & Lonard 1987; Judd et al. 1989; Lonard & Judd 1989; Judd et al. 1991; Lonard et al. 1991; Everitt et al. 1991; Everitt et al. 1992; Lonard & Judd 1993; Judd et al. 1994; Lonard & Judd 1997; Judd et al. 1998; Lonard & Judd 1999; Everitt et al. 1999; Lonard et al. 1999; Judd et al. 2007) but little is known of the composition of freshwater and brackish wetland communities on South Padre Island or any of the other Texas barrier islands.
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THE TEXAS JOURNAL OF SCIENCE-VOL. 61, NO. 2, 2009
Judd et al. (1977) reported that dense meadows of fresh water marsh communities occurred within the secondary dunes and vegetated flats topographic zone of South Padre Island and identified five common species. Similarly, Lonard et al. (1999) commented that depressions that often support development of marsh communities occur frequently in the secondary dunes and vegetated flats topographic zone. These wetland plant communities were said to be dominated by a combination of sedges and grasses including Scirpus pungens (= Schoenoplectus pungens), Spartina patens^ Fimbristylis castanea, Fuirena simplex and Rhynchospora color ata by Lonard et al. (1999). Thus, the only information available is a partial list of species that occur in the wetlands of South Padre Island. A complete list of species for even one wetland is lacking and there is no information on the abundance of the species comprising a wetland community or the fidelity of species among wetland sites. Consequently, a quantitative comparison of wetland communities at 14 sites on South Padre Island is provided herein to rectify these insufficiencies in the knowledge of the vegetation of South Padre Island.
Materials and Methods
The locations of wetland communities studied are given in Table 1. Four of the 14 sites contained standing water at the time of sampling. Salinity was recorded at each of the four sites using a temperature compensated hand-held refractometer (Table 1). Marshes were considered freshwater if salinity was 0.0 to 0.5 ppt and brackish if salinity was 0.5 to 17.0 ppt .
The line intercept method (Canfield 1941) was used to quantify species abundance. Seventy meters of transects were sampled at each site. Each transect was divided into 10 m intervals and readings were taken along the length of each interval. First, the total cover of dead vegetation intercepted was recorded without regard to species. For live vegetation, each species intercepted by the line was rated individually without separation into strata. Species and foliage cover were recorded and from these data the
JUDD «& LONARD
85
Table 1. Study site locations, dates of sampling, and mean salinity of sites with standing water.
Site Location Sample Date Mean Salinity (ppt)
|
1 |
26°09’43.26” |
'N, |
97°10’27.49” |
' W |
5-21-07 |
dry |
|
2 |
26°10’13.16” |
'N, |
97°10’32.18” |
w |
5-21-07 |
dry |
|
3 |
26°13’00.52” |
'N, |
97°10’56.16” |
w |
6-14-07 |
dry |
|
4 |
26°13’04.89” |
N, |
97°10’57.26” |
w |
6-14-07 |
dry |
|
5 |
26°13’25.55” |
N, |
97°10’57.67” |
w |
5-21-07 |
2.0 |
|
6 |
26°14’22.16” |
N, |
97°11’ 10.28” |
w |
8-4-07 |
0.0 |
|
7 |
26°14’28.30” |
N, |
97°11’09.16” |
w |
9-24-07 |
5.5 |
|
8 |
26°14’47.10” |
N, |
97°11’14.44” |
w |
9-24-07 |
dry |
|
9 |
26°17^03.69” |
N, |
97°11 ’45.26” |
w |
11-5-07 |
dry |
|
10 |
26° 17’ 5 1.20” |
N, |
97°11’55.86” |
w |
11-5-07 |
dry |
|
11 |
26°19’ 12.36” |
N, |
97°12’1L11” |
w |
3-26-08 |
diy |
|
12 |
26°19’29.37” |
N, |
97°12’2L68” |
w |
3-26-08 |
12.0 |
|
13 |
26°20’44.42” |
N, |
97°12’36.77” |
w |
3-27-08 |
dry |
|
14 |
26°21’33.38” |
N, |
97°12’48.32” |
w |
3-27-08 |
dry |
frequency of occurrence, relative frequency, relative cover and an importance value, which is the sum of relative frequency and relative cover, were calculated. The importance value was used to determine dominant species.
Similarity of species composition among wetland sites was calculated using Sorensen’s Coefficient of Community (Krebs 1999). Species importance value was used as the measure of abundance for calculating species diversity indices. Species diversity was assessed using the Shannon diversity index (Brower et al. 1998; Krebs 1999). Evenness was determined as the ratio of heterogeneity (H’) to maximum heterogeneity (H’ max) (Brower et al. 1998; Krebs 1999). Nomenclature and common names follow Jones &Wipff (2003).
Results
Study sites were located in the southern two-thirds of South Padre Island along a south to north axis in the secondary dune and vegetated flats topographic zone (Judd et al. 1977). Distance between successive study locations ranged from 120 m to 5,010 m (mean = 1,846.6 m, SD = 1,764.9 m). Twenty-four different species were found in the 14 sites sampled (Table 2). Twenty of
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THE TEXAS JOURNAL OF SCIENCE-VOL. 61, NO. 2, 2009
Table 2. Species present, their periodicity, growth form and percent occurrence among sites.
|
Species |
Periodicity |
Growth Form |
% Occurrence |
|
Andropogon glomeratiis |
Perennial |
Grass |
78.6 |
|
Eragrostis secimdiJJora |
Perennial |
Grass |
7.1 |
|
Panicum amariim |
Perennial |
Grass |
57.1 |
|
Paspalum monostachyum |
Perennial |
Grass |
64.3 |
|
Schizachyriwn littorale |
Perennial |
Grass |
50.0 |
|
Spartina patem |
Perennial |
Grass |
71.4 |
|
Sporobolus airoides |
Perennial |
Grass |
14.3 |
|
Sporohohis virginicus |
Perennial |
Grass |
71.4 |
|
Eleocharis geniculata |
Annual |
Sedge |
42.9 |
|
Fimbristylis castanea |
Perennial |
Sedge |
21.4 |
|
Fuirena simplex |
Perennial |
Sedge |
85.7 |
|
Rhynchospora colorata |
Perennial |
Sedge |
57.1 |
|
Schoenoplectus pungens |
Perennial |
Sedge |
92.9 |
|
Typha domingensis |
Perennial |
Cattail |
14.3 |
|
Agalinus sp. |
Annual |
Broad-leaved herbaceous |
28.6 |
|
Bacopa monnieri |
Perennial |
Broad-leaved herbaceous |
21.4 |
|
Blutaparon vermiciilare |
Perennial |
Broad-leaved herbaceous |
7.1 |
|
Borrichia frutescens |
Perennial |
Broad-leaved suffrutescent |
35.7 |
|
Conoclinium betonicifolium |
Perennial |
Broad-leaved herbaceous |
92.9 |
|
Flaveria brownii |
Annual |
Broad-leaved herbaceous |
7.1 |
|
Iva texensis |
Annual |
Broad-leaved herbaceous |
100.0 |
|
Lythnim alatum |
Perennial |
Broad-leaved herbaceous |
21.4 |
|
Samolus ebracteatus |
Perennial |
Broad-leaved herbaceous |
71.4 |
|
Sol id ago sempervirens |
Perennial |
Broad-leaved herbaceous |
78.6 |
the species were perennials and four were annuals. Eight species were grasses, five were sedges, 10 were broad-leaved herbaceous species and one species was a cattail (Table 2). No woody species were found. Thirteen of the species occurred in more than half of the sites and Iva texensis (sumpweed) was present at each site. Conoclinium betonicifolium (mist flower) and Schoenoplectus pungens (bulrush) each occurred in all but one of the wetlands (92.9%).
Sampling at Site 1 produced 14 species (58.3% of the total). Site 2 added four new species and resulted in 75% of the total for the 14 sites. After Site 2, no more than a single species was added
JUDD & LONARD
87
at a site. Sampling through Site 9 produced 95.8% of the total species and only a single new species was added thereafter (at Site 12).
Species richness at the wetland sites ranged from 7 to 14 and 1 1 of the wetlands (78.6%) had 12 or more species (Table 3). Mean species richness was 11.9 (SD = 2.17) and the 95% confidence interval ranged from 10.6 to 13.2. Species diversity values ranged from 0.533 to 1.005 (Table 3). Mean species diversity was 0.855 (SD = 0.134) and the 95% confidence interval extended from 0.778 to 0.932. Evenness showed even less variation (Table 3). The mean was 0.797 (SD = 0.084) and the 95% confidence interval ranged from 0.750 to 0.844.
Judd & Lonard (2004) provide data on species richness, species diversity, and evenness in freshwater, brackish, and saltwater marshes in the Rio Grande Delta of the Texas mainland adjacent to South Padre Island. The means for freshwater and brackish marshes were calculated from their data and compared with the means for these parameters in the South Padre Island wetlands. Six mainland freshwater marshes had a mean species richness of 25.3 (SD = 6.25), mean species diversity of 1.394 (SD = 0.120), and mean evenness of 0.788 (SD = 0.05). Nine mainland brackish marshes had a mean species richness of 17.9 (SD = 5.578), mean species diversity of 1.262 (SD = 0.184) and mean evenness of 0.783 (SD = 0.056). South Padre Island wetlands had significantly lower species richness than both freshwater (t = 7.279, df, P < 0.001) and brackish (t = 3.656, 2\ df, P < 0.01) mainland marshes. Likewise, South Padre Island wetlands had significantly lower species diversity than mainland freshwater marshes (t = 8.502, 18 df,P< 0.001) or mainland brackish marshes (t = 5.700, 21 df^P< 0.001). However, there was no significant difference in evenness between South Padre Island wetlands and either mainland freshwater marshes (/ = 0.243, df, P > 0,5) or mainland brackish marshes (t = 0.44, 21 df,P> 0.5).
88
THE TEXAS JOURNAL OF SCIENCE-VOL. 61, NO. 2, 2009
Table 3. Comparison of species ricliness (N), species diversity (H’), and evenness (J’) among wetlands on South Padre Island, Texas.
|
Wetland |
N |
H’ |
J’ |
|
1 |
14 |
1.005 |
0.877 |
|
2 |
13 |
0.787 |
0.708 |
|
3 |
13 |
0.848 |
0.761 |
|
4 |
12 |
0.947 |
0.878 |
|
5 |
14 |
1.001 |
0.873 |
|
6 |
12 |
0.876 |
0.812 |
|
7 |
14 |
0.918 |
0.801 |
|
8 |
13 |
0.809 |
0.726 |
|
9 |
13 |
0.994 |
0.892 |
|
10 |
10 |
0.899 |
0.899 |
|
11 |
12 |
0.775 |
0.719 |
|
12 |
8 |
0.667 |
0.738 |
|
13 |
7 |
0.533 |
0.631 |
|
14 |
12 |
0.904 |
0.838 |
Similarity in species composition among marshes was high (Table 4) with coefficients for 91 pair-wise comparisons ranging from 0.300 to 0.857. The mean coefficient of similarity was 0.644 (SD = 0.138) and the 95% confidence interval of the mean ranged from 0.615 to 0.673. Most of the wetlands shared 62% to 67% of their species. The similarity is significantly greater (t = 9.499,104 df,P< 0.001) than the mean of 0.322 {SD = 0.116) for 15 coefficients of freshwater marshes and the mean of 0.258 {SD = 0.123) for 36 coefficients of brackish water mainland marshes {t = 16.176, 125 df,P< 0.001) reported for the adjacent Texas mainland by Judd & Lonard (2004).
Cover of dead plant material ranged from 17.1% to 97.3% among the sites. The mean was 67.4% {SD = 26.1). Cover of live plants ranged from 27.4% to 80.5% and the mean was 56.9% {SD = 22.7). Much of the dead and live plant material overlapped, but relatively little of the surface was bare. The top three species in importance were abundant in both frequency (range 57.1% to 100%) and cover. The sum of the relative cover for the top three species in importance at a site ranged from 63.5% to 97.7%. The other species present at a site contributed little to the abundance of
JUDD & LONARD
89
Table 4. Comparison of Sorensen’s community similarity coefficients among freshwater and brackish wetlands of South Padre Island, Texas.
|
Site |
Site |
||||||||||||
|
2 |
3 |
4 |
5 |
6 |
7 |
8 |
9 |
10 |
11 |
12 |
13 |
14 |
|
|
1 |
.667 |
.593 |
.692 |
.714 |
.615 |
.786 |
.593 |
.593 |
.667 |
.615 |
.636 |
.476 |
.692 |
|
2 |
.846 |
.800 |
.741 |
.720 |
.815 |
.615 |
.692 |
.696 |
.720 |
.381 |
.400 |
.640 |
|
|
3 |
.720 |
.741 |
.720 |
.741 |
.615 |
.538 |
.696 |
.640 |
.381 |
.300 |
.640 |
||
|
4 |
.769 |
.750 |
.769 |
.720 |
.720 |
.818 |
.750 |
.500 |
.421 |
.750 |
|||
|
5 |
.846 |
.857 |
.815 |
.741 |
.750 |
.692 |
.455 |
.381 |
.769 |
||||
|
6 |
.769 |
.800 |
.640 |
.727 |
.667 |
.500 |
.526 |
.750 |
|||||
|
7 |
.741 |
.815 |
.750 |
.615 |
.455 |
.476 |
.692 |
||||||
|
8 |
.769 |
.696 |
.640 |
.476 |
.400 |
.640 |
|||||||
|
9 |
.696 |
.640 |
.381 |
.400 |
.640 |
||||||||
|
10 |
.727 |
.444 |
.353 |
.818 |
|||||||||
|
11 |
.500 |
.421 |
.833 |
||||||||||
|
12 |
.667 |
.600 |
|||||||||||
|
13 |
.526 |
vegetation at the site. Consequently, data on species importance are presented for only the first three species in importance at each site (Table 5). Schoenoplectus pungens (bulrush) was among the top three species in importance in 13 of the wetlands (92.9%) and it was the dominant species in nine wetlands (64.3%) (Table 5). Fuirena simplex (umbrella grass) and Spartina patens (marshhay cordgrass) each were dominant in two wetlands and Andropogon glomeratus (bushy bluestem) was dominant in one (Table 5). Two of the dominants were sedges (bulrush and umbrella grass) and two were grasses (bushy bluestem and marshhay cordgrass). None of the broad-leaved species were dominants and only four were one of the top three species at a particular site.
Discussion
Water in the wetlands of the secondary dunes and vegetated flats zone of South Padre Island occurs as a result of rainfall. Thus, it is fresh when it falls and it becomes progressively more brackish as water evaporates and the remaining standing water accumulates salt from wind transport. Consequently, a given wetland might contain freshwater if sampled soon after a rain and brackish water if
90
THE TEXAS JOURNAL OF SCIENCE-VOL. 61, NO. 2, 2009
sampled a week or more later. Thus, South Padre Island may not have wetlands that are permanently fresh or brackish. Salinity varies with the proximity of rain events. The wetlands are dry much of the time; especially so in drought years. Only 28.6% of the wetlands contained water at the time we sampled them. This was likely due to the fact that rainfall was below normal in seven of the 1 1 months of this study.
Each of the South Padre Island wetlands was sampled only once. Thus, it is not known if there is significant seasonal variation in any of the parameters studied here. However, it seems unlikely because only four species (16.7 % of the total, Table 2) are annuals and only two of these four species ranked in the top three species in importance at a given site (Table 5). None of the four species was dominant at a site.
South Padre Island freshwater and brackish wetlands have fewer species and lower species diversity than mainland freshwater and brackish marshes of the adjacent Rio Grande Delta (Judd & Lonard 2004), but evenness is similar in the island and mainland wetlands. Only six (24%) of the species occurring in South Padre Island wetlands in this study were also found in mainland wetlands by Judd & Lonard (2004). All six species occurred in brackish marshes on the mainland. Schoenoplectus pungens and Conoclinhim betonicifolium occurred only in mainland brackish marshes, Typha domingensis and Bacopa monnieri were found in freshwater, brackish, and salt marshes of the adjacent mainland. Sporobolus virginicus and Borrichicia frutescens occurred in brackish and salt marshes on the mainland. Three of the species were dominant in one or more marshes on the mainland. Typha domingensis was dominant in one of six freshwater marshes and in three of nine brackish marshes on the mainland. Borrichia frutescens was dominant in one of nine brackish marshes and two of 1 1 salt marshes on the mainland. Sporobolus virginicus was dominant in two salt marshes on the mainland. None of the dominant species in island wetlands were also dominant in
JUDD & LONARD
91
Table 5. Comparison of species importance among freshwater and brackish wetlands on South Padre Island, Texas, Freq. = frequency, Rel. Freq. = relative frequency, Rel. Cover = Relative Cover, Imp. Val. = importance value (sum of relative frequency and relative cover).
|
Site |
Species |
Freq. |
Rel. Freq. |
% Cover |
Rel. Cover |
Imp. Val. |
|
1 |
Schoenoplectiis pungem |
100.0 |
14.3 |
14.23 |
35.5 |
49.8 |
|
Spartina patens |
85.7 |
12.2 |
11.21 |
28.0 |
40.2 |
|
|
Iva texensis 1 1 additional species |
85.7 Total |
12.2 Cover |
5.61 40.03 |
14.0 |
26.2 |
|
|
2 |
Schoenoplectus pimgens |
100.0 |
15.7 |
65.64 |
81.6 |
97.3 |
|
Iva texensis |
87.5 |
13.7 |
4.31 |
5.4 |
19.1 |
|
|
Conoclinium betonicifolinm 1 0 additional species |
87.5 Total |
13.7 Cover |
2.16 80.5 |
2.7 |
16.4 |
|
|
3 |
Schoenoplectiis pimgens |
100.0 |
17.9 |
13.13 |
47.9 |
65.8 |
|
Iva texensis |
100.0 |
17.9 |
10.31 |
37.6 |
55.8 |
|
|
Spartina patens 10 additional species |
85.7 Total |
15.4 Cover |
1.09 27.44 |
4.0 |
19.4 |
|
|
4 |
Schoenoplectus pungem |
100.0 |
13.7 |
15.34 |
36.2 |
49.9 |
|
Solidago sempervirem |
100.0 |
13.7 |
5.96 |
14.0 |
27.7 |
|
|
Spartina patem 9 additional species |
100.0 Total |
13.7 Cover |
5.66 42.41 |
13.3 |
27.0 |
|
|
5 |
Schoenoplectus pungem |
100.0 |
10.1 |
14.60 |
31.2 |
41.3 |
|
Iva texensis |
100.0 |
10.1 |
11.00 |
23.5 |
33.6 |
|
|
Andropogon glomeratus 1 1 additional species |
100.0 Total |
10.1 Cover |
7.60 46.70 |
16.3 |
26.4 |
|
|
6 |
Schoenoplectus pungem |
100.0 |
14.0 |
30.70 |
59.8 |
73.8 |
|
Conoclinium betonicifolinm |
100.0 |
14.0 |
5.54 |
10.8 |
24.8 |
|
|
Spartina patem 9 additional species |
100.0 Total |
14.0 Cover |
2.59 51.38 |
5.0 |
19.0 |
|
|
7 |
Fuirena simplex |
100.0 |
12.3 |
34.86 |
55.6 |
67.9 |
|
Andropogon glomeratus |
100.0 |
12.3 |
16.84 |
26.9 |
39.2 |
|
|
Schoenoplectus pungem 1 1 additional species |
100.0 Total |
12.3 Cover |
2.80 62.68 |
4.5 |
16.8 |
|
|
8 |
Fuirena simplex |
100.0 |
14.3 |
62.61 |
79.9 |
94.2 |
|
Schoenoplectus pungem |
100.0 |
14.3 |
6.71 |
8.6 |
22.9 |
|
|
Panicum amarum 10 additional species |
100.0 Total |
14.3 Cover |
2.09 73.34 |
2.7 |
17.0 |
|
|
9 |
Schoenoplectus pungem |
100.0 |
11.5 |
16.03 |
25.1 |
36.6 |
|
Eleocharis geniculata |
71.4 |
8.2 |
16.30 |
25.5 |
33.7 |
|
|
Panicum amarum |
100.0 |
11.5 |
10.36 |
16.2 |
27.7 |
10 additional species Total Cover 63.89
92
THE TEXAS JOURNAL OF SCIENCE-VOL. 61, NO. 2, 2009
Table 5. Cont.
|
Site |
Species |
Freq. |
Rel. Freq. |
% Cover |
Rel. Cover |
Imp. Val. |
|
10 |
Schoenoplectus pimgens |
100.0 |
14.0 |
24.10 |
32.1 |
46.1 |
|
Andropogon glomeratiis |
100.0 |
14.0 |
23.11 |
30.8 |
44.8 |
|
|
Fuirena simplex |
100.0 |
14.0 |
10.83 |
14.4 |
28.4 |
|
|
1 additional species |
Total |
Cover |
75.07 |
|||
|
11 |
Schoenoplectus pimgens |
100.0 |
19.4 |
47.94 |
62.7 |
82.1 |
|
Borrichia frntescens |
100.0 |
19.4 |
21.40 |
28.0 |
47.4 |
|
|
Bacopa monnieri |
85.7 |
16.7 |
2.90 |
3.8 |
20.5 |
|
|
9 additional species |
Total |
Cover |
76.48 |
|||
|
12 |
Spartina patens |
100.0 |
25.0 |
30.36 |
54.0 |
79.0 |
|
Schoenoplectus pimgens |
100.0 |
25.0 |
19.61 |
34.9 |
59.9 |
|
|
Borrichia frntescens |
85.7 |
21.4 |
4.97 |
8.8 |
30.2 |
|
|
5 additional species |
Total |
Cover |
56.18 |
|||
|
13 |
Spartina patens |
100.0 |
36.8 |
60.27 |
91.7 |
128.5 |
|
Borrichia frntescens |
57.1 |
21.1 |
0.63 |
1.0 |
22.2 |
|
|
Iva texensis |
42.9 |
15.8 |
1.17 |
1.8 |
17.6 |
|
|
4 additional species |
Total |
Cover |
65.74 |
|||
|
14 |
Andropogon glomeratiis |
85.7 |
15.0 |
11.99 |
34.9 |
49.9 |
|
Schoenoplectus pnngens |
100.0 |
17.5 |
7.73 |
22.5 |
40.0 |
|
|
Spartina patens |
100.0 |
17.5 |
5.81 |
16.9 |
34.4 |
|
|
9 additional species |
Total |
Cover |
34.33 |
mainland wetland communities. Clearly the island wetland communities are markedly different than wetland communities of the adjacent mainland. They have fewer species, mostly different species, and different dominant species. It is unlikely that additional sampling on South Padre Island would have added many more species because sampling through the first nine sites resulted in 23 of the 24 species found. Sampling five more sites produced only one species. Similarity of species composition among freshwater and brackish wetlands of South Padre Island is high. The higher similarity among island wetlands is likely related to the much lower total species richness (24 species) compared to the mainland freshwater and brackish marshes (81 species each).
JUDD & LONARD
93
Baccus & Horton (1979) identify 13 species that occur in the low marshy areas of the heavily vegetated barrier flat at Padre Island National Seashore. Thus, species richness was similar to what we found at South Padre Island (mean = 1 1.9, 95% confidence interval = 10.6 to 13.2). However, similarity in species composi¬ tion was modest. Only five of the 13 species Baccus & Horton (1979) list for Padre Island National Seashore were found among the 14 sampling sites in this study. This might be six species in common if the Eleocharis sp. they list was E. geniculata. Species in common increases to eight if species known to occur on South Padre Island are included (Lonard et al. 1978) but not found in this study, and it might be increased to nine if the Eleocharis sp. was E. geniculata^ E. montevidensis, or E. obtusa, which are known to be present on South Padre Island (Lonard et al. 1978; this study). Nelson et al. (2001) compare the floras of Matagorda Island, Mustang Island, North Padre Island and South Padre Island. Each species in the wetlands of South Padre Island is known to occur on North Padre Island.
Baccus & Horton (1979) found that the dominant species among the wetland species was Eleocharis interstincta. Eleocharis interstincta was not found in this study and Lonard et al. (1978) did not find it on South Padre Island. A different species of Eleocharis {E. geniculata) was present at six of the 14 wetlands sampled, but it was abundant at only one site (2”*^ in importance at Site 9).
Nelson et al. (2000) reported on the vegetation and fioristics of four communities in the Big Ball Hill region of Padre Island National Seashore. They identified Andropogon glomeratus and Spartina patens as dominants in the lowland subcommunity of the barrier flat community. Borrichia frutescens, Hydrocotyle bonariensis, Samolus ebracteatus, and Schoenoplectus pungens were listed as species typically present in the lowland sub¬ community. They do not suggest that this list is complete for the lowland sites. All of the species, except H, bonariensis were present among the sites studied at South Padre Island, but only
94
THE TEXAS JOURNAL OF SCIENCE-VOL. 61, NO. 2, 2009
Spartina patens occurred in Baccus & Horton’s (1979) list of species occurring in low marshy areas of the vegetated flats of Padre Island National Seashore. Thus, there is less similarity in species present in lowland barrier flat communities on North Padre Island than there is between either of the studies and the species present in the wetlands of South Padre Island.
Mean species richness in the barrier flat community (both low and higher elevations) of Big Ball Hill region of Padre Island National Seashore was reported to be 20.3 (Nelson et al. 2000). This is almost double the mean species richness of 11.9 found among the wetlands at South Padre Island. It is not surprising since only the lowland component of the barrier flats was included. Nelson et al. (2000) reported a mean species diversity for the barrier flat community of 0.58 and a mean evenness of 0.61. They do not provide a measure of variance for either mean, but both means appear to be significantly lower than those reported here because the values fall below the 95% confidence intervals for species diversity and evenness in wetlands at South Padre Island.
Conclusions
Based on the meager data available, it appears that species richness at wetland sites is similar on the northern and southern portions of Padre Island, but there is only modest similarity in species composition of wetland communities. There is considerable variation in species importance among South Padre Island sites and marked variation between southern and northern portions of Padre Island. Additional study of Padre Island and other Texas barrier islands is needed to ascertain if the differences in composition of barrier island freshwater and brackish wetland communities reported here are stochastic or related to variation in environmental variables.
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Lonard, R. 1. & F. W. Judd. 1981. The terrestrial flora of South Padre Island, Texas. Texas Memorial Museum Miscellaneous Papers No. 6, 74 pp.
Lonard, R. 1. & F. W. Judd. 1989. Phenology of native angiosperms of South Padre Island, Texas. Pp. 217-222, in Proceedings Eleventh North American Prairie Conference. T. Bragg and J. Stubbendieck (Eds.). Univ. Nebraska Printing, Lmcoln, Nebraska, 293 pp.
Lonard, R. L, F. W. Judd, J. H. Everitt & D. E. Escobar. 1991. Roadside associated disturbance on coastal dunes. Pp. 2823-2836, in Proceedings Seventh Symposium on Coastal and Ocean Management, “Coastal Zone ‘91”. American Soc. of Civil Engineers. Long Beach, California, 3800 pp.
Lonard, R. I. & F. W. Judd. 1993. Recovery of vegetation of barrier island washover zones. Pp. 2324-2331, in Proceeding of the Eighth Symposium on Coastal and Ocean Management, “Coastal Zone ‘93”. American Soc. Civil Engineers. New Orleans, Louisiana, 3512 pp.
Lonard, R. 1. & F. W. Judd. 1997. The biological flora of coastal dunes and wetlands. Sesuviiim portulacastnim (L.) L. Journal of Coastal Research, 13(1):96-104.
Lonard, R. 1. & F. W. Judd. 1999. The biological flora of coastal dunes and wetlands. Ipomoea imperati (Vahl) Griseb. Journal of Coastal Research, 15(3):645-652.
Lonard, R. L, F. W. Judd, J. H. Everitt, D. E. Escobar, M. A. Alaniz, 1. Cavazos III & M. R. Davis. 1999. Vegetative change on South Padre Island, Texas, over twenty years and evaluation of multispectral videography in determining vegetative cover and species identity. Southwestern Naturalist, 44(3):26 1-271.
Nelson, A. D., J. R. Goetze, I. G. Negrete, V. E. French, M. P. Johnson & L. M. Macke. 2000. Vegetational analysis and floristics of four communities in the Big Ball Hill, region of Padre Island National Seashore. Soutliwestem Naturalist, 45(4):43 1-442.
Nelson, A., J. Goetze & A. Lucksinger. 2001. A comparison of the flora of northern Padre Island to that of Matagorda Island, Mustang Island and southern Padre Island, Texas. Occas. Papers, Museum of Texas Tech University, Number 209:1-23.
FWJ at; Qudd@utpa.edu
TEXAS J. OF SCI. 61(2);97-118
MAY, 2009
SEASONAL TROPHIC ECOLOGY OF THE WHITE-ANKLED MOUSE, PEROMYSCUS PECTORALIS (KODENTIA: MURID AE)
IN CENTRAL TEXAS
John T. Baccus, John M. Hardwick, David G. Huffman and Mark A. Kainer
Wildlife Ecology Program, Department of Biology Texas State University, San Marcos, Texas 78666
Abstract-Fruits and seeds, green foliage, and animal matter composed the seasonal diets of Peromysciis pectoralis in central Texas. Based on changes in foods consumed, five distinct seasons were delineated. Trophic diversity differed among seasons, with diversity highest in summer and lowest in winter. Diets for winter and autumn were more similar; whereas, diets for winter and late spring, winter and summer, and late spring and autumn were more dissimilar. Peromysciis pectoralis in central Texas are primarily frugivorous/granivorous herbivores with omnivorous tendencies reflecting opportunistic feeding habits.
Species of Peromyscus have been characterized as granivores with omnivorous tendencies that reflect opportunism in feeding habits (Cogshall 1928; Baker 1971; Montgomery 1989). Most dietary studies have compared two or more closely related species in sympatry and generally found Peromyscus are efficient foragers with broad diets consisting of seeds, fruits, green vegetation, and arthropods (Cogshall 1928; Hamilton 1941; Jameson 1952; Williams 1959; M'Closkey & Fieldwick 1975; Grant 1978; Knuth & Barrett 1984). Before interspecific interactions between potentially competing congeners can be fully determined, studies of each species in the absence of potential competitors are needed to ascertain the breadth of the trophic niche. In addition, climatic and phenological events may cause notable changes in community structure that affect the quantity and quality of food resources and shape the trophic niche of a species (Waser 1978a; 1978b). Seasonality in diet is evident in populations of most northern species of Peromysus, Because of the paucity of seasonal data for southern populations, a nonexistent or limited dietary cycle in these populations has been suggested (Montgomery 1989).
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THE TEXAS JOURNAL OF SCIENCE, VOL. 61, NO. 2, 2009
The white-ankled mouse, Peromyscus pectoralis Osgood, occurs in a variety of habitats over the central Mexican Plateau and Sierra Madre Oriental in Mexico northward to southeastern New Mexico and western and central Texas into southern Oklahoma. The species has a propensity for rocky environments, especially rock outcrops (Kilpatrick & Caire 1973; Schmidly 1972; 1974; Baccus & Horton 1984; Etheredge et al. 1989). Although substantial information exists about the habitat affinities of this species, the trophic niche of this mouse is poorly known. Alvarez (1963) observed the species eating fruits of nopal (prickly pear, Opuntia lindheimeri) cactus in Tamaulipas, Mexico. In Texas, Davis (1974) reported consumption of juniper berries, hackberry seeds, and acorns in central Texas. Schmidly (2004) mentioned the lack of a detailed food habits study for the species and speculated the diet consisted of seeds, cactus fruits, lichen, fungi, and insects. Here, the first detailed analysis and description of the seasonal trophic niche of P. pectoralis in central Texas is presented. No other sympatric congeners (i.e., P. attwateri) inhabited the study site (Mullican & Baccus 1990); thus, no accounting for interspecific competition or differential use of resources was necessary in the analysis.
Methods
White-ankled mice were collected 5 km W. San Marcos, Hays County Texas (29°47' N, 97°58' W) in an abandoned limestone quarry at the eastern periphery of its distribution. The landscape consists of large to medium size, strewn boulders and truncated limestone outcrops. Ashe juniper trees (Juniperus ashei) dominate the woody vegetation with trees and shrubs of green sumac {Rhus virens), Texas persimmon (Diospyros texana), sugar hackberry (Celtis laevigata), plateau live oak (Quercus fusiformis), agarito (Mahonia trifoliolata), and Roosevelt weed {Baccharis neglecta) also present. Herbaeceous vegetation consists of Johnsongrass {Sorghum halepense). King Ranch bluestem {Bothriochola ischaemum), little bluestem {Schizachyrium scoparium), Texas wintergrass {Stipa leucotricha), threeawn grass {Aristida sp.).
BACCUS ET AL.
99
prickly pear, frostweed (Verbesina virginica), Lindheimer senna (Cassia lindheimeriana), knotted hedgeparsley (Torilis nodosa), prairie bluet (Heydotis nigricans), Drummond skullcap (Scutellaria drumondii), white sweetclover (Melilotus albus), oneseed croton (Croton monanthogynus), Indianmallow (Abutilon incanum), common sorrel (Rumex acetosella), sensitivebriar (Schrankia roemeriana), pepperweed (Lepidiim virginicum), and Texas bluebonnet (Lupinus texensis). Plant taxonomy followed Hatch et ah (1990).
Thomthwaite (1948) classified the climate of Hays County as C1B4 (dry subhumid, mesothermal) with a mean annual potential evapotranspiration of 99.7 to 114 cm. The mean monthly
o
maximum temperature is 35 C (July) with a mean monthly minimum of 5°C (January). Mean annual precipitation is 85.7 cm. During this study, annual precipitation was below normal (76 cm).
Monthly collections between October 1976 and September 1977 were accomplished by Museum Special snap-traps set along 100 trap-station transects (spacing 15 m) during 12 consecutive days each month (total for study = 14,400 trap-days). Age (Schmidly 1972), standard external measurements, gender, and reproductive condition were recorded for each mouse. White-ankled mice were collected under Texas Scientific Permit SPR-0890-234.
Quantitative evaluations of stomach contents from 149 (67 females and 82 males) P. pectoralis followed relative-occurrence evaluation and histomicroscopic methods (Sparks & Malechek 1968; Free et al. 1970; Hansson 1970; Westoby et al. 1976; Ellis et al. 1977; Dawson & Ellis 1979; Cockbum 1980; Copley &
Robinson 1983; Mclnnis et al. 1983; Copson 1986; Carron et al.
2
1990). Stomach contents were washed through a 0.125-nim sieve, homogenized, equally partitioned, and placed on 5 microscopic slides. These contents were considered as a whole or 100% irrespective of the extent of stomach fill (Hansson 1970). Twenty randomly selected microscopic fields with food items were
100
THE TEXAS JOURNAL OF SCIENCE, VOL. 61, NO. 2, 2009
examined per slide under lOOX magnification (total fields examined = 14,900). Identified food items in each field were recorded. Reference slides were also prepared of plant and animal matter from the collection site after mincing in a blender to mimic mastication.
Identification of food items and classification categories were based on anatomical or morphological structures of plant and animal matter. However, some matter due to extensive mastication remained unidentified. Ingested bait was ignored. Food categories applied to stomach contents were: (I) fruits and seeds-remains of testa, endosperm, exocarp, or individual minute seeds; (2) green foliage-leaf or stem tissues; (3) larval insects- nonsclerotized soft- bodies; (4) adult insects-sclerotized parts such as antennae, elytra, mouthparts, wings, or appendages; and (5) animal matter-primarily muscle tissue and hair. Fruits and seeds were combined as a food category because of a strong tendency of co-occurrence (Pitts & Barbour 1979). Calculations of percent frequency (%f), percent volume (%v) and relative importance (I) for each food item followed Obrtel & Holisova (1974; 1981). Composition
percentages were obtained by dividing the total number of fragments of a given food item by the total number of fragments of all foods encountered. Analyses showed no difference in percent frequency of food items in diets of males and females; therefore, data for males and females were pooled.
Seasonal variation in food habits of small mammals has been primarily demonstrated by two methods. A season is defined by one method as a set number of months, usually four periods of three months, and food items enumerated within a season (Hamilton 1941; Whitaker 1966; Houtcooper 1978; Luo & Fox 1994). The second method lists food items consumed each month (Jameson 1952; Myers & Vaughan 1964; Bradley & Mauer 1971; Luce et al. 1980; Armgard & Batzli 1996). Both methods fail to reveal the dynamics of rapid dietary change. It is possible that seasonal change in animal diets may not be reflected by the four customary
BACCUS ET AL.
101
seasons; rather, based on dietary changes, one might find fewer or a greater number of seasons.
An Index of Change based on dietary dynamics was developed using a two-day moving average of the abundance of food items for groups of a set number of mice. The difference between group means for two consecutive such groups of mice was divided by the
|
mean collection date of the mice in Change is represented by the formula: |
both groups. The Index of |
||
|
V |
m+k |
V |
m+2k |
|
z |
(Z-) |
- z |
(Z-) |
|
j=l |
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i=m+k+l |
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where;
k = number of mice included in the first or second half (group) of the moving mean interval
m = accession number of the first mouse in the interval, with m incrementing by unity after each solution of the expression
X = percent composition of food item j in mouse i V = total number of different food items
d = Julian day of capture for mouse i
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THE TEXAS JOURNAL OF SCIENCE, VOL. 61, NO. 2, 2009
Seasonal recognition was determined by the extent of an abrupt change in the diet. For the purposes of this study, any change >10 was defined as a substantial dietary change and recognized as the beginning of a season. Also, the stability of the period following an abrupt change was considered. If the Index of Change did not vary by a factor >5 during a period of time, this sequence of days was considered as the term of a season. The next change in the index >10 marked the start of the next season.
Preference for food items was determined by a modified Ivlev's Index of Electivity (Ivlev (1961; Jacobs 1974; Krebs 1999). The electivity index indicated whether a plant was consumed in amounts similar to availability in the environment or active selection of the food. A value of zero indicated randomness in resource selection, a positive index indicated the food was selected in amounts greater than would be expected by chance encounter, and a negative index signified consumption of a food in quantities lower than predicted by randomness. The z test for comparing sample proportions (Sokal & Rholf 1969) was used to determine differences in male and female diets.
Seasonal diversity in the diet was calculated by Brillouin's Index of Diversity because samples were treated as collections rather than random samples from a larger biological community (Margalef 1958; Pielou 1966; Krebs 1999). Seasonal overlap in diet was determined by Morisita's Index of Similarity (Morisita 1959; Krebs 1999). The overlap coefficient varies from 0 when diets are completely distinct (no food categories in common) to 1 when diets are identical. Values >0.60 indicate significant overlap (Zaret & Rani 1971), but this should not be construed as statistically significance. Seasonal differences in the proportion of plant and animal matter in the diet were tested by a Goodness-of-Fit test.
Herbaceous vegetation occurring on the study site was assessed in January, April, August and November by randomly dropping a 0.5 m x 1 m quadrat 100 times in the study area. From these data.
BACCUS ET AL.
103
Table 1. Characteristics of the seasonal diet of Peromyscus pectoralis in central Texas.
|
Criterion |
Winter |
Early Spring |
Late Spring |
Summer |
Autumn |
|
Sample |
|||||
|
size (n) |
39 |
21 |
23 |
31 |
35 |
|
Number |
|||||
|
of items (S) |
8 |
10 |
8 |
15 |
12 |
|
Plant (%) |
5 (62.5) |
7 (70.0) |
5 (62.5) |
11(73.3) |
8 (66.7) |
|
Animal (%) |
3 (37.5) |
3 (30.0) |
3 (37.5) |
4 (26.4) |
4(33.3) |
|
Equally |
|||||
|
common species |
6.19 |
7.44 |
7.25 |
9.32 |
7.82 |
|
Trophic |
|||||
|
diversity (H) |
2.52 |
2.78 |
2.71 |
3.736 |
2.87 |
percent cover of each plant species was estimated (Myers & Vaughan 1964). Seed abundance was sampled by placing a 25 cm X 10 cm quadrat in the lower right comer of the larger quadrat at 10 sampling locations, removing the top 1-2 cm of soil, and screening soil samples through a series of descending size sieves (2.0 mm- 180 pm). Seeds were removed, counted, and identified to species.
The arthropod fauna was sampled monthly by sweeping through the ground vegetation along each trap-line with an insect net (38- cm diameter) (Beiner 1955). Arthropods inhabiting the foliage of trees were not sampled.
Results
Twenty-three food items (18 plant and 5 animal), broadly categorized into 3 trophic groups (fruit and seed, green foliage, and animal matter), comprised the seasonal diet of P. pectoralis in central Texas (Table 1). No mouse exclusively consumed plant or animal matter. There was no difference in percent frequency of food items in diets of males and females (z = 0.0936, P > 0.34). The percent frequency, percent volume, and importance value of food items in the diet varied seasonally (Table 2). Prickly pear foliage, larval and adult insects, and arachnids were the only food items consumed in all seasons. Ten food items had a percent fre-
Table 2. Percent frequencies (%f), percent volumes (%v) and importance values (I) of items identified in the seasonal diet of Feromyscus pectoral is in central Texas.
Winter Early Spring Late Spring Summer Autumn
104
THE TEXAS JOURNAL OF SCIENCE, VOL. 61, NO. 2, 2009
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BACCUS ET AL.
105
quency of < 5%. These foods were a miscellaneous assortment of animal tissues, green foliage, seeds, fruits, and possibly flower inflorescence. Twenty-two percent of stomachs had plant fragments so masticated that identification only as dicot material was possible. No monocot, lichen, or fungal materials were identified in any stomach. The greatest number of different food items found in any one stomach was 6 (X= 3.26, SE = 0.73 ). Based on percent volume and percent frequency, 2 trophic categories (fruit and seed and animal matter) composed the bulk of seasonal diets. Seeds and fruits were the most frequently encountered category in the seasonal diet, occurring in 87% of stomachs. Ashe juniper berries were the most frequently consumed fruit. Arthropods were the primary animal matter in the seasonal diet with 84% of stomachs containing mostly insect fragments. Insects consumed were from the following taxa: Order Hymenoptera, Families Formicidae and Apidae; Order Coleoptera, Family Scarabaeidae; Order Orthoptera, Family Gryllidae; Order Collembola; Order Lepidoptera, Family Pyralidae; and Order Diptera.
Five seasons (winter, December-January; early spring, February- March; late spring, April-May; summer, June-August; and autumn, September- November) were delineated by an Index of Change (Fig. 1). Morisita's Index of Similarity indicated no two seasons had unity (Table 3), yet some seasons were similar because of dietary overlap >0.60. The temporal continuity of resource use by white-ankled mice and dynamic changes in the diet demonstrated a general trend in which the immediate juxtaposed seasons to a given season were most similar (i.e., winter diet was most similar to the previous season, autumn, and the following season, late spring). The exception to this trend was autumn. A similarity value (0.42) between summer and autumn diets indicated substantial dissimilarities between these juxtaposed seasons; however, autumn and winter diets had the highest similarity. Furthermore, the autumn diet was more similar to the early spring diet. The communality of diet for these three seasons was based on the extent
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THE TEXAS JOURNAL OF SCIENCE, VOL. 61, NO. 2, 2009
40 r
Figure 1. Eidex of change in the diet of Peromysciis pectoralis collected in central Texas as a function of date and season. Each of the five major peaks of the graph represent the start of a season (M Dec = winter, E Feb = early spring, E Apr = late spring, E Jun = sununer, E Sept = Autumn). Letters representmg months mark the early, middle, and late portions of each month.
of fruit and seed use (primarily Ashe juniper berries) by white- ankled mice.
The substantial and almost exclusive use of the fruit and seed category was the distinctive feature of the winter diet (Table 2, Fig. 2). As a result, the winter diet was the most homogenous and least diverse of any season. The high use of fruit and seed in comparison to minimal consumption of animal matter (arthropods) and green foliage resulted in low seasonal diversity. Only Ashe juniper and green sumac berries were important staples, continuing the trend first seen in autumn of a preponderance of fruit and seed in the diet. The importance value (74.6) for Ashe juniper berries in winter was the highest importance value of any food item for any season. The highest seasonal percent volume (88.4%) of a trophic category (fruit and seed) occurred during winter. Plant matter in the winter diet was greater than animal matter {X^= 67.2; df = 1; P < 0.01).
The early spring was transitional with a decrease in the use and importance of the fruit and seed category (32.6% of overall seasonal percent volume) and an increase in the consumption and
BACCUS ET AL.
107
Table 3. Seasonal overlap in the diet of Peromyscus pect oralis (above diagonal) in centrs Texas as measured by Morisita’s Index of Similarity and number of food itenr common to all pair-wise seasonal comparisons (below diagonal).
|
Season |
Winter |
Early Spring |
Late Spring |
Summer |
Autumn |
|
Winter |
- |
0.61 |
0.367 |
0.394 |
0.88 |
|
Early Spring |
6 |
- |
0.688 |
0.622 |
0.603 |
|
Late Spring |
4 |
7 |
- |
0.657 |
0.392 |
|
Summer |
4 |
7 |
7 |
- |
0.418 |
|
Autumn |
7 |
6 |
4 |
6 |
- |
importance of green foliage. Three trophic categories (fruit and seed, green foliage, and animal matter) comprised the diet. Residual Ashe juniper berries and hackberries in the environment (Table 4) and new, succulent foliage of white sweet clover, oneseed croton, and unidentified dicot herbage were important plant items in the diet. Larval and adult insect consumption increased (26.7% of overall seasonal percent volume), but arthropod use ranked lower in importance than fruit and seed and green foliage (40.7% of overall seasonal percent volume). Early spring trophic diversity was higher than winter. Consumption of residual winter berries and new green foliage resulted in higher plant matter use than animal matter in the early spring diet (A'^ = 21.67; df = 1; P < 0.01).
A shift in resource use in late spring to consumption of green foliage and animal matter supplanted fruit and seed use in the diet. The array of herbaceous plants in the diet expanded; however, extreme mastication of foliage made identification difficult and most material was classified as unidentified dicot herbage. Based on percent frequency, percent volume, and importance value, the most important food consumed during late spring was larval insects. Because of high consumption of larval insects, late spring was the only season where percent volume of animal matter (57.4%) exceed percent volume of plant matter in the diet. The most common larval insect in stomachs was the lepidopteran moth family, Pyralidae. Although there was a higher consumption of animal matter for this season, animal and plant matter use was similar (V^= 3.24; df = 1; /> > 0.1).
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THE TEXAS JOURNAL OF SCIENCE, VOL. 61, NO. 2, 2009
□ Fruit and Seed m Foliage □Animal Matter
Winter Early Late Summer Autumn Spring Spring
Season
Figure 2. Seasonal changes in the three major food categories in the diet of Peromyscus pectoral is in central Texas.
The summer diet was the most heterogeneous of any season. White-ankled mice continued to eat green herbaceous foliage (23.6% of overall seasonal percent volume), but percent volume for most herbs was small. Stem and fruit use of prickly pear was the highest for any season. However, with maturation of grass and woody plant seeds, the importance of seeds and fruits in the diet increased (34.2% of overall seasonal percent volume), but percent volume for most species was low. Adult insect consumption was greatest in summer. Arthropods as a trophic group persisted as the most important food category (41.0% of overall seasonal percent volume). Adult crickets (Family Gryllidae) and beetles (Family Scarabaeidae) were the most common insects consumed. The highest consumption of arachnids occurred during summer. Trophic diversity (3.74) and richness (15 different food items) were the highest for any season. Materials attributable to 3 trophic categories were consumed during this season, and with increased
BACCUS ET AL.
109
Table 4. Seasonal availability of the food resource of Per omy sens pect oralis. Fruits and seeds are the total number of items counted in ten 0.25 m^ quadrats. Green foliage is the estimated percent occurrence in one hundred 0.5 m“ quadrats.
|
Item |
Winter |
Spring |
Summer |
Autumn |
|
Fruit and Seed Jimipertis ashei |
222 |
38 |
61 |
|
|
Rhus Virens |
21 |
5 |
||
|
Celtis laevigata |
4 |
|||
|
Quercus fusiformis |
5 |
23 |
||
|
Sorghum halepense |
40 |
60 |
||
|
Cassia Lindheimeriana |
20 |
|||
|
Diospyros texana |
3 |
|||
|
Green Foliage Sorghum halepense |
8 |
14 |
23 |
20 |
|
Bothriochola ischaemum |
8 |
17 |
28 |
31 |
|
Stipa leucotricha |
22 |
15 |
2 |
15 |
|
Melilotus albus |
28 |
16 |
8 |
|
|
Opuntia lindheimeri |
5 |
3 |
2 |
4 |
|
Croton monant hog\mus |
1 |
4 |
9 |
|
|
Shrankia roemeriana |
1 |
1 |
||
|
Tor ills nodosa |
19 |
8 |
2 |
|
|
Lepidium virginicum |
1 |
2 |
||
|
Houstonia nigiicans |
4 |
1 |
||
|
Lupinus texensis |
1 |
|||
|
Rumex acetosella Abutilon incanum |
4 |
3 |
3 |
seed use, there was a preponderance of plant matter in the summer diet. However, there was no difference between plant and animal matter use (X^= 2.56; df = 1; P > 0.2).
Autumn was a transitional season because of shifts and changes in the diet. Fruit and seed consumption (86.2% of the overall seasonal percent volume) increased and supplanted the importance of green foliage and arthropods in the diet (Fig. 2). This season was distinguished by an abrupt increase in the consumption of Ashe juniper and green sumac berries and prickly pear fruit. Arthropod use (12.0% of overall seasonal percent volume) decreased sub¬ stantially in comparison to summer. Trophic diversity decreased
10
THE TEXAS JOURNAL OF SCIENCE, VOL. 61, NO. 2, 2009
because fewer food items were consumed. The consumption of berries and seeds and a diminished use of arthropods resulted in a diet dominated by plant matter (X^= 56.8; df = 1; P < 0.01).
Peromyscus pectoralis preferred certain foods in different seasons. Texas persimmon seeds had the highest electivity value (0.66) for any food item. No Texas persimmon trees occurred along trap-lines, and few trees were in the immediate study area. There were, however, an abundance of scattered raccoon {Procyon lotor) scats with Texas persimmon seeds in the study area. These scats concentrated Texas persimmon seeds in high density patches that provided an immediate access to seeds that otherwise were unavailable.
The most common fruit eaten was Ashe juniper berries. Even though the ground under and around juniper trees was often covered by berries, the electivity value (0.12) indicated only a slight preference for this food item. Since the quantity of Ashe juniper berries consumed by white-ankled mice was commensurate with availability (Table 4), P. pectoralis opportunistically fed on these berries. Hackberry and green sumac berries were not as common as Ashe juniper berries and availability was lower; however, electivity indices for these fruits (0.53 and 0.42, respectively) indicated selection by white-ankled mice. White sweetclover was the most abundant herbaceous plant in the spring plant availability sample (28% ground coverage). The electivity index for white sweetclover foliage (0.13) was similar to Ashe juniper indicating consumption was commensurate with availability. The negative electivity indices for seeds and/or foliage of Johnsongrass (-0.93), King Ranch bluestem grass (-0.96), prickly pear (-0.59), oneseed croton (-0.91), prairie bluet (-0.95), and Lindheimer senna (-0.99) indicated avoidance. No stomachs contained live oak acorns, agarito berries, and seeds or foliage of little bluestem grass, sensitivebriar, knotted hedgeparsley, pepperweed, Texas bluebonnet, common sorrel, or Indianmallow.
BACCUS ET AL.
Ill
Discussion
Species of Peromyscus are opportunistic feeders with variable use of food resources by season and availability. Major trophic categories in the diet are seeds, fruits, green plants, and animal matter (Montgomery 1989). Studies of the food habits of P. maniculatus^ P. leucopus, P. californicus, P. eremicus, P. truei, and P, boylii (= attwateri) indicated either a moderate to common use of seeds, rare to common use of animal matter, rare to moderate use of green vegetation in all species except P. attwateri, and rare to moderate use of fruits (Brown 1964; Whitaker 1966; Flake 1973; Kritzman 1974; Vaughan 1974; Meserve 1976; Wolff et al. 1985).
Peromyscus food habits vary from season to season. Wolff et al. (1985) found univariate differences between seasons for seven of eight categories of food items in diets of P. maniculatus and P. leucopus. Both species ate more fleshy fruit in summer, more moths and butterflies in autumn, and more nuts in autumn and winter than other seasons. Hamilton (1941) reported that 180 P. leucopus noveboracensis collected between November and April in central New York consumed more arthropods than nuts/seeds or green plant matter. The diet between May and October was primarily arthropods with lesser amounts of fruits, nuts/seeds, and fungi. Whitaker (1963) found the primary food in the summer diet of 142 P. leucopus from New York was nuts/seeds with lesser amounts of arthropods and green plant matter. In addition, Whitaker (1966) stated 1 13 P. maniculatus from Indiana consumed principally nuts/seeds with lesser amounts of arthropods and green plant matter. Martell and Macauley (1981) found arthropods were the most common item and nuts/seeds, fruits, and fungi were less common with green plant matter and achlorophyllous plant matter present in miniscule amounts in stomach contents of 712 P, maniculatus taken between May and September in northern Ontario. Brown (1964) analyzed stomach contents of 20 P. attwateri collected in March, June, September, and December in southern Missouri and found seed use highest in June and lowest in March, insect use highest in December and lowest in June, fruit or
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berry use highest in March and lowest in June, consumption of green plant matter highest in June and September and lowest in March and December, and bulb fragments use highest in September and lowest in June.
There was a definite seasonal variation in the diet of P. pectoralis in contrast to the suggestion by Montgomery (1989) that southern populations of Peromyscus indicate little or no annual dietary cycle. Dietary trends of this species resemble the diet of Peromyscus athvateri and other species of Peromyscus; yet, there are differences. The seasonal diet of P. pectoralis appears opportunistic, especially in autumn and winter use of Ashe juniper berries, spring use of green foliage, and spring and summer consumption of insects. In contrast, plant matter dominated the winter diet (percent volume 91%), but the percent volume in the summer diet was only 42.6%. No other studies of Peromyscus have indicated this high a consumption of plant matter during winter (Montgomery (1989). Brown (1964) found only low or trace amounts of green plant matter in the diet of P. attwateri with the greatest amount of plant matter consumed being seeds.
As in other species of Peromyscus, consumption of animal matter by the white-ankled mouse had seasonal importance, especially insect use. Although insect abundance was monitored using sweeping of vegetation, this method did not provide adequate samples of the availability of the insects consumed by P. pectoralis during this study. Most adult insects eaten by P. pectoralis were ground crickets or beetles. The most consumed larval insects were catepillars of a pyralid moth that inhabits Ashe juniper trees. Insect consumption in late spring and summer were the highest reported for Peromyscus for these seasons (Flake 1973, Kritzman 1974, M’Closkey and Fieldwick 1975, Batzli 1977). Overall a similar consumption of animal matter by P. pectoralis and P. attwateri occurred in spring, summer, and autumn (Brown 1964). Insect use by P, pectoralis and P. athvateri in early spring and autumn was comparable, but winter consumption was dissimilar. The disparity
BACCUS ET AL.
113
in insect consumption during winter by P. pectoral is in central Texas compared to other species of Peromyscus was probaly phenological. The mild winters of central Texas allows for an extended period of activity by adult insects compared to those inhabiting northern latitudes and high altitude environs where winter temperatures are below freezing for an extended time. In Hays County, Texas, it is not unusual to have <5 days in winter with temperatures at or below freezing.
A major difference in the diet of P. pec tor alls compared to other species of Peromyscus was the importance of fruits in the seasonal diet. Peromyscus pectoralis began to eat friuts and seeds in summer as they matured with highest consumption of these foods in autumn extending into winter. Ashe juniper and green sumac berries were important components of the autumn through winter diets when abundance and availabilty was at a maximum in the habitat of P. pectoralis. Residual hackberries in the environment were important in the early spring through summer. Prickly pear fruits became impotant in summer through autumn with maturation of fruits. All of these berries and fruits became abundant and important in the diet of P. pectoralis based on their maturation and abundance in the environment (Table 4). Although the electivity index for Ashe juniper berries indicated a slight preference by white-ankled mice, the index value did not indicate the importance of this food in the diet. The high percent frequency of occurrence in the environment and percent volume in stomachs confirm the importance of this food in the seasonal diet and opportunism of P. pectoralis. Ashe juniper berries were most abundant between 15 December and 25 February. This period of high abundance of Ashe juniper berries overlapped the time when juvenile mice were most common in the population. Green sumac berries also had high abundance during this period. The high use of Ashe juniper and green sumac berries may have been the result of young white- ankled mice learning to eat this food in their natal environment and conditioning of adults to associate with habitats where berries are abundant (Drickamer 1970; 1976).
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The abundance of green foliage was highest in spring through autumn for most herbaceous species except Stipa leucotricha that had highest availability in winter. The phenology for most herba¬ ceous vegetation is invigorated growth during spring (Schmidly 2004). Peromysciis pectoralis had the highest consumption of the green foliage of herbaceous vegetation in early and late springwhen availability was highest. When available, green vegetation was a very common food of P. maniculatiis (Kritzman 1974), moderately common in the diets of P. californicus and P. truei (Merritt 1974), but rarely consumed by P. leucopus (Whitaker 1966) and P. eremicus (Meserve 1976).
In a comparison of the size of food items consumed, larger berries and seeds had a positive electivity index; whereas, minute seeds had negative values (i.e., compare hackberry and green sumac berries vs. Johnsongrass and King Ranch bluestem grass seeds). Kantak (1983) found northern populations of both wild caught Peromyscus maniculatus bairdii and Peromyscus leucopus noveboracensis preferred larger size grass seeds of Andropogon. Moriarty (1977) suggested that size and selections of food items were critical expenses related to search time incurred by an animal while foraging. Both Ashe juniper and sumac berries were readily available seasonally, and foraging and handling times necessary to encounter and eat these items were probably minimal (Moriarity 1977). Otherwise, the diversity of food items consumed by P. pectoralis and the implied trophic niche was similar to other species of Peromyscus,
In one of the first food habits of a southern species of Peromyscus, this study delineated by an Index of Change a five season (winter, early spring, late spring, summer, and autumn) pattern of trophic ecology for Peromyscus pectoralis in central Texas. The species had considerable variation in the seasonal diet, and is primarily a frugivorous/granivorous herbivore with omnivorous tendencies reflecting opportunistic feeding habits .
BACCUS ET AL.
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Acknowledgments
Thanks are extended to R. W. Manning, M. F. Small, J. G. Brant, T. R. Simpson, and an anonymous reviewer for critical reviews of the manuscript. A special thanks is extended to E. Longcope for permission to collect on his property. Funding for this study came from a Texas State University Faculty Enhancement grant to J. T. Baccus.
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JTB at: jb02@txstate.edu
TEXAS J. OF SCI. 61(2): 119-130
MAY, 2009
CHANGES IN VEGETATION PATTERNS AND THEIR EFFECT ON TEXAS KANGAROO RATS (DIPODOMYS ELATOR)
Allan D. Nelson, Jim R. Goetze*, Elizabeth Watson and Mark Nelson
Department of Biological Sciences, Box T-OlOO,
Tar! et on State University, Stephenville, Texas 76401 and ^Science Department, Laredo Community College Laredo, Texas 78040
Abstract-Investigations of vegetation in Wichita County, Texas indicate that changes in patterns of grazing and the introduction of non-native plant species may affect populations of the Texas kangaroo rat. Intensely and moderately grazed areas were compared to each other and to a previous investigation involving an ungrazed pasture dominated by introduced Japanese brome (Bromiis japoniciis). Thirty Dipodomys elator were trapped at the intensely and moderately grazed sites, whereas only two animals were caught on the periphery of the ungrazed site in Wichita County. In addition, the moderately grazed site was compared to the intensely grazed site and no significant differences in vegetative richness or percentages grass and forb were found between sites. Height of vegetation, percentage bare ground and woody species coverage were significantly different in comparisons between the two grazed sites. Because the two sites contained populations of D. elator, it appears that they can use moderately to heavily grazed habitats as burrow locations and can tolerate significant differences in vegetation height and amount of bare ground and woody vegetation. They rarely use ungrazed sites as habitat and, in a previous investigation, an ungrazed site was significantly different from the grazed sites in vegetational height, percentage bare ground, and percentage grass coverage. Grazing regimes, amount of bare ground coverage, and introduction of tall, dense-growing grasses may be important eonsiderations in managing habitat for Texas kangaroo rats. Moderately to heavily grazed sites may provide better habitat for these state-threatened mammals.
Dipodomys elator (Merriam 1894) is a state threatened species. The International Union for the Conservation of Nature (1986) lists habitat loss and degradation resulting from agricultural and infrastructure development as major threats. Though degradation such as fragmentation and loss of habitat have played important roles, changes in vegetation patterns may also be important. Much historic range of the Texas kangaroo rat has been fragmented by extensive cultivation within the Rolling Plains Region of Texas and adjacent regions of Oklahoma (Correll & Johnston 1970).
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Cultivation fragmented the grasslands and only those areas unsuitable for cultivation were left in their natural state. These fragments were fenced by ranchers and grazed by cattle and provided some habitat for the Texas kangaroo rat. However, because of a decline in ranching, some of these pasturelands are no longer grazed and have been invaded by introduced species such as Japanese brome. Additionally, lack of fire has allowed the increase of woody vegetation such as honey mesquite (Prosopis glandulosa) and lotebush (Ziziphus obtiisifolia). In some cases, Texas kangaroo rats used these woody species as burrow sites because the plants collected wind-blown soil and the Texas kangaroo rats dig burrows at their bases. However, as mesquites mature, their shade changes the vegetation composition sometimes favoring introduced grasses like Japanese brome, which grows densely and changes the habitat so that it is more suitable for other types of small mammals.
Mesquite forest was not seen as a problem by the Texas Parks and Wildlife Department (TPWD) because of the assumption that this habitat was required for Texas kangaroo rats. However, perceptions regarding threats to the species and ideas about future management have changed. Research has suggested that (1) mesquite is not a critical component of D. elator habitat (Stangl et al. 1992; Goetze et al. 2007), (2) grazing may benefit D. elator (Stangl et al. 1992; Stasey 2005; Goetze et al. 2007), and (3) Texas kangaroo rats opportunistically use human structures that collect friable soils as burrow sites (Stangl et al. 1992; Stasey 2005; Goetze et al. 2007). Schmidly (2004), which is used by TPWD as their main source of small mammal data for the state, states that heavily grazed rangeland and the eroded sites of rangeland roadways may provide optimum habitat. NatureServe (2008) states that vegetation has become overgrown and that rangeland practices that result in dense growth of grasses or invasion of non-native grasses have degraded habitat because the Texas kangaroo rat thrives in heavily grazed or otherwise disturbed conditions. NatureServe (2008) further states that habitat for D. elator consists of sparsely vegetated areas that may or may not include honey mesquite, including
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heavily grazed land, disturbed areas, and areas along fencerows adjacent to cultivated fields and roads. These current statements are quite different from Davis & Schmidly (1994), who stated that Texas kangaroo rat burrows invariably entered the ground at the base of a mesquite and the primary threat contributing to the rarity of the species was the clearing of mesquite brush.
Currently, the only relatively large populations of Texas kangaroo rats known in Wichita County occur in pastures with small or scattered mesquite, and burrows are often not associated with mesquite at all, but rather with lotebush, prairie mounds (natural, elevated, and relatively bare areas possibly uplifted by clay soils swelling in cracks; Diggs et al. 1999), or in areas where man¬ made berms occur due to road, fence, and oilfield construction, or in association with old (>30 years), unbumed brush piles where wood has decayed leaving a mound of loose friable soil (Stangl et al. 1992; Goetze et al. 2007). Stangl et al. (1992) hypothesized that grazing bison and prairie dogs, along with fire, historically maintained the type of disturbances needed by the Texas kangaroo rat. Also, prolonged drought likely played an important role in fire frequency and maintaining short vegetation with intermittent bare patches of soil. Natural prairie heterogeneity such as prairie mounds (Diggs et al. 1999; Goetze et al. 2007) appear to be important in providing the type of habitat needed by the Texas kangaroo rat before cattle grazing and human mediated disturbances were used opportunistically as burrow sites (Stangl et al. 1992). In areas where cattle no longer graze or at sites where native vegetation has been replaced by introduced species, it appears that populations of Texas kangaroo rats have declined.
Ecological characterization of burrows in situations that lacked grazing as a component are rare (Martin & Matocha 1992; Stasey 2005). Martin & Matocha (1992) trapped for 10 trap nights and characterized a burrow where a single Texas kangaroo rat was trapped in association with a fence row adjacent to a gravel county road in Motley County, Texas. No other mammals were captured. This capture site contained vegetation characteristic of a disturbed
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site and was adjacent to a field of Sudan grass. At the capture site there was 30.2% bare ground, 65% grasses and 4.8% forb (Martin & Matocha 1992).
Stasey (2005) trapped for 972 trap nights in a mesquite forest with an understory dominated by Japanese brome. His site was within 4.0 km of a large and persistent Texas kangaroo rat population in Wichita County where the grazing regime is heavy (Goetze et al. 2007). During his investigation, he caught only two kangaroo rats on the periphery of the mesquite forest habitat. One was caught in a friable clay soil that had blown in and accumulated around the comer posts that supported the gate leading into the pasture and the other was captured along the fence separating this pasture from a wheat field where a berm had accumulated due to plowing next to the fence line. Stasey (2005) caught Sigmodon hispidus, Peromysciis leucopus, and P. maniculatiis in the core of the ungrazed site. In the core of the ungrazed pastureland, where no Texas kangaroo rats were captured, seven quadrats were sampled to assess vegetation characteristics. Percent bare ground had a mean of 10.9%, grasses 63.7%, and forbs 16.1%, whereas the mean average herbaceous height was 49.0 cm (Stasey et al. 2005).
Because identifying habitat critical to the survival of the species is a research priority (Jones et al. 1988), the purpose of this investigation was to compare a moderately grazed site to that of a heavily grazed site, both of which have populations of kangaroo rats. These data were then compared to data from ungrazed sites dominated by Japanese brome (Stasey 2005) and vegetation associated with a disturbed roadside (Martin & Matocha 1992).
Materials and Methods
The study area is in Wichita County on the east side of the intersection of highways 1739 and 2384 and is a privately owned ranch that is moderately grazed pasture (0.30 head per ha). Coordinates at the entrance of the ranch are 34.05423 N, 98.81721 W. The pastureland is fenced, has small mesquite (less than 2 m. in height), and has several old oil field storage sites. Mesquite density
NELSON ET AL.
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at the site is 168/ha. This site was compared to a nearby population of Texas kangaroo rat known in Wichita County and its locality and history have previously been described (Stangl et al. 1992; Goetze et al. 2007). Grazing at this site is intense (0.81 head/ha) and it has about 54 small (less than 2m in height with most under 1 m) mesquite/ha (Goetze et al. 2007).
All trapping was done using 7.5 by 8.8 by 30 cm Sherman traps with rolled oats as bait. Traps were set just before dark and checked early the next day. Based on parameters set by Stangl et al. (1992) and Stasey (2005) regarding burrow entrance diameter, angle of entry, and vegetation, suspected burrows were selected at the sites and three traps were placed around each burrow entrance.
All vegetation data was quantified in May so that direct comparisons could be made, thus eliminating seasonal vegetative changes. For burrows where at least one Texas kangaroo rat was caught, one square meter quadrats were centered around burrow entrances and percentage cover, grass, forb, bare ground, and woody vegetation (when present) was recorded (Goetze et al. 2007). Vegetative richness and height were measured and the dominant grass, forb, and woody species of each quadrat were identified (Goetze et al. 2007). Quantitative data was compared using SPSS 14.0 (SPSS, Inc. 2005). A Mann Whitney test was used to test for significant differences in richness and percentages of grasses, forbs, bare ground, and woody vegetation between the two grazed sites. In addition, data from a previous study (Stasey 2005) at a site that was ungrazed was included in a Kruskal-Wallis analysis to test for significant differences between the grazed and ungrazed sites.
Dominant vegetation at the site was identified using floras for the state and for north central Texas (Correll & Johnson 1970; Diggs et al. 1999). Voucher specimens are deposited in the Tarleton State University Herbarium (TAG).
The specific location of each burrow was recorded in decimal degrees using a Garmin GPS- 12 unit and burrows were classified as
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being associated with human-mediated disturbances such as old brush piles and fence rows, or other available natural habitats that included prairie mounds, which are elevated, open areas formed by clay soil shrinkage and swelling (Diggs et al. 1999), or accumulation of soil at the base of lotebushes or honey mesquites (Goetze et al. 2007; Table 1).
Results
At the moderately grazed site, three traps were placed around each of 12 burrows which resulted in the capture of 10 D. elator. No other rodents were captured. Three of the animals were caught in each of the traps placed at one burrow and two were caught in the three traps surrounding another burrow site. The dominant grass at five of the seven burrows was little barley (Hordeum pusilhim) with buffalograss (Buchloe dactyloides) and rescue grass {Bromus catharticus) being dominant at the other two burrows (Table 1). The dominant forb at six of the seven burrows was Texas broom weed {Gutierrezia texana) with Virginia pepperweed (Lepidium virginicum) being dominat at the other burrow (Table 1). Five of the seven quadrats had honey mesquite (Prosopis glandulosa) as the dominant woody vegetation and two contained no woody vegetation (Table 1). Two burrows were associated with fence rows and five with honey mesquite (Table 1).
At the heavily grazed site, three traps were placed around each of 22 burrows which resulted in the capture of 1 8 D. elator. Of these, 10 burrow sites were analyzed for vegetation and burrow associations. At the heavily grazed site, little barley was always the dominant grass and most quadrats contained Virginia pepperweed as the dominant forb (Table 1). Other herbaceous dominants included Texas broomweed, hog potato {Hoffmannseggia glaiica), and western ragweed {Ambrosia psilostachya) (Table 1). Woody vegetation was evenly distributed between lotebush and honey mesquite. At the heavily grazed site, five burrows were associated with old brush piles, two with prairie mounds, one with a fence row, and one each with lotebush and honey mesquite (Table 1).
NELSON ET AL.
125
Table 1. Dominant vegetation and burrow classifications at the two study sites. Dominant forbs are broomweed {Gutierrezia texana), hog potato {Hoffmanmegia glauca), pepperweed (Lepidhim virginicum), and ragweed {Ambrosia psilostachy^a). Dominant grasses are barley {Hordeum pmillum), buffalo grass {Biichloe dactyloides), and rescue grass {Bromiis catharticm). Woody vegetation includes lotebush {Zizyphus obtiisifolia) and mesquite (Prosopis glandiilosa). Biurow classifications included in this table are defined in the methods section of this paper.
Moderately grazed burrows:
|
Burrow # |
1 |
2 |
3 |
4 |
5 |
6 |
7 |
|
FORBS |
|||||||
|
Broomweed |
X |
X |
X |
X |
X |
X |
|
|
Pepperweed |
X |
||||||
|
GRASS |
|||||||
|
Barley |
X |
X |
X |
X |
X |
||
|
Buffalo |
X |
||||||
|
Rescue |
X |
||||||
|
WOODY VEG. |
|||||||
|
Mesquite |
X |
X |
X |
X |
X |
||
|
None |
X |
X |
|||||
|
Burrow assoc. |
|||||||
|
Fence |
X |
X |
|||||
|
Mesquite |
X |
X |
X |
X |
X |
||
|
Heavily grazed burrows: |
|||||||
|
Burrow # |
1 |
2 |
3 |
4 |
5 |
6 |
7 8 9 10 |
FORBS
Broomweed
Hog potato
Pepperweed
Ragweed
Unknown
GRASS
Barley
WOODY VEG. Lotebush Mesquite None
Burrow assoc. Fence Lotebush Mesquite Old brush pile Prairie mound
XXX
XXX
X
X X
X
X X
X
X
X
X
X
X
X
X
X
X
X X X X X X
X X
X
X X
X
X X
X
X
X
X
126
THE TEXAS JOURNAL OF SCIENCE, VOL. 61, NO. 2, 2009
Average herbaceous height, percentage bare ground, and percentage woody vegetation were significantly different between heavily and moderately grazed sites (Table 2). Percentage forbs, grasses, and other categories such as rocks and stumps, as well as richness were not significantly different between sites (Table 2).
Average herbaceous height (P = 0.001), percentage bare ground (P = 0.009) and grasses (P = 0.009) were significantly different when comparing the moderately and heavily grazed sites as well as the ungrazed site examined by Stasey (2005).
Discussion
Little barley, Texas broomweed, hog potato, Virginia pepperweed, and western ragweed occur in disturbed habitats (Diggs et al. 1999). These plants were dominant species associated with burrows of Texas kangaroo rats and their occurrence is likely caused by disturbances such as grazing of cattle and rodent activity around the burrows. Habitat of D. elator was dominated by short, herbaceous vegetation (2.0 - 40.0 cm in height). There is general agreement that D. elator requires a sparse, short-grassland habitat (Dalquest & Collier 1964; Roberts & Packard 1973; Carter et al. 1985; Stangl et al. 1992), and findings from this current study support this conclusion. These findings also indicate that grazing may be important in maintaining sparse, short grassland habitat. When comparing two grazed sites and an ungrazed site (Stasey 2005), the only significant differences were in average herbaceous vegetation height and percentage bare ground and grass. Grazing can change these three parameters, which appear to be important in maintaining Texas kangaroo rat habitat. As previously discussed, this is complicated by the dominance of the introduced grass, Bromus japonicas at the ungrazed site and additional studies need to be conducted at ungrazed sites containing native vegetation. However, based on the lack of D. elator at this site and the relative abundance at the grazed sites, it appears that grazing plays a role in maintaining suitable habitat for Texas kangaroo rats. Lack of grazing significantly increased vegetation height at the ungrazed
NELSON ET AL.
127
Table 2. Comparison of heavily and moderately grazed sites for average herbaceous height, percentage coverage of bare ground, forbs, grasses, woody, other (rocks, stumps, posts, etc.), and riclmess. Comparisons are made using means, standard deviations (in parentheses), and ranges [in brackets] and evaluated using Wilcoxon Mann- Whitney test. Significant differences at P < 0.05 are denoted by an asterick.
|
Heavily Grazed |
Moderately Grazed |
P-value |
|
|
Avg. Herb. Height |
7.1 (±7.9) [2.0-40.0] |
24.5 (±12.7) [9.0-29.4] |
0.0001* |
|
% Bare Ground |
49.9 (±24.0) [0.0-80.0] |
20.7 (±18.1) [5.0-60.0] |
0.024* |
|
% Forbs |
16.5 (±13.1) [1.0-35.0] |
33.7 (±22.6) [15.0-67.0] |
0.133 |
|
% Grasses |
24.60 (±18.9) [1.0-55.0] |
20.1 (±15.6) [1.0-45.0] |
0.623 |
|
% Woody |
6.0 (±15.8) [0.0-50.0] |
26.1 (±26.5) [0.0-60.0] |
0.037* |
|
% Other |
2.0 (±4.2) [0.0-2.0] |
0.0 (±0.0) [O.O-O.O] |
0.222 |
|
Riclmess |
6.2 (±2.4) [3.0-10.0] |
7.6 (±1.8) [6.0-10.0] |
0.137 |
site, which on average was double the moderately grazed site and seven times greater than the heavily grazed site. Percentage of grasses was about three times greater on average at the ungrazed site when compared to grazed sites. Percentage bare ground, on average was about one-half that of the moderately grazed site and about one-fourth that of the heavily grazed site. This tall, dense coverage by grasses may impede Texas kangaroo rat movement, inhibit their ability to see potential predators, and may make burrow construction difficult. Lack of bare ground likely inhibits their dust bathing activities.
Burrows at the grazed site compare favorably to the burrow ecological characteristics reported from Motley County (Martin & Matocha 1992). In the classification system used for burrows and described in the Materials and Methods, this burrow would have been a fence line association and the animals were likely using soil that accumulated at the base of the fence. Although no grazing was reported at this site, the value reported for bare ground percentage (30.2%) compares favorably with the grazed sites in this investigation but forb percentage (4.8%) was low and grass percentage was high (65%). The location of this burrow in a fence row berm may have provided the friable soil preferred for burrow development. Its location at the edge of a sudan field adjacent to a gravel road (Martin & Matocha 1992) may have provided enough
128
THE TEXAS JOURNAL OF SCIENCE, VOL. 61, NO. 2, 2009
disturbance to maintain bare patches for dust bathing and for foraging trails that still allow the rats to spot predators.
Of the 17 burrows examined in this investigation, 47% were associated with human disturbances including old brush piles and fence rows. The other burrows were associated with more natural sites such as shrubs and prairie mounds. In the heavily grazed site most burrows were associated with 30 year old brush piles, while at the moderately grazed site most were associated with honey mesquite. Second in number of burrow associations at the heavily grazed site was prairie mounds and none of this association was observed at the moderately grazed site. Heavy grazing might make prairie mounds more suitable as burrow sites, since that was the only place this habitat association occurred. At the heavily grazed site, lotebush and honey mesquite associations were equal in number while no lotebush associations were observed at the moderately grazed site. This is likely because the moderately grazed site had woody vegetation dominated by honey mesquite whereas the heavily grazed site had some lotebush available. The type of shrub is probably not as important as is the accumulation of loose, friable soil at the base of the shrubs.
Extrinsic disturbance caused by grazing, fire, or drought, and natural landscape heterogeneity such as prairie mounds probably is important for burrow site selection in Texas kangaroo rats. The slight elevation of prairie mounds may provide more bare ground because of a drier microclimate and better drainage. Also, the animals can dig their more characteristically horizontal openings into the sides of these mounds. Opportunistic use of any natural or manmade disturbance where friable soil accumulates such as around shrubs, the bases of rocks, fence lines, cattle pens, pasture and oil field roads, abandoned equipment, old, unbumed brush piles with most of the wood decayed have been observed (Stangl et al. 1992; Goetze et al. 2007). Almost one-half of the burrows in this investigation may be characterized as such, supporting hypotheses of opportunistic use made by others (Stangl et al. 1992; Stasey
NELSON ET AL.
129
2005; Goetze et al. 2007). These manmade disturbances likely mimic natural prairie heterogeneity.
Investigations of Texas kangaroo rats that examine symbiosis with prairie dogs, effects of fire in maintaining habitat, the role of drought on habitat, and additional research into the influence of natural prairie heterogeneity and grazing regimes are critical for understanding the animal’s niche. Surveys need to be conducted at Buffalo Creek Reservoir and Lake Arrowhead State Park to ascertain if D, elator occurs in any protected natural areas (pnas) in Wichita County or if not, if suitable habitat is available in protected natural areas. Also, based on the results of this investigation, managers of pnas may need to consider grazing as a management practice to promote the development of habitat for the Texas kangaroo rat and other organisms that require grazing as a disturbance.
Acknowledgments
We would like to thank Oscar and Edith Goetze for allowing access to their properties in Wichita County and for room and board while conducting fieldwork. Tarleton State University Organized Faculty Research provided funding for parts of this project. This study was conducted under Texas Parks and Wildlife permit SPR- 0496-775.
Literature Cited
Carter, D. C., W. D. Webster, J. K. Jones, Jr., C. Jones & R. D, Suttkus. 1985.
Dipodomys elator. Mammalian Species, 232: 1-3.
Correll, D, S. & M. C. Johnston. 1970. Manual of the vascular plants of Texas.
Texas Research Foundation. Renner, Texas. 1083 pp.
Dalquest, W. W. & G. Collier. 1964. Notes on Dipodomys elator, a rare kangaroo rat. Southwestern Nat, 9:146-150.
Davis, W. B. & D. J. Schmidly. 1994. The mammals of Texas. Texas Parks and Wildlife Press. Austin, TX, 338 pp.
Diggs, G. M., B. L. Lipscomb & R. J. O’Kennon. 1999. Shinners & Mahler’s Illustrated Flora of North Central Texas. Botanical Research Institute of Texas. Fort Worth, Texas, 1626 pp.
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Goetze J. R, W. C. Stasey, A. D. Nelson, & P. D. Sudman. 2007. Habitat attributes and population size of Texas kangaroo rats on an intensely grazed pasture in Wichita County, Texas. The Texas J. of Sci., 59(1):1 1-22.
International Union for Consei*vation of Nature and Natural Resources. 1986. 1986 lUCN red List of threatened animals. lUCN. Cambridge, U. K., 105 pp.
Jones, C., M. A. Bogan & L. M. Mount. 1988. Status of the Texas kangaroo rat {Dipodomys elator). The Texas J. of Sci., 40(3):249-258.
Martin, R. E. & K. G. Matocha. 1991. The Texas kangaroo rat, Dipodomys elator, from Motley County, Texas, with notes on habitat attributes. Southwestern Nat., 36:354-356.
Merriam, C. H. 1894. Preliminaiy descriptions of eleven new kangaroo rats of the genera Dipodomys and Perodipus. Proc. Biol. Soc. Washington, 9:109-1 16.
NatureServe. 2008. NatureServe Explorer: An online encyclopedia of life [web application]. Version 7.0. NatureServe, Arlington, Virginia. Available http://www.natureserve.org/explorer. (Accessed: September 4, 2008 ).
Roberts, J. D. & R. L. Packard. 1973. Comments on movements, home range and ecology of the Texas kangaroo rat, Dipodomys elator Merriam. J. Mamm., 54:957-962.
Schmidly, D. J. 2004. The mammals of Texas, revised edition. University of Texas Press, Austin, Texas, 501 pp.
Stangl, F. B., Jr., T. S. Schafer, J. R. Goetze & W. Pinchak. 1992. Opportunistic use of modified and disturbed habitat by the Texas kangaroo rat {Dipodomys elator). The Texas J. of Sci., 44(l):25-35.
Stasey, W. C. 2005. An evaluation of Texas kangaroo rat {Dipodomys elator): Biological habits and population estimation. Unpublished Masters Thesis. Tarleton State University, 45 pp.
SPSS, Inc. SPSS 14.0 brief guide. 2005. Prentice Hall. Upper Saddle River, New Jersey, 245 pp.
ADN at: nelson@tarleton.edu
TEXAS J. OF SCI. 61(2): 131-146
MAY, 2009
BREEDING BIOLOGY OF THE
BARN SWALLOW (HIRUNDO RUSTICA) IN NORTHEAST TEXAS WITH TEMPORAL AND GEOGRAPHIC COMPARISONS TO OTHER NORTH AMERICAN STUDIES
K. T. Turner and J. G. Kopachena
Department of Biological and Environmental Sciences Texas A&M University-Commerce, Commerce, Texas 75429
Abstract.-The reproductive output of American bam swallows (Hirimdo nistica erythrogaster) was studied over a five year period at a colony in northeast Texas. Clutch size, hatching success, nestling success, and nesting success were all found to vary significantly among years suggesting that the swallows were influenced by annual changes in enviromnental conditions. However, the observed annual variations in clutch size, hatching success, and nesting success were well within the range observed among 14 other studies in North America. The greatest sources of mortality were hatch failure, followed by infanticide and ectoparasites. These sources of mortality were also common in other studies. Despite the wide geographic range of bam swallows in North America, there were no latitudinal trends in clutch size, hatching success, or nesting success. Lastly, in the 44 years spanned by the analysis, there was no evidence of changes in reproductive output, suggesting that American bam swallows have not yet been obviously impacted by global climate change.
Barn swallows (Hirundo nistica) have been well studied, especially in Europe. They have been used to study the adaptive value of colonial nesting (Snapp 1976; Shields & Crook 1987), the effects of parasitism (Saino et al. 1998; Barclay 1988; Kopachena et al. 2000; Merino et al. 2000; Moller 2000), sexual selection (Saino & Moller 1996; Kose et al. 1999; Perrier et al. 2002; Saino et al.
2002) and immunocompetence (Saino & Moller 1996; Saino et al. 1997; Merino et al. 2000; Hasselquist et al. 2001; Saino et al.
2003) . In North America studies on the breeding biology of barn swallows have been conducted in West Virginia (Samuel 1971), New York (Ramstack et al. 1998), and Kansas (Thompson 1961; Anthony & Ely 1976). Two studies on breeding biology were performed in Texas, one in Brazos County (Barr 1979) and one in south central Texas (Martin 1974). A third study in Texas examined the effect of a selenium-contaminated lake on the reproductive
132
THE TEXAS JOURNAL OF SCIENCE-VOL. 61, NO. 2, 2009
success of bam swallows in Rusk County (King et al. 1994).
Because of their broad geographical distribution and ease of study, bam swallows should make a good model species to study temporal and geographic patterns in reproductive success and behavior. Such studies can be useful in elucidating how species with broad distributions can adapt to variations in climate and resource availability.
This study documented the breeding biology of bam swallows at a colony in northeast Texas for a five-year period. The data are used to provide baseline data on this species in this region and to document temporal variation in breeding parameters across years. These data are used to compare with breeding parameters described in the literature from other locations in North America. Lastly, a comparison of temporal and spatial variation is used to determine if there are geographic trends in breeding output.
Materials and Methods
During the breeding seasons of 1998 through 2002, 369 nests were studied at a colony near Commerce, Texas. The nests were located under two parallel two-lane bridges located 2.3 km south of the junction of State Highway 50 and Loop 178. The nests were checked at least once a day from April 1 through July 31 of each year. In 1998, nests were checked between 14:00h and 17:00h CDT. For the remaining years, the nests were checked between 08:00h and 10:30h CDT. Nest initiation date was defined as the date on which an egg first appeared in a nest. Each nest was given a unique number upon initiation.
Nestlings in each nest were marked with a unique combination of toenail clippings on the day of hatching and again on the sixth day post-hatching (St. Louis et al. 1989). Nests were checked daily until fledging. If a nestling died, the cause of death, where possible, was noted. Causes of death were categorized as follows. Eggs that failed to hatch were noted as failed to hatch. Barn
TURNER & KOPACHENA
133
swallows in both Europe and North America practice infanticide (Crook & Shields 1985; Moller 1994). In the current study, infanticide was identified by the presence of eggs on the ground below the nest or the presence of chicks on the ground below the nest. In the latter case, most chicks were dead or dying and usually had evidence of trauma on the abdomen. Chicks found on the ground that were over 12 days of age and which were otherwise healthy were considered to have fledged early. Infanticide was stratified into infanticide during the incubation period and infanticide during the nestling stage. Many nests were infected with swallow bugs {Oeciaciis vicarius), tropical fowl mites {Ornithonyssus bursa), or both. In heavily infested nests the chicks were noticeably exsanguinated and jaundiced. Deaths that occurred in these nests were attributed to the parasites. In some nests, nestlings showed signs of decline in the absence of obvious parasite infections, while in other cases nestlings died shortly after hatching without apparent cause. In either case the cause of death was assigned as unknown. Similarly, nestlings that disappeared prior to the twelfth day were assumed to have died from unknown causes.
Each nestling’s mass and right primary feather length was measured at twelve days post hatching. A 50g spring scale was used to measure nestling mass to the nearest O.lg. Digital calipers were used to measure the primary feather length to the nearest 0.01mm. Clutch size, brood size at hatch, brood size on day 12, and per capita mortality rate for whole broods were calculated.
The temporal pattern of nests containing eggs showed a distinctly bimodal distribution for all years, indicating that the majority of pairs were double-brooded. Since adult pairs were not marked, this distribution was used to define first and second broods.
To compare the data collected in northeast Texas with other studies a literature survey was conducted. Data using the same measures of mean clutch size, hatching success, and fledging success as used in the current study were obtained from 14 studies
134
THE TEXAS JOURNAL OF SCIENCE-VOL. 61, NO. 2, 2009
in which location and year of study were provided. For each study, the latitude of the study area was recorded. Along with the current study, data spanning 44 years and over 19® of latitude were collected. These data were used to examine the extent of variation in reproductive output among studies and to determine whether reproductive output has changed over time or varies relative to latitude.
Statistical analyses were done using SAS (Version 9.1). Where parameters were not normally distributed, non-parametric statistics were used.
Results
In all years the modal clutch size was five (Fig. 1). However, the average clutch size varied among years, being highest in 1999 and lowest in 1998 (Kruskal- Wallis Test, Chi-Square Approxi¬ mation, X^= 11.44, df = 4, p = 0.0220). Clutch size also varied between first and second broods. Five-egg clutches were most common in first broods, whereas four-egg clutches were more common in second broods (Fig. 2) (Chi-Square, 2 by 2 Contingency Table, = 29.91, df = \, p < 0.0001). Clutch size varied significantly among years for first broods (Kruskal- Wallis Test, Chi-Square Approximation, X^= 17.36, df^ 4, /? = 0.0016), but not for second broods (Kruskal-Wallis Test, Chi-Square Approximation, 3.81, df= 4,p = 0.4317).
Hatching success for all years combined is summarized in Table 1. It was measured as the percentage of eggs that hatched and as the percentage of nests experiencing complete hatch failure (whole clutch loss. Table 1). The percentage of eggs hatching varied significantly among years (Chi-Square, 2 by 5 Contingency Table, X^ = 23.20, df = 4, p < 0.0001) whereas there was little annual variation in the number of whole clutches lost (Chi-Square, 2 by 5 Contingency Table, X^ = 5.96, df= 4, /7 = 0.2022). The proportion of eggs hatching did not differ between first and second broods
TURNER & KOPACHENA
135
Clutch Size
Figure 1. Distribution of clutch sizes for each year from 1998 through 2002. Number of clutches monitored each year were as follows: 1998 = 86, 1999 = 105, 2000 = 42, 2001 =55, 2002 = 81.
Clutch Size
Figure 2. Distribution of clutch sizes for first and second broods.
Table 1. Breeding success of bam swallows at a colony in northeast Texas from 1998 tln ough 2002. Means are expressed as mean + standard deviation. Numbers in parentheses are sample sizes.
136
THE TEXAS JOURNAL OF SCIENCE-VOL. 61, NO. 2, 2009
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TURNER & KOPACHENA
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(Chi”Square, 2 by 2 Contingency Table, = 1.60, df = p = 0.2059). Similarly, there was no statistical difference between first and second broods relative to whole clutch losses (Chi-Square, 2 by 2 Contingency Table, 1.68, df= \,p = 0,1949).
Nestling success for all years combined is also summarized in Table 1. It was measured as the percent of nestlings that hatched and survived to day twelve and by the percent of nests with eggs that hatched that experienced whole brood loss during the nestling period. Survivorship of nestlings varied significantly from year to year for second broods (Chi-Square, 2 by 5 Contingency Table,
= 21.95, df= A,p = 0.0002), but not for first broods (Chi-Square, 2 by 5 Contingency Table, X^ = 7.53, df = 4, p = 0.1104). First broods had higher survival than second broods (Chi-Square, 2 by 2 Contingency Table, X^ = 21.88, df ^ 1, /? < 0.0001). However, during the nestling period, whole brood losses did not differ significantly between first and second broods (Chi-Square, 2 by 2 Contingency Table, X^ = 0.03, df= \,p = 0.8625) or among years (Chi-Square, 2 by 5 Contingency Table, X^ = 6.74, df = 4, p = 0.1503).
Total nesting success (nesting success) was determined as the number of eggs laid that resulted in chicks surviving to day twelve (Table 1). Percent survival of nestlings until day 12 varied significantly among years (Chi-Square, 2 by 5 Contingency Table, X^== 30.92, df= 4,p < 0.0001) and was higher for first broods than for second broods (Chi-Square, 2 by 2 Contingency Table, X^ = 5.80, df= 4,p = 0.016). The percentage of whole brood loss varied significantly among years (Chi-Square, 2 by 5 Contingency Table, X^ = 13.93, df= 4, p = 0.0075), but did not differ overall between first and second broods (Chi-Square, 2 by 2 Contingency Table, X^ = 0.99,#= 1,/? = 0,3197).
Measurements of mass and primary feather length were taken on the 12^^ day after hatching (Table 1). First broods generally had higher mean mass than did second broods (Wilcoxon Two-Sample
138
THE TEXAS JOURNAL OF SCIENCE-VOL. 61, NO. 2, 2009
Failed to Infanticide Infanticide Parasites Unknown Hatch Eggs Nestlings
Figure 3. Causes of mortality for all cases observed from 1998 through 2002. For more detail on causes of mortality, see text.
Test, Normal Approximation, -6.9451, n = 162, 110, p < 0.0001) and mass also varied among years for both first (Kruskal-Wallis Test, Chi-Square Approximation, = 21.91, df= 4, p = 0.0002) and second broods (Kruskal-Wallis Test, Chi-Square Approximation, X^= 33.32, df= 4,p< 0.0001). On the other hand, there was no difference in primary feather length among years (Kruskal-Wallis Test, Chi-Square Approximation, = 5.12, df= 4, p = 0.2748) or between first and second broods (Wilcoxon Two- Sample Test, Normal Approximation, 1.5635, 162, 110, =
0.1179).
For both first and second broods the most common source of mortality was hatch failure; more than a third of all mortalities were hatch failures (Fig. 3). However, with the exception of infanticide during the nestling period, the frequency for all causes of mortality varied significantly between first broods and second broods (Chi- Square, 2 by 5 Contingency Table, = 61.11, df= 4, p < 0.0001) (Fig. 3). Hatch failure, infanticide during incubation, and mortality
TURNER & KOPACHENA
139
due to parasites were all higher for first broods than for second broods. The number of unknown mortalities was higher for second broods than for first broods.
The values for clutch size^ hatching success, and fledging success (mean number of chicks surviving to day 12, Table 1) were well within the range of values obtained in the 14 studies used for comparison (Table 2). The geographic variance in clutch size, hatching success, and fledging success observed among these studies did not differ from the among year variance of these same measures observed in this study (Folded F-test for Equality of Variance; clutch size, /= 2.42, df= 12, 4, /? = 0.4073; hatching success, /= 2.79, df= 4,7,p = 0.2244; fledging success, /= 2.49, df = 8, 4,/? = 0.3954).
The data were used to determine if reproductive success varied relative to latitude or the year of study. There was no statistical correlation between clutch size, hatching success, or fledging success and latitude (Pearson’s r: clutch size, r = 0.35, n= 14, /? = 0.2201; hatching success, r = 0.157, = 9, /? = 0.2163; fledging
success, r = 0.046, n = 10, /? = 0.8991). Similarly, there was no significant correlation between clutch size, hatching success, or fledging success and year of study (Pearson’s r: clutch size, r = 0.199, n = 14, jf? = 0.4955; hatching success, r = -0.133, n = 9, p = 0.7330; fledging success, r = -0.320, n=\0,p = 0.3667).
Discussion
Clutch size, hatching success, nestling success and total nesting success of barn swallows at the Texas colony were found to vary considerably between years. This likely reflects variations in resource availability, which, in turn, is a product of variations in climatic variables (Stenseth et al. 2002). In northeast Texas, temperatures are lower and precipitation is higher in May and June than in July and August. Such conditions are likely to contribute to higher nesting success in first broods than in second broods. Furthermore, as conditions become hotter and drier in July and
Table 2. Breeding data collected from other studies conducted in North America.
140
THE TEXAS JOURNAL OF SCIENCE-VOL. 61, NO. 2, 2009
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For two-year studies, the first year of the study was used. For studies longer than two years, tlie median year was used.
TURNER & KOPACHENA
141
August, the annual reproductive output in bam swallows becomes more variable, suggesting that the birds are more sensitive at this time to fluctuations in resource availability. The tendency for first broods to do better than second broods is a trend that is common in temperate zone nesting birds (Perrins 1970). However, among bam swallows deviations from this pattern have been documented in Kansas (Anthony & Ely 1976) and West Virginia (Samuel 1971)
Measures of clutch size, hatching success, and fledging success also varied considerably among the geographic locations documented in the literature. However, the variation among geographic locations did not differ from the variation among years in the current study. Given that there was also no trend in breeding output relative to latitude or date, and given that most of the cited studies were short term (one or two years), it seems unlikely that there is substantial difference among geographic localities in overall, long term reproductive performance among bam swallow populations in North America.
Hatch failure was the single greatest source of mortality in the current study, followed closely by infanticide during the egg and nestling period. Hatch failure is apparently rather common in many bam swallow populations (Brown & Brown 1999) and appears to be mainly due to infertility (Moller 1994). Infertility was likely the main source of hatch failure in the current study as well, since unhatched eggs seldom showed signs of development when they were examined.
Infanticide was cited as the major source of nestling mortality in Denmark (Moller 1994) and as the second most frequent cause of mortality in New York (Sheilds & Crook 1987). Other studies in North America, make no mention of infanticide. There are two possible reasons for this. First, both the Sheilds & Crook (1987) study and the current study were conducted on large colonies and the rate of infanticide increases with colony size and population density (Moller 2004). If other studies were conducted at much
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THE TEXAS JOURNAL OF SCIENCE-VOL. 61, NO. 2, 2009
smaller colonies, then infanticide may be less common and less easily detected. Secondly, the other studies may not have considered the possibility that bam swallows exercise infanticide. In these cases, cases of infanticide may have simply been categorized as egg loss or nestling loss. Infanticide in North American populations of bam swallows remains poorly documented and is in need of further study.
Bam swallows are well known to harbor a variety of ectoparasites (Brown & Brown 1999). Ectoparasites were con¬ sidered to be the single greatest source of mortality in New York (Shield & Crook 1987) and in Manitoba (Barclay 1988) and this may be tme in many other populations as well (Brown & Brown 1999). However, the types of ectoparasites seem to vary considerably from one area to another. For example, the sole ectoparasite observed associated with bam swallow nests in Manitoba were hematophagous mites (Barclay 1988). In New York, nests were infected with blow flies (Protocalliphora sp.). In the current study, bam swallow nests were found to be infected with both tropical fowl mites {Ornithonyssus bursa) and swallow bugs (Oeciacus vicarius). Swallow bugs have apparently spread from associations with cliff swallows and are now widespread in bam swallow colonies in northeast Texas (Kopachena et al. 2007).
Interestingly no latitudinal trend in clutch size was found for North American bam swallows. In Europe and Asia, Bam Swallow clutches are smaller at low latitudes and larger at high latitudes (Moller 1994). Similar trends occur in other species in both western and eastern hemispheres. Thus increasing clutch size with increasing latitude has been found in house wrens nesting from South America through Canada (Young 1994), eastern bluebirds nesting in the United States (Dhondt et al. 2002), and great tits nesting in Spain, Eurasia, North Africa, and the Netherlands (Sanz 1998). However, some species do not conform to this pattern. For example Red-breasted Sapsuckers (Sphyrapicus ruber) and Red- naped Sapsuckers {Sphyrapicus nuchalis) show no latitudinal trends
TURNER & KOPACHENA
143
in clutch size (Walters et* al 2002). Sanz (1997) found a variation in clutch size in Pied Flycatchers relative to latitude in a study in central Spain, the Netherlands, and Great Britain, but Jarvinen (1989) did not find this to be true in Finland. In the case of North American bam swallows there does not appear to be sufficient latitudinal stratification of resource availability and constraints on reproduction to warrant latitudinal trends in clutch size.
Climate change has been shown to affect reproductive ecology of birds in recent years (Gordo et al. 2004; Both et al. 2006; Visser et al. 2006). However, we found that clutch size, hatching success, and fledging success among barn swallows has not varied substantially from 1956 to 2000. Thus, there is no evidence that global warming is affecting North American bam swallows based on this rather crude analysis. This result may not be surprising given that bam swallows, as an adaptable generalist species, seem well adapted to accommodating environmental fluctuations and novel conditions.
Acknowledgements
The research was supported by three Texas A&M University- Commerce Mini Grants and a Texas A&M Univerisity-Commerce faculty research grant. The field assistance of Dr. Tony Buckley, Greg Potts, and Sigrid Slemp is gratefully acknowledged.
Literature Cited
Altemus, E. L. 1977. Bam swallow nesting data. Cassinia, 56:24-25.
Anthony, L. W. & C. A. Ely. 1976. Breeding biology of bam swallows in west- central Kansas. Kansas Om. Soc. Bull., 27(4):37-43.
Barclay, R. M, R. 1988. Variation in the costs, benefits, and frequency of nest reuse by bam swallows {Hirundo rustica). Auk, 105:53-60.
Barr, A. L, 1979. Nesting success, growth rates, and recruitment of bam swallows Hirundo rustica in Brazos County, Texas. Unpublished MS Thesis, Texas A&M University, College Station, Texas, 50pp.
Both, C., S. Bouwhuis, C. M. Lessells & M. E. Visser. 2006. Climate change and population declines in a long-distance migratoiy bird. Nature, 44:81- 83.
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Brown, C. R. & M. B. Brown. 1999. Bam swallow {Hirundo rusticd). Pp. 1-32 in The Birds of North America, No. 452 (A. Poole & F. Gill, eds.). The Birds of North America, Inc., Philadelphia, PA.
Crook, J. R. & W. M. Shields. 1985. Sexually selected infanticide by adult male bam swallows. Anim. Behav., 33:754-761.
Dhondt, A. A., T. L. Kast & P. E. Allen. 2002. Geographical differences in seasonal clutch size variation in multi-brooded bird species. Ibis, 144:646-651.
Goodman, S. M. 1982. A test of nest cup volume and reproductive success in the bam swallow. Jack-Pine Warbler, 60: 107-1 12.
Gordo, O., L. Brotons, X. Ferrer & P. Comas. 2004. Do changes in climate patterns in wintering areas affect the timing of the spring arrival of trans-Saharan migrant birds? Global Change Biology, 11: 12-21.
Gme, C. E., T. J. O’Shey & D. J. Hoffman. 1984. Lead concentrations and reproduction in highway-nesting bam swallows. Condor, 86:383-389.
Hasselquist, D., M. F. Wasson & D. W. Winkler. 2001. Humoral immunocompetence con’elates with date of egg-laying and reflects work load in female tree swallows. Behav. Ecol., 12:93-97.
Jarvinen, A. 1989. Clutch-size variation in the Pied Flycatcher Ficedula hypoleuca. Ibis, 131:572-577.
Johnsgard, P. A. 1979. Birds of the Great Plains: the breeding species and their distribution. Univ. Nebraska Press, Lincoln, xlv+539 pp.
Johnston, R. F. 1960. Directory to the bird-life of Kansas. Univ. Kansas Mus. Nat. Hist. Misc Publ., 23:1-69.
King, K. A., T. W. Custer & D. A. Weaver. 1994. Reproductive success of bam swallows nesting near a selenium-contaminated lake in East Texas, USA. Env. Poll., 84:53-58.
Kopachena, Jeffrey G., Anthony J. Buckley & Greg A. Potts. 2000. Effects of the American swallow bug {Oeciacus vicarius) on reproductive success of bam swallow (Hinmdo rustica). Tex. J. Sci., 52(1): 33-47.
Kopachena,. J. G., B. L. Cochran & T. B. Nichols. 2007. The incidence of American swallow bugs {Oeciacus vicarius) in bam swallow {Hirundo rustica) colonies in northeast Texas. J. Vector Ecol., 32: 280-284.
Kose, M., R. Mand & A. P. Moller. 1999. Sexual selection for white tail spots in the bam swallow in relation to habitat choice by feather lice. Anim. Behav., 58:1201-1205.
Lohoefener, R. 1980. Comparative breeding biology and ethology of colonial and solitary nesting bam swallows {Hirundo rustica) in east-central Mississippi. Ph.D. Dissertation, Mississippi State University, Mississippi, ix+72 pp.
Martin, R. F. 1974. Syntoptic culvert nesting of cave and bam swallows in Texas. Auk, 91:776-782.
McGinn, D. B. & H. Clark. 1978. Some measurements of swallow breeding biology in lowland Scotland. Bird Study, 25:109-1 18.
Merino, S., A. P. Moller, & F. de Lope. 2000. Seasonal changes in cell-mediated immunocompetence and mass gain in nestling bam swallows: a parasite-mediated effect? Oikos, 90:327-332.
TURNER & KOPACHENA
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Moller, A. P. 1991. Clutch size, nest predation, and distribution of avian unequal competitors in a patchy environment. Ecology, 72:1336-1349.
Moller, A. P. 1994. Sexual selection and the bam swallow. Oxford Univ. Press,
Oxford, x+365pp.
Moller, A. P. 2000. Survival and reproductive rate of mites in relation to resistance of their bam swallow hosts. Oecologia, 124:351-357.
Moller, A. P. 2004. Rapid temporal change in frequency of infanticide in a passerine bid associated with change in population density and body condition. Behav. Ecol., 15:462-468.
Perrier, C., F. de Lope, A. P. Moller & P. Ninni. 2002. Stmctural coloration and sexual selection in the bam swallow Hirimdo rustica. Behav. Ecol., 13:728-736.
Peixins, C. M. 1970. The timing of birds’ breeding seasons. Ibis, 112:242-255.
Ramstack, J. M., M. T. Murphy, & M. R. Palmer. 1998. Comparative reproductive biology of three species of swallows in a common environment. Wilson Bull., 110:233-243.
Saino, N., A. M. Bolzem & A. P. Moller. 1997. Immunocompetence, ornamentation, and viability of male bam swallows {Hirundo rustica). Proc. Nat. Acad. Sci., 94:549-552.
Saino, N., S. Calza & A. P. Moller. 1998. Effects of a dipteran ectoparasite on immune response and growth trade-offs in bam swallow, Hirimdo rustica, nestlings. Oikos, 81:217-228.
Saino, N. & A. P. Moller. 1996. Sexual ornamentation and immunocompetence in the bam swallow. Behav. Ecol., 7:227-232.
Saino, N., M. Incagli, R.Martinelli, & A. P. Moller. 2002. Immune response of male bam swallows in relation to parental effort, corticosterone plasma levels, and sexual ornamentation. Behav. Ecol., 13:169-174.
Saino, N., R. Ambrossini, R. Martinelli, P. Ninni, & A. P. Moller. 2003. Gape coloration reliably reflects immunocompetence of bam swallow {Hirimdo rustica) nestlings. Behav. Ecol., 14:16-22.
Samuel, D. E. 1971. The breeding biology of bam and cliff swallows in West Virginia. The Wilson Bull., 83:284-301.
Sanz, J. J. 1997. Geographic variation in breeding parameters of the pied flycatcher Ficedula hypoleuca. Ibis, 139: 107-1 14.
Sanz, J. J. 1998. Effeets of geographic location and habitat on breeding parameters of great tits. Auk, 1 15:1034-1051.
Shields, W. H. & J. R. Crook. 1987. Bam Swallow coloniality: A net cost for group breeding in the Adirondacks? Ecology, 68:1373-1386.
Smith, H. G. & R. Montgomerie. 1991, Sexual selection and the tail ornaments of North American bam swallows. Behav. Ecol. and Sociobiol., 28:195-201.
Snapp, B. D. 1976. Colonial breeding in the bam swallow {Hirundo rustica) and its adaptive significance. Condor, 78:471-480.
St. Louis, V. L., J. C. Barlow & J. R. A. Sweerts. 1989. Toenail-clipping: a simple technique for marking individual chicks. J. Field Omithol., 60:21 1-215.
Stenseth, N., A. Mysetemd, G. Ottersen, J. W. Hurrell, K. Chan & M. Lima. 2002. Ecological effects of climate fluctuations. Science, 297:1292-1296.
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Thompson, M. C. 1961. Observations on the nesting success of the Bam Swallow in South-Central Kansas. Kansas Om. Soc. Bull., 13(2):9-11.
Visser, M. E., L. J. M. Holleman, & P. Gienapp. 2006. Shifts in caterpillar biomass phenology due to climate change and its impact on the breeding biology of an insectivorous bird. Oecologia, 147:164-172.
Walters, E. L., E. H. Miller, & P. E. Lowther. 2002. Red-breasted Sapsucker {Sphyrapicus ruber) and Red-naped Sapsucker {Sphyrapicus nuchalis). Pp. 1-32 in The Birds of North America, No. 663 (A. Poole & F. Gill, eds.). The Birds of North America, Inc., Philadelphia, PA.
Young, B. E. 1993. Geographical and seasonal patterns of clutch-size variation in House Wrens. The Auk, 1 1 1:545-555.
JGK at: Jeff_Kopachena@tamu-commerce.edu
TEXAS J. SCI. 61(2), MAY, 2009
147
GENERAL NOTES
REPRODUCTIVE CYCLE OF THE CENTRAL AMERICAN MABUYA, MABUYA UN MARGIN ATA (SQUAMATA: SCINCIDAE) FROM COSTA RICA
Stephen R. Goldberg
Department of Biology’, Whittier College, PO Box 634 Whittier, California 90608
The Central American mabuya, Mabuya iinimarginata is a common diurnal skink ranging from Colima and Veracruz, Mexico to Panama at 1-1,500 m where it inhabits a variety of habitats (Savage 2002). Information on its reproduction is in Webb (1958), McCoy (1966), Fitch (1973), Alvarez del Toro (1982), Savage (2002) and Guyer & Donnelly (2005). Females give birth to live young. The purpose of this paper is to add to the knowledge of the reproductive biology of M unimarginata from a histological analysis of gonadal material. The first information on the M unimarginata testicular cycle is presented. New minimum sizes for reproduction in males and females of M unimarginata are reported.
A total of 25 adult males (mean snout-vent length, SVL = 64.8 mm ± 7.4 SD, range = 51-77 mm) and 30 females (SVL = 70.0 mm ± 11.0 SD, range = 50-92 mm) from Costa Rica were examined from the herpetology collection of the Natural History Museum of Los Angeles County (LACM), Los Angeles, California.
The left testis was removed from males and the left ovary was removed from females for histological examination. Tissues were embedded in paraffin, sectioned at 5 pm and stained with Harris’hematoxylin followed by eosin counterstain (Presnell & Schreibman 1997). Histology slides are deposited in LACM. An unpaired Mest was used to compare male and female mean body sizes and the relationship between female SVL and litter size was
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examined by linear regression analysis using Instat, vers. 3.0b, Graphpad Software, San Diego, CA.
Material examined -1\\q following specimens of M unimarginata from Costa Rica (by province) were examined: Guanacaste: {n = 22) LACM 166201, 166202, 166204, 166211, 166214, 166219, 166226, 166228, 166230, 166231, 166234-
166236, 166240, 166244, 166245, 166249-166251, 166257,
166260, 166264. Heredia: = 1) LACM 166252. Limon: {n=\2) LACM 166203, 166210, 166215, 166218, 166220, 166227,
166243, 166253, 166262, 166265, 166266, 166277. Puntarenas: {n = 20) LACM 166200, 166213, 166216, 166224, 166225, 166238, 166239, 166241, 166242, 166248, 166255, 166258, 166261,
166269, 166271-166275, 166279.
Three stages in the testicular cycle (Table 1) were present: (1) regressed (= quiescence), seminiferous tubules contain Sertoli cells and spermatogonia; (2) recrudescence (= recovery), proliferation of cells in the germinal epithelium is in progress, primary, secondary spermatocytes and, in some cases, spermatids are present; (3) spermiogenesis (= sperm production), lumina of seminiferous tubules lined by spermatozoa; clusters of metamorphosing spermatids are present. The smallest reproductively active male (spermiogenesis in progress) measured 52 mm SVL (LACM
166279) and was collected in February. This likely represents a new minimum size for maturity of M. unimarginata males. Spermiogenesis occurred in all months except August (only 3 males examined), suggesting that sperm production may be continuous.
The mean body size of M. unimarginata females was significantly larger than that of males (unpaired t test, t = 2.0, df= 53, P = 0.05). Females ovulate tiny eggs which develop to live young. The smallest reproductively active female measured 50 mm SVL (2 mm diameter eggs in oviducts) and was from May (LACM 166234). This likely represents a new minimum size for maturity of M. unimarginata females. Reproductive activity (Table 2) was
TEXAS I SCI 61(2), MAY, 2009
149
recorded in all months sampled, suggesting reproduction may be continuous. One female from February (LACM 166231) contained corpora lutea and convoluted oviducts indicating parturition had recently occurred. Females with discernible embryos were seen in April and June to September. Linear regression analysis indicated a significant positive correlation between female body size (SVL) and developing eggs and/or embryos: n = 30, r = 0.48, P = 0.007, Y = ~0.13 + 0.07X.
The finding of males exhibiting recrudescence from June to September, and one male each from July and September with regressed testes, suggests there may be some seasonality in the testicular cycle of M unimarginata. In contrast, only spermiogenic males were reported for the sympatric gecko, Lepidoblepharis xanthostigma, by Goldberg (2008).
Fitch (1973) reported two females from March that contained well-developed embryos and suggested births may be concentrated around March. The finding of one female from February that had recently given birth supports the hypothesis of Fitch (1973). In contrast, Webb (1958) reported that M unimarginata (as Mabuya mabouya) from southern Mexico gave birth to 4-6 young in June and July. The size for sexual maturity in males was estimated at 56 mm SVL and for females at 62 mm, with a suggestion that females as small as 56 mm SVL were mature (Webb, 1958). Alvarez del Toro (1982) reported M unimarginata (as Mabuya brachypoda) gave birth to 4-6 young in June through August in Chiapas, Mexico. McCoy (1966) reported M unimarginata (as Mabuya brachypoda) from southern El Peten Province, Guatemala contained 6-9 embryos. Somma & Brooks (1976) reported M. unimarginata (as Mabuya mabouya) from Dominica collected in February, August, September and December contained embryos.
While it is apparent that M unimarginata from Costa Rica has an extended reproductive cycle with activity exhibited in all months, subsequent work is needed to elucidate details of the
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THE TEXAS JOURNAL OF SCIENCE-VOL. 61, NO. 2, 2009
Table 1. Monthly conditions in testicular cycle of 25 Mabuya iinimarginata from Costa Rica. Values are the numbers of males exhibitmg each of the three conditions.
|
Month |
n |
Regression |
Recrudescent |
Spermiogenesis |
|
January |
1 |
0 |
0 |
1 |
|
February |
1 |
0 |
0 |
1 |
|
March |
1 |
0 |
0 |
1 |
|
May |
2 |
0 |
0 |
2 |
|
June |
6 |
0 |
1 |
5 |
|
July |
4 |
1 |
1 |
2 |
|
August |
3 |
0 |
3 |
0 |
|
September |
6 |
1 |
2 |
3 |
|
October |
1 |
0 |
0 |
1 |
Table 2. Monthly stages in the ovarian cycle of 30 Mabuya iinimarginata from Costa Rica. Sizes of ovulated follicles are in mm. The post-partum female from February contained corpora lutea and convoluted oviducts.
|
Month |
n |
2 mm |
3-5 nun |
>6 nun |
Post-partum |
|
February |
2 |
0 |
1 |
0 |
1 |
|
April |
4 |
2 |
1 |
1 |
0 |
|
May |
1 |
1 |
0 |
0 |
0 |
|
June |
7 |
1 |
5 |
1 |
0 |
|
July |
6 |
2 |
4 |
0 |
0 |
|
August |
1 |
0 |
0 |
1 |
0 |
|
September |
5 |
1 |
1 |
3 |
0 |
|
October |
4 |
3 |
1 |
0 |
0 |
ovarian cycle (e.g., seasonal and geographic variation in timing of parturition).
Acknowledgment
I thank Christine Thacker (Natural History Museum of Los Angeles County) for permission to examine M unimarginata. Specimens are part of the CRE (Costa Rica Expeditions) collection donated to LACM by Jay Savage in 1998.
Literature Cited
Alvarez del Toro, M. 1982. Los Reptiles de Chiapas, Tercera Edic. Coleccion Libros de Chiapas, Tuxtla Gutienez, Chiapas, 248 pp.
TEXAS I SCL 61(2), MAY, 2009
151
Fitch, H. S. 1973. A field study of Costa Rican lizards. Univ. Kansas Sci. Bull., 50:39- 126.
Goldberg, S. R. 2008. Notes on the reproductive biology of the Costa Rica scaly-eyed gecko, Lepidoblepharis xanthostigma (Squamata: Gekkonidae), from Costa Rica. Bull. Chicago Herpetol, Soc., 43:130-131.
Guyer, C. & M. A. Donnelly. 2005. Amphibians and Reptiles of La Selva, Costa Rica, and the Caribbean Slope. A Comprehensive Guide. University of California Press, Berkeley, viii + 299 pp.
McCoy, C. J. 1966. Additions to the herpetofauna of southern El Peten, Guatemala. Herpetologica, 22:306-308.
Presnell, J. K. & M. P. Schreibman. 1997. Humason’s Animal Tissue Techniques. 5* Ed., Johns Hopkins Press, Baltimore, xix + 572 pp.
Savage, J. M. 2002. The Amphibians and Reptiles of Costa Rica. A Herpetofauna Between two Continents, Between two Seas. The University of Chicago Press, Chicago, 934 pp.
Somma, C. A. & G. R. Brooks. 1976. Reproduction in Anolis oculatm, Ameiva fmcata and Mabuya mabouya from Dominica. Copeia, 1976:249-256.
Webb, R. G. 1958. The status of the Mexican lizards of the genus Mabuya. Univ. Kansas Sci. Bulk, 38:1303-1313.
SRG at: sgoldberg@whittier.edu
NEW GEOGRAPHIC DISTRIBUTION RECORDS FOR PARAJULID MILLIPEDS (DIPLOPODA: JULIDA),
IN ARKANSAS AND TEXAS
Chris T, McAllister and Henry W. Robison
RapidWrite, 102 Brown Street Hot Springs National Park, Arkansas 71913 and Department of Biology, Southern Arkansas University Magnol ia, A rkansas 71754
The primary North American milliped family Parajulidae ranges from Yakutut, Alaska, and James Bay, Ontario, to western El Salvador (Shelley 2008), This large and complex assemblage of taxa includes the genus Aniulus Chamberlin which, at present, contains at least 22 species inhabiting various habitats from the Atlantic Ocean to southwestern Utah, and north to south, from southern Quebec to southern Texas and Arizona (Shelley 2001; McAllister et ak 2009). Another group, the subgenus Hakiulus,
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ranges from the vicinity of the Canadian border in North Dakota and Michigan to the Rio Grande in Texas and east to west, extending from central Ohio to eastern Michigan to southwestern Colorado (Shelley 2000). There are currently eight species of Aniuliis within the subgenus Hakiulus; one of these, Aniuliis (Hakiulus) amophor (Chamberlin), was described from material collected along Turtle Creek, Kerr County, Texas (Chamberlin 1940). Since then, additional records of A. {Hakiulus) amophor have been reported only from Texas (Chamberlin & Hoffman 1958; Hoffman 1999; Shelley 2000). Herein, this study provides a significant distributional record for A. {Hakiulus) amophor in Arkansas, as well as 13 new county records for other species/subspecies Aniuliis in Texas.
Between October 2002 and November 2007, millipeds were collected from various sites in Arkansas and Texas. Collecting techniques involved using a potato rake to move debris, turning decaying logs, peeling bark off fallen trees, and moving leaf litter and rocks; pitfall trapping was used at only one site. Following preliminary identification, specimens were placed in vials containing 70% ethanol and shipped to Rowland M. Shelley at the North Carolina State Museum of Natural Sciences, Raleigh, North Carolina (NCSM) for verification of identification. Voucher specimens were subsequently deposited in the NCSM. Taxa recovered are presented below along with distributional (state, county, specific locality, number of millipeds and sexes, collection date) information.
Annotated List of Species
Aniulus {Hakiulus) amophor (Chamberlin).“ARKANSAS: Union Co., El Dorado (33.1244°N, 92.3957°W), S. 27 November 2007. A single male specimen was collected with a pitfall trap from a yard in urban habitat. This is the first time this species has been reported from a state outside of Texas. This milliped was previously known from Bexar, Comal, DeWitt, Gonzales, Guadalupe, Jasper, Jim Wells, Karnes, Kerr, Live Oak, San
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Patricio, Wharton, and Wilson counties. The new disjunct site reported herein is ca. 365 km NE of the most proximate locality of A. (Hakiulus) amophor in Jasper, Jasper Co., Texas. Other myriapods collected at this site included Eurymerodesmus angularis Causey and Hemiscolopendra marginata (Say).
Compared to northern Arkansas where the late Nell B. Causey (1910-1979) did most of her work (Causey 1950; 1951; and others), little is known about the general milliped fauna of southern Arkansas. New records for Arkansas millipeds were reported by McAllister et al. (2002a; 2002b; 2003) and McAllister & Shelley (2008). In addition, several miscellaneous taxonomic papers by Shelley (1990), Shear (2003), Shelley & McAllister (2006) and Shelley et al. (2006) reported millipeds from various southern Arkansas counties. Obviously, additional collecting of millipeds should be attempted in this part of the state as well as eastern Arkansas where there are few records.
Aniulus (Hakiuhis) diversijrom diversifrons (Wood).-TEXAS: Bowie Co., 11.3 km N DeKalb off CR (County Road) 3207, 2(S, 3$, 23 November 2004; Delta Co., Cooper Lake State Park, Doctors Creek Unit, S, 3 January 2003; Hood Co., Fort Spunky off CR 1120, 3(5', 49, 17 February 2005; Marion Co., Berea Six off FM 728, (5^, $, 2 juvs., 23 October 2002; Titus Co., Argo, off FM 1993 at Snake Creek, 10 November 2003. These sites (Fig. 1) document five new county records for A. (Hakiulus) diver sifi^ons diversifrons. It has previously been reported from much of the central United States, including Arkansas, Illinois, Michigan, Minnesota, Missouri, North Dakota, Ohio, Oklahoma, and Texas (Shelley 2000). In Texas, this milliped was known previously from Anderson, Baylor, Brown, Cherokee, Colorado, Dallas, Erath, Grayson, Hamilton, Hopkins, Hunt, Lavaca, Milam, Potter, Randall, Smith, Stonewall, Travis, Val Verde, and Wilson counties (Stewart 1969; Shelley 2000).
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Figure 1. Distribution of Aniuhis spp. in Texas (solid symbols = new records; open symbols = literature records). A. (Hakiulns) diversifrom diversifrom (stars); A. (Hakhilits) diversifrom neomexicamis (crosses); A. (Hakiulus) diversifrom intergrades (diamonds); A. brazomis (dots); A. craterm craterus (squares); A. craterus intergrades (triangles); A. fluviatilis (inverted triangles).
Aniiilus {Hakiulus) diversifrons neomexicanus (Chamberlin).- TEXAS: Brown Co., Brownwood State Park, 20.9 km NNW Brownwood, 27 November 2002; Limestone Co., Confederate Reunion Grounds State Park, 6(5^, 189, 21 December 2002. This milliped was previously known from Colorado and New Mexico, and Hudspeth, Potter, and Randall counties, Texas (Shelley 2000). Two new county records are documented herein (Fig. 1) that are considerable distances east of previous Texas localities in the Panhandle and Guadalupe Mountains areas of the state.
Aniulus (Hakiulus) diversifrons intergrades.-TEXAS: Coleman Co., 3.2 km E Talpa off US 67, 2S, 29, juv., 23 December 2006; Tom Green Co., San Angelo, 156 Las Lomas Trail, 6S, 79, 4 juvs., 13 November 2005 & 24 December 2006. These specimens display gonopodal characters intermediate between those of two races, A. (Hakiulus) diversifrons diversifrons and A. (Hakiulus) diversifrons
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neomexicanus (Chamberlin). Shelley (2000) previously reported similar intergrades from Garza Co., Texas, and Larimer Co., Colorado, and the new sites (county records. Fig. 1) are a considerable distance northwest and southeast, respectively, from those localities.
Aniulus brazonus Chamberlin .-TEXAS: Dallas Co., Cedar Hill State Park, Talaha Trail, S, 2$, 16 November 2002. This represents only the second record of A. brazonus ever documented, as the species was previously known only from the type locality in Brazos County, Texas (Shelley 2001). These specimens were collected underneath leaf litter and decaying logs in prairie habitat dominated by mesquite, live oak, and ashe juniper; the new site (Fig. 1) is ca. 240 km N of the type locality.
Aniulus craterus craterus Chamberlin.-TEXAS: Kimble Co., South Llano River State Park, 3.2 km S Junction, 6S, 2$, 22 February 2003; 1.6 km NE Telegraph off US 377 at Llano River, 3(?, 3$, 21 February 2004; 8.0 km SW Junction off US 377 at Bailey Creek, c?, 21 February 2004. This milliped was previously reported from Bandera (Loomis 1959) and Bexar and Kerr counties (Shelley 2001). This study documents a new county record (Fig. 1) in the Edwards Plateau (Hill Country), the northernmost localities for^. craterus in the state.
Aniulus craterus intergrades.-TEXAS: Uvalde Co., Gamer State Park, Crystal Cave, 2 March 2004. These specimens display gonopodal characters intermediate between those of two subspecies, A. craterus craterus and^. craterus fill Loomis. This is the first time, to the author’s knowledge, that Aniulus millipeds have been reported from Uvalde County (see Fig. 1).
Aniulus fluviatilis Chamberlin.-TEXAS: Hood Co., Fort Spunky off CR 1 120, 3(5^, 20 February 2004. This represents a new county record as A. fluviatilis was known previously from Brazos and Polk counties (Causey 1952; Shelley 2001). The new site (Fig.
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1) is a considerable distance northwest and west of previously reported localities into the Cross Timbers area of the state. Specimens were collected underneath rocks in disturbed shortgrass prairie habitat dominated by mesquite, ashe juniper, live oak, and cottonwood.
Acknowledgments
We thank Dr. R. M. Shelley (NCSM) for specimen identification and curatorial assistance, the Arkansas Game and Fish Commission and Texas Parks and Wildlife Department for scientific collecting permits issued to CTM, and J. T. McAllister, III, D. Moore, T. Ratliff, and T. Sciara for assistance in collecting.
Literature Cited
Causey, N. B. 1950. Five new Arkansas millipeds of the genera Eiirymerodesmus and Paresmiis (Xystodesmidae). Ohio J. Sci., 50:267-272.
Causey, N. B. 1951. On Eurymerodesmidae, a new family of Diplopoda (Strongylosomidae), and a new Arkansas species of Eurymerodesmus. Proc. Arkansas Acad. Sci., 4:69-71.
Causey, N. B. 1952. New species and records of paraiulid millipeds from Texas. Texas J. Sci., 4(2):200-203.
Chamberlin, R. V. 1940. New genera and species of North American Paraiulidae. Bull. Univ. Utah, 30 [Biol. Ser. 5]: 1-39.
Chamberlm, R. V. & R. L. Hoffean. 1958. Checklist of the millipeds of North America. U.S. Nat. Mus. Bull., 212:1-236.
Hoffman, R. L. 1999. Checklist of the millipeds of North and Middle America. Virginia Mus. Nat. Hist. Spec. Publ., 8:1-584.
Loomis, H. F. 1959. Millipeds collected enroute from Florida to San Antonio, Texas, and vicinity. J. Washington Acad. Sci., 49:157-163.
McAllister, C. T. & R. M. Shelley. 2008. New records of eurymerodesmid millipeds (Diplopoda: Polydesmida) from Arkansas, Kansas, Louisiana, Oklalioma, and Texas. J. Arkansas Acad. Sci., 62:155-158.
McAllister, C. T., R. M. Shelley & J. T. McAllister, III. 2002a. Millipeds (Artluopoda: Diplopoda) of the Ark-La-Tex. 11. Distributional records for some species of western and central Arkansas and eastern and southeastern Oklahoma. J. Arkansas Acad. Sci., 56:95-98.
McAllister, C. T., R. M. Shelley & J. T. McAllister, III. 2003. Millipeds (Arthiopoda: Diplopoda) of the Ark-La-Tex. III. Additional records from Arkansas. J. Arkansas Acad. Sci., 57:115-121.
McAllister, C. T., R. M. Shelley & S. E, Trauth. 2009. Aniuhis garius (Chamberlin, 1912), a widespread milliped in central and eastern North America (Julida: Parajulidae: Aniulini). Spec. Publ. Virgmia Mus. Nat. Hist., 16:229-238.
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McAllister, C. T., C. S. Harris, R. M. Shelley & J. T. McAllister, III. 2002b. Millipeds (Arthropoda: Diplopoda) of the Ark-La-Tex. 1. New distributional and state records for seven counties of the west Gulf Coastal Plain of Arkansas. J. Arkansas Acad. Sci., 56:91-94.
Shear, W. A. 2003. Branneria bonocuhis n. sp., a second species in the North American milliped family Brarmeriidae (Diplopoda: Chordeumatida: Brannerioidea). Zootaxa, 233:1-7.
Shelley, R. M. 1990. Revision of the milliped family Eurymerodesmidae (Polydesmida:
Chelodesmidea). Mem. American Entomol. Soc., 37:1-112.
Shelley, R. M. 2000. Parajulid studies II. The subgenus Hakwlus Chamberlin (Julida:
Parajulidae: Parajulinae: Aniulmi). Myriapodologica, 6:121-145.
Shelley, R. M. 2001. A synopsis of the milliped genus Aniidiis Chamberlin (Julida:
Parajulidae: Parajulinae: Aniulini). Texas Mem. Mus., Speleol. Monogr., 5:73-94. Shelley, R. M. 2008. Way down south: the milliped family Parajulidae (Julida: Parajulini) in Mexico and Central America; first records from El Salvador and the Baja California peninsula. Zootaxa, 1893:1-37.
Shelley, R. M. & C. T. McAllister. 2006. Composition and distribution of the milliped tribe Pachydesmini west of the Mississippi River (Polydesmida: Xystodesmidae). W. North Amer. Nat., 66:45-54.
Shelley, R. M., C. T. McAllister & M. F. Medrano. 2006. Distribution of the milliped genus Narceus Rafinesque, 1820 (Spirobolida: Spirobolidae): Occurrences in New England and west of the Mississippi River: A summary of peripheral localities; and first records from Connecticut, Delaware, Maine, and Minnesota. W. North Amer. Nat., 66:374-389.
Stewart, T. C. 1969. Records of millipeds in twenty five northeast Texas counties. Texas J. Sci., 20(4):383-385.
CTM at: drctmcallister@aol.com
NOTEWORTHY RECORDS OF DRAGONFLIES (ODONATA: ANISOPTERA) FROM JONES AND TAYLOR COUNTIES OF CENTRAL TEXAS
Thomas E. Lee, Jr., Amisha J. Patel, Benjamin W. Johnson and Roy C. Vogtsberger*
Department of Biology, Abilene Christian University Abilene, Texas 79601 and ^Department of Biology, Midwestern State University Wichita Falls, Texas 76308
There is growing interest in the biology of dragonflies (Odonata: Anisoptera) among both amateur naturalists and professional biologists (e.g., Dunkle 2000; Kondratieff 2000; Merritt & Cummins
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1996; Milne & Milne 1994; Needham & Westfall 1955; Needham et al. 2000; Silsby 2001). Little is known of the dragonfly fauna of the Southern Rolling Plains (Abbott 2001), although Abbott et al. (2003) provided a recent synopsis of dragonflies from the Texas Panhandle.
Reported below are the partial results of recent collecting efforts from the contiguous central Texas counties of Jones and Taylor. This study examined the holdings from Abilene Christian University Natural History Collection (ACUNHC) and Hardin- Simmons University Invertebrate Collection (HSUIC), which provided records for 23 species of anisopterans, of which eight are from the families Aeshnidae, Corduliidae, and Libellulidae. Eight taxa were geo¬ graphically noteworthy, and are listed below. The majority of the specimens were collected between 1966 and 1977, although some specimens were taken as recently as 2001. Identifications were based on Merritt & Cummins (1996) and Dunkle (2000). Kondratieff (2000) and Reece & McIntyre (2008) provided the basis for detennination of geographic significance.
Family Aeshnidae
Rhionaeschna multicolor (Hagen I861).-Taylor County: un¬ specified locality, 1 (ACUNHC 0956). The specimen represents a county record, with the most proximate record from adjoining Jones County.
Family Corduliidae
Didymops transversa (Say 1839).-Taylor County: Abilene, 1 (HSUIC 4). This specimen represents a county record and range extension of approximately 200 km to the north from Kimble County.
Epitheca costalis (Selys 1871).“Taylor County: unspecified locality, 3 (ACUNHC 0998, ACUNHC 0999, and ACUNHC 01000); Abilene, 1 (HSUIC 2). These specimens represent a county record and range extension of approximately 200 km to the north from Kimble County.
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N eurocordulia xanthosoma (Williamson 1908) -Jones County: unspecified locality, 1 (ACUNHC 01003). This specimen represents a county record and range extension of approximately 200 km to the northwest from San Saba County.
Family Libellulidae
Libellula luctuosa (Burmeister 1839) —Jones County: Hawley Farm, Clear Fork of the Brazos River, 3 (ACUNHC 0489, ACUNHC 0736, and ACUNHC 0737); Lake Fort Phantom Hill, 1 (ACUNHC 0545). These specimens represent a county record, with the most proximate record from adjoining Taylor County.
Pachydiplax longipennis Burmeister 1839. -Jones County: Hawley Farm, Clear Fork of the Brazos River, 1 (ACUNHC 0589). This specimen represents a county record, with the most proximate record from adjoining Taylor County.
Plathemis lydia (Drury 1773). -Jones County: Hawley Fanu, Clear Fork of the Brazos River, 1 (ACUNHC 0740); Lake Fort Phantom Hill, 2 (ACUNHC 0516 and ACUNHC 0517). These specimens represent a county record, with the most proximate record from adjoining Taylor County.
Tramea lacerata Hagen 1861. -Jones County: Hawley Farm, Clear Fork of the Brazos River, 1 (ACUNHC 0495). Taylor County: Abilene, 1 (HSUIC 13). These specimens represent county records, with the most proximate record from approximately 80 km to the north from Coleman County.
Literature Cited
Abbott, J. C. 2001. Distribution of dragonflies and damselflies (Odonata) in Texas.
Trans. American Entomol. Soc., 127:189-228.
Abbott, J. C., R. A. Belirstock & R. R. Larsen. 2003. Notes on the distribution of Odonata in the Texas Panhandle, with a summary of new state and county records. Southwestern Nat., 48(3):444-449.
Dunkle, S. W. 2000. Dragonflies Through Binoculars: A Field Guide to Dragonflies of North America. Oxford Univ. Press, New York, 266 pp.
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Kondratieff, B. C. 2000. Dragonflies and Damselflies (Odonata) of the U. S. Jamestown, North Dakota; Northern Prairie Wildlife Research Center, US Geological Survey (government web page).
Merritt, R. W. & K. W. Cummins (eds.). 1996. An hitroduction to the Aquatic Insects of North America, ed. Kendall/Hunt Publ. Co., Dubuque, Iowa, 862 pp.
Milne, L. & M. Milne. 1994. National Audubon Society Field Guide to North American Insects and Spiders. Alfred A. Knopf, New York, 989 pp.
Needliam, J. G. & M. J. Westfall, Jr. 1955. A Manual of the Dragonflies of North America. Univ. of California Press, Berkeley, xii + 615 pp.
Needham, J. G., M. J. Westfall, Jr. & M. L. May. 2000. Dragonflies of North America.
Scientific Publishers, Gainesville, Florida, 615 pp.
Reece, B. A. & N. E. McIntyre. 2008. Dragonfly (Odonata: Anisoptera) Holdings of the Museum of Texas Tech University. Occasional Papers, Museum of Texas Tech University, 279:1-13.
Silsby, J. 2001. Dragonflies of the World. Smithsonian Institution Press, Washington,
216 pp.
TEL at: lee@biology.acu.edu
THE TEXAS ACADEMY OF SCIENCE, 2009-2010
OFFICERS
William J. Quinn, St. Edward’s University Benjamin A. Pierce, Southwestern University Romi L. Burks, Southwestern University Raymond C. Mathews, Jr., Texas Water Dev. Board Fred Stevens, Schreiner University Diane B. Hyatt, Texas Water Development Board Ned E. Strenth, Angelo State University Frederick B. Stangl, Jr., Midwestern State University John A. Ward, Brooke Army Medical Center AAAS Council Representative: James W. Westgate, Lamar University International Coordinator: Armando J. Contreras, Universidad Autonoma de N.L.
DIRECTORS
2007 Renard L. Thomas, Texas Southern University Bob Murphy, Texas Parks and Wildlife Department
2008 Christopher M. Ritzi, Sul Ross State University Andrew C. Kasner, Audubon Texas
2009 Ana B. Christensen, Lamar University Thomas L. Arsuffi, Texas Tech at Junction
SECTIONAL CHAIRPERSONS
Anthropology: Raymond Mauldin, University of Texas at San Antonio Biomedical: G. Scott Weston, University of the Incarnate Word Botany: David Lemke, Texas State University
Cell and Molecular Biology: Magaly Rincon-Zachary, Midwestern State University
Chemistry and Biochemistry: J. D. Lewis, St. Edward’s University
Computer Science: James McGuffee, St. Edward’s University
Conservation Ecology: Wendi Moran, Hardin-Simmons University
Environmental Science: Kenneth R. Summy, University of Texas-Pan American
Freshwater Sciences: Matt Chumchal, Texas Christion University
Geosciences: Chris Barken, Stephen F. Austin State University
Marine Sciences: Larry D. McKinney, Harte Research Institute
Mathematics: Elsie M. Campbell, Angelo State University
Physics: David L. Bixler, Angelo State University
Science Education: Patricia Ritschel-Trifilo, Harden-Simmons University
Systematics and Evolutionary Biology: Tara Maginnis, St. Edward’s University
Terrestrial Ecology and Management: Richard Patrock, St. Edward’s University
COUNSELORS
Collegiate Academy: David S. Marsh, Angelo State University Junior Academy: Vince Schielack, Texas A&M University
President:
President Elect: Vice-President:
Immediate Past President: Executive Secretary: Corresponding Secretary: Managing Editor: Manuscript Editor: Treasurer:
PERIODICALS
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THE TEXAS JOURNAL OF SCIENCE
Volume 61, No. 3 August, 2009
CONTENTS
Nesting Ecology of Golden Mice {Ochrotomys nuttalli) in Eastern Texas.
By Cody W Edwards and Andy P. Bradstreet . . . . . 163
The Sand Dollar Periarchus lyelli (Echinoidea: Clypeasteroida: Scutelliformes) in the Caddell Formation (Upper Eocene) of Texas.
By Louis G. Zachos . . . . . . . 181
Mixed Infections of Nasopharyngeal Bots, Cephenemyia spp. (Oestridae) in
White-Tailed Deer {Odocoileus virginianus) and Mule Deer {Odocoileus hemionus) of Texas.
By Samuel W. Kelley . . . 187
Karyotype Diversity Among and Within Avian Taxa: A Simple Test in R.
By Michael F. Small, Michael R. J. Forstner and John T, Baccus . 195
The Arkansas Endemic Fauna: An Update with Additions, Deletions,
A Synthesis of New Distributional Records, and Changes in Nomenclature.
Chris T. McAllister, Henry W. Robison and Michael E. Slay . . . 203
Selection of Available Post-Fire Substrate by the Ground Skink,
Scincella lateralis (Squamata: Scincidae).
By Charles M. Watson . . . . . . . .....219
General Notes
Reproduction in Smith’s Green-Eyed Gecko, Gekko smithii (Squamata: Gekkonidae).
By Stephen R. Goldberg . . . . . 225
The Long-Tailed Weasel Mustela frenata (Mammalia: Mustelidae) in Baja California, Mexico.
By Gorgonio Riiiz-Campos, Roberto Martlnez-Gallardo,
Salvador Gonzdlez-Guzmdn and Jorge Alaniz-Garcla . . . 229
Stomach Contents of Calidris minutilla (Charadriiformes: Scolopacidae) Wintering at a Freshwater Reservoir in West-Central Texas.
By Andrew C. Kasner, Randall H. Ruddick, and Terry C. Maxwell . . . 233
Recognition of Special Members . . . . . 240
THE TEXAS JOURNAL OF SCIENCE EDITORIAL STAFF
Managing Editor:
Ned E. Strenth, Angelo State University Manuscript Editor:
Frederick B. Stangl, Jr., Midwestern State University Associate Editors:
Allan D. Nelson, Tarleton State University Jim R. Goetze, Laredo Community College Associate Editor for Botany:
Janis K. Bush, The University of Texas at San Antonio Associate Editor for Chemistry:
John R. Villarreal, The University of Texas-Pan American Associate Editor for Computer Science:
Nelson Passos, Midwestern State University Associate Editor for Geology:
Ernest L. Lundelius, University of Texas at Austin Associate Editor for Mathematics and Statistics:
E. Donice McCune, Stephen F. Austin State University
Manuscripts intended for publication in the Journal should be submitted in TRIPLICATE to:
Dr. Allan D. Nelson Department of Biological Sciences Tarleton State University Box T-OlOO
Stephenville, Texas 76402 nelson@tarleton.edu
Scholarly papers reporting original research results in any field of science, technology or science education will be considered for publication in The Texas Journal of Science. Instructions to authors are published one or more times each year in the Journal on a space-available basis, and also are available on the Academy's homepage at:
www.texasacademyofscience.org
AFFILIATED ORGANIZATIONS American Association for the Advancement of Science,
Texas Council of Elementary Science Texas Section, American Association of Physics Teachers Texas Section, Mathematical Association of America Texas Section, National Association of Geology Teachers Texas Society of Mammalogists
TEXAS T OF SCL 6 1(3): 163- 180
AUGUST, 2009
NESTING ECOLOGY OF GOLDEN MICE {OCHROTOMYS NUTTALLF) m EASTERN TEXAS
Cody W* Edwards and Aady P* Bradstreet
Department of Environmental Science and Policy, George Mason University 4400 University Drive, MSN 5F2, Fairfax, Virginia 22030 and Department of Biology, Stephen F. Austin State University Nacogdoches, Texas 75961
Abstract -Golden mice {Ochrotomys nuttalli) construct distinctive arboreal nests throughout much of their range. Little is known of the arboreal nature of golden mice in eastern Texas and previous studies have produced conflicting results. Live- trapping (7,150 trap nights) was conducted in four East Texas counties: Angelina, Houston, Nacogdoches, and San Augustine. Golden mice were trapped at two locations in Nacogdoches County and one location in San Augustine County. Results indicate viable populations of golden mice remain in eastern Texas, although additional surveys are needed. Fourteen golden mice were radio-tracked at the Stephen F. Austin State University Experimental Forest (Nacogdoches County, Texas) to determine nest site selection during two seasons. No evidence of arboreal nesting in golden mice was found during the summer. However, significant levels of arboreal nest use were recorded during autumn. The lack of ground-level structural diversity in eastern Texas forests in conjunction with seasonal flooding may cause terrestrial nest locations to become a limiting resource among small mammals during autumn.
Resumen.-Los ratones dorados {Ochrotomys nuttalli) construyen nidos arboreos muy distintivos a lo largo de todo su ambito. Sin embargo, se conoce muy poco de la naturaleza arborea de los ratones dorados en el Este de Texas, y los estudios previos han obtenido resultados divergentes. Se distribuyeron trampas (7,150 trap nights) en cuatro distritos del Este de Texas: Angelina, Houston, Nacogdoches y San Augustine, capturando ratones dorados en dos localidades en el distrito de Nacogdoches y en una localidad en el distrito San Augustine. Nuestro estudio indica que aun existen poblaciones viables de ratones dorados en el Este de Texas, aunque resulta necesario obtener mas registros. Catorce ratones dorados fiieron monitoreados para determinar preferencia del lugar de anidamiento durante dos estaciones en el Stephen F. Austin State University Experimental Forest (Nacogdoches, Texas). No se encontro evidencia de anidamiento arboreo durante el verano. Sin embargo, niveles significativos de anidamiento arboreo fiieron registrados durante el otono. La deficiencia en diversidad estructural de niveles bajos en el este de Texas, en conjunto con inundaciones estacionales, puede ocasionar que las localidades para anidamiento terrestre sean un recurso limitante para mamiferos pequenos durante el otono.
The habitats of golden mice {Ochrotomys nuttalli) vary from densely forested lowlands and floodplains to sandy upland pine
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communities (Linzey & Packard 1977). However, McCarley (1958) found that isolated upland communities seldom contained golden mice, suggesting floodplains may serve as focal points for dispersal. The main factor influencing the ecological distribution of this species is density of underbrush (McCarley 1958). The dense understory of golden mouse habitat is often composed of various plant species including honeysuckle (Lonicera sp.), greenbrier (Smilax sp.), grapevine {Vitis sp.), and poison ivy {Toxicodendron radicans) (Goodpaster & Hoffmeister 1954). Linzey (1968) found that the predominant food items of golden mice were greenbrier and blackberry {Rubus sp.) seeds and invertebrates.
Golden mice are considered highly arboreal and posses well developed abdominal musculature, a semi-prehensile tail, and large plantar tubercles indicative of an arboreal lifestyle. Several authors (Barbour 1942; Goodpaster & Hoffmeister 1954; Packard & Gamer 1964; Linzey 1968; Linzey & Packard 1977; Frank & Layne 1992) have described the nests and feeding platforms of golden mice. Briefly, arboreal nests are globular stmctures averaging 150-200 mm long, 100-125 mm wide, 100-200 mm high, and weighing 10- 30 g. Arboreal nests are usually located 1. 5-4.5 m above the ground and are interwoven in thickets of greenbrier, grapevine, and honeysuckle. However, some have been found as high as 10 m above ground in pine {Pinus sp.^ and cedar {Juniperus sp.) trees. Feeding platforms are similar to arboreal nests, but are bulkier and incomplete, often being open ended with only a shallow covering. No distinct feeding platforms have been observed other than those found by Barbour (1942) and Goodpaster & Hoffmeister (1954) in Kentucky. Further, Barrett (2007) questioned the use of feeding platforms by golden mice.
Arboreal nesting has been documented in varying degrees throughout the range of golden mice. Several authors (Klein & Layne 1978; Wagner et al. 2000; Morzillo et al. 2003) suggested arboreal nests could be used to avoid predation. Arboreal nesting may also provide protection during extreme weather conditions. Arboreal and semi-arboreal small mammals show high survival and
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retention of previous home range following short-term flooding events (Stickel 1948; McCarley 1959; Packard & Gamer 1964). McCarley (1959) noted that a one- week inundation resulted in a differential rate of mortality between cotton mice {Peromyscus gossypinus) and golden mice. About 60% of cotton mice remained following recession of the water, whereas 84% of golden mice were recaptured on the plot within previously established home ranges. Packard & Gamer (1964) noted that the habitat shift from terrestrial to arboreal nests took place each year well in advance of the autumn rains indicating that this behavior may have an ecological and climatic basis.
Goodpaster & Hoffmeister (1954) documented the use of ground nests by golden mice after finding only empty arboreal nests during the summer. McCarley (1958) and Pearson (1953) failed to locate arboreal nests in eastern Texas and northern Florida indicating exclusive use of ground nest locations. Subsequent investigations by Easterla (1968) and Frank & Layne (1992) revealed that ground nests are located just below the leaf litter or under logs and are similar in composition to arboreal nests. The mechanisms regulating nest-site selection are not known and the use of ground nests is likely underestimated (Frank & Layne 1992).
Despite evidence of continuous arboreal nest occupation in some populations of golden mice (Morzillo et al. 2003), no researcher has shown exclusive use of arboreal nests. Compared to arboreal nests, ground refugia may require significantly less investment of time and energy to constmct and maintain. Terrestrial refuge locations also provide better temperature moderation, providing a thermoregulatory advantage (Goodpaster & Hoffmeister 1954; Klein & Layne 1978; Frank & Layne 1992) and may provide better protection from predators. Packer & Layne (1991) showed that golden mice forage extensively on the ground. Foraging at ground level has been indicated throughout their range as evinced by numerous captures from live traps placed on the ground. While foraging on the ground, terrestrial locations may provide a quicker
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route of escape during attempted predation events (Morzillo et al. 2003).
Simultaneous refuge use is a common occurrence in golden mice and has been used to indicate sociality (Linzey & Packard 1977; Dietz & Barrett 1992; Morzillo et al. 2003). However, most support of group nesting in golden mice was obtained from studies conducted in the northern portions of its geographic range (Barbour 1942; Goodpaster & Hoffmeister 1954; Blus 1966; Dietz & Barrett 1992; Morzillo et al. 2003). Furthermore, much of these data were collected during autumn. The thermoregulatory benefits of nesting and huddling have been well documented in golden mice (Sealander 1952; Knuth & Barrett 1984; Peles & Barrett 2007). Because of the geographical and seasonal aspects of previous work, group nesting in golden mice could be little more than an artifact of thermoregulatory huddling. Frank & Layne (1992) reported simultaneous refuge use in 8.2% of golden mice and group sizes of no more than two.
Golden mice are considered only apparently secure (AS) in Texas (Feldhamer & Morzillo 2007). Very few golden mice have been captured in Texas during the past two decades and there is a need to assess and monitor their population status (Schmidly 2004).
One hypothesis for the potential decline of golden mice in eastern Texas is changing land use patterns. Because of its affinity for mid-successional stage habitats, golden mice are dependent upon regular disturbance (cutting, wind damage, etc.). Fire, whether natural or prescribed, creates a landscape mosaic favorable to golden mouse occupation. Absence of a regular fire regime has led to the loss of mid-successional understory vegetation in much of eastern Texas. Additional conservation concerns of golden mice are discussed by Feldhamer & Morzillo (2007).
Objectives were to: (1) determine the population status
(presence/absence) of golden mice in four eastern Texas counties
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(Angelina, Houston, Nacogdoches, and San Augustine; Fig. 1), and (2) describe the nesting ecology of golden mice during two distinct seasons at the western extent of their geographic range. Specific questions addressed included: (1) Determine the microhabitat characteristics at nesting locations of golden mice in summer and autumn. (2) Determine the extent of simultaneous nest use and its potential implications for social behavior.
Materials and methods
Study area.SmwQys were conducted for golden mice in four eastern Texas counties (Angelina, Houston, Nacogdoches, and San Augustine; Fig. 1). Sites were located in early successional sapling forests, mid-successional mixed pine-hardwood forests, and mature pine forests. The surveys were concentrated in mesic, mid- successional forests due to O, nutt allies known affinity for these habitats in eastern Texas (McCarley 1958; Packard & Gamer 1964; Schmidly 2004).
The Stephen F. Austin Experimental Forest (SFAEF) is a 1,036 ha tract located 15 km southwest of Nacogdoches, Texas (Fig. 1). This area is part of the Angelina National Forest and is administered through the Southern Research Station in cooperation with Stephen F. Austin State University. The SFAEF consists of approximately 730 ha of bottomland hardwood forest with the remainder being upland pine and mixed pine-hardwood forests. A 2.5 ha grid of 144 stations spaced at 10 m intervals was established in an ecotone area of mixed pine-hardwood forest. Dominant woody plant species included slash pine {Pinus elliottii), loblolly pine (P. taeda), sweetgum {Liquidambar styraciflua), greenbrier, blackberry, and grapevine.
Trapping procedure -GQnQml population surveys were conducted from April-August 2003 and Febmary-July 2004. The SFAEF study plot was surveyed July, September, and November 2004. Population surveys were conducted by setting transects of 50 Sherman live traps (H.B. Sherman, Tallahassee, Florida) spaced 15
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Fig. 1. Locations of counties surveyed during golden mice research project.
m apart. Traps were placed in areas of suitable golden mouse habitat (on ground and above ground in vines) with 100-300 total traps per survey location. Sampling of the study plot involved placing traps within 1 m of designated trap stations. Trapping was conducted for 2-5 consecutive nights using a bait mixture of wild birdseed, rolled oats, peanut butter, and raisins. All captured individuals were identified to species, sexed, and uniquely marked by toe-clipping (Kumar 1979). Age class was defined as either adult or juvenile on the basis of relative size, weight, and pelage coloration (Layne 1960; Linzey & Linzey 1967). Males with descended testes and females that were either pregnant, lactating, or
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had perforate vulva were considered to be in reproductive condition. Mice were released at the point of capture.
Radiotelemetry and daytime refugia of golden mice were located using radiotelemetry during two distinct seasons. The summer radiotelemetry was conducted from 25 July to 20 September 2004, whereas autumn radiotelemetry occurred from 15 November 2004 to 5 January 2005. Small mammal radio transmitters (2.0 g; Blackburn Transmitters, Nacogdoches, Texas) mounted on zip-ties were attached around the neck of each mouse. Transmitters were designed to have a range of approximately 200 m and a battery life of 60 days. The range was variable depending on vegetation density and depth below ground, but highly directional at close range and accurate within 0.5 m.
Mice were weighed and fitted with transmitters in the field and released at the point of capture. At least 12 hours elapsed between release and first relocation attempt. Mice were located through standard radiotelemetry techniques (White & Garrott 1990; Millspaugh & Marzluff 2001) using a 3 element Yagi antennae and a R-1000 receiver (Communication Specialists Inc., Orange, California). Locations were marked using nylon stake flags.
Characterization and analysis of microhabitat -Micro\idib\t2it variables were measured at each ground location, arboreal location, and random locations. Length, width, depth, height above ground, and plant species used as substrate for construction were recorded for arboreal nests. Six independent variables were measured at each refuge and the randomly selected control site. Variables measured included depth (cm) of soil litter layer, distance (m) to nearest dead wood (log or stump) greater than 10 cm in diameter, distance (m) to nearest vine suitable for climbing, distance (m) to nearest tree with a DBH greater than 7.5 cm, mean percentage of area blocked visually by vegetation from 0-1 m on a Im by Im density board, read at 90° increments at a distance of 3 m from the nest or random point, and mean percentage of area blocked visually
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by vegetation from 1-2 m on a Im by Im density board, read at 90° increments at a distance of 3 m from the nest or random point. Selected variables were modified from Dueser & Shugart (1978), Frank & Layne (1992), and Morzillo et al. (2003) and were selected to minimize correlation and redundancy between measurements. Random sites were used to characterize the available microhabitat conditions present on the study plot. Forty-eight locations were selected using random number generation during each season.
Because microhabitat data were collected during different times of the year, seasonal variation was possible. Non-parametric Mann- Whitney tests of the independent variables were used to compare microhabitat data collected during the two sampling periods. Only random sites were used to test seasonality, as microhabitat differences at nest sites could be caused by factors other than seasonal variation. Forward stepwise discriminant function analysis (DFA) was used to evaluate which microhabitat variables were best for predicting nest site location (Table 1). Model selection was evaluated at a significance level of 0.10.
All data were checked for univariate normality using the Shapiro- Wilks’ Test and for multivariate normality using the Mardia Test. Statistical analyses were performed in JMP 5.0.1 (SAS Institute Inc., Cary N.C., 1989-2002) and SAS 9.1 (SAS Institute Inc., Cary, N.C., 2002-2003).
Results
Population survey efforts consisted of 7,150 trap nights and resulted in the capture of 297 individuals representing eight genera (Table 2). Overall trap success was 4.2%. Peromyscus sp. {n = 156) comprised 52.5% of individuals captured. Twenty-six golden mice were captured in Nacogdoches and San Augustine Counties. Four individuals were captured in San Augustine County, whereas six and 16 individuals, respectively, were captured from two locations in Nacogdoches County.
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Table 1. Dependent variables used in discriminant function analysis (DFA).
|
Statistical Analysis |
Dependent Variables |
|
DFA 1 |
Golden mice ground nests Golden mice arboreal nests |
|
DFA 2 |
Random locations Ground nest locations |
|
DFA 3 |
Random locations Arboreal nest locations |
|
Table 2. Total captures of individuals during population survey. |
||
|
Species |
# of Captures |
% of Captures |
|
Peromyscus spp. |
156 |
52.5 |
|
Reithrodontomys fulvescens |
42 |
14.1 |
|
Neotoma floridana |
33 |
11.1 |
|
Ochrotomys nuttalli |
26 |
8.8 |
|
Blarina carolinensis |
23 |
7.7 |
|
Sigmodon hispidus |
11 |
3.7 |
|
Cryptotis parva |
4 |
1.4 |
|
Cardinalus cardinalus |
2 |
0.7 |
|
TOTAL |
297 |
100 |
Radiotelemetry -Vom golden mice (two males and two females) were radio-tracked during the summer resulting in 95 locations at 13 unique refugia. All located refugia were terrestrial. A thorough search of the plot failed to yield any evidence of arboreal nesting. Additionally, six males and four females were radio-tracked during the autumn resulting in 185 locations at 26 unique refugia. Of the 26 unique refugia, 18 were located at terrestrial sites and eight arboreal nests were found. By additional searching of the surrounding area, three additional arboreal nests were discovered that appeared to be in use.
Golden mice utilized an average of 3.0 refugia per individual during autumn and 4.7 refugia per individual during summer.
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Golden mice used significantly fewer refugia in the autumn than in the summer {U= 35.5, P = 0.02).
Sequential use, defined as the same location used by multiple individuals at different times, was observed in 40% of golden mice refugia. No seasonal differences were present in sequential refuge use and sequential use was not documented at any arboreal locations. Simultaneous use (group nesting), defined as the use of the same refuge site by different individuals at the same time, was not documented.
Arboreal nests were used only in autumn. Nests ranged from 0.6-2. 1 m above ground and were constructed in a variety of substrates (Table 3). Eight of the 10 radio-collared mice were documented using arboreal nests, but not exclusively. The number of ground refugia used by arboreal nesting individuals ranged from 1-4. All four females were tracked to an arboreal location and four of the six males were found in arboreal nests. Two males used ground nests exclusively.
Microhabitat use.-No seasonal variation was found in any of the variables (P > 0.20). Due to the lack of seasonal affects in available habitat, seasons were pooled for subsequent analysis.
Distance to nearest vine, distance to nearest coarse woody debris, and distance to nearest tree were retained using the stepwise DFA classification procedure as important variables distinguishing golden mice ground refugia from arboreal nests. The model constructed using these variables correctly classified 100% of observations. Stepwise logistic regression retained the same three variables. This model was highly significant (X^ = 57.14, P < 0.0001, = 1.00). A greater distance to coarse woody debris, less
distance to nearest vine, and less distance to nearest tree were positively associated with arboreal nest locations.
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Table 3. Arboreal nest locations and dimensions.
Nest Dimensions
|
Substrate |
Height (m) |
Length (cm) |
Width (cm) |
Depth (cm) |
|
Sweetgum* |
1.2 |
12 |
10 |
10 |
|
Sweetgum |
1.9 |
11 |
8 |
10 |
|
Sweetgum |
1.1 |
14 |
9 |
12 |
|
Devil’s Walking Stick (Aralia spinosa) |
1.4 |
10 |
9 |
8 |
|
Privet {Ligustrum japonicum) |
0.9 |
15 |
13 |
13 |
|
Loblolly Pine Sapling |
1.3 |
10 |
9 |
9 |
|
Greenbrier |
0.8 |
18 |
9 |
8 |
|
Greenbrier |
0.6 |
11 |
8 |
13 |
|
Greenbrier* |
2.1 |
15 |
8 |
11 |
|
Greenbrier |
0.8 |
13 |
8 |
13 |
|
Yaupon* {Ilex vomitoria) |
1.4 |
18 |
12 |
13 |
* Active nests discovered, but not documented through radiotelemetry.
Distance to nearest coarse woody debris, distance to nearest vine, and depth of litter layer were retained using the stepwise DFA classification procedure as important variables distinguishing ground refugia from random locations. The model constructed using these variables correctly classified 89% of observations. Stepwise logistic regression retained the same three variables as significant. This model was statistically significant = 156.14, P < 0.0001, = 0.59). A greater depth of litter layer, a greater
distance to coarse woody debris, and a greater distance to nearest vine were positively associated with random locations.
Distance to coarse woody debris and distance to nearest vine were retained using the stepwise DFA classification procedure as important variables distinguishing arboreal nests from random locations. The model constructed using these two variables correctly classified 97% of observations. Stepwise logistic regression retained the same two variables as significant. This model was statistically significant (X^ = 56.76, P < 0.0001, =
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1.00). A greater distance to coarse woody debris and a greater distance to the nearest vine were associated positively with random locations.
Discussion
Feldhamer & May croft (1992) suggest behavioral traits of O, nuttalli may result in underestimation of home range and population density of the species. Although all mice captured in this study were captured on the ground, their arboreal nature may make trapping through conventional means less successful. Golden mice are also known to be more trap shy than many sympatric small mammals (Feldhamer & Maycroft 1992). This was evident in the present study, as only five of a total of 26 golden mice were captured during the first night at a trapping location. Seven golden mice were captured on the second night, while nine were captured on the third night at a given location. It is suggested that adequate sampling techniques should include both arboreal and terrestrial placement of traps and multiple trap nights at each location.
Historically, golden mice have been considered a habitat specialist (Dueser & Shugart 1979; Dueser & Hallett 1980). Most mice captured during this study were captured in dense understory vegetation. However, golden mice were also found in areas considered suboptimal for occupation, including a pine sapling monoculture and mature pine forest. Both of these locations possessed little to no understory vegetation. This is consistent with researcher’s results from southern Illinois, where golden mice were found in a variety of habitats (Blus 1966; Morzillo et al. 2003). Whiting & Fleet (1987) described the small mammal composition within four different types of even-age pine stands in East Texas: seedling, sapling, pole, and sawtimber. Golden mice were captured in each forest type with the largest percentage of total captures occurring in the sapling stands {n = 42%) and the smallest percentage of captures occurring in sawtimber {n = 16%). These data suggest that golden mice may occur in a broader range of
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habitats in eastern Texas. However, the relationship between habitat type and fitness has yet to be investigated.
The common occurrence of golden mice in early and mid- successional stages suggests that regular disturbance may be an important component in maintaining populations and enhancing habitat. Periodic disturbance creates a mosaic habitat and increases early successional seed-producing species important to golden mice (Morzillo et al. 2003).
Refuge use~J\\Q use of daytime refugia and nests are vital to small mammals for protection from extreme environmental conditions, predator avoidance, and security for offspring (Frank & Layne 1992). Results from this study indicate golden mice in eastern Texas generally use fewer refugia and exhibited greater refuge fidelity during the autumn sampling period.
Sequential use was observed in 40% of golden mice refugia and might indicate a familiarity with the refuge locations of conspecifics and close social grouping. Further, golden mice have a high degree of home range overlap and exhibit little to no evidence of territoriality (McCarley 1958; Morzillo et al. 2003).
Although no simultaneous refuge use was documented, not all mice on the study grid were outfitted with radiotransmitters. It is possible that untagged individuals were occupying the same refuge site, but were not detected. However, it is likely that researchers would have observed such groupings had aggregations occurred. Frank & Layne (1992) recorded simultaneous refuge use in 8.2% of golden mice locations in Florida. They found refuge use was higher in the autumn and involved only two individuals. Conversely, group nesting in golden mice has been reported commonly from their northern range, with as many as eight individuals occupying the same nest (Barbour 1942; Goodpaster & Hoffmeister 1954; Howell 1954; Dunaway 1955; Layne 1958). The lack of group nesting in eastern Texas supports the hypothesis that group nesting in golden mice may be a thermoregulatory
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mechanism to conserve energy at low temperatures and not necessarily a difference in social behavior (Frank & Layne 1992).
Refuge site microhabitat. -Duq to the presence or absence of leaves, vegetation density measurements generally vary between seasons. No statistical difference was found among variables between seasons. The lack of seasonal variation is likely due to a high abundance of woody stems within the understory vegetation.
Neither measurement of understory density was retained in the discriminant function models. This is surprising because of the known affinities of golden mice for dense understory habitats. However, these measurements were not retained primarily due to an abundance of dense understory vegetation throughout the study plot. Natural forests in eastern Texas are a mosaic matrix of isolated patches of dense vegetation separated by intervening regions of open forest floor (McCarley 1958). Given the abundance of understory vegetation on the study plot, constructed models could not discriminate between true refugia and random locations. Additionally, there is no means of assessing how many of the random sites were “near” a ground nest.
Importance of woody .-Distance to coarse woody debris
was the most important variable in determining the location of ground refugia. Woody debris, including fallen logs, snags, and stumps, is important in the distribution and occurrence of many small mammalian species (Strecker & Williams 1929; Ivey 1949; Easterla 1968; Graves et al. 1988). Coarse woody debris serves as habitat for invertebrates and fungi eaten by small mammals, retains moisture, and provides important navigational cues (McCay 2000). The SFAEF has little ground-level structural diversity. Therefore, ground nesting species have few alternatives to the use of stumps, root boles, and their associated decomposing root systems in which to seek refuge. Rock outcroppings are not present and burrows of larger vertebrates and standing snags were rare on the study plot. The finite number of suitable ground refuge locations creates an environment in which competition could play an important role.
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Distance to coarse woody debris was retained as an important variable in the microhabitat of golden mice arboreal nests. Arboreal nests of golden mice typically were closer to woody debris than would be predicted from random locations. The use of ground refiigia, in addition to arboreal nests, may provide alternative means of escape when faced with predation. Packard & Gamer (1964) reported flushing an adult male golden mouse from a nest. After 10 min of harassment, the mouse leaped from the vines and vanished into an underground burrow system from which it could not be extracted.
Importance of climbing vine-\i was expected that distance to climbing vines would be an important variable retained in the discrimination of arboreal nests. Vines provide a common substrate in which arboreal nests are constmcted (Linzey & Packard 1977). With one exception, arboreal nests found in this study were either constmcted entirely within vines or used vines as anchoring support to a tree or shmb. Vines provide mice with multiple escape pathways when faced with predation pressure.
Distance to nearest vine suitable for climbing was also retained in the discrimination model of ground refugia. Ground refugia were closer to climbing vines than would be expected from random locations. Golden mice are able climbers and commonly seek refuge in trees or bushes when released from live-traps (Linzey & Packard 1977). As mentioned with arboreal nests, constmcting terrestrial refugia within close proximity to climbing vines may provide alternative options of escape.
Prior to this research, there have been two studies of golden mice nesting behavior in eastern Texas. McCarley (1958) found no evidence of arboreal nesting in eastern Texas, whereas Packard & Gamer (1964) discovered numerous arboreal nests at two sampling localities in Nacogdoches County, Texas. It was noted that from 1955 to 1957, Nacogdoches County, Texas experienced the worst drought on record for this area. Since 1901, the average annual rainfall reported for Nacogdoches County, Texas is 122 cm. In
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contrast, the average annual rainfall recorded from 1955 to 1957 was 81 cm. Rainfall totals recorded during 1961 and 2004 (the year this research was conducted) were above average at 137 cm and 173 cm, respectively. Further, approximately 30% of the study plot established at the SFAEF had standing water for much of the autumn monitoring season. These results support those of Packard & Gamer (1964). Golden mice in eastern Texas seemingly use arboreal nests only during the autumn. The lack of ground-level stmctural diversity in eastern Texas forests in conjunction with seasonal flooding may cause terrestrial nest locations to become a limiting resource for golden mice during autumn. It should be noted that supplemental nest boxes were provided by McCarley (1958). The timing of occupation of these nest boxes closely coincides with the timing of the shift from terrestrial to arboreal habitats reported by Packard and Gamer (1964) and by this study. Arboreal nesting seems to be of adaptive value to golden mice populations in eastern Texas.
Acknowledgments
We gratefully acknowledge the assistance of S. Johnson and S. Williams for help during fieldwork. We thank P. Blackburn for the constmction and design of all radio transmitters used in this study. T. Henry and S. Johnson assisted in production of figures and tables. For critical reviews of this manuscript, we thank G. A. Feldhamer, C. Jones, E. McTavish, R. D. Stevens, and Jim Goetze. Partial funding was provided by a Grants-In-Aid of Research award from The American Society of Mammalogists (to APB) and by the Department of Biology at Stephen F. Austin State University.
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Packer, W. C. & J. N. Layne. 1991. Foraging site preferences and relative arboreality of small rodents in Florida. The American Midland Naturalist, 125:187-194.
Pearson, P. G. 1953. A field study of Peromyscus populations in gulf hammock, Florida. Ecology, 34:199-207.
Peles, J. D. & G. W. Barrett. 2007. The golden mouse: a model of energetic efficiency. Pp. 135-149 in The golden mouse: ecology and conservation (Barrett and Feldhamer, editors). Springer Publishing, New York, 239pp.
Schmidly, D. J. 2004. The Mammals of Texas. First edition. Texas Parks and Wildlife Department, Austin, 544 pp.
Sealander, J. A., Jr. 1952. The relationship of nest protection and huddling to survival of Peromyscus at low temperature. Ecology, 33:63-71.
Stickel, L. F. 1948. Observations on the effect of flood on animals. Ecology, 29:505-507.
Strecker, J. K. & W. J. Williams. 1929. Mammal notes from Sulphur River, Bowie County, Texas. Journal of Mammalogy, 10:259.
Wagner, D. M., G. A. Feldhamer & J. A. Newman. 2000. Microhabitat selection by golden mice (Ochrotomys nuttalli) at arboreal nest sites. The American Midland Naturalist, 144:220-225.
White, G. C. & R. A. Garrott. 1990. Analysis of Wildlife Radio-Tracking Data. Academic Press, San Diego, 383 pp.
Whiting, R. M. & R. R. Fleet. 1987. Bird and small mammal communities of loblolly-shortleaf pine stands in East Texas. USFS Gen. Tech. Report S068:49- 66.
CWE at: cedward7@gmu.edu
TEXAS J. OF SCI. 61(3):181-186
AUGUST, 2009
THE SAND DOLLAR PERIARCHUS LYELLl (ECHINOIDEA: CLYPEASTEROIDA: SCUTELLIFORMES)
IN THE CADDELL FORMATION (UPPER EOCENE) OF TEXAS
Louis G. Zachos
Department of Paleobiology MRC~121 National Museum of Natural History, Smithsonian Institution P.O.Box 37012, Washington, DC 20013-7012
Abstract. -The occurrence of the sand dollar echinoid Periarchus lyelli in the Upper Eocene Caddell Formation of Texas is confirmed. This extends the geo¬ graphic range of this Gulf Coast index fossil west from Mississippi to Texas.
The sand dollar echinoid Periarchus lyelli (Conrad) is a distinctive and well-known element of the fauna of Upper Eocene (Jackson) marls and limestones across the eastern Gulf of Mexico and lower Atlantic coastal plain. Hurricane Rita struck the Texas coast in September, 2005, and caused significant erosion on the northern shore of the Sam Rayburn Reservoir and created fresh exposure of sandstones and shales of the Upper Eocene Caddell Formation in the immediate vicinity of the type area. A number of specimens of Periarchus lyelli were collected from these exposures following the storm. This report documents a geographic range extension of the species west from Mississippi to Texas.
Study Area and Methods
The Caddell Formation was named by Dumble (1915) after the town of Caddell in southern San Augustine County, Texas (Figure 1). The town site was inundated by the Sam Rayburn Reservoir in the 1960s, although the cemetery remains. The type section was determined by Eargle (1959) and the locality was redescribed by the Gulf Coast Section of Economic Paleontologists and Mineralogists (1966) before inundation by the reservoir. The old town site is near the Harvey Creek Recreation Area at the end of FM2390 about 10 miles (by road) from Broaddus. There are poorly preserved fragments of sand dollar echinoids collected from this area in the Rio Bravo Collection (Molineux 2008) at the Texas
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Periarchus lyelli
Periarchus lyelli
5 10 15 Kilometers
Fig. 1. Study Area. (A) Gulf of Mexico and Atlantic coastal plain showing Upper Eocene occurrences of Periarchus lyelli. Each circle represents a county with one or more localities where P. lyelli has been reported. (B) San Augustine County, Texas. The Harvey Creek Recreation area is marked by a box located at 31°12’30” N, 94°15’45’' W. (C) Harvey Creek Recreation Area on the northeast shore of Sam Rayburn Reservoir. Type locality for the Caddell Formation, which outcrops along the outlined shoreline. Each triangle marks a location from which P. lyelli was collected in situ. (The formation dips towards the southeast).
Natural Science Center. The original collecting locality for these specimens, as recorded by specimen labels more than century old, was in a southward- facing slope of the valley of the Angelina River at Caddell. Loose cobbles and boulders of indurated sandstone contained fragments of sand dollars. In September, 2005, the eye of Hurricane Rita crossed the area and caused significant erosion on the northern shore of Sam Rayburn Reservoir. This erosion exposed fresh sections of sandstone and shale of the Caddell
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Formation. Outcrops along the irregular shoreline are now best accessed by boat, and the exposure of the formation extends from the boat ramp at the Harvey Creek Recreation Area to approximately 3 km southeastward, exposing a stratigraphic interval about 35 m thick. The lowest interval of the section is composed of interbedded argillaceous, iron oxide impregnated sandstone and sandy clay, with trace fossils and poorly preserved (moldic) megafauna. This is overlain by a fine-grained unit with calcareous lenses several meters in diameter containing the large oyster Crassostrea gigantissima (Finch). A thin layer of calcareous, very shelly sand less than a meter thick overlies the shale, grading upwards into indurated sandstone which weathers into large concretionary masses. Well-preserved fragments (Fig. 2a) of Periarchus lyelli are found in the thin calcareous unit and relatively whole specimens (Fig, 2b) occur on the weathered surfaces of the upper sandstone. Both occurrences are associated with unidentified nummulitid foraminifera.
Material Examined
All fossil material collected has been cataloged in the collections of the Nonvertebrate Paleontology Laboratory (NPL) of the Texas Natural Science Center (TNSC), on the Pickle Research Campus of the University of Texas at Austin.
Discussion
Sand dollar echinoids, members of the order Clypeasteroida, first appeared in the fossil record of the Gulf of Mexico coastal plain in the early part of the Middle Eocene. The oldest known sand dollars from this region are the putative species Protoscutella mississippiensis found near the top of the Tallahatta Formation in western Alabama. Various nominal species of Protoscutella are found in abundance in slightly younger deposits from Texas to North Carolina. Periarchus lyelli first appeared in the Middle Eocene and by the Late Eocene it became the predominant species of sand dollar. Oddly, although the oldest occurrence of P. lyelli is
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Fig. 2. Periarchus lyelli from the Caddell Formation, Sam Rayburn Reservoir. (A)
TNSC NPL19819, from shelly calcareous bed. (B,C) TNSC NPL19815, aboral and
left side, from concretionary sandstone boulder. Scale bars 1 5 mm.
in the Cook Mountain Formation in east Texas, the species was not definitely known from the Upper Eocene Jackson Group in Texas. Fragmentary evidence in the TNSC Rio Bravo Collection was suggestive of the occurrence of the species, but is not definitive.
Periarchus lyelli was first described by Conrad (1834) from (probably) the Moodys Branch Formation below Claiborne Bluff on the Alabama River (Monroe County, Alabama). The species is characterized by significant morphologic variability and widespread geographic distribution. This has resulted in several closely related species being described then variously reduced to synonyms or subspecies of P. lyelli by different authors. The species is especially abundant in the Moodys Branch Formation and equivalents from Mississippi east and north to North Carolina and as far south as central Florida. It has not been found in the Moodys Branch Formation exposures along the Quachita River in central Louisiana (Huner 1939), but Cooke (1942; 1959) reported that fragments of sand
ZACHOS
185
dollars attributable to this species were found by T,W. Vaughan in the Moody s Branch Formation exposed at Montgomery Landing (Creole Bluff) on the Red River in Louisiana (now inundated by water dammed behind navigational locks on the river). The species is not listed in the fauna from Montgomery Landing in Schiebout & van den Bold (1986), but Vaughan’s specimens (27 small fragments) are in the Smithsonian paleobiology collections, catalog number USNM 164680, and do appear to be attributable to P. lyelli. Clark & Twitchell (1915) reported some occurrences of P. lyelli in Texas, but all of these were misidentifications of Protoscutella mississippiensis. The occurrence of P. lyelli noted by Cooke (1959) is from a Cook Mountain Formation locality in Sabine County, Texas (see Zachos & Molineux 2003). A probable identification of P. lyelli for the material in the Rio Bravo collection was reported by Zachos & Molineux (2003), but the latest collections reported here were taken in situ from the Caddell Formation and confirm the identification.
Better preserved specimens collected from the Caddell Formation show the conical “Chinese haf ’ profile characteristic of the putative subspecies P. lyelli pileussinensis (Figure 2c). This variety is generally found in Jackson (Bartonian) deposits and is evidence that the Texas occurrence is of equivalent age to the Moody s Branch Formation or younger deposits in the eastern Gulf of Mexico coastal plain.
Carter et al. (1989) showed that Periarchus lyelli in all its variants preferred a sand substrate. Carter & McKinney (1992) presented evidence that distribution patterns in Upper Eocene echinoid faunas were related to facies patterns, particularly in relation to sand/mud ratios. The extension of the geographic range westward into Texas demonstrates that P. lyelli had a preference for sandy substrate but was tolerant of composition (quartz/glauconite vs. calcite/aragonite) and minor variation in water temperature represented by differences in environmental regimes that included the Atlantic coast of the Carolinas and the carbonate platform of Florida.
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Acknowledgments
Appreciation is extended to A. Molineux, Texas Natural Science Center, Austin for assistance with the collections of the Non- Vertebrate Paleontology Laboratory, and to C. Ciampaglio and T. Yancey for their critical review of the manuscript. This work was supported by the Geology Foundation of the Jackson School of Geosciences at the University of Texas at Austin., and by the Smithsonian Institution Fellowship Program.
Literature Cited
Carter, B. D., T. H. Beisel, W. B. Branch & C. M. Mashbum. 1989. Substrate preferences of Late Eocene (Priabonian/Jacksonian) echinoids of the eastern Gulf Coast. Jour. Paleo., 63:495-503.
Carter, B. D. & M. L. McKinney, 1992. Eocene echinoids, the Suwannee Strait, and biogeographic taphonomy. PaleobioL, 18:299-325.
Clark, W. B. & M. W. Twitchell. 1915. The Mesozoic and Cenozoic Echinodermata of the United States. U.S. Geol. Surv. Monograph 54, 341 pp.
Conrad, T. A. 1834. Descriptions of new Tertiary fossils from the southern states. Jour.
Acad. Nat. Sci. Philadelphia, Ser. 1, v. 7:130-157.
Cooke, C. W. 1942. Cenozoic irregular echinoids of eastern United States. Jour. Paleo., 16:1-62.
Cooke, C. W. 1959. Cenozoic echinoids of eastern United States. U.S. Geol. Surv. Prof Paper 321, Hi + 106 pp.
Dumble, E. T. 1915. Problem of the Texas Tertiary sands. Geol. Soc. Am. Bull. 26:447- 476.
Eargle, D. H. 1959. Stratigraphy of Jackson Group (Eocene), south-central Texas.
Amer. Assoc. Petrol. Geol. Bull. 43:2623-2635.
Gulf Coast Section of the Society of Economic Paleontologists and Mineralogists. 1966. Caddell Formation (U. Eocene) Type Locality, GCS of SEPM Type Localities Project Unit IV. Gulf Coast Assoc. Geol. Soc. Trans, 16:393-394.
Huner, J. 1939. Geology of Caldwell and Winn Parishes. Louisiana Geol. Surv. Bull. 15,356 pp.
Molineux, A. 2008. The Rio Bravo Collection: Preserving a unique collection for future research in the Gulf Coast section. Gulf Coast Assoc. Geol. Soc. Trans. 58:699-700. Schiebout, J. A. & W. van den Bold. 1986. Montgomery Landing Site, Marine Eocene (Jackson) of Central Louisiana, Thirty Sixth Annual Meeting of the Gulf Coast Association of Geological Societies, Baton Rouge, vi + 238pp.
Zachos, L. G. & A. Molineux. 2003. Eocene echinoids of Texas. Jour. Paleo. 77:491- 508.
LZ at: lg_zachos@alumni.utexas.net
TEXAS T OF SCI. 6 1(3): 187 A 94
AUGUST, 2009
MIXED INFECTIONS OF NASOPHARYNGEAL BOTS, CEPHENEMYIA SPP. (OESTRIDAE) IN WHITEMAILED DEER {ODOCOILEUS VIRGINIANUS) AND MULE DEER (ODOCOILEUS HEMONUS) OF TEXAS
Samuel W. KeOey
U.S. Geological Survey Wichita Falls, Texas 76308
Ahsir^ti -Cephenemyia spp. are widespread oestrid flies whose larvae parasitize various cervid hosts, yet attempts to pathologize their significance as well as delineate their taxonomy, dispersal potential, and distribution remain ambiguous. This report provides new records of mixed Cephenemyia spp. infections in both mule deer (Odocoileus hemionus) and white-tailed deer (Odocoileus virginianus) in west and north-central Texas, including C, jellisoni, C, phobifer, and C pratti, thereby filling a substantial void in previous southern distribution reports. Possible ecological and pathological implications are discussed including the need for a taxonomic review of the genus Cephenemyia plus dispersal, hybridization, and vector potential for chronic wasting disease in cervid hosts.
Members of the genus Cephenemyia (Diptera: Oestridae) are stout bee-like flies (Fig. 1) whose larvae parasitize the nasal passages and pharyngeal regions of a variety of cervid hosts within the Holarctic ecozone. Gravid females of most North American Cephenemyia species are believed to larviposit into the nostrils of their hosts (Golini et al. 1968; Anderson 2001), where larvae migrate, feed, and grow within various nasopharyngeal regions of the host including the retropharyngeal pouches, soft palate, under the tongue, glottis, and throughout the nasal passages. Mature third instars travel out of the nostrils and pupate in the soil with adult emergent times variable and purportedly dependent upon ambient temperatures (Bennett 1962; Hair et al. 1969; Nilssen 1997).
While Cephenemyia spp. infections are known to cause deleterious effects within cervid hosts, their total impact upon cervid ecology remains unclear. Dated reports indicate that the bots may cause severe pathogenesis including death of the hosts (Walker 1929; Bruce 1931; Cowan 1946); however, more recent studies report gadding and physiological trauma but downplay the risk of
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Figure 1. Adult Cephenemyia jellisoni reared from a larva found in a mule deer
{Odocoileus hemionus) from Jeff Davis County, Texas.
host death or debilitation (Cogley 1987; McMahon & Bunch 1989; but see Johnson et al. 1983). A recent study by Lupi (2005) posited that Cephenemyia spp. could serve as vectors for chronic wasting disease (CWD) to cervids due to their proximity to host structures potentially rich in prion rods and their ability to replicate and express prion proteins. Ingestion of similar encephalopathic- infected fly larvae and pupae has caused rodent host infections within a previously infection-free sample (Post et al. 1999).
Four species of Cephenemyia have been documented in the south-central and southeast-central regions of Texas (Fig. 2): C. pratti Hunter 1915, C phobifer (cf. Van Volkenberg & Nicholson 1943; Bennett & Sabrosky 1962), C. jellisoni (cf. Bennett & Sabrosky 1962), and C. albina Taber & Fleenor 2004; Fleenor & Taber 2007. Samuel & Trainer (1971) also described larvae
KELLEY
189
Figure 2. Regional distribution by state and county of Cephenemyia spp. in Texas, Oklahoma, and New Mexico based on published records. Cephenemyia spp. from Wilbarger and Jeff Davis counties, Texas represent new locality records in the state.
encountered in the southern Gulf Coast region of the state but could not positively identify the species. Adjoining state records for Cephenemyia include C. jelUsoni from eastern Oklahoma (Hair et al. 1969) and C. jelUsoni plus C. pratti from New Mexico (Townsend 1941; Bennett & Sabrosky 1962). Cephenemyia phobifer occurs in Louisiana (Bennett & Sabrosky 1962; Kellogg et al. 1971), yet none were found in a large sample of deer {n= 151) examined from Arkansas (Kellogg et al. 1971). Weber (1992) states that C. pratti is the only known species from Mexico, though other Cephenemyia species are thought to occur in northern Mexico
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as well. This study reports the first records of Cephenemyia spp. from north-central and west Texas.
Methods
In February 2008 a Cephenemyia-infQciQd white-tailed deer {Odocoileus virginianus) was found dead 13 km S of Vernon, Wilbarger County, Texas (34^01’ 12” N, 99^ 14' 31” W; elev. 372 m) in an area predominately used for cattle rangeland and crop cultivation. Cause of death was unknown, as it was estimated to have been dead for two days and was heavily scavenged.
Subsequently, in December 2008, a Cephenemyia-mfQCtQd mule deer {Odocoileus hemionus) was shot in the Davis Mountains, 21.7 km SE of Ft. Davis, Jeff Davis, County, Texas (30° 31' 01" N, 103° 44' 16" W; elev. 1557 m) in an area primarily reserved for hunting activities.
Both male deer were aged following traditional tooth wear methods (Severinghaus 1949). Live third instar larvae from both cervid hosts were placed into separate glass containers half full of sand, covered with light leaf litter, and kept indoors (21 C) for 48 h to facilitate pupariation. Larvae failing to undergo pupariation were identified using available keys (Bennett & Sabrosky 1962) and stored in 80 percent ethanol. Larval specimens were deposited in the U.S. National Parasite Collection (USNPC), Beltsville, Maryland (101515-101517). An emergent adult specimen was identified and deposited in the Midwestern State University insect collection, Wichita Falls, Texas.
Results
The infected white-tail deer’s estimated age was 8.5 yrs. Eighteen Cephenemyia spp. larvae were found within the nasal passages and back of the pharynx in addition to one puparia found within the nasal passages. The mule deer was aged at 9.5 yrs, and
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three third instar Cephenemyia larvae were noticed crawling out of the nose after the deer had been in cold storage for two days. A subsequent examination revealed no additional larvae, and it is unknown if any larvae escaped before the head was examined. Regarding bot larvae from the white-tail deer, none successfially pupated except the puparia initially discovered within the nasal passages. Dissection of the whitetail-host puparia after 10 months revealed a moldy, degenerated, unidentifiable specimen. One of three mule deer-host larvae successfully pupated, and the adult emerged 27 days later.
The emergent mule deer-host bot fly was identified as C. jellisoni. The other two mule deer-host larvae were identified as C. pratti, indicating a mixed infection. Of the 18 larvae from the white-tail deer in Wilbarger County, 15 were identified as C. jellisoni (83%), and three as C phobifer (17%), providing another example of mixed Cephenemyia spp. infection within the same host. All specimens of Cephenemyia jellisoni, C. pratti, and C phobifer represent new geographic records within Texas (Fig. 2).
Discussion
Distributions of several species within the genus Cephenemyia overlap, and mixed infections among cervid hosts may be common, but comprehensive ranges of Cephenemyia spp. remain unknown. A major hindrance to the study of Cephenemyia spp. distributions and their ecology stems from the paucity of captured adult specimens. Adult botflies have morphological characteristics (hair patterns, density, and color, plus wing infuscation, and arista coloration) that allow for easier identification than larvae. Larvae are encountered far more frequently in dead cervid hosts but are practically impossible to rear to maturity if they fail to pupariate soon after removal from the host. Identification of third instar larvae can prove troublesome as key larval characteristics (spine counts, anterior spiracle morphology) sometimes vary or overlap among described species; moreover, a single larva is often inadequate for species identification (Bennett & Sabrosky 1962).
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Nevertheless, larval specimens encountered in this study aligned closely on average with descriptions in available keys.
Previously published Cephenemyia spp. vouchers provide vague zonal boundaries for tentative identifications; however, dispersal potential of these volant insects and their cursorial-saltatorial hosts is large. Dispersal of bots may be compounded by the frequency of exotic cervid spp. introductions and relocations. Additionally, hybridization among sympatric Cephenemyia spp. may be possible as it is in other dipterans (Stevens & Wall 1996; Dos Santos et al. 2001). It is unknown what morphological effect such hybridi¬ zations could have on both larval and adult specimens, though phenotypic intergrades seem likely. Mixed infections of Cephenemyia spp. in cervids may also confound some efforts at larval species identification. Hence, the genus Cephenemyia remains in a confused taxonomic state (Cogley 1991).
Taxonomically, the genus Cephenemyia could benefit greatly from a thorough phenotypic and genotypic review, and additional molecular studies may generate new information regarding differences among species. Furthermore, field studies could be conducted regarding cervid host ingestion of Cephenemyia larvae and pupae exposed to CWD prions or larvipositing within CWD- free deer by adult botfly females that formerly parasitized CWD- infected deer as larvae. Such research may reveal what role, if any, Cephenemyia spp. play in the transmission of CWD. Presently, a control plan for wild herds is unfeasible, yet Ivermectin® has proved 100% effective in Cephenemyia removal from captured white-tailed deer in Mexico (Weber 1992) and may prove a useful treatment in epidemiological areas among small captive herds.
Acknowledgments
A special thanks is given to Roy Vogtsberger of Midwestern State University for all of his helpful commentary.
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Literature Cited
Anderson, J. R. 2001. Larviposition by nasopharyngeal bot fly parasites of Columbian black-tailed deer: a correction. Med. Vet. EntomoL, 15:438-442. Bennett, G. F. & C. W. Sabrosky. 1962. The nearctic species of the genus Cephenemyia (Diptera, Oestridae). Can. J. ZooL, 40:431-448.
Bennett, G. F, 1962. On the biology of Cephenemyia phobifera (Diptera: Oestridae), the pharyngeal bot of the white-tailed deer, Odocoileus virginianus. Can. J. ZooL, 40:1195-1210.
Bruce, E. A. 1931. Records of insects affecting wildlife in B. C. Rep. Vet. Dir. Gen., Can. Dep. Agr. Append., 5:71-73.
Cogley, T. P. 1987. Effects of Cephenemyia spp. (Diptera: Oestridae) on the nasopharynx of black-tailed deer {Odocoileus hemionus columbianus). J. Wildl.
Dis., 23:596-605.
Cogley, T. P. 1991. Distribution of bot larvae, Cephenemyia spp. (Diptera: Oestridae) from white-tailed deer {Odocoileus virginianus) in Florida. Florida EntomoL, 74:479-481.
Cowan, I. M. 1946. Parasites, diseases, injuries, and anomalies of the Columbian black-tailed deer, Odocoileus hemionus columbianus (Richardson) in British Columbia. Can. J. Res., 24:71-103.
Dos Santos, P., K. Uramoto & S. R. Matioli. 2001. Experimental hybridization among Anastrepha species (Diptera: Tephritidae): production and morphological characterization of Fi hybrids. Ann. EntomoL Soc. Am., 94:717-725.
Fleenor, S. B. & S. W. Taber. 2007. Description of the female and first-instar larva of a new bot fly species from central Texas. Southwest. EntomoL, 32:37-41. Golini, V. L, S. M. Smith & D. M. Davies. 1968. Probable larviposition by Cephenemyia phobifer (Clark) (Diptera: Oestridae). Can. J, Zoo., 46:809-814. Hair, J. A., D. E. Howell, C. E. Rogers & J. Fletcher. 1969. Occurrence of the pharyngeal bot Cephenemyia jellisoni in Oklahoma white-tailed deer, Odocoileus virginianus. Ann. EntomoL Soc. Am., 62:1208-1210.
Hunter, W. D. 1915. A new species of from the United States. Proc.
EntomoL Soc. Wash., 17:169-173.
Johnson, J. L., J. B. Cambell, A. R. Doster, G. Nason & R. J. Cagne. 1983. Cerebral abscess and Cephenemyia phobifer in a mule deer in central Nebraska. J. Wildl. Dis., 19:279-280.
Kellogg, F. E., T. P. Kistner, R. K. Strickland & R. R. Gerrish. 1971. Arthropod parasites collected from white-tailed deer. J. Med. Ent., 8:495-498.
Lupi, O. 2005. Risk analysis of ectoparasites acting as vectors for chronic wasting disease. Med. Hypotheses, 65:47-54.
McMahon, D. C. & T. D. Bunch. 1989. Bot fly larvae {Cephenemyia spp., Oestridae) in mule deer {Odocoileus hemionus) from Utah. J. Wildl. Dis.,
25:636-638.
Nilssen, A. C. 1997. Effect of temperature on pupal development and eclosion dates in the reindeer oestrids Hypoderma tarandi and Cephenemyia trompe (Diptera: Oestridae). Environ. EntomoL, 26:296-306.
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Post, K., D. Riesner, V. Walldorf & R. Melhom. 1999. Fly larvae and pupae as vectors for scrapie. Lancet 122:199-204.
Samuel, W. M. & D. O. Trainer. 1971. Pharyngeal botfly larvae in white-tailed deer. J. Wildl. Dis., 7:142-146.
Severinghaus, C. W. 1949. Tooth development and wear as criteria of age in white¬ tailed deer. J. Wildl. Manage., 13:195-216.
Stevens, J. & R. Wall. 1996. Species, sub-species and hybrid populations of the blowflies Lucilia cuprina and Lucilia sericata (Diptera: Calliphoridae). Proc. R. Soc. Lond.B., 263:1335-1341.
Taber, S. W. & S. B. Fleenor. 2004. A new bot fly species (Diptera: Oestridae) from central Texas. Great Lakes Ent., 37:76-80.
Townsend, C. H. 1941. An undescribed American Cephenemyia. J. N.Y. Entomol. Soc., 49:161-163.
Van Volkenberg, H. L. & A. J. Nicholson. 1943. Parasitism and malnutrition of deer in Texas. J. Wildl. Manage., 7:220-223.
Walker, C. R. 1929. Cephenomyia s^^.kxXXmgdLQox. Science 69:646-647.
Weber, W. 1992. Valoracion clinica del efecto de la Ivermectina contra Cephenemyia spp en venados cola blanca. Vet. Mex., 23:239-242.
SWK at: skelley@usgs.gov
TEXAS J. SCL 61(3): 195-202
AUGUST, 2009
KARYOTYPE DIVERSITY AMONG AND WITHIN AVIAN TAXA:
A SIMPLE TEST IN R
Michael F. SmaO, Michael R. J. Forstner and John T. Baccus
Department of Biology, Wildlife Ecology Program Texas State University - San Marcos San Marcos, Texas 78666
Abstract -Taxonomic categories should be representative of natural groupings based on a shared lineage. Approaches to implementing this tenet are numerous and diverse with molecular methods such as gene sequencing being the most common today. This study suggests that one approach, the use of diploid chromosome characteristics, has been underutilized in avian species, particularly compared to other higher taxa. It is further suggested that a primary cause of this lack of information is because avian chromosomes are more difficult to study than other vertebrate groups. Consequently, a common statistical method is demonstrated to determine if variation in diploid chromosome number is greater between avian taxonomic groups than within them, as would be expected. An example is demonstrated using the powerful, free software package Program R. Implications of these results are also discussed.
Resumen.-Categorias taxonomicas deberian ser representatives de los grupos sobre la base de un linaje compartido. Enfoques para la aplicacion de este principio son multiples y con diversos metodos moleculares como la secuenciacion de genes es el mas comun el dia de hoy. Sugerimos que un enfoque, el uso de cromosomas diploides caracteristicas, ha sido subutilizado en las especies de aves, especialmente en comparacion con otros taxa superiores. Ademas, sugerimos que una de las principales causas de esta falta de informacion se debe a que los cromosomas aviar son mas dificiles de estudiar que otros grupos de vertebrados. En consecuencia, demostrar un metodo estadistico comun para determinar si la variacion en el numero diploide de cromosomas aviar es mayor entre los grupos taxonomicos que dentro de ellos, como era de esperar. Demostramos esta usando el gran alcance, libre del paquete de software R. Programa Consecuencias de nuestros resultados son tambien discutidos.
A karyotype is a characterization of an entire set of chromosomes from an individual with regard to number, size, and shape (Shields 1982). For more than 30 years researchers have acknowledged that karyotypes represent part of an individuaTs phenotype (Chiarelli & Capanna 1973) alongside its inherent link to the genome. With more recent technological advances in karyological techniques, this is even truer today.
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The purpose of this paper is intended as both informative with regard to application of a simple but efficient mechanism to evaluate genomic diversity and attempts to address and integrate two distinct issues that are believed to be of valuable as approaches in avian karyology and statistical analysis that have been ignored and often misrepresented. Foremost among concerns is emphasiz¬ ing the gap in karyological knowledge of avian chromosomes versus other vertebrate taxa and second demonstrating the useful¬ ness and flexibility of the free statistical package R.
Avian chromosomes -OnQ critical and often overlooked aspect of the advances in genomics has been, and remains, the dearth of information for avian karyotypic and even general cytogenetic data. Shields (1982) was among the first to point out that avian cyto¬ genetics research effort has lagged behind that of other vertebrate taxa. The authors are in agreement, and believe this is still the case for a very fundamental reason. Avian karyotypes are more difficult to work with than other vertebrate taxa.
There are fewer studies of avian karyology than in other craniate groups (De Boer & Van Brink 1984). From about 1970 to 1980 the number of identified avian karyotypes doubled (Shields 1982). However, at that time, only about 5-10% of the about 9,000 extant species of birds had been karyotyped, many poorly (Shields 1983). Although progress has undoubtedly been made in elucidating karyotypes of avian species in recent years, to what degree remains undocumented. Shields (1982) also pointed out that no compre¬ hensive cytogenetic analysis of a population of any wild bird species has been undertaken. This is currently still correct.
The descriptions of bird karyotypes are inherently more proble¬ matic than those of other vertebrate groups because of higher chromosome numbers, small numbers (8~15 pairs) of macro¬ chromosomes, and 30-40 pairs of microchromosomes. Makino et al. (1956) described a diploid number of 80 as definitive for mourning doves {Zenaida macroura), however, Benirschke & Hsu
SMALL, FORSTNER & BACCUS
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(1971) found In = 78. Microchromosomes are difficult to accurate¬ ly count because of small size and morphological uniformity. It is not uncommon for the diploid number to be reported within a range because of differences in number of microchromosomes (usually ± 2) between cells. Small et al. (1993) reported finding three distinct diploid numbers, not in a single species, but in the same tissue from a single individual. This was not the result of difficulties in technique, as numerous, well spread karyotypes were examined, and meiotic karyotypes showed similar variability (Small 1991). As the case in numerous species, the difference was in the number of microchromosomes.
Consequently, in general, current cytogenetic studies of avian chromosomes focus on specific macrochromosomes, which are highly conserved (Stock & Mengden 1975, Derjusheva et al. 2004) or sex chromosomes (Ellegren 2000). However, microchromo¬ somes are not unimportant components of the avian karyotype, particularly given that nucleolus organizer regions in avian species are located on microchromosomes (Small 1991). This is supported by recent work on the chicken genome project which shows that microchromosomes are gene rich and subsequently important components of avian genomes (Douaud et al. 2008).
Program /^.-Program R is essentially a free, downloadable version of S-Plus (Insightfiil Corporation). In our experience it is an extremely powerful program for ecological analyses with excellent graphing capabilities. However, despite recent commer¬ cial efforts (Dalgaard 2002, Maindonald & Braun 2006), no comprehensive, downloadable user’s guide exists for Program R. Consequently, this study presents a detailed example of application of R to encourage researchers and students to make an effort to learn and use this program.
Integrating R and ATaTjo/og^y.-Systematists have classified species into discrete taxonomic groups in an effort to facilitate an understanding of the structure and nature of diversity. Therefore,
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THE TEXAS JOURNAL OF SCIENCE-VOL. 61, NO. 3, 2009
classification of species into taxa has attempted to separate organisms into natural groups. Additionally, taxonomy today explicitly seeks to group taxa based on their evolutionary history (i.e., phylogeny; Cracraft 1981). Consequently, the nature of karyotypes makes it reasonable to expect them to reflect that natural relationship. Thus, lower variation within taxonomic groups than between them, in regard to karyotype should be expected.
Methods
Karyotype character variation can be analyzed using a linear mixed effects (Ime) model with taxa (i.e., family, order, etc.) as a random factor, karyotypic characteristic (i.e., diploid number, fundamental number, etc.) as the response variable, and species as replicates. This allows partitioning of sources of variation in an unbalanced data set. Data can be analyzed using Program R computer software (R Development Core Team 2005) with maximum likelihood estimates in all analyses. Program R uses restricted maximum likelihood estimates as the default for Ime models, which may yield slightly different results than other software if not taken into account. Unrestricted maximum likelihood estimates are used in this example.
An example using Program R cor/e.-Below is an example model code using diploid numbers from six avian families (this is for illustration so sample sizes are small). Explanations are given in italics bounded by # symbols:
> diploid.number<-scan()
# creates a database to store the diploid numbers #
# the number preceding the colon denotes the numerical level of the next entry #
1: 76 80 80 76 76 80 80 76 76 76 76 76 76 76 86 78 76 78 74 78 76 76 78 68
# Columbidiae #
25:86 78 74 76 76 76 76 80 80
# Troglodytidae #
34: 78 52 68 52 68 60 60 68 72 56
SMALL, FORSTNER & BACCUS
199
# Ciconiidae #
44: 78 92 80 82 82 80
# Anatidae #
50: 54 48 48 52 52 86
# Falconidiae #
56: 92 92 84 108 108 94 88 92 90 92
# Picidae #
66:
Read 65 items
# data is entered in separate strings for each taxa (in this case ‘family”) #
> family<-factor(rep(LETTERS[l:6],c(24,9,10,6,6,10)))
# creates a sequence of letters A-F designating families such that there are 24 “A ”s, 9 “B ”s, etc. #
> number<-data.frame(family,diploid.number)
# creates a matrix of families and diploid numbers #
> diploid<-
lme(diploid.number~l,data=number,random=~l I family, method="ML")
# creates a data file to store the model information; Ime tells R to use linear mixed-effects model and method=”ML” tells R to use unrestricted maximum likelihood #
> summary(diploid)
# displays output of the analysis #
Example data output:
Linear mixed-effects model fit by maximum likelihood
Data: number
AlC BIG 460.9535 467.4767
logLik
-227.4768
Random effects:
Formula: ~1 | family
(Intercept) Residual
StdDev: 11.95630 6.842518
Fixed effects: diploid.number ~ 1
Value Std.Error
(Intercept) 75.27702 5.009927
DF t-value p-value
59 15.02557 0
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THE TEXAS JOURNAL OF SCIENCE-VOL. 61, NO. 3, 2009
Standardized Within-Group Residuals:
Min Q1 Med
-1.7211003 -0.4350450 -0.1427550
Q3 Max
0.3062634 4.1461398
Number of Observations: 65 Number of Groups: 6
>intervals(lme(diploid.number~l,data=number,random=~l|family,method="ML")) # provides 95% Confidence Intervals #
Approximate 95% confidence intervals
Fixed effects:
lower
(Intercept) 65.3296 attr(, "label")
[1] "Fixed effects:"
Random Effects:
Level: family
lower
sd((Intercept)) 6.629736
est.
75.27702
upper
85.22445
est.
11.95630
upper
21.56240
# among group variance and 95%) confidence intervals #
Within-group standard error:
lower est. upper
5.712406 6.842518 8.196206
# within group variance and 95% confidence intervals #
Results
The output of this model gives intercept and residual standard deviations. Squaring the intercept standard deviation gives among taxa variance and squaring the residual standard deviation gives within taxa variance. From these data, percent variance attributable to each source can be calculated as well as confidence intervals. In this example (11.95630^ [(11.95630^+(6.842518^)] gives percent variance among families and 1-(1 1.95630^)/ [(11.95630^+
(6.842518^)] gives percent variance within familes, 75.3 and 24. 7%, respectively.
SMALL, FORSTNER & BACCUS
201
Discussion
One of the key difficulties in examining generalized trends in karyotypic evolution is sample size. In the example presented here, the vast majority of variance, 75%, is attributable to among family variation, yet there is no significant difference at a < 0,05. Thus, a power analysis may be warranted to demonstrate either a more appropriate sample size or a-level.
Another consideration in using this test is determining which karyotypic characteristic is appropriate for analysis. In groups with highly conserved karyotypes, such as birds (Derjusheva et al. 2004), differences in diploid number likely result from centromeric fissions and fusions (Burt 2002). In such cases, ftindamental number may be a more biologically relevant measure of variance than diploid number.
This example describes a relatively simple statistical test to partition variation in karyotypes. This paper is intended as an example of a potentially useful technique and is not intended to address all considerations researchers should consider (e.g., homoplasy). It is not intended to suggest that karyology is a better method than analysis of mitochondrial or nuclear DNA, but is unique and complimentary, and certainly should be considered when addressing issues of taxonomy. Consequently, as presented, the methodology is applicable to any appropriate data set.
Acknowledgments
The authors thank F. W. Wekerly, B. S. Cade, G. V. Roslik, and A. P. Kryukov, and an anonymous reviewer for helpful and encouraging comments on drafts of this manuscript.
Literature Cited
Benirschke, K. & T. C. Hsu. 1971. Chromosome atlas: fish, amphibians, reptiles,
and birds. Springer- Verlag, New York, 208 pp.
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Burt, D. W. 2002. Origin and evolution of avian micrchromosomes. Cytogenet. and Genome Res., 96:97-1 12.
Chiarelli, A. B. & E. Capanna. 1973. Cytotaxonomy and vertebrate evolution. Academic Press, New York 783 pp.
Cracraft, J. 1981. Toward a phylogenetic classification of the recent birds of the world (Class Aves). Auk, 98:681-714.
Dalgaard, P. 2002. Introductory statistics with R. Springer, New York, NY, 364 pp.
Douaud, M., K. Feve, M. Gams, V. Fillon, S. Bardes, D. Gourichon, D. A. Dawson, O. Hanotte, T. Burke, F. Vignoles, M. Morrison, M. Tixier-Boichard, A. Vignal & F. Pitel. 2008. Addition of the microchromosome GGA25 to the chicken genome sequence assembly through radiation hybrid and genetic mapping. BMC Genomics, 9: 129. Published online 2008 March 17. doi: 10.1186/1471-2164-9- 129.
De Boer, E. M. & J. M. Van Brink. 1982. Cytotaxonomy of the Ciconiiformes (Aves), with eight species new to cytology. Cytogenet. Cell Genet., 34:19-34.
Derjusheva, S., A. Kuganova, F. Habermann & E. Gaganskya. 2004. High chromosome conservation detected by comparative chromosome painting in chicken, pigeon and passerine birds. Chromosome Res., 12: 715-723.
Ellegren, H. 2000. Evolution of the avian sex chromosomes and their role in sex determination. Trends in Ecology & Evolution, 15:188-192,
Makino, S., T. Udagawa & Y. Yamashina. 1956. Karyot3T>ic studies in birds. 2: A comparative study of chromosomes in the Columbidae. Caryologia, 8:275-293.
Maindonald, J. & J. Braun. 2006. Data Analysis and Graphics Using R: An Example-based Approach. Cambridge University Press, Cambridge, U.K.
R Development Core Team (2005). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org.
Shields, G. F. 1982. Comparative avian C34ogenetics: a review. Condor, 84:45-58.
Shields, G. F. 1983. Bird chromosomes. Pp. 189-209, in Current Ornithology, (R. F. Johnson, ed.). Plenum Press, New York. 1 : 1-402.
Small, M. F. 1991. The karyology of the white- winged dove {Zenaida asiatica) in Texas. Unpublished M.S. thesis, Sul Ross State Univ., Alpine, Texas, 88 pp.
Small, M. F., K. M. Hogan & J. F. Scudday. 1993. The karyotype of the White¬ winged Dove. Condor, 95:1051-1053.
Stock, A. D. & G. A. Mengden. 1975. Chromosome banding pattern conservatism in birds and nonhomology of chromosome banding patterns between birds, turtles, snakes, and amphibians. Chromosoma, 50(l):69-77.
MFS at: ms81@txstate.edu
TEXAS I OF SCI. 61(3):203=-218
AUGUST, 2009
THE ARKANSAS ENDEMIC FAUNA:
AN UPDATE WITH ADDITIONS, DELETIONS,
A SYNTHESIS OF NEW DISTRIBUTIONAL RECORDS,
AND CHANGES IN NOMENCLATURE
Chris T* McAllister, Henry W. Robison and Michael E. Slay
RapidWrite, 102 Brown Street, Hot Springs National Park, Arkansas 71913 Department of Biology, Southern Arkansas University Magnolia, Arkansas 71754 and The Nature Conservancy, 601 North University Avenue Little Rock, Arkansas 72205
Abstract -This study provides an update to the endemic biota of Arkansas by adding 19 species to the state list, including two fungi, three gastropods, one araneid, two opilionids, two pseudoscorpions, one diplopod, three collembolans, two trichopterans, one coleopteran, one dipteran and one hymenopteran. In addition, seven species (one pseudoscorpion, one collembolan, one bivalve, one ephemeropteran, and three trichopterans) are removed from the state list and a synthesis of new distributional records and changes in nomenclature are provided for several species. This update brings to 126 the number of endemic species of the state.
Robison et aL (2008) provided the most recent compilation on the endemic biota of Arkansas. Their update brought to 113 (10 species of plants and 103 species/subspecies of animals) the total number of Arkansas endemic flora and fauna. However, several species were inadvertently overlooked. The following 19 species are added to the list of Arkansas endemics: two fungi, three gastropods, one araneid, two opilionids, two pseudoscorpions, one diplopod, three collembolans, two trichopterans, one coleopteran, one dipteran, and one hymenopteran. In addition, seven species (one pseudoscorpion, one collembolan, one bivalve, one ephemer¬ opteran, and three trichopterans) are removed from the state list; a synthesis of new distributional records are added for two gastropods, one coleopteran, and one amphibian, and changes in nomenclature are provided for three gastropods and two coleopterans. This update brings to 126 the number of endemic species of the state.
204 THE TEXAS JOURNAL OF SCIENCE-VOL. 6 1 , NO. 3, 2009
Table 1. Biota added to the state list of endemic species of Arkansas and counties of occurrence.
|
Taxon |
County/Counties |
Reference |
|
Fungi |
||
|
Dictyostelium caveatum |
Stone |
Landolt et al. (2006) |
|
Cryptovalsaria americana |
Polk |
Vasilyeva & Stephenson (2007) |
|
Animalia |
||
|
Daedalochila bisontes |
Madison, Newton, Searcy |
Coles & Walsh (2006) |
|
Xolotrema occidentale |
Independence, Stone |
Walsh & Coles (2002) |
|
Marstonia ozarkemis |
Baxter |
Hershler (1994) |
|
Neoleptoneta arkansa |
Stone |
Gertsch (1974) |
|
Crosbyella distincta |
Boone |
Goodnight & Goodnight (1942) |
|
Crosbyella roeweri |
Benton |
Goodnight & Goodnight (1942) |
|
Apochthonius diabolus |
Washington |
Muchmore (1967) |
|
Apochthonius titanicus |
Stone |
Muchmore (1976) |
|
Aliulus carrollus |
Benton, Carroll, Searcy, |
|
|
Washington |
Hoffman (1999) |
|
|
Typhlogastnira fousheensis |
Independence |
Christiansen & Wang (2006) |
|
Pygmarrhopalites youngsteadti |
Newton |
Zeppelini et al. (2009) |
|
Pygmarrhopalites buffaloensis |
Newton |
Zeppelini et al. (2009) |
|
Cheumatopsyche robisoni |
Garland, Montgomery, Polk Moulton & Stewart (1996) |
|
|
Lepidostoma lescheni |
Logan, Montgomery |
Moulton et al. (1999) |
|
Heterosternuta ouachitus |
Howard, Izard, Newton, Pike, Randolph, Searcy, |
|
|
Sharp* |
Longing & Hazzard (2009) |
|
|
Atomosia arkansensis |
Hempstead |
Barnes (2008) |
|
Idris leedsi |
Johnson |
Masner & Denis (1996) |
* There are natural heritage records that also exist for Johnson and Pope counties (NatureServe 2009).
List of Species
Material included following is a listing of the species added (Table 1) and removed from the state endemic list, including a synthesis of new distributional records and changes in nomenclature for other endemic biota.
Additions to the State Endemic Fauna
Fungi, Mycetozoa, Dictyosteliaceae Dictyostelium caveatum Waddell 1982
This cellular slime mold was described by Waddell (1982) from a single isolate found on bat guano in total darkness in Blanchard Springs Caverns, Stone County, Arkansas. It is considered to be a
MCALLISTER, ROBISON & SLAY
205
true Arkansas endemic found in a single Ozark cave to date (Landolt et al. 2006).
Sordariomycetes
Cryptovalsaria americana Vasilyeva &l Stephenson 2007
This fungus was described by Vasilyeva & Stephenson (2007) from specimens collected from the Ouachita Mountains Biological Station, 6.5 km west of Big Fork, Polk County, Arkansas. Collections of C americana were taken from the living bark of hazel alder (Alnus serrulata).
Animalia, Mollusca, Gastropoda, Polygyridae
Daedalochila (syn. Millerelix) bisontes Coles & Walsh 2006
The Buffalo River liptooth, Daedalochila bisontes was previously thought to be D. (Millerelix) peregrina from specimens deposited in the Causey collection at the University of Arkansas- Fayetteville and the Hubricht collection at the Field Museum of Natural History-Chicago (Coles & Walsh 2006). It is considered imperiled (G2) in rounded global status (NatureServe 2009). The species inhabits limestone outcrops in the Ozarks, including Madison, Newton, and Searcy counties (Walsh & Coles 2002; Coles & Walsh 2006).
Xolotrema occidentale (Pilsbry & Ferriss 1907)
The Arkansas wedge, Xolotrema occidentale (syn. Triodopsis occidentalis) is known only from Independence and Stone counties, Arkansas (Pilsbry & Ferriss 1907; Walsh & Coles 2002). This snail is considered critically imperiled (Gl) in rounded global status by NatureServe (2009) and a species of special concern in the state by the Arkansas Game and Fish Commission (Anonymous 2004).
Hydrobiidae
Marstonia ozarkensis (Hinkley 1915)
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THE TEXAS JOURNAL OF SCIENCE-VOL. 61, NO. 3, 2009
The Ozark pyrg, Marstonia ozarkensis (formerly Pyrgulopsis ozarkensis) is known only from the type locality, the North Fork of the White River above Norfolk, Baxter County, Arkansas (Hershler 1994). Thompson & Hershler (2002) re-evaluated eastern North American species assigned to Pyrgulopsis and recognized them as distinct species of the genus Marstonia. Interestingly, Wu et al. (1997) lists a single site on the North Fork of the White River in Ozark County, Missouri for M ozarkensis. However, efforts to relocate this species beyond the single reported location in Missouri have been unsuccessful (Natureserve 2009). This snail has also likely been extirpated in Arkansas (Wu et al. 1997). It is considered G1 in rounded global status (NatureServe 2009) and a species of special concern in Arkansas (Anonymous 2004).
Arthropoda, Araneae, Leptonetidae
Neoleptoneta arkansa (Gertsch 1974)
This troglophilic spider was described by Gertsch (1974) from Blanchard Springs Caverns, Stone County, Arkansas. Dorris (1985) included the species as Leptoneta arkansa in her checklist of Arkansas spiders.
Opiliones, Phalangodidae
Crosby ella distincta Goodnight & Goodnight 1942
This harvestman (an eyeless obligate cavemicole) was described by Goodnight & Goodnight (1942) from specimens collected in Wagler’s Cave near Harrison, Boone County, Arkansas. It is considered critically imperiled (SI) in the state (NatureServe 2009).
Crosby ella roeweri Goodnight & Goodnight 1942
This harvestman species was described by Goodnight & Goodnight (1942). Specimens were collected in Tom Danforth Cave, Benton County, Arkansas. This is an eyed troglophile that is considered SI in Arkansas (NatureServe 2009).
MCALLISTER, ROBISON & SLAY
207
Pseudoscorpiones, Chthoniidae
Apochthonius diabolus Muchmore 1967
Muchmore (1967) described A. diabolus from a single male specimen from DeviFs Den Cave at DeviFs Den State Park, Washington County, Arkansas. This obligate cavemicole is considered SI in the state (NatureServe 2009).
Apochthonius titanicus Muchmore 1976
This pseudoscorpion was described by Muchmore (1976) from individuals collected from Blanchard Springs Caverns, 5.6 km east of Fifty Six, Stone County, Arkansas. Specimens were found under a piece of paper near “The Titans”. This obligate cavemicole is considered SI in Arkansas (NatureServe 2009).
Diplopoda, Julida, Parajulidae
Aliulus carrollus Causey 1950
This milliped was included as a state endemic by Robison & Allen (1995) but inadvertently overlooked and not included by Robison et al. (2008). The species was reported by Robison & Allen (1995) from Carroll and Washington counties. However, additional specimens have been reported from Benton and Searcy counties (Hoffman 1999). The species may eventually be found in adjacent states as the type locality (Blue Spring, Carroll County) is just south of the Missouri line (Causey 1950) and sites in Benton and Washington counties are close to eastern Oklahoma,
Hexapoda, Collembola, Hypogastmridae
Typhlogastrura fousheensis Christiansen & Wang 2006
This springtail species was described by Christiansen & Wang (2006) from Foushee Cave, Independence County, Arkansas. A single adult was collected by Norman and Jean Youngsteadt in May 1978. Additional adult specimens were collected 27 years later by the same collectors from bat guano in the same cave on 18 March 2005 (Christiansen & Wang 2006).
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Arrhopalitidae
Pygmarrhopalites youngsteadtii Zeppelini, Taylor & Slay 2009
Specimens of this springtail species were collected from Tom Barnes Cave, Newton County, Arkansas (Zeppelini et al. 2009). This cave is located in the Ozarks within the Buffalo National River.
Pygmarrhopalites buffaloensis Zeppelini, Taylor & Slay 2009
The holotype was collected from Walnut Cave, Newton County, Arkansas (Zeppelini et al. 2009). This cave is located near the Buffalo River, about 26 km upstream from the cave where P. youngsteadtii was collected.
Trichoptera, Hydropsychidae
Cheumatopsyche robisoni Moulton & Stewart 1 996
This caddisfly was described by Moulton & Stewart (1996) from specimens collected from Strawn Spring, 0.8 km east of Caddo Gap, Montgomery County, Arkansas. Additional specimens of C robisoni were collected from other sites in Garland, Montgomery and Polk counties, Arkansas (Moulton & Stewart 1996). It appears this species is endemic to small, spring-fed streams in the Ouachita Mountain physiographic subregion. With additional collecting, C. robisoni may be found just across the border in LeFlore County, Oklahoma (along Rich Mountain) as specimens are available from sites just to the east. This species is considered critically imperiled (Gl) in rounded global status (NatureServe 2009).
Lepidostomatidae
Lepidostoma lescheni Bowles, Mathis & Weaver 1994
A single male L. lescheni was collected from Slocum Spring on Mt. Magazine, Logan County, Arkansas, and described by Bowles et al. (1994). Additional specimens (both males and females) were collected from several sites in seep locations in the central Ouachita Mountain region of the state in Montgomery County (Moulton et al.
MCALLISTER, ROBISON & SLAY
209
1999). A report (Weaver 2002) of the species from Missouri and Oklahoma is erroneous (S. R. Moulton II pers. comm.). However, additional collecting may reveal populations in similar seep areas of eastern Oklahoma. This species is considered G1 in rounded global status (NatureServe 2009).
Coleoptera, Dytiscidae
Heterosternuta ouachitus (Matta &Wolfe 1979)
The species was originally described as Hydroporus ouachitus by Matta & Wolfe (1979). The subgenus Heterosternuta was elevated to generic status by Matta & Wolfe (1981). The species was originally reported from sites in the Ouachita Mountains (Matta & Wolfe 1981). However, Pippenger & Harp (1985) reported the range of H. ouachitus reaches into the Ozark Mountains (Janes Creek, Randolph County). More recently, Harp & Robison (2006) reported H. ouachitus from the Strawberry River system in Izard and Sharp counties. Additional specimens were reported from Long Creek (Searcy County), Beech Creek (Newton County), and West Lafferty Creek (Izard County) by Longing & Haggard (2009). Interestingly, Wolfe (2000) mentioned in couplets of keys to Heterosternuta beetles, H, ouachitus probably occurs outside of Arkansas; however, specimens have not yet been collected from adjacent states or elsewhere (S. D. Longing, pers. comm.). The species is considered imperiled (S2) in the state (NatureServe 2009).
Diptera, Asilidae
Atomosia arkansensis Barnes 2008
This robber fly was described by Barnes (2008) from specimens collected in blackland prairie at Grandview Prairie Wildlife Management Area near Columbus, Hempstead County, Arkansas. The species is ranked SI in the state (NatureServe 2009) due to its limited range.
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Hymenoptera, Scelionidae
Idris leedsi Masner & Denis 1996
A parasitoid wasp, Idris leedsi was described from a single female collected using yellow pan traps from Baker Spring, 35.4 km NW of Clarksville, Johnson County, Arkansas (Masner & Denis 1996). Scelionids are solitary primary parasitoids of eggs of various spiders (Johnson 1992).
Species Removed from the State Endemic Fauna
Bivalvia, Unionidae
Villosa arkansasensis (Lea 1862)
The Ouachita creekshell was reported to be an Arkansas endemic by Robison & Allen (1995) from Clark, Garland, Howard, Montgomery, Pike, Polk and Saline counties. In addition, it was subsequently listed as an endemic by Robison et al. (2008). However, Galbraith et al. (2008) report specimens of V. arkansasensis from the Little River system of McCurtain County, Oklahoma. It is a species of special concern in Arkansas (Anonymous 2004).
Pseudoscorpiones, Neobisiidae
Tartarocreagris ozarkensis (Hoff 1945)
This pseudoscorpion was described as Microcreagis ozarkensis by Hoff (1945) from specimens collected from Devil’s Den State Park and Farmington, Washington County, Arkansas (Hoff 1945). The species (=M ozarkensis) was included as an Arkansas endemic by Allen (1988), Robison & Allen (1995) and Robison et al. (2008). It is now known from additional localities in Arkansas (Clark and Pulaski counties) and Latimer County, Oklahoma (Muchmore 2001), and is ranked SI in the state (NatureServe 2009).
MCALLISTER, ROBISON & SLAY
211
Collembola, Entomobryidae
Pseudosinella dubia Christiansen 1960
Christiansen (1960) described this troglobitic springtail from specimens collected from Devil’s Den Kitchen Cave, Devil’s Den Cave, and Granny Dean Cave, Washington County, Arkansas. It was again reported from Devil’s Den Cave by Peck & Peck (1982). Subsequently, the species was reported from a cave in Dent County, Missouri, and a cave in Adair County, Oklahoma (Slay et al. 2009).
Ephemeroptera, Ephemerellidae
Dannella provonshai (McCafferty 1977)
This mayfly was originally described by McCafferty (1977) from specimens collected on the Mulberry River, Johnson County, Arkansas. Robison & Allen (1995) reported it was known only from the type locality and Robison et al. (2008) included D. provonshai in their list of endemics. However, the species has now been reported from Alabama, Kentucky, New York, and Tennessee (McCafferty & Webb 2006; NatureServe 2009; Ogden et al. 2009). In Arkansas, D. provonshai is ranked SI (NatureServe 2009).
Trichoptera, Helicopsychidae
Helicopsyche limnella Ross 1938
Ross (1938) originally described this caddisfly from an unknown Arkansas county. Unzicker et al. (1970) listed seven sites for H, limnella in Benton, Crawford, Madison, and Washington counties. Robison & Allen (1995) included Benton, Clark, Crawford, Franklin, Garland, Hot Spring, Johnson, Madison, Montgomery, Polk, Saline, and Washington counties in the range of H. limnella. The species was also included in the Arkansas endemic biota list of Robison et al. (2008). However, H. limnella has now been reported from Missouri and Oklahoma (Moulton & Stewart 1996).
Hydroptilidae
Ochrotrichia robisoni Frazer & Harris 1991
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This microcaddisfly species was described by Frazer & Harris (1991) from specimens collected from Bear Creek at St, Hwy 7, 3.2 km south of Hollis, Perry County, Arkansas. The species is SI in Arkansas (NatureServe 2009) and has been reported recently from Oklahoma (Moulton & Stewart 1996).
Psychomyiidae
Paduniella nearctica Flint 1967
This caddisfly was originally described from specimens collected from Devil’s Den State Park, Washington County, Arkansas (Flint 1967); additional records include Johnson County, Arkansas (Moulton & Stewart 1996). As such, it was included as a state endemic species by Robison & Allen (1995) and Robison et al. (2008). However, P. nearctica has now been reported from southern Missouri (Moulton & Stewart 1996).
New Distributional Records and/or Changes in Nomenclature Gastropoda, Polygyridae
Daedalochila (syn. Millerelix) peregrina (Rehder 1932)
The White Liptooth was reported as Polygyra peregrina in Robison & Allen (1995) and Robison et al. (2008). However, Coles & Walsh (2006) found that the diagnostic characters used to define the genus Millerelix sensu Emberton (1995) were unreliable and placed member species into the senior genus Daedalochila Beck. The species is known from Izard, Marion, Newton, Searcy and Stone counties (Robison & Smith 1982). Walsh & Coles (2002) reported D. peregrina from Carroll County. This snail is G2 in rounded global status (NatureServe 2009) and a species of special concern in Arkansas (Anonymous 2004).
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Patera clenchi (Rehder 1932)
The Calico Rock oval, P. clenchi was reported by Hubricht (1972) only from a rock slide on Mt, Nebo, Yell County, Arkansas. Robison & Smith (1982), Robison & Allen (1995) and Robison et al. (2008) reported P. clenchi as Mesodon clenchi from Izard and Yell counties. Walsh & Coles (2002) reported two new distributional records for P. clenchi in Searcy and Scott counties. It is considered G1 in rounded global status (NatureServe 2009) and a species of special concern in the state (Anonymous 2004).
Inflectarius magazinensis (Pilsbry & Ferriss 1907)
This Magazine Mountain shagreen is only known to occur on the north slope of Mt. Magazine in the Ozark National Forest of Logan County, Arkansas (Pilsbry & Ferriss 1907). It was listed as an Arkansas endemic by Robison & Smith (1982), Robison & Allen (1995) and Robison et al. (2008) as Mesodon magazinensis. Caldwell (1986) was unable to verify L magazinensis from the south slope of Mt. Magazine; however, additional specimens were reported from the north slope by Walsh & Coles (2002). Its limited range makes it particularly sensitive to any habitat alteration and it is therefore listed as SI in Arkansas (NatureServe 2009), as an endangered species in the state (Anonymous 2004), and as a threatened species by the U.S. Fish and Wildlife Service on 17 April 1989 (Anonymous 1989).
Coleoptera, Dytiscidae
Heterosternuta sulphuria (Malta & Wolfe 1979)
This predaceous diving beetle was originally described as Hydroporus sulfurus by Malta & Wolfe (1979) and included as an Arkansas endemic by Robison & Allen (1995). The subgenus Heterosternuta was elevated to the generic level by Malta & Wolfe (1981). Specimens of this endemic species were originally collected from Sulphur Springs, Benton County, Arkansas (Malta & Wolfe 1979). Additional historical records include sites in Izard,
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Newton, and Searcy counties. More recently, however. Longing & Haggard (2009) reported new distributional records for H. sulphuria in Benton, Newton, and Washington counties, including the first report of the species from the entrance of a cave. With additional collecting, this d3discid may eventually be found outside of Arkansas in adjacent states (S. D. Longing, pers. comm.).
Chordata, Amphibia, Caudata, Plethodontidae
Plethodon caddoensis Pope & Pope 1951
The Caddo Mountain salamander, Plethodon caddoensis was reported to be an Arkansas endemic in Howard, Montgomery, and Polk counties (Robison & Allen 1995). Trauth & Wilhide (1999) reported new geographic records for P. caddoensis from two sites in Pike County. This salamander is considered a species of special concern in the state (Anonymous 2004).
In summary, the present study brings to 126 species the number of endemic biota of Arkansas. Nineteen species have been added to the state list since the last update in 2008. In addition, seven species (one pseudoscorption, one springtail, one bivalve, one ephemeropteran, and three caddisflies) are removed from the state list and a synthesis of new distributional records is added for two endemic gastropods, one endemic coleopteran, and one endemic amphibian. Changes in nomenclature are provided for three endemic gastropods and two endemic coleopterans.
Acknowledgments
Appreciation is extended to D. Bowles (National Park Service), G. L. Harp (Arkansas State University), G. Leeds (U. S. Forest Service), S. D. Longing (UA-Fayetteville), J. C. Morse (Clemson University), S. R. Moulton, II (U.S. Geological Survey), F. Spiegel (UA-Fayetteville), S. Stephenson (UA-Fayetteville), and J. S. Weaver, III (New Hampshire) for providing information on Arkansas endemics. We also thank S. R. Moulton, II for critically reviewing the manuscript. Funding for MBS was provided by the
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Arkansas Game and Fish Commission, The Nature Conservancy (Arkansas Field Office), and U. S. Fish and Wildlife Service (Arkansas Ecological Services).
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Anonymous. 2004. Arkansas endangered, threatened, and species of special concern (January 9, 2004). Arkansas Game & Fish Comm. Rep., Little Rock, Arkansas, 6
pp.
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Caldwell, R. S. 1986. Status of Mesodon magazinensis (Pilsbry and Ferriss), the Magazine Mountain middle-toothed snail. Grant No. 84-1 for Arkansas Nongame Species Preserv. Prog., Little Rock, Arkansas, 1 8 pp.
Causey, N. B. 1950. New genera and species of millipeds-Paraiulidae (Juloidea). Proc. Arkansas Acad. Sci., 3:45-58.
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Christiansen, K. & H. Wang. 2006. A revision of the genus Typhlogastrura in North American caves with description of five new species. J. Cave Karst Stud., 68:85- 98.
Coles, B. F. & G. E. Walsh. 2006. Daedalochila sp. nov. from northwest Arkansas, U.S.A., the anatomy of the Polygyra pUcata group, and the validity of the genus Millerelix Pratt, 1981 (Gastropoda: Pulmonata: Polygyridae). American Malacol. Bull., 21:99-112.
Dorris, P. R. 1985. A check-list of spiders of Arkansas. Proc. Arkansas Acad. Sci., 39: 34-39.
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Galbraith, H. S., D. E. Spooner & C. C. Vaughn. 2008. Status of rare and endangered freshwater mussels in southeastern Oklahoma. Southwest. Nat., 53:45-50.
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Longing, S. D. & B. E. Haggard. 2009. New distribution records of an endemic diving beetle, Heterosternuta sulphuria (Coleoptera: Dytiscidae: Hydroporinae), in Arkansas with comments on habitat and conservation. Southwest. Nat., 54:357-361.
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Moulton, S. R. IL, H. W. Robison & B. G. Crump. 1999. The female of Lepidostoma lescheni (Trichoptera: Lepidostomatidae), with new distributional records for the species. Entomol. News, 1 10:85-88.
Muchmore, W. B. 1967. New cave pseudoscorpions of the genus Apochthonius (Arachnida: Chelonethida). Ohio J. Sci., 67:89-95.
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Muchmore, W. B. 1976. New species of Apochthonius, mainly from caves in central and eastern United States (Pseudoscorpionida. Chthoniidae). Proc. Biol. Soc. Washington, 89:67-80.
Muchmore, W. B. 2001. Review of the genus Tartar ocreagis, with descriptions of new species (Pseudoscorpionida: Neobisiidae). Texas Mem. Mus., Speleol. Mon., 5:57-72.
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Ogden, T. H., J. T. Osborne, L. M. Jacobus & M. F. Whiting. 2009. Combined molecular and morphological phylogeny of Ephemerellinae (Ephemerellidae: Ephemeroptera), with remarks about classification. Zootaxa, 1991:28-42.
Pilsbry, H. A. & J. H. Ferriss. 1907. Mollusca of the Ozarkian fauna. Proc. Acad. Nat. Sci. Philadelphia, 1906:529-556.
Peck, S. B. & J, H. Peck. 1982. Invertebrate fauna of Devils Den, a sandstone cave in northwestern Arkansas. Proc. Arkansas Acad. Sci., 36:46-48.
Pippenger, M. A, & G. L. Harp. 1985. Dytiscidae from Randolph County, Arkansas. Proc. Arkansas Acad. Sci., 39:146-147.
Robison, H. & R. T. Allen. 1995. Only in Arkansas: a study of the endemic plants and animals of the state. Univ. Arkansas Press, Fayetteville, xii + 121 pp. Robison, H. W. & K. L. Smith. 1982. The endemic flora and fauna of Arkansas. Proc. Arkansas Acad. Sci., 36:52-57.
Robison, H., C. McAllister, C. Carlton & G. Tucker. 2008. The Arkansas endemic fauna: an update with additions and deletions. J. Arkansas Acad. Sci., 62:84-96. Ross, H. H. 1938. Descriptions of new North American Trichoptera. Proc. Washington Entomol. Soc., 40:1 17-124.
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Unzicker, J. D., L. Argus & L. O. Warren. 1970. A preliminary list of the Arkansas Trichoptera. J. Georgia Entomol. Soc., 5:167-174.
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Waddell, D. R. 1982. A predatory slime mould. Nature, 298:464-466.
Walsh, G. W. & B. F. Coles. 2002. Distributions and geographical relationships of the polygyrid land snails (Mollusca, Gastropoda, Polygyridae) of Arkansas. J. Arkansas Acad. Sci., 56:212-219.
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Weaver, J. S., IIL 2002. A synonymy of the caddisfly genus Lepidostoma Rambur (Trichoptera: Lepidostomatidae), including a species checklist. Tijdschrift voor EntomoL, 145:173-192.
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Series, No. 5. Missouri Dept. Conservation: Jefferson, Missouri, 97 pp.
Zeppelini, D., S. J. Taylor & M. E. Slay. 2009. Cave Pygmarrhopalites Vargovitsh, 2009 (Collembola, Symphypleona, Arrhopalatidae) in United States. Zootaxa, 2204:1-8.
CTM at: drctmcallister@aol.com
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AUGUST, 2009
SELECTION OF AVAILABLE POST-FIRE SUBSTRATE BY THE GROUND SKINK, SCINCELLA LATERALIS (SQUAMATA: SCINCIDAE)
Charles M. Watson
Department of Biology, The University of Texas at Arlington Arlington, Texas 76019
Abstract -Burning of the forest floor alters the structural components that constitute the organic substrate. Many small animal species inhabit this layer, which typically consists of leaf litter from surrounding trees. The availability of a species’ preferred substrate can be a factor in the rate of recolonization following a fire. Using pair-wise choice trials within a controlled environment, preference of substrate typically available after a bum by Scincella lateralis was determined. These skinks primarily select hardwood leaf litter and secondarily choose pine needle litter and pine bark slough. Bare ground was usually avoided. These findings indicate that S. lateralis may not be able to completely recolonize a site until after the first seasonal leaf fall following a fire.
The effects of fire on populations of various reptiles have been well documented (Wilgers & Home 2006; Brown 2001; Granberry et al. 1994). Braithewaite (1987) found that varied fire regimes affect lizard populations differently, depending on such factors as fire intensity, duration, and seasonality. Kahn (1960) determined that the presence of unaltered refuge sites can buffer the effects of fire on certain lizard populations. For many temperate leaf-litter dwelling species, fire leaves behind limited and sparse refuge (Watson 2004), The present study determines the selectivity of the ground skink, Scincella lateralis, to four substrate components that are available at varying degrees after a fire in a mixed hardwood/pine forest. Scincella lateralis makes a sound experimental subject due to the species’ abundance, small size, and limited vagility. This animal is found in temperate wooded areas where there is sufficient water, cover, and food (Brooks 1967). However, the leaf-litter layer within the forest, or at forest’s edge, is considered typical habitat for this species (Fitch & von Achen 1977).
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The ground skink depends on leaf litter and other structural organic components of the forest floor for refuge (Brooks 1967). The complete destruction of decaying leaf material may dramatically affect recovery of this species within burned sites. Conversely, if the ground skink will utilize pine needle litter or pine bark slough, both of which are relatively abundant following a fire, it may be able to persist and recolonize burned sites more rapidly. This experiment aims to determine the selection of individual ground skinks to four prominent substrate types found after a bum in a mixed hardwood/pine forest ecosystem in eastern Texas.
Methods & Materials
Six experimental chambers were used, each measuring 32 cm by 77 cm at the base, providing 2464 cm^ of area. This area was uniformly covered by approximately 3 cm of sifted topsoil. Individual chambers contained two of the four treatments for habitat preference, each making up half of the surface area. Substrate treatments, with the exception of bare ground, were loosely arranged aggregates of the treatment substrate approxi¬ mately 5 cm thick. These six chambers cover all of the possible comparisons for these treatments. The four treatments are as follows:
Hardwood leaf litter broad leaves, predominantly from
Quercus sp. This substrate type is generally destroyed in a bum and will not be present until the following fall. The leaves that make up this layer are broad and can serve as cover for S. lateralis.
Pine leaf /zY/er. -Needles from Finns taeda. This substrate type will be present shortly after a bum and will continue to accumulate throughout the year. This is due to the fact that the needles of pine trees are persistent, and their leaf fall is not seasonnaly limited (Vines 1990). The needles that make up this layer are thin and can only serve as refuge in aggregate.
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Pine slough -T\{m pieces of scorched pine bark that accumulate at the base of the tree in the months following a bum. The bark pieces that make up this layer stmcturally resemble hardwood leaves, providing broad areas of cover and stmcture. However, these units are more dense than comparably sized leaves.
Bare ground large organic substrate present. This repre¬ sents the majority of a site’s substrate immediately following a bum.
A total of 10 animals of unknown sex (five adults, snout-to-vent length of 42-5 1mm; five juveniles, snout-to-vent length of 29- 34mm) were obtained from natural populations in Smith and Dallas counties, Texas. The organic substrates were collected from sites within Tyler State Park and heated to temperatures in excess of 65°C. The elevated temperatures ensured the elimination of prey items from the material. This was verified by observation of subsamples of this substrate under a stereomicroscope. No live invertebrates were noted.
Trials were performed under fluorescent lighting at 2TC. Individuals were each transferred to the center of the chamber, with a treatment to either side of six experimental chambers. The animal was then allowed a 10-min period of acclimation to the chamber. After this period, the investigator approached the chamber and marked which substrate type that the animal was in at time of initial detection. The skink typically was visible when the chamber was approached, and immediately retreated to cover. Each trial was repeated 20 times for each animal.
Data were analyzed as recommended by Cherry (1998). Confidence intervals were determined for the mean number of times that a specimen was observed in each substrate, given equal opportunity to choose between substrates. There were no significant differences noted between age groups for any of the treatments. Therefore, the values of both age classes were
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Figure 1. Mean (± 95% Cl) substrate choice values for Scincella lateralis given a maximum of 60 potential observations for each type. HLL = Hardwood Leaf Litter, PNL = Pine Needle Litter, PS = Pine Bark Slough, BG = Bare Ground.
combined into one sample to increase power. Significance was determined between substrates if no values were shared within the constructed 95% confidence intervals (Figure 1).
Results & Discussion
Bare ground exhibited the lowest mean frequency (x = 1.0, 95% Cl : [0.3, 1.7]), and a significant preference was exhibited for hardwood leaf litter over all three other treatments (x = 47.6 95% Cl : [43.2, 52.0]). Pine slough (x = 34.3, 95% Cl : [30.6, 38.0]) and pine needle litter (x = 37.5, 95% Cl : [33.8, 41.2]) exhibited overlap of the constructed confidence intervals, thereby exhibiting no significant selection between these treatments.
The top layer of substrate on the forest floor is typically comprised of dead and decaying organic material. Fire dramatically alters the makeup of this substrate layer, thereby altering the primary habitat of S. lateralis. Watson (2004) found, from data gathered in Smith County, Texas, that the presence of structural organic material is reduced by over 75% following a fire. Preference for those substrates that are most decimated by fire may prove to be a limiting factor in recolonization by this species.
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223
The preference of hardwood leaf litter for cover is consistent with literature regarding other skink species (Fitch 1954). However, the three other substrates are the most commonly available in the period immediately following a bum and preceding the annual leaf fall (Watson 2004). Potential costs to this animal as related to these substrates may be a factor into substrate selection. The probability of detection of the ground skink by avian predators is increased in the absence of refiigia (Smith 1997). Pine needle litter does not provide effective cover unless it is present in aggregate and the density of the pine slough may not allow for free movement of the lizard when it is arranged in a compact manner at the base of a tree. Further reasons for the substrate preferences may be dependant on the availability of prey. There is little doubt that the acquisition of prey and the ability to hide from predators play heavily in microhabitat selection.
The preferred microhabitat type for the ground skink is that which is in shortest supply following a fire. Other factors, such as prey availability and proximity to undisturbed habitat, may also affect the recovery of this species following a fire. Invertebrate communities, which constitute the prey of S. lateralis, are often initially eradicated with the burning of leaf litter, further tying the recovery of this species to the return of the leaf litter layer and associated fauna (Abbot et al. 2002; Bird 1997). Therefore, ground skinks may not be able to recolonize an area completely until hardwood leaf litter is present in pre-bum amounts, which may take over three years (Watson 2004). Furthermore, the community stmcture of the leaf litter layer may not reach the pre-bum state for many years afterwards, potentially limiting the fiill recovery of S. lateralis populations. The recovery of this species following a bum is nevertheless basically tied to substrate availability and its timeline for recovery may be delayed for months following the event, beginning with the first leaf fall and the associated accumulation of hardwood leaf litter.
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Acknowledgments
I would like to thank Daniel Formanowicz and Laura Gough for their input and encouragement over the duration of this project as well as Jessie Meik, Brian Fontenot, and Rebbekah Watson for their pre-submission editorial expertise.
Literature Cited
Abbot, I., T. Burbidge, K. Strehlow, A. Mellican, & A. Wills. 2002. Logging and burning impacts on cockroaches, crickets and grasshoppers, and spiders in Jarrah forest, Western Australia. For. Ecol. Manage., 174:383-399.
Bird, S. 1997. The effects of silvicultural practices on soil and leaf litter arthropods in an East Texas pine plantation. Unpublished Ph. D. dissertation. Texas A&M Univ., College Station, 193pp.
Braithwaite, R. W. 1987. Effects of fire regimes on lizards in the wet - dry tropics of Australia. J. Trop. Ecol., 3(3):265-275.
Brooks, G. R. 1967. Population ecology of the Ground Skink, Lygosoma laterale. Ecol. Monogr.,37(2):71-87.
Brown, G. W. 2001. The influences of habitat disturbance on reptiles in a Box-Ironbark eucalypt forest of southeastern Australia. Biodiversity and Conservation, 10(2): 161- 176.
Cherry, S. 1998. Statistical tests in publications of The Wildlife Society. Wildl. Soc. Bull., 26(4):947-953.
Fitch, H. S. 1954. Life History and Ecology of the Five-lined Skink, Eumeces fasciatus. Univ. Kansas Press, Lawrence, KS, 156pp
Fitch, H. S. & P. L. von Achen. 1977. Spatial relationships and seasonality in the skinks Eumeces fasciatus and Sciucella laterale in Northeastern Kansas. Herpetologica, 33(3):303-313.
Cranberry, C. H., D. G. Neary & L. D. Harris. 1994. Effects of high-intensity wildfire and silvicultural treatments on reptile communities in Sand-Pine Scrub. Conservat. Biol., 8(4):1047-1057.
Kahn, W. C. 1960. Observations on the effect of a bum on a population of Sceloporus occidentalis. Ecology, 41(2):358-359
Smith, D. G. 1997. Ecological factors influencing the antipredator behaviors of the ground skink, Scincella lateralis, Behav. Ecol., 8(6):622-629.
Vines, R. A. 1990. Trees, Shmbs, and Woody Vines of the Southeast. Univ. of Texas Press, Austin, TX, 1 1 04pp
Watson, C. M. 2004. The Effects of Controlled Burning on Ground Skink Populations in a Mixed Pine-Hardwood Habitat of East Texas. Unpublished M.S. Thesis., Univ. of Texas at Arlington. 47pp.
Wilgers, D. J. & E. A. Home. 2006. Effects of different bum regimes on Tallgrass Prairie herpetofaunal species diversity and community composition in the Flint Hills, Kansas. J. Herpetol., 40(l):73-84.
CMW at: cwatson@uta.edu
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GENERAL NOTES
REPRODUCTION IN SMITH’S GREEN-EYED GECKO, GEKKO SMITHII (SQUAMAT A: GEKKONIDAE)
Stephen R. Goldberg
Department of Biology, Whittier College, PO Box 634, Whittier, California 90608
Smith’s green-eyed gecko, Gekko smithii is known from Sarawak, Sabah, Kalimantan, and Brunei (Borneo) and southern Thailand, West Malaysia, Sumatra, Nias, Java and the Nicobar Archipelago of India (Das 2007). It is the largest Bornean gecko (Das 2007). There is information on egg laying of G. smithii in Manthey & Grossmann (1997), Rogner (1997) and Das (2007). The purpose of this note is to provide additional information on the reproductive cycle of G. smithii from a histological examination of museum specimens.
A sample of 43 G smithii consisting of 20 males (mean SVL = 162.3 mm ± 14.3 SD, range = 133-178 mm) and 23 females (mean SVL - 153.4 mm ± 1 1.9 SD, range = 134-175 mm) collected 1960- 1990, from Borneo, Indonesia and Malaysia was borrowed from the herpetology collection of the Field Museum of Natural History (FMNH), Chicago, Illinois, USA.
For histological examination, the left testis was removed from males and the left ovary was removed from females. Enlarged follicles (> 5 mm length) or oviductal eggs were counted {in situ). Tissues were embedded in paraffin and cut into sections of 5 pm. Slides were stained with Harris hematoxylin followed by eosin counterstain (Presnell & Schreibman 1997). Slides of testes were examined to determine the stage of the spermatogenic cycle. Slides of ovaries were examined for the presence of yolk deposition or corpora lutea. Histology slides were deposited in the Field Museum of Natural History (FMNH) herpetology collection. An unpaired t-
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test was used to compare G. smithii male and female mean SVLs using Instat (vers. 3.0b, Graphpad Software, San Diego, CA).
The following G. smithii were examined: Borneo, Sabah State, Tawau Division, Lahad Datu District, FMNH 246237; Sarawak State, Fourth Division, Miri District, FMNH 129494, 131521; Third Division, Kapit District, FMNH 145834, 145835, Fourth Division, Bintulu District, FMNH 148996-148998, 150731, 150733-150735, 150737-150739; Malaysia, Selangor State, Petaling District: FMNH 185107, 185111-185114, 185116, 185117, 185119-185126, 185133, 185135-185137, 185139, 185140-185142, 185144, 185145; Indonesia, North Sumatra, FMNH 209498- 209500, 209502.
Males of G. smithii were significantly larger than females (unpaired Mest, df = A\, t = 2.22, P = 0.032). The only stage observed in the testicular cycle was spermiogenesis in which the lumina of the seminiferous tubules were lined by sperm or clusters of metamorphosing spermatids. Spermiogenesis was noted in the following males (sample size in parentheses): January (2); February (1); March (7); April (7); May (1); September (1); November (1). The smallest reproductively active (spermiogenic) male measured 133 mm SVL (FMNH 185137).
Four stages were noted in the ovarian cycle of G smithii (Table 1): (1) quiescent (no yolk deposition); (2) early yolk deposition, basophilic yolk granules are present; (3) enlarged yolk-filled ovarian follicles, > 5 mm diameter; and (4) oviductal eggs with eggs in oviducts. The smallest reproductively active female measured 141 mm SVL (FMNH 150733) contained two oviductal eggs and was collected in November. Mean clutch size for 11 females was 2.0. A clutch size of two is typical for many gekkonids (Vitt 1986) and was reported for G. smithii by Das (2007).
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Table 1. Monthly stages in the ovarian cycle of G. smithii.
|
Month |
n |
Quiescent |
Early yolk deposition |
Enlarged follicles > 5 mm |
Oviductal eggs |
|
February |
2 |
1 |
0 |
0 |
1 |
|
March |
7 |
0 |
1 |
3 |
3 |
|
April |
1 |
0 |
0 |
0 |
1 |
|
June |
1 |
0 |
0 |
0 |
1 |
|
July |
4 |
2 |
1 |
0 |
1 |
|
October |
2 |
0 |
2 |
0 |
0 |
|
November |
5 |
2 |
2 |
0 |
1 |
|
December |
1 |
0 |
1 |
0 |
0 |
The presence of reproductively active females and males in all months sampled suggests G. smithii exhibits year-round reproductive activity. These samples are too small to ascertain peaks in reproduction, if any exist. Rogner (1997) reported that a captive G. smithii laid two clutches one week apart. Multiple annual clutches of two eggs were reported by Manthey & Grossmann (1997). McKeown (1996) reported the congener Gekko gecko may lay a pair of eggs each month in Hawaii. No histological evidence was found that multiple clutches were produced as indicated by, for example, corpora lutea from a previous clutch and concomitant yolk deposition for a subsequent clutch. However, these data shows an extended period of reproductive activity in natural populations, and along with reports from Rogner (1997) and Manthey & Grossmann (1997), it is expected that G. smithii produce several clutches of eggs each year.
Inger & Greenberg (1966) reported similar results in their examination of the reproductive cycles of the gekkonids Cyrtodactylus malayanus and C. pubisulcus from a Bornean rain forest. In both species, males produced sperm throughout the year, gravid females were present in most months, and no distinct breeding season was evident. Similar results were also reported for the geckos Hemidactylus platyurus {= Cosymbotus platyurus),
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THE TEXAS JOURNAL OF SCIENCE-VOL. 61, NO. 3, 2009
Hemidactylus frenatus and Gehyra mutilata (= Peropus mutilatus) from West Java, Indonesia by Church (1962) and Dixonius siamensis from Thailand (Goldberg 2008). The above studies suggest extended periods of reproduction may be typical for gekkonid lizards from tropical southeast Asia. However, in view of the great diversity of gekkonid species from southeast Asia (Uetz & Hallermann 2009) subsequent investigations of the reproductive cycle of many additional species will be needed to test this hypothesis.
Acknowledgments
I thank Alan Resetar (Field museum of Natural History), Chicago, Illinois for permission to examine G. smithii.
Literature Cited
Church, G. 1962. The reproductive cycles of the Javanese house geckos, Cosymbotus platyurns, Hemidactylus frenatus, md Peropus mutilatus. Copeia, 1962:262-269. Das, 1. 2007. Amphibians and Reptiles of Brunei. Natural History Publications
(Borneo) Kota Kinabalu Sabah, Malaysia. 200 pp.
Goldberg, S. R. 2008. Reproduction in the Siamese leaf-toed gecko, Dixonius siamensis (Squamata: Gekkonidae) from Thailand. Texas J. Sci., 60(3):233-238.
Inger, R. F. & B. Greenberg. 1966. Annual reproductive patterns of lizards from a Bornean rain forest. Ecology, 47 : 1 007-1 02 1 .
Manthey, U. & W. Grossmann. 1997. Amphibien & Reptilien Siidostasiens. Natur und Tier Verlag, Munster, Germany, 512 pp.
McKeown, S. 1996. A Field Guide to Reptiles and Amphibians in the Hawaiian Islands.
Diamond Head Publishing, Inc., Los Osos, California, 172 pp.
Presnell, J. K. & M, P. Schreibman. 1997. Humason’s Animal Tissue Techniques. 5*^ Edit. The Johns Hopkins Press, Baltimore, 572 pp.
Rogner, M. 1997. Lizards, Vol. 1, Krieger Publishing Company, Malabar, Florida, 317
pp.
Uetz, P,, & J. Hallermann. 2009. TIGR Reptile Database: http:/www.reptile- database.org. (accessed 7 December 2009).
Vitt, L. J. 1986. Reproductive tactics of sympatric gekkonid lizards with a comment on the evolutionary and ecological consequences of invariant clutch size. Copeia, 1986:773-786.
SRG at: sgoldberg@whittier.edu
TEXAS J. SCL 61(3), AUGUST, 2009
229
THE LONG-TAILED WEASEL MUSTELA FRENATA (MAMMALIA: MUSTELIDAE) m BAJA CALIFORNIA, MEXICO
Gorgonio Ruiz-Campos, Roberto Martmez-GaDardo,
Salvador Gonzalez-GuzmaE and Jorge Alaniz-Garcia
Facultad de Ciencias, Universidad Autonoma de Baja California,
Apdo. Postal 233, Ensenada, Baja California, 22800, Mexico
The long-tailed weasel Mustela frenata Lichtenstein 1831 has the largest range of any mustelid in the Western Hemisphere, with a known distribution extending from southern Canada throughout the United States, Mexico, and Central America, and into northern South America, Mustela frenata occurs in a variety of habitats from alpine-artic to tropical, but does not inhabit arid biotopes or deserts. Its favored habitats include brush land and open timber, brushy borders of croplands, grasslands along creeks and lakes, and swamps (Svendsen 2003),
The long-tailed weasel is considered a generalist predator that consumes a wide variety of small vertebrates. Rodents and immature rabbits are preferred prey, however shrews, moles, bats, birds, bird eggs, snakes, invertebrates, and carrion may be consumed as alternative prey (Sheffield 1999).
The density of the long-tailed weasel throughout its range is generally low, and its presence varies from uncommon to rare. Owing to low densities and periodic fluctuations of its populations in North America, this species is listed as endangered, threatened, rare, or of special concern in many states and provinces (Sheffield 1999), This species is not listed in any special category of conservation in Mexico,
Of the ten subspecies of M frenata known to occur in Mexico (Hall 1981), M frenata latirostra inhabits a small portion of northwestern Baja California (Huey 1964). The first published record of this subspecies in Baja California is referable to Federal
230
THE TEXAS JOURNAL OF SCIENCE-VOL. 61, NO. 3, 2009
Highway No. 1 near Rosarito (10 mi S Tijuana) (Huey 1964). The second record as reported by Ralston & Clark (1971) at this same highway near La Mision (32° 3’ N, 116° 54’ W) on 7 Apr 1968. Additionally, there is one previously unreported voucher specimen in the Museum of Vertebrate Zoology, University of Califomia- Berkeley (MVZ- 148254), which was collected by W. E. Glanz 2 mi WSW Maneadero (31° 42’ 0.0” N, 116° 35’ 24.0” W) on 13 Dec 1974.
Five recent records of M frenata latirostra are documented in this paper for several localities within northwestern Baja California (Fig. 1). Voucher specimens obtained during the study were deposited in the Mammal Collection of the Universidad Autonoma de Baja California (UABC) at Ensenada. The details of these records are as follows: A male (UABC-093) was found dead in a cultivated field at Valle de Maneadero, 14 km S Ensenada (3U 44' 37" N, 116° 35' 54" W), on 12 Aug 2000. Standard measurements of this specimen were 405 mm, total length [TL]; 107 mm, tail length [CL]; 44 mm, hind foot length [HFL]; weight [W], 288 g). A female (U ABC-092) was collected in the Valle de Guadalupe, 36 km NE Ensenada, on 24 May 2005 (32° 03’ 30” N, 116° 35’ 09” W). Standard measurements of UABC-092 were 360 mm TL, 150 mm CL, 36 mm HFL, 149 g W (Fig. 2). A second male (UABC- 107) was captured in the L.A. Cetto vineyard at Valle de Guadalupe on 15 Jul 2003 (32° 07’30” N, 116° 28’ 40” W). The standard measurements of the second male were 345 mm TL, 140 mm CL, 36 mm HFL, 100 g W. The first two specimens (UABC-092 and 093) were preserved as skin and skull vouchers, whereas the third specimen was preserved in ethanol. Selected cranial measurements in millimeters of UABC-092 and UABC-093 were respectively as follows: zygomatic breadth 21.9 and 28.3, braincase height 14 and 17, upper jaw length 17 and 18, lower jaw length 24.7 and 30.4, and least interorbital breadth 6.4 and 9.4.
TEXAS I SCI. 61(3), AUGUST, 2009
231
Fig. 1. Historical and recent records of Mustela frenata latirostra in Baja California, Mexico. VR = visual record, and SR = specimen record.
Figure 2. Female Mustela frenata latirostra (UABC-092) collected at Valle de Guadalupe, 36 km NE Ensenada, Baja California, on 24 May 2005. Photograph by Gorgonio Ruiz-Campos.
A fourth record corresponds to a head in taxidermy belonging to Ramon Femat. Mr. Femat obtained the weasel in 1997 while hunting near the mouth of the Rio Santo Domingo at W Vicente
232
THE TEXAS JOURNAL OF SCIENCE-VOL. 61, NO. 3, 2009
Guerrero (30° 43' N, 116° 02' W). Finally, a fifth record is based upon a sight record from San Telmo de Arriba, in the vicinity of the Sierra San Pedro Martir, on 25 May 2002 (30° 58’ 09” N, 116° 05’ 33” W) (Ruben Bustamante, pers. comm.). Based upon these specimens, the current distribution of M frenata latirostra in northwestern Baja California may be extended southward to the coastal valley of the Rio Santo Domingo. Future intensive sampling may confirm the presence of this subspecies as far as 30° N latitude at the boundary the Californian faunal province (Bancroft, 1926).
Acknowledgements
We thank Areli Castillo, Francisco J. Valverde and Hector Yee for helping us with field sampling and preparation of specimens. Also, we grateftilly acknowledge Ruben Bustamante and Ramon Femat for providing the records for San Telmo de Arriba and Lower Rio Santo Domingo, respectively. Likewise we thank two anonymous reviewers for their useful comments that improved the content and clarity of the manuscript.
Literature Cited
Bancroft, G. 1926. The faunal areas of Baja California del Norte. Condor, 28(5): 209-215.
Hall, R. E. 1981. The mammals of North America. John Wiley & sons. New York,
1181 pp.
Huey, L. M. 1964. Mammals of Baja California, Mexico. Transactions of the San Diego Society of Natural History, 13(7):85-168.
Ralston, G. L. & W. H. Clark. 1971. Occurrence of Mustela frenata in northern Baja California, Mexico. The Southwestern Naturalist, 16(2):209.
Sheffield, S. R. 1999. Long-Tail weasel {Mustela frenata). Pp. 169-171 in (D.E. Wilson & S. Ruff, eds.). The Smithsonian Book of North American Mammals. Smithsonian Institution Press. Washington, 750 pp.
Svendsen, G. E. 2003. Weasel and Black-footed Ferret {Mustela species). Pp. 650- 661 in (G.A. Feldhamer, B.C. Thompson & J.A. Chapman, eds.), Wild Mammals of North America. The Johns Hopkins University Press, Baltimore, 1216 pp.
G. R-C at: gruiz@uabc.mx
TEXAS J. SCI. 61(3), AUGUST, 2009
233
STOMACH CONTENTS OF CALIDRIS MINUTILLA (CHARADRIIFORMES: SCOLOPACIDAE) WINTERING AT A FRESHWATER RESERVOIR IN WEST-CENTRAL TEXAS
Andrew C. Kasner, Randall H. Ruddick, and Terry C. Maxwell
Department of Biology, Wayland Baptist University,
1900 West 7th Street, Plainview, Texas 79072,
Department of Biology, Lamar University, P.O. Box 10037 Beaumont, Texas 77710 and Department of Biology, Angelo State University San Angelo, Texas 76909
Sandpipers (Charadriiformes: Scolopacidae) feed primarily on invertebrates (Skagen & Oman 1996). Shorebird diets consist primarily of polychaete and oligochaete worms (Schneider 1987; Davis 1996; Tsipoura & Burger 1999), amphipods (Wilson & Parker 1996; Shepherd & Boates 1999), horseshoe crab (Limulus polyphemus) eggs (Tsipoura & Burger 1999), and insects, especially dipterans (Schneider 1987; Alexander et al. 1996; Davis 1996). Few dietary studies have focused on sandpipers at inland sites (Alexander et al. 1996; Davis 1996), and all of these focused on migrating populations. Studies are needed to determine the dietary preferences of sandpipers wintering at inland sites in order to better understand why some individuals remain at more northern latitudes over winter, when populations of invertebrate prey are likely at their lowest levels of the year. It is of particular importance to determine whether shorebirds at inland sites are able to locate high quality food resources (easily captured and digested; predictable in occurrence) or must subsist on low quality food items (difficult to capture or digest; unpredictable occurrence). Furthermore, habitat heterogeneity is typically lower at inland, freshwater reservoirs (such as in this study) compared to coastal areas, and it is likely that prey diversity and potentially abundance is similarly poor relative to coastal regions.
The purpose of this research was to determine the diet of wintering sandpipers at an inland freshwater reservoir. Least Sandpipers (Calidris minutilla) and Western Sandpipers {Calidris
234
THE TEXAS JOURNAL OF SCIENCE-VOL. 61, NO. 3, 2009
mauri) migrating along the Central Flyway (Smith et al. 1991; Neill 1992; Davis 1996; DeLeon 1996) winter in small numbers (<100 individuals per flock with only one or two flocks observed on any given day) in west-central Texas (Tarter 1997; Kasner 1999). This paper reports analysis of stomach contents from wintering sandpipers collected at Twin Buttes Reservoir, Tom Green County, in west-central Texas.
A total of 14 birds representing two species of Calidris, Least Sandpiper (C. minutilla, j7=13) and Western Sandpiper (C mauri, n=\), were collected. On 17 January 1998 and 28 February 1998, six Least Sandpipers and one Western Sandpiper were collected from an algal mudflat on the west shore of the south pool of Twin Buttes Reservoir, near the mouth of the South Concho River, Tom Green County, Texas. Birds were observed foraging on the mudflat, wading in water approximately one to five centimeters deep. On 19 January 2002, seven Least Sandpipers were collected on the north shore of the south pool of Twin Buttes Reservoir. Birds at this site were foraging in a flooded area of Bermudagrass (Cynodon dactyl on) over a mud and gravel substrate. Avian specimens were deposited in Angelo State Natural History Collections, Department of Biology, Angelo State University, San Angelo, Texas.
Bird stomachs were injected with ten percent formalin through the mouth and esophagus with a hypodermic syringe immediately after collection. Esophagus and stomach were removed from each specimen in the lab later the same day. Stomach, esophagus, and contents were stored in 10% formalin for analysis. Each stomach and esophagus was dissected, contents were identified to the lowest taxonomic rank possible (family or genus), and heads and other parts were counted using a Bausch and Lomb 2X compound dissecting microscope. Percent composition (proportion of total stomach contents) of prey was visually determined for specimens collected in 1998. For each specimen collected in 2002, stomach and esophagus was dissected and flushed with formalin onto filter
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paper in a Buchner funnel. Additional formalin was used to disperse aggregations of contents on the filter-fiinnel, recording the volume of formalin used for flushing/dispersing. After being allowed to air dry for 24 hrs, contents were identified using Merritt & Cummings (1984) and grouped. Each subset of the contents was massed (mg) using a Mettler balance and percent mass was calculated for each type of item. To control for mass of formalin contributing to stomach content mass measurements, a control trial was conducted using filters and formalin. The two filters were massed and then treated with 20 mL and 40 mL of formalin, respectively (representing the minimum and maximum volumes of formalin used for flushing/dispersing contents), allowed to air dry for 24 hrs, and massed to determine the mass of residual formalin in the filter (mg/mL). Mass contribution of formalin averaged 1.5 mg/mL of formalin used for flushing. Data were adjusted for the contribution of formalin to mass measurements.
Stomach contents of all seven specimens in 1998 consisted almost exclusively (>95%) of chironomid (Diptera: Chironomidae) larvae, with all stomachs completely full. Mean number of chironomid heads was 176.4 heads/stomach, with approximately 15% of chironomids in each stomach completely intact (Table 1). The remaining contents consisted of unidentified insect parts, one adult mesoveliid (Hemiptera: Mesoveliidae), and two seeds (Table 1). Additionally, all stomachs contained small amounts of minerals (calcite or quartz), small pebbles, and strands of filamentous green algae. Unidentified insect parts were suspected to be primarily Coleopteran (many wing fragments and robust, dark colored leg fragments and jaw fragments), however, this is speculative because fragments were too incomplete for identification.
All but one of the seven stomachs from 2002 contained identifiable fragments (heads, jaws, and/or legs) of Coleoptera (Table 2), Families represented included Curculionidae {Emphyastes, Stenopelmus, Tanysphyrus), Dytiscidae (Rhantus), Hydrophilidae (Berosus), and Elmidae. Hemiptera was also present
236
THE TEXAS JOURNAL OF SCIENCE-VOL. 61, NO. 3, 2009
Table 1. Stomach contents of Calidris minutilla {n=6) collected 17 January and 28 February 1998 at Twin Buttes Reservoir, Tom Green County, Texas.
|
specimen Number |
No. Chironomid heads |
Other prey items |
|
1003-TCM3776 |
138 |
1 mesoveliid, misc. |
|
1003-TCM3777 |
201 |
miscellaneous |
|
1003-TCM3778 |
221 |
miscellaneous |
|
1012-TCM3782 |
153 |
2 seeds, misc. |
|
1012-TCM3783 |
174 |
miscellaneous |
|
1012-TCM3784 |
205 |
miscellaneous |
in one specimen, but only two heads were found, therefore mass was not measurable and not included in Table 2. Minerals (calcite and quartz) and pebbles contributed a large proportion of overall mass in each specimen from 2002, indicative of a hard diet, such as Coleoptera, that would require more mechanical digestion. In specimens from 1998, the diet was primarily softer Chironimids, and much less mineral content was observed. Alternatively, inefficient foraging on beetles in the flooded Bermuda-grass habitat could have led to accidental intake of minerals and pebbles. One specimen in 2002 also contained small seeds (Table 2). The remaining unidentified contents were insect fragments lacking sufficient detail for identification and strands of filamentous green algae.
These findings are consistent with other studies in the types of prey found and proportion of prey types. Chironomids were previously found to be an important component of the diet of calidrine sandpipers (Schneider 1987; Alexander et al. 1996; Davis 1996; Skagen & Oman 1996), however, the highest reported average percentage was 80.1% (Davis 1996). This study found the percentage of chironomid larvae to be greater than 95% for all specimens in 1998, but the small sample size and limited number of collection dates precludes any inference that this is significantly greater than other studies, and chironomids were noticeably absent in 2002 specimens. The frequent occurrence of Chironomidae in 1998 specimens and Coleoptera in 2002 specimens suggests that these groups may be important prey in winter, however, Coleop-
TEXAS J. SCL 61(3), AUGUST, 2009
237
Table 2. Stomach contents of Calidris minutilla collected 19 January 2002 (percent by mass [mg]).
|
specimen No. |
Coieoptera (% mass) |
Minerals (% mass) |
Seeds (% mass) |
Unidentified (% mass) |
|
20021 |
0.0 |
32.9 |
0.0 |
67.1 |
|
20022 |
5.0 |
40.7 |
0.0 |
54.4 |
|
20023 |
4.3 |
12.0 |
0.4 |
83.2 |
|
20024 |
13 |
36.6 |
0.0 |
62.2 |
|
20025 |
5.5 |
39,2 |
0.0 |
55.3 |
|
20026 |
3.0 |
28.4 |
0.0 |
68.6 |
|
20027 |
1.8 |
37.8 |
0.0 |
60.4 |
|
Mean |
3.0 |
32.5 |
0.06 |
64.5 |
terans were much less abundant in 2002 specimens than Chironomids were in 1998 specimens, Coleopteran prey are harder and less energetically rewarding due to increased need for mechanical digestion using minerals and extended time required for digestion compared to soft-bodied chironomid larvae. Minerals also take up space that could otherwise be used for additional prey contents. Indeed, a high percentage of minerals were found in stomachs from 2002, either due to accidental intake or potentially to aid maceration of hard-bodied beetles. Alternatively, habitat differences where birds were foraging in 1998 compared to 2002 could account for the differences observed in stomach contents.
Results suggest that sandpipers wintering at reservoirs in the region are generalists in diet, with prey capture dependent on ephemeral populations of aquatic invertebrates and terrestrial invertebrates existing on or near the shoreline. It is likely that hydrologic features play some role in aquatic insect populations at such sites. For example, in 1998 when specimens contained chironomids, foraging occurred on mudflats under conditions of slowly receding reservoir levels with no recent runoff events. However, in 2002, when specimens contained primarily coleopterans, recent runoff events had caused reservoir levels to rise, flooding shorelines and providing a source of invertebrates that would more commonly be found in streams or terrestrial habitats
238
THE TEXAS JOURNAL OF SCIENCE-VOL. 61, NO. 3, 2009
than on reservoir shorelines (e.g., Elmidae and Curculionidae). Rising water levels flooding flats covered with Bermudagrass and winter temperatures in clear, clean water would allow the occurrence of a unique aquatic insect community compared to drought periods with turbid, receding water levels.
Colwell & Landrum (1993) found nonrandom distributions of sandpipers in relation to fine-scale variations in prey abundance. Sandpipers at this study site appear to use available habitats equally (Kasner 1999), and may choose prey opportunistically as they are encountered in ephemeral aggregations. Hockey et al. (1992) suggest that nonbreeding wader populations are proportionate to the carrying capacity of coastal wetlands along a latitudinal gradient. If this is also applicable to freshwater, inland sites, the results of this study suggest that chironomid and coleopteran populations may be a limiting factor for sandpipers wintering in west-central Texas. Local abundances of sandpipers in winter are low relative to the extent of habitat that is generally available, suggesting ecological factors other than habitat may be limiting. Further investigation of prey populations is necessary to answer these questions. Future research should consider the spatio-temporal dynamics of invertebrate abundance during the winter months at the site.
Acknowledgments
We would like to thank Dr. Richard Harrel and Dr. Ned Strenth for assistance and verification of insect identification. We thank Dr. Kim Withers for helpful suggestions to improve this manuscript. Collections made under permits held by T. Maxwell (USFWS Permit MB674149-1, Texas Scientific Collecting Permit SPR-0290-021).
Literature Cited
Alexander, S. A., K. A. Hobson, C. L. Gratto-Trevor & A. W. Diamond. 1996. Conventional and isotopic determinations of shorebird diets at an inland stopover: the importance of invertebrates and Potamogeton pectinatus tubers. Can. J. Zool., 74(6):1057-1068.
TEXAS J. SCI. 61(3), AUGUST, 2009
239
Colwell, M. A. & S. L. Landrum. 1993. Nonrandom shorebird distribution and fine- scale variation in prey abundance. Condor, 95:94-103.
Davis, C. A. 1996. Ecology of Spring and Fall Migrant Shorebirds in the Playa Lakes Region of Texas. Unpublished Ph.D. dissertation, Texas Tech Univ., Lubbock, Texas, 204pp.
DeLeon, M. T. 1996. Use of habitat and behavior of migrant shorebirds in North Dakota. Unpublished M.S. thesis, Texas Tech Univ., Lubbock, Texas, 97pp..
Hockey, P. A. R., R. A. Navarro, B. Kalejta & C. R. Velasquez. 1992. The riddle of the sands: Why are shorebird densities so high in southern estuaries? Am. Nat., 140(6):961-979.
Kasner, A. C. 1999. Effects of abiotic factors on inland wintering Least Sandpipers (Calidris minutilla). Unpublished M.S. thesis, Angelo State Univ., San Angelo, Texas, 48pp.
Merritt, R. W. & K. W. Cummings. 1984. An Introduction to the Aquatic Insects of North America, 2"^* ed. Kendall/Hunt Publishing Co., Dubuque, Iowa, 722pp..
Neill, R. L. 1992. Recent trends in shorebird migration for North-central Texas. Southw. Nat., 37(l):87-88.
Schneider, C. J. 1987. Comparative Ecology of Two Guilds of Shorebirds on the South Texas Coast. Unpublished M.S. thesis, Univ. Texas, Austin, Texas, 45pp.
Shepherd, P. C. F. & J. S. Boates. 1999. Effects of a commercial baitworm harvest on Semipalmated Sandpipers and their prey in the Bay of Fundy Hemispheric Shorebird Reserve. Con. Biol., 13(2):347-356.
Skagen, S. K. & H. D. Oman. 1996. Dietary flexibility of shorebirds in the western hemisphere. Can. Field-Nat., 1 10(3):419-444.
Smith, K. G., J. C. Neal & M. A. Mlodinow. 1991. Shorebird migration at artificial fish ponds in the prairie-forest ecotone of Northwestern Arkansas. Southw. Nat., 36(1):107-113.
Tartar, D. G. 1997. A field checklist birds of the Concho Valley Region, Texas, 3"^^^ revision.
Tsipoura, N. & J. Burger. 1999. Shorebird diet during spring migration stopover on Delaware Bay. Condor, 101:635-644.
Wilson, W. H. Jr. & K. Parker. 1996. The life history of the amphipod, Corophium volutator: The effects of temperature and shorebird predation. J. Exp. Mar. Biol.,Ecol. 196:239-250.
ACK at: kasnera(gwbu.edu
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Goldberg, Stephen R. Killebrew, Don W. Marsh, David S. Strenth, Ned E.
SUSTAINING MEMBERS
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Lee, Thomas E. Jr. Valdes, Arcadio
SUPPORTING MEMBERS
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THE TEXAS ACADEMY OF SCIENCE, 2009-2010
OFFICERS
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2007 Renard L. Thomas, Texas Southern University Bob Murphy, Texas Parks and Wildlife Department
2008 Christopher M. Ritzi, Sul Ross State University Andrew C. Kasner, Audubon Texas
2009 Ana B. Christensen, Lamar University Thomas L. Arsuffi, Texas Tech at Junction
SECTIONAL CHAIRPERSONS
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Mathematics: Elsie M. Campbell, Angelo State University
Physics: David L. Bixler, Angelo State University
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Volume 61 Number 4 November 2009
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THE TEXAS JOURNAL OF SCIENCE
Volume 6 1 , No. 4 November, 2009
CONTENTS
Gas Exchange Rates of Sun and Shade Leaves of Sophora secundlflora
(Leguminosae, Texas Mountain Laurel).
By Mitsuru Furuya and O. W. Van Auken 243
Characterization of Arsenic-Tolerant Bacterial Cultures from the Lower Laguna Madre of South Texas.
By Gemma A. Berlanga, Michael W Persans, Thomas M. Eubanks
and Kristine L. Lowe 259
Diversity and Abundance of Unionid Mussels in Three Sanctuaries on the Sabine River in Northeast Texas.
By Neil B. Ford, Jessica Gullett and Marsha E. May 279
Morning and Evening Densities of White-Winged and Mourning Doves in the Lower Rio Grande Valley, Texas.
By Michael F. Small, Margaret L. Collins, John T. Baccus
and Steven J. Benn 295
General Notes
Prevalence of Hematozoan Parasites (Apicomplexa) in some common Passerine Birds (Passeriformes) from East-Central Oklahoma.
By Michael D. Bay and Kenneth D. Andrews 3 1 1
Notes on Reproduction of the Knob-Scaled Lizard, Xenosaurus grandis (Squamata: Xenosauridae), from Veracruz, Mexico.
By Stephen R. Goldberg 3 1 7
Population Dynamics of an Established Reproducing Population of the Invasive Apple Snail {Pomacea insularum) in Suburban Southeast Houston, Texas.
By Colin H. Kyle, Matthew K Trawick, James P. McDonough
and Romi L. Burks 323
Recognition of Special Members 328
Index to Volume 61 (Subject, Authors & Reviewers) 329
Postal Notice
335
THE TEXAS JOURNAL OF SCIENCE EDITORIAL STAFF
Managing Editor:
Ned E. Strenth, Angelo State University Manuscript Editor:
Frederick B. Stangl, Jr,, Midwestern State University Associate Editors:
Allan D. Nelson, Tarleton State University Jim R. Goetze, Laredo Community College Associate Editor for Botany:
Janis K. Bush, The University of Texas at San Antonio Associate Editor for Chemistry:
John R. Villarreal, The University of Texas-Pan American Associate Editor for Computer Science:
Nelson Passos, Midwestern State University Associate Editor for Geology:
Ernest L. Lundelius, University of Texas at Austin Associate Editor for Mathematics and Statistics:
E. Donice McCune, Stephen F. Austin State University
Manuscripts intended for publication in the Journal should be submitted in TRIPLICATE to:
Dr. Allan D. Nelson Department of Biological Sciences Tarleton State University Box T-OlOO
Stephenville, Texas 76402 nelson@tarleton.edu
Scholarly papers reporting original research results in any field of science, technology or science education will be considered for publication in The Texas Journal of Science. Instructions to authors are published one or more times each year in the Journal on a space-available basis, and also are available on the Academy's homepage at:
www.texasacademyofscience.org
AFFILIATED ORGANIZATIONS American Association for the Advancement of Science,
Texas Council of Elementary Science Texas Section, American Association of Physics Teachers Texas Section, Mathematical Association of America Texas Section, National Association of Geology Teachers Texas Society of Mammalogists
TEXAS J. OF SCI. 61(4):243-258
NOVEMBER, 2009
GAS EXCHANGE RATES OF
SUN AND SHADE LEAVES OF SOPHORA SECUNDIFLORA (LEGUMINOSAE, TEXAS MOUNTAIN LAUREL)
Mitsuru Furuya* and O. W. Van Auken
Department of Biology, University of Texas at San Antonio San Antonio, Texas 78249 "^Current address:
7-1 1-20 Nakagawa, Tsuzuki-ku Yokohama-shi Kanagawa-ken, 224-0001 Japan
Abstract.-Gas exchange rates of sun and shade leaves of Sophora secundiflora (Leguminosae, Texas Mountain Laurel) were measured. Maximum photosynthetic rates (^max), light saturation points, dark respiration rates (Rd), stomatal conductance rates and ambient light levels for sun leaves were significantly different than shade leaves. There were no significant differences between sun and shade leaves for the light compensation point, transpiration rates, leaf water potential, leaf mass or leaf area. Mean A^ax rates were 12.94 ± 0.58 (± one SE) pmolC02/mVs for sun leaves and 7.49 ± 1.35 pmolC02/ m^/s for shade leaves. Mean Rd rates were 3.48 ± 0.44 pmolC02/m^/s for sun leaves and 2.28 ± 0.21 pmolC02/m ^/s for shade leaves. Mean g^ rates were 0.24 ± 0.02 molH20/m Vs for sun leaves and 0.12 ± 0.02 molH20/m Vs for shade leaves. A^ax rates for sun leaves were within levels expected for sun plants, but A^ax rates for shade leaves were fairly high as well. Sophora secundiflora sun and shade leaves also had high Rd rates which suggest that this is not a sun or shade species. The ranges of many of the other measurements overlapped and were not significantly different suggesting this species is an intermediate or facultative species. This would explain why it is present in full sun and shaded or partially shaded habitats in central Texas and other areas where it is found.
Communities are composed of a variety of species that occur together spatially and temporally (Begon et al. 2006). Measuring the density and basal area of plants found in these terrestrial communities is relatively easy to do (Van Auken et al. 2005). In addition, taking population data from these plant communities, ranking the species from highest to lowest, and showing which ones have the greatest basal area or density is relatively routine. Species in a community are found together because they require or are tolerant of the conditions present in specific areas or habitats. However, sorting out the characteristics or factors that determine why a species is dominant is much more challenging. It is also very difficult to ascertain why similar species fit together or exist in communities. Some species are restricted to open habitats, some to woodlands or forests, and others seem to occur at the edge or in-between communities (Begon et al.
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THE TEXAS JOURNAL OF SCIENCE-VOL. 61, NO. 4, 2009
2006). Factors that cause these limitations might be biotic or abiotic, but are not always easy to delineate. Light levels, soil depth, soil moisture, nutrient levels, competition between species, biotic characteristics, or combinations of these factors are all possibilities (Valladares & Niinemets 2008).
In the central Texas Edwards Plateau region, savannas are associated with Juniperus-Quercus woodlands or forests in many areas (Van Auken et al. 1981; Van Auken & McKinley 2008; Van Auken & Smeins 2008). A species found in many of these communities is Sophora secundiflora (Ort.) DC. (Leguminosae, Texas Mountain Laurel) (Van Auken et al. 1981). It has not been reported as a dominant species, but a secondary species with lower density and basal area (Van Auken et al. 1981). However, it forms almost mono- specific communities in some open habitats especially on drier and shallow soils including ridges and some south facing slopes. In addition, isolated plants are found below the canopy in some communities. As a Legume, it could establish in disturbances or low nutrient soils, but no studies were found concerning its establishment or successional status.
Physiological differences between plants native to shady habitats compared to those found in full sun are fairly well known (Begon et al. 2006; Valladares & Niinemets 2008). There are major differences in most photosynthetic characteristics. Shade plants usually have lower photosynthetic rates at high light levels, light saturate at lower light levels (light saturation), have lower light compensation points (photosynthetic rate equals respiration rate) and lower dark respiration rates (Boardman 1977; Larcher 2003; Valladares & Niinemets 2008). Sun plants characteristically have higher transpiration and stomatal conductance rates (Young & Smith 1980). Some species display adaptive crossover and are capable of acclimating to high or low light environments, thus they could have a broader ecological niche (Givnish 1988; Givnish et al. 2004). In addition, shade leaves from plants grown in full sun have been used as surrogates for plants grown in shade conditions to understand a species’ ecological requirements (Hamerlynck & Knapp 1994).
FURUYA & VAN AUKEN
245
Gas exchange rates of sun and shade leaves of Sophora secundiflora were measured. Based on most information about this species, it was hypothesized that S. secundiflora is a sun plant and would have a high maximum photosynthetic rate, light saturation point, light compensation point, respiration, conductance, and transpiration compared to shade adapted plants.
Methods
Study species. -Sophora secundiflora (Texas Mountain Laurel, Leguminosae) is a shrub or small tree. It is a North American species native to Texas, New Mexico, and northeastern Mexico (Correll & Johnston 1979). Sophora secundiflora grows 5 to 8 m tall with a maximum canopy diameter of about 3 m. It has 5 to 13 cm long, pendulous clusters of purple or blue, fragrant flowers in spring. Leaves are usually dark-green, glossy, evergreen, alternate, and pinnately compound. Sophora secundiflora is reported to grow in full sun or partial shade on well-drained soil (Enquist 1987). It seems to tolerate hot, windy conditions, alkaline or wet, but not compacted soil. Plants may have a deep root system although characteristics of the rooting system are unreported.
Study area -This field study was carried out on the southern edge of the Edwards Plateau region of central Texas just south of the Balcones Escarpment (Correll & Johnston 1979; Van Auken et al. 1981; Van Auken & McKinley 2008). The Balcones Escarpment consists of a rough, well-drained area, with elevations increasing from approximately 213 m above mean sea level (AMSL) at the southern edge to between approximately 500 and 700 m AMSL near the center, but in most places the increase in elevation is abrupt. Most of the subsurface of the area is Cretaceous limestone, and soils are usually shallow, rocky or gravelly on slopes, and deep in broad valleys and flats (Taylor et al. 1962; NRCS 2006). Soils are dark colored and calcareous with usually neutral or slightly basic pH.
Mean annual temperature of the area is 20.0°C with monthly means ranging from 9.6°C in January to 29.4°C in July (NOAA 2004). Mean annual precipitation is 78.7 cm and bimodal, with peaks
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THE TEXAS JOURNAL OF SCIENCE-VOL. 61, NO. 4, 2009
occurring in May and September (10 J cm and 8.7 cm, respectively), with little summer rainfall and high evaporation (Thomthwaite 1931; NOAA 2004).
Vegetation is Juniperus-Quercus savanna or woodland and is representative of savannas and woodlands found throughout this region, but higher in woody plant density than savanna communities farther to the west (Van Auken et al. 1979; 1980; Van Auken et al. 1981; Smeins & Merrill 1988). The high density woody species are Juniperus ashei (Ashe juniper) and Quercus virginiana {=Q. fusiformis, Live oak) followed by Diospyros texana (Texas persimmon) and Sophora secundiflora. Associated with these woodlands are relatively small grasslands and sparsely vegetated intercanopy patches or gaps (openings between canopy patches) (Van Auken 2000). The major herbaceous species below the canopy is Carex planostachys (Cedar sedge) (Wayne & Van Auken 2008). In the grasslands and gaps Aristida longiseta (Red three-awn), Bouteloua curtipendula (Side-oats grama), Bothriochloa {=Andropogon) laguroides (Silver bluestem), B. ischaemum (KR bluestem), various other C4 grasses, and a variety of herbaceous annuals are common (Van Auken 2000).
Measurements exchange rates as a ftinction of light level or photosynthetic flux density (PFD) were measured and plotted for sun and shade leaves of Sophora secundiflora plants (Hamerlynck & Knapp 1994). There were five replications (individual leaves) measured for each leaf type. All plants sampled were approximately 2 m talk Sun leaves were on the outermost, southern facing canopy branches of plants growing in the full sun and shade leaves were on the innermost branches of these plants. Shade leaves from full sun plants were used as surrogates for shade plants (Hamerlynck & Knapp 1994).
Measurements were made within ± 3 hr of solar noon with a LI- COR® infrared gas analyzer (LI-6400). Irradiances were generated by the LI-COR LED red-blue light source using a light curve program with the LI-COR, a gas flow rate of 400 pmol/s, and a CO2
FURUYA & VAN AUKEN
247
concentration of 400 jimol/mol. One mature, undamaged, fully expanded leaflet per replication and leaf type was used with the 2 by 3 cm chamber. The LI-COR 6400 was run at approximate ambient summer, midday, daytime temperature (35®C) and relative humidity (50%), and was calibrated daily. Response data were recorded after at least two minutes when a stable total coefficient of variation was reached (<0.3%), usually less than five minutes. Light response curves were started at a PFD of 2000 pmol/m^/s for sun leaflets and 1800 jLimol/mVs for shade leaflets and then decreased to 1800 or 1600, 1400, 1200, 1000, 800, 600, 400, 200, 100, 75, 50, 25, 10, 5, and 0 jLimol/mVs (16 or 17 total measurements).
The measurements included net photosynthesis, stomatal conductance, and transpiration. Repeated measure ANOVAs were utilized to determine if significant differences occurred between leaflet types. A one way ANOVA was used to determine if net photosynthesis, stomatal conductance, and transpiration were significantly different between the PFD’s tested (Sail et al. 2001). Shapiro- Wilks tests were used to test for normal distributions and the Bartlett’s Test was used to test for homogeneity of variances. Data were log transformed for analyses due to unequal variances as necessary.
The maximum photosynthesis (A^ax), PFD at A^ax, transpiration at ^max, conductance at A^ax, light saturation point, dark respiration, light compensation point, and the quantum yield efficiency (initial slope) were determined for each replicate, and means were calculated. The ^max was the highest net photosynthesis rate. Light saturating photosynthesis was the PFD when the slope of the initial rate line reached the A^ax- Dark respiration was the gas exchange rate at a PFD of 0 pmol/m^/s (y-intercept of the line for the initial slope or rate). The light compensation point was calculated as the PFD when the photosynthetic rate = 0 pmol COi/m^/s (x-intercept of the line for the initial slope or rate). The quantum yield efficiency or initial slope was calculated using the dark value and increasing PFDs until the regression coefficient of the slope decreased (150 pmol/m^/s PFD) (Wayne & Van Auken 2009).
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THE TEXAS JOURNAL OF SCIENCE-VOL. 61, NO. 4, 2009
A pooled Mest (Sail et al. 2001) was used to detect significant difference between leaf types for photosynthetic rates (Amax), light saturation, dark respiration, transpiration at A^ax, conductance at A^ax, and quantum yield efficiency. Due to unequal variances, light compensation and PFD at A^nax were compared using a standard ^test. Significance level for all tests was 0.05. Ambient PFD was also measured for each sun and shade leaf with the LI-COR® integrating quantum sensor at the time the light response curves were initiated (LI-COR, Inc, Lincoln, NE).
Pre-dawn xylem water potential -VxQ-ddmn xylem water potential {Px) measurements were made for leaves of each plant (Scholander et
al. 1965). Xylem water potential of sun and shade leaves was measured with the model 1000 PMS® pressure chamber (PMS, Instrument, Co. Corvallis, OR). Samples of each leaf type were collected with a sharp knife and put in a zip lock plastic bag with a wet paper towel between 4:30 and 5:00 am. The plastic bag was put in a cooler with ice to insure that would not change. measurements were made within 45 minutes of harvest.
Soil moisture measurements -W ohxmoXnc soil moisture measure¬ ments were made using time domain reflectometry (TDR) with a TRIME portable TDR soil moisture meter (TRIME-FM) (MESA System Co. Medfield, ME). TDR is a transmission line technique used to determine soil water content by inserting two parallel metal rods in a soil matrix to make measurements (Topp & Reynolds 1998; Noborio 2001). Soil water content was measured in five positions below the canopy of each plant. The five positions were the four cardinal compass points and the site next to the bole of the plant. Soil water content of five plants was sampled between 10:00 and 11:00
am. The site next to the bole of the plant was on the south side, and the other locations were approximately 10 cm from the bole. Data from five sites (north, south, east, west, and the site next to the plant) around each plant were pooled and a mean and standard error was determined.
FURUYA & VAN AUKEN
249
Figure L Photosynthetic light response curves for sun (♦) and shade (□) leaves of Sophora secundijlora. There were significant differences in photosynthetic rates for sun and shade leaves of S. secundiflora (repeated measured ANOVA, F=7.6934, P^O.0242). Error bars represent ± one standard error of the mean. Different letters between light levels indicate significant differences between sun leaves (upper case) or shade leaves (lower case) and between leaf types (*).
Leaflet area and total leaflet dry mass-ArQ?i (LA) and total dry mass (Mooney & Gulmon 1982) of five sun and five shade leaflets were measured to determined mass per unit area (LMA) (g/cm^). The sun and shade leaflets previously used to make gas exchange measurements were collected to determine leaf area and total dry mass. Leaflets were dried at 60®C to a constant mass prior to weighing.
Results
The photosynthetic response for the two leaf types was significantly different over the light levels measured (Repeated Measure ANOVA; Fig. 1). At PFD’s above 400 pmol/m^/s, sun leaves had significantly higher photosynthetic rates than shade leaves (/-test; P < 0.05), while at PFD’s lower than 400 pmol/m^/s, shade leaves generally had higher rates than sun leaves, but values were not significantly different (/-test, P > 0.05). Photosynthetic rates for the sun leaves continued to increase from 600 to 2000 pmolW/sec, but
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THE TEXAS JOURNAL OF SCIENCE-VOL. 61, NO. 4, 2009
Figure 2. Stomatal conductance curves for sun (♦) and shade (□) leaves of Sophora secundiflora. There were significant differences in stomatal conductance rates for sun and shade leaves of S. secundiflora (repeated measured ANOKA, F=5.6495, P=0.0448). Error bars represent ± one standard error of the mean. Different letters between light levels indicate significant differences between sun leaves (upper case) or shade leaves (lower case) and between leaf types (*).
not significantly. The same was true for the shade leaves except there were no significant differences between treatments at 200 and 1800 jLimol/mVs, the highest light treatment used for the shade leaves. Stomatal conductance of the sun and shade leaves were significantly different over the light levels examined (Repeated Measure ANOVA\ Fig. 2). However, the stomatal conductance rate for the sun leaves did not change significantly over the light levels tested (One way ANOVA) and the same was true for the shade leaves. However, the sun leaves had higher conductance rates at most light levels tested (Student’s Mest). Transpiration rates of the two leaf types were not significantly different over the light levels measured (Repeated Measure ANOVA; Fig. 3). At all light levels tested, the transpiration rate was higher for the sun leaves, but not significantly higher (Students Mest; P > 0.05).
The maximum photosynthetic rate (A^ax) of S. secundiflora sun leaves was 12.9 pmol C02/m^/s and occurred at the maximum PFD
FURUYA & VAN AUKEN
251
E
o
9
o
E
B
®
m
oc
c
o
w
Im
’E
m
E
m
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0 500 1000 1500 2000
PFD (|jmol/m2/s)
Figure 3. Transpiration curves for sun (♦) and shade (□) leaves of Sophora secundiflora. There were no significant differences in transpiration rates for sun and shade leaves of S. secundiflora (repeated measured ANOVA, F=L4992, P=0.2556). Error bars represent ± one standard error of the mean. Different letters between light levels indicate significant differences between sun leaves (upper case) or shade leaves (lower case) and between leaf types (*).
measured (2000 jimol/m^/s) (Table 1). The rate was approximately L7 times that of the shade leaves (7.5 pmol C02/m^/s), which occurred at a PFD of 1000 pmol/m^/s). Light saturation for sun leaves was 355 pmol/m^/s, which was significantly higher than the light saturation of shade leaves (210 pmol/m^/s). The light compensation point of sun leaves was 61 pmol/m^/sec which was 1.5 times greater than the light compensation point of shade leaves at 41 pmol/m^/s but not significantly different (Table 1). The dark respiration of sun leaves was 3.5 pmol COa/m^/s and was 1.5 times greater than the dark respiration of shade leaves at 2.3 pmol C02/m^/s and these values were significantly different. The quantum yield efficiency or the initial slope (slope of the line from 0-150 pmol/m^/s) was not significantly different between the sun or shade leaves (Table 1). Conductance at was significantly higher for sun leaves compared to shade leaves, but there was no significant difference in transpiration rates (Table 1).
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THE TEXAS JOURNAL OF SCIENCE-VOL. 61, NO. 4, 2009
Table 1. Means and standard error (SE) for the maximum net photosynthetic rates (Amax), light level at the Amax, light saturation (Lsat), light compensation points (Rd/a), dark respiration rates (Rd), initial slope or quantum yield efficiency (IS), stomatal conductance rates, transpiration rates (E), leaflet areas (LA), leaflet mass, leaflet mass per unit area (LMA), ambient light level, and pre-dawn xylem water potential (T^x) of sun and shade leaves for Sophora secundiflora and soil moisture (%).
|
Leaf type (Mean ± one SE) |
||
|
Parameter |
Sun |
Shade |
|
^max ()LimolC02/mVs) |
12.9 (0.6) a* |
7.5 (1.4) b |
|
PDF at.4niax |
2000 (0) |
1000 (0) |
|
^sat |
355 (35) a |
210 (20) b |
|
Rd/a (pmol/mVs) |
61 (13) a |
41 (3) a |
|
Rd (pmolC02/mVs) |
3.5 (0.4) a |
2.3 (0.2) b |
|
IS (pmolC02/(jLimol quanta) |
0.0490 (0.0022) a |
0.0550 (0.0021) a |
|
gs(molH20/mVs)at^max |
0.24 (0.02) a |
0.12 (0.02) b |
|
E (mmolH20/m^/s) at |
6.24 (0.78) a |
4.67 (0.93) a |
|
LA (cm“) |
12.0 (1.9) a |
12.8 (1.0) a |
|
EM (g) |
0.22 (0.03) a |
0.23 (0.03) a |
|
LMA (g/cm^) |
0.019 (0.001) a |
0.018 (0.001) a |
|
Ambient Light (pmol/mVs) |
1216 (78) a |
394(95) b |
|
'Px (Mpa) |
-0.90 (0.10) a |
-1.12 (0.06) a |
|
Soil Moisture (%) |
9.4 (1.6) |
* Means in the same row followed by the same letter are not significantly different at the 0.05 level.
There were no significant differences in the leaflet area, leaflet mass or specific leaflet mass (Table 1). Ambient light levels were significantly different for the two leaf types, with the sun leaves being exposed to 3.1 times more light (Table 1). In addition, the of the sun and shade leaves was not significantly different, but the surface soil was dry, having only 9.4 ±1.6 % moisture.
FURUYA & VAN AUKEN
253
Discussion
As hypothesized, sun leaves of Sophora secundiflora, which is commonly found growing in high light environments in Central Texas (Van Auken et al. 1981), had a high maximum photosynthetic rate (^max)? typical of species found growing in open habitats (Begon et al. 2006). Other photosynthetic parameters, including light saturation, light compensation, dark respiration, conductance, and transpiration, were high for sun adapted leaves. However, shade leaves had relatively high gas exchange parameters as well. These responses are not consistent with findings for shade plants, but for plants that are sun plants or are intermediate or facultative species (Boardman 1977; Hull 2002; Larcher 2003; Givnish et al. 2004; Begon et al. 2006; Valladares & Niinemets 2008).
Although Sophora secundiflora is a native species with a fairly broad distribution and is used as an ornamental over much of its range, very little is known about its photosynthetic capabilities. No studies have been identified which evaluate the physiological responses or growth responses of this species to light levels or other factors. The parameters measured for both leaf types suggest that this species is not a sun or shade species, but an intermediate or facultative species. Therefore, it can grow in sun or shade or intermediate light habitats.
In general, true understory species have much lower photo¬ synthetic rates than the rates reported for S. secundiflora in the current study. Photosynthetic rates of three understory montane spruce forests species found in central Europe all had rates 27-65 % lower (3.4 - 5.5 pmol C02/m^/s) than S. secundiflora shade adapted leaves (Hattenschwiler & Komer 1996). In addition to these lower ^max rates, the European forest species reached light saturation at much lower irradiance (~200 pmolW/s) levels than sun leaves of S. secundiflora (355 ± 36 pmolW/s), although shade leaves of S. secundiflora were light saturated at about the same level as the forest understory species (210 ± 20 pmolW/s). Arnica cordifolia (Asteraceae), an herbaceous perennial which grows in the understory of lodgepole pine forests in southeastern Wyoming, also had
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photosynthetic rates 44-53% lower than S. secundiflora shade adapted leaves (3.5 - 4.2 |LimolC02/mVs), but reached light saturation at the same level as the S. secundiflora sun leaves at 350 pmol C02/m^/s (Young & Smith 1980). Polygonum virginianum (Polygonaceae), an herbaceous perennial found in the forest understory and at the forest’s edge in the eastern United States, had an A^ax of ~ 3 pmolC02/mVs at a light saturation of ~ 500 pmolW/s (Zangerl & Bazzaz 1983). Car ex planostachys from the central Texas Edwards Plateau Juniperus woodland understory had an value of 4.9 ± 0.3 pmolC02/m^/s which was 65 % of the value for shade leaves of S. secundiflora and reached light saturation at 151 ± 43 pmol/m^/s (Wayne & Van Auken 2009). While S. secundiflora is typically found growing in open habitats or the edge of woodlands, its high Araax for shade adapted leaves compared to other herbaceous shade plants would suggest it is an intermediate or facultative sun species, and could grow in a variety of light environments including edge habitats.
True sun plants are adapted to high light conditions and have high rates of gas exchange. For example, Abutilon theophrasti an early successional herbaceous perennial had rates between 15-25 pmolC02/mVs (Wieland & Bazzaz 1975; Bazzaz 1979; Munger et al. 1987a; Munger et al. 1987b; Hirose et al. 1997; Lindquist & Mortensen 1999). Two oaks of gallery forest in tall grass prairies of northeastern Kansas, Quercus muehlenbergii and Q. macrocarpa had ^max rates 1.40-2.02 times higher than S. secundiflora at 18-26 pmolC02/mVs for sun leaves and 11-13 pmolC02/mVs or 1.47-1.73 times higher for shade leaves (Hamerlynck & Knapp 1994).
Plants can acclimate to the variability of the light environment in which they live, particularly early successional species or plants from disturbed (open) communities (Bazzaz & Carlson 1982). Polygonum pensylvanicum, a colonizing annual of open fields, had an^^ax of ~ 12 |LimolC02/mVs at ~ 1500 pmol/mVs when plants from a shaded-habitat (200 pmol/mVs) were measured (Bazzaz & Carlson 1982; Zangerl & Bazzaz 1983); however the rate was - 24 pmol/mVs at ~ 1800 pmol/m^/s when plants from a full sun habitat were measured (Bazzaz
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& Carlson 1982). The high light individuals we sampled in the present study were growing in an area which received 1216 ± 78 pmol/m^/s (~ 60% full sunlight). We might expect that individuals from higher light environments could have higher maximum photosynthetic rates, while those from lower light environments would be lower. Further studies would be needed to determine if S. secundiflora does acclimate to variability in the light environment as reported for other species.
The dark respiration of sun leaves of S. secundiflora (3.5 ± 0.4 pmolC02/m^/s) is similar to other sun-adapted plants (Hamerlynck & Knapp 1994). This rate is 1.52 times higher than the of shade adapted leaves of S. secundiflora. However, the for shade adapted leaves of S. secundiflora is about 4.6 times higher than rates for other shade adapted species (Hirose & Bazzaz 1998; Hull 2002). Dark respiration for shade-adapted species is typically lower than sun- adapted species, due to the lower metabolism of shade-adapted species (Bjorkman 1968; Bazzaz & Carlson 1982). Polygonum pensylvanicum grown at 200 pmol/mVs had a respiration rate of ~ 0.5 pmolC02/m^/s, although the rate was twice as high when plants from full sun were measured (Bazzaz & Carlson 1982).
Other photosynthetic parameters reported in this study for S. secundiflora are similar to those values reported in the literature. Quantum yield efficiency reported here (0.049 and 0.055 pmolC02/pmol quanta, sun leaves and shade leaves respectively) are within the range or similar to values (0.035 - 0.052 pmolC02/pmol quanta) reported for other species (Hirose et al. 1997). Stomatal conductance and transpiration reported in the current study were similar to other studies, however many factors affect these parameters (Wieland & Bazzaz 1975; Zangerl & Bazzaz 1984; Yun & Taylor 1986; Munger et al. 1987a; Munger et al. 1987b; Stafford 1989).
The sun and shade leaves of S. secundiflora show some distinct and varied photosynthetic responses. These differential physiological responses to various light levels more than likely are contributors to the niche breadth observed for this species in the field. In general.
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resource utilization is spatially partitioned among species along complex environmental gradients^ such as changes in light from open areas to woodland or forest edges (Wayne & Van Auken 2009). The ability of S. secundiflora to reach high photosynthetic rates at lower light level, its light saturation, and light compensation point allows it to exist in a variety of communities. At light levels below 300 ILimolC02/m^/s, data suggests that other more shade tolerant species would probably be able to out-compete S. secundiflora. At light levels above 300 pmolC02/mVs, S. secundiflora could dominate, in part because it has photosynthetic rates as high as or higher than most co-occurring species (Grunstra 2008).
Acknowledgements
We would like to thank the Center for Water Research at The University of Texas at San Antonio for support provided for the senior author. Help from M. Grunstra and J. K. Bush during various stages of the study is truly appreciated.
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oscar.vanauken@utsa.edu
TEXAS J. OF SCL 61(4):259-278
NOVEMBER, 2009
CHARACTERIZATION OF
ARSENIC-TOLERANT BACTERIAL CULTURES FROM THE LOWER LAGUNA MADRE OF SOUTH TEXAS
Gemma A. Berlanga, Michael W. Persans, Thomas M. Eubanks and Kristine L. Lowe
Department of Biology, University ofTexas-Pan American Edinburg, Texas 78539
Abstract -Two forms of arsenic are found in the environment: As(V) and As(III), the latter being more toxic, water-soluble, and mobile. Microorganisms may increase the mobility of arsenic by reducing As(V) to As(III); however, detoxification and immobilization can occur via the oxidation of As(III) to As(V). The US EPA has set a minimum contaminant level of 10 parts per billion (ppb) for arsenic in drinking water. The research objective was to confirm the presence of arsenic-tolerant bacteria in the Lower Laguna Madre of south Texas. Sediment samples were collected and inoculated into growth media which contained either 2 mM As(III) or 2 mM As(V) to enrich for As(III)-tolerant and As(V)-tolerant bacteria, respectively. Twenty six (26) As(III)-tolerant and 12 As(V)-tolerant cultures were obtained. Most isolates were small white colonies of Gram-positive rods. Biochemical tests using commercially-made test strips showed that As(V)-tolerant isolates displayed greater resource usage compared to As(III)-tolerant isolates but overall, few cultures demonstrated a wide-range of biochemical capabilities. Isolates with distinct morphological and biochemical phenotypes were subjected to Polymerase Chain Reaction (PCR) amplification and sequencing of the 16S rRNA genes to identify the bacteria. Closest sequence matches were to the eubacterial genera Mycoplasma, Salinispora, Frankia, and Pelodictyon. These results suggest that the Lower Laguna Madre is inhabited by a diverse group of microorganisms able to tolerate toxic concentrations of different arsenic species.
Arsenic contamination is a significant problem in the environment because arsenic is toxic and carcinogenic. Although arsenic may exist in several oxidation states, it is typically found in two forms in the environment; arsenate (As(V)), which is typically insoluble, and arsenite (As(III)), which is water soluble and more toxic (Stumm & Morgan 1996). Insoluble As(V) often precipitates to the bottom of bodies of water making the arsenic immobile, but soluble As(III) is mobile and of much greater concern. The US EPA has set a Maximum Contaminant Level (MCL) of 10 ppb for total arsenic (As(III) + As(V)) in drinking water (USEPA 2001). A
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1995 Study showed sediment arsenic levels greater than 27,000 ppb in the Upper Laguna Madre (Barrera et al. 1995).
The Laguna Madre is a hypersaline estuary, one of only five in the world, with an average salt content ranging from 35 to 45 ppt; however, salt concentrations higher than 80 ppt have been reported (Quannen & Onuf 1993; Tunnell & Judd 2002; Whelan et al. 2005). The high salinity of the Laguna Madre is due to the fact that there are few freshwater inputs into the estuary and few outlets. The Lower Laguna Madre receives fresh water discharged from the highly-impacted Arroyo Colorado and from precipitation; however, the estuary is shallow (average depth 1.5 m) (Tunnell & Judd 2002). Salts concentrate during periods of drought and high rates of evaporation occur in the summer due to the warm regional climate of South Texas, Regional pollution has resulted in toxic chemical concentrations in water, sediment, and animals of the Laguna Madre (Davis et al. 1995). Among the contaminants at toxic concentrations is arsenic. Much of the arsenic detected in the Lower Rio Grande Valley of Texas and along the US-Mexico border is attributed to past usage of arsenical pesticides, but may also be related to sewage treatment discharge into regional waterways and non-point sources (Davis et al. 1995; Tunnell & Judd 2002).
Davis et al. (1995) reported that large amounts of arsenic were present in the Lower Laguna Madre; however, this study did not distinguish between insoluble As(V) and toxic, soluble As(III). Arsenic is also of concern in the Arroyo Colorado, a waterway in South Texas that is part of the natural drainage system for the Lower Rio Grande Valley and lies on the north of the Rio Grande Delta. The Arroyo Colorado is part of a floodway system, receives treated wastewater from several towns, runs through the Port of Harlingen, and discharges into the Lower Laguna Madre. Elevated arsenic levels have been detected in the Arroyo Colorado, most likely due to agricultural runoff (Wells et al, 1988). Thus, arsenic in the Laguna Madre presents a potential threat to the ecosystem
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and may impact organisms in the lagoon. Some microorganisms may increase the mobility of arsenic by reducing As(V) to As(III) (Macy et al. 2000), However, aquatic plants and microorganisms may lessen the toxicity of arsenic by immobilizing it via oxidation, methylation, or accumulation (Oremland et al. 2002, Bentley & Chasteen 2002, Schmoger et al. 2000).
As(V) and As(III) can change oxidation state by chemical or biological processes. In marine sediments, As(V) can form a variety of insoluble mineral compounds that are structurally similar
'j
to phosphates. These occur when arsenate anions (ASO4 ") react with transition metals, such as iron and manganese (Smedley & Kinniburgh 2002). Reduction of metal-arsenate minerals can occur under low redox (reducing) conditions, thus liberating the arsenic as As(III). As(III) typically exists as soluble arsenic acids, such as H3ASO3, at marine pH values (Smedley & Kinniburgh 2002).
Biologically-mediated transformations of arsenic depend on the form of arsenic involved. As(V) may be reduced to As(III) by anaerobic sediment bacteria through dissimilatory anaerobic respiration (Newman et al. 1998, Macy et al. 2000). Plants can reduce As(V) to As(III) through a detoxification mechanism (Meharg & Hartley- Whitaker 2002) or the bioaccumulation of arsenic may take place in plant tissues (Davis et al. 1995). Arsenic can also be detoxified via biomethylation in microorganisms, algae, plants, and animals (Wang et al. 2004). Methylation detoxifies arsenic by making it volatile, converting it to gaseous forms (Qin et al. 2006). Reduction of As(V) to As(III) can potentially release arsenic bound to sediment particles or bound in minerals, and may impact the mobility of arsenic in the Laguna Madre ecosystem. Increased arsenic mobility will potentially impact plants and animals by introducing toxic, soluble As(III) into sediment pore waters and estuary waters. Conversely, As(III) oxidation is an important detoxification reaction since the resulting As(V) is less toxic and less bioavailable (Oremland et al. 2002).
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The macro-ecology of the Laguna Madre has been extensively studied for decades. Several rare, endangered, threatened, and migratory animal species feed or nest in the Laguna Madre. Despite this, little is known about the microbial ecology of the Laguna Madre and the importance of microorganisms in nutrient and chemical cycling within the sediments of the ecosystem. Interest in microbial ecology has increased dramatically as the importance of microorganisms within sediments and subsurface environments are related to biogeochemistry, bioremediation, and biotechnology (Atlas & Bartha 1998; Nealson 1997). The interplay between biologically-mediated As(III) oxidation and biologically- mediated As(V) reduction is important in determining the fate of arsenic species in the Laguna Madre. In this research, culture- based and molecular methods were used to characterize bacterial populations that demonstrated tolerance to As(III) or As(V).
Materials and Methods
Sample collection. samples (approximately 50 g) were collected in March 2007 from the top 10 cm of sediment at four sites in the Lower Laguna Madre (Figure 1). Samples were transported on ice to the laboratory. The collection sites were: LMT-050 (N26°08n7.4”,W97M0’4L0”), located near the South Padre Island Wastewater Treatment Plant; South Bay (SB; N26°02’48” W97Mr3.3”); site ABC (N26°10’09.7” W97Mr 05.3”) and LMT-051 (N26°10’09.7”,W97Mr05.3”). All sites were south of the mouth of the Arroyo Colorado and have been described previously (Whelan et al. 2005).
Enrichment cultures for arsenic-oxidizing and arsenic-reducing bacteria. from each site was homogenized and 1 g was placed into sterile 20-mL glass vials containing 10 mL of minimal liquid medium (Lowe et al. 2000). The final concentrations and composition of the medium was (per liter): CH3COO Na [15 mM], (NH4)2S04 [0.9 mM], K2HPO4 » 3H2O [0.57 mM], KH2PO4 [0.33 mM], NaHCOs [0.2 mM], NazEDTA ^ 2H2O [7pM], H3BO3 [6pM], FeS04 • 7H2O [0.6 ^M], C0CI2 • 6H2O [0.5 (iM], Ni(NH4)SOA •
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Figure 1. Map of the Lower Laguna Madre showing the sampling locations. (From Whelan et al. 2005).
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6H2O [0,5 juM], Na2Mo04 • 2H2O [0,4 |liM], Na2Se04 (anhyd) [0,15 juM], MnS04 * H2O [0,13 |aM], ZnS04 ^ 7H2O [0,1 jaM], CUSO4 * 5H2O [0.02 jLiM], casamino acids [0.01% w/v], Vitamin Bi [0.001 mg mL“^], L-arginine HCl [0.02 mg mL“^], L-glutamic acid [0,02 mg mL'^], L"glutamine [0.02 mg mF^], L-serine [0.04 mg mL"^], MgS04 *7H20 [1 mM], CaCl2 • 2H2O [0.5 mM] and NaCl [3% w/v]. After sterilization, the medium was amended with either As(V) (Na2HAs04 •7H2O) or As(III) (NaAs02) to a final concentration of 2 mM. Vials with As(V) as the terminal electron acceptor were placed in glass canisters with an anaerobic gas generating system (BBL GasPak, Becton Dickenson Co., Cockeysville, MD), Vials containing As(III) were incubated in an aerobic environment. Cultures were performed in triplicate. Vials were incubated at 25°C until there was visible turbidity. Once there was visible growth in the vials, the samples were streaked onto the appropriate medium as described above plus 1.5% Bacto Agar (Difco-BBL, Sparks, MD) to isolate pure colonies.
Isolation of As (III) -tolerant and As (V) -tolerant bacteria-ThQ As(III) enrichment vials that showed bacterial growth were inoculated onto appropriate agar consisting of minimal media with As(III), These samples were incubated aerobically for 14 d at 25°C. Resulting isolated colonies were sub-cultured on the same medium and incubated aerobically at 25°C. Agar plates that had been inoculated from the As(V) enrichment vials were incubated at 25 °C in glass canisters with an anaerobic gas generating system (BBL GasPak, Becton Dickenson Co., Cockeysville MD) for 30 d. The resulting cultures were sub-cultured on the same medium and incubated in an anaerobic environment at 25°C.
Random As(III)-tolerant and As(V)-tolerant bacterial isolates from the arsenic media agar plates were chosen for ftirther investigation. Isolates were characterized by Gram-stain and by observed colony morphology (i.e., color, size, shape). Biochemical profiles for isolates were generated using API 20E® strips
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(bioMerieux Inc., Durham, NC). Isolates were stored in 25% glycerol at -80°C for molecular studies.
API 20E® strips 20E® strips include enzymatic tests for fermentation or oxidation of glucose, mannitol, inositol, sorbitol, rhamnose, saccharose, melibiose, amygdalin, and arabinose, along with nitrate reduction to nitrite and nitrate reduction to nitrogen gas. API 20E® strips also test for the presence of P-galactosidase, arginine dihydrolase, lysine decarboxylase, ornithine decarboxylase, citrate utilization, H2S production, urease, tryptophan deaminase, indole production, acetoin production (Voges ~ Proskauer), and gelatinase. API 20E® tests were performed according to the manufacturer’s instructions. The number and types of positive tests were tabulated for the isolates and used to construct biochemical profiles of the As(III)“tolerant and As(V)-tolerant cultures. The API 20E® profiles were used to compare biochemical phenotypes amongst the isolates.
Molecular identification of isolates -yio\QCu\^x identification of the isolated As(III)-tolerant and As(V)-tolerant bacteria was performed by the Polymerase Chain Reaction (PCR) amplification and sequencing of the 16S ribosomal RNA (16S rRNA) genes (Sambrook & Russell 2001). Genomic DNA was extracted from the bacterial isolates using the QIAamp DNA Mini Kit (Qiagen, Valencia, CA). Extracted genomic DNA integrity was verified on a 1% agarose electrophoresis gel. Genomic DNA concentration was quantified by reading the absorbance in a UV-VIS spectro¬ photometer at 260 nm. Purity of the extracted DNA was determined by the ratio of the absorbances at 260 and 280 nm. Ratios of 260/280 absorbance measurements were between 1.7 and 2.0 for all samples; thus, the extraction yielded mostly DNA (Sambrook & Russell 2001).
A sample (50 ng) of template genomic DNA was placed in a 0.5 mL thin-walled PCR tube with 25 pL of PCR Master Mix (Promega, Madison, WI). PCR primers used to amplify the 1505 bp target of the 16S rRNA gene were 5'- AGA GTT TGA TCC
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TGG CTC AG ~ 3' (forward) and 5'- ACG GCT ACC TTG TTA CGA CTT - 3' (reverse) (Integrated DNA Technologies, Coralville, lA). The final concentration of each primer was 10 pM. The total PCR mixture volume was 50 pL. The PCR mixture was placed into a MyCycler PCR thermocycler (Bio Rad, Hercules, CA) and heated to 95°C for 6 min in order to initially denature the template DNA. After the initial denaturation, 40 cycles were run with the following conditions: denaturing at 95°C for 30 sec, annealing of the primers at 52°C for 30 sec, and primer extension at 72°C for 30 sec. A final extension at 72°C for 1 min was done and the PCR products were held at 4°C. An aliquot (5 pL) of the PCR products was visualized by electrophoresis on a 1% agarose gel. The remaining PCR product mixture was purified using a Wizard PCR Clean Up Kit (Promega, Madison, WI). Purified PCR products were used for DNA sequencing described below.
For sequencing, a second round of PCR was done using a commercially-available sequencing kit (Genome Lab DTCS Quick Start Kit; Beckman Coulter, Fullerton CA) according to the manufacturer ’ s instructions. Dye-tagged dideoxynucleotides (ddUTP, ddGTP, ddCTP, and ddATP) were added to terminate elongation (Sambrook & Russell 2001). The resulting PCR product was loaded into an automated DNA sequencer (CEQ 8000 Genetic Analysis System; Beckman Coulter, Fullerton, CA). The sequences were compared to known bacterial sequences available in the National Center for Biotechnology Information Basic Local Alignment Search Tool (BLASTN) database (www.ncbi.nml.nih. gov/BLAST) to identify the microorganisms (Altschul et al. 1997).
Results and Discussion
Pure colonies {n = 26) were successfully isolated from As(III) enrichments [Table 1]; 12 pure colonies were isolated from As(V) enrichments [Table 2]. Every isolate cultured in As(III) media was 100% Gram-positive [Table 1]. The As(III) Gram stain results were unusual because marine sediments usually contain mixtures of Gram-positive and Gram-negative bacteria (Atlas & Bartha 1998).
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Table 1 . Morphology of Laguna Madre bacteria isolated from As(III)-contaimng media. As(III)"tolerant bacteria were isolated from the Laguna Madre from different sites. Isolates were streaked onto minimal media supplemented with 2 mM As(III) and incubated aerobically for 14 d. Cells were Gram-stained and the colony morphology was visually observed and recorded. All isolates were Gram-positive and smooth in appearance.
|
Isolate |
Sediment Source |
Shape |
Appearance |
|
AS3-A |
South Bay |
bacillus |
white, small , round |
|
AS3-B |
South Bay |
bacillus |
white, round |
|
AS3--C |
ABC |
bacillus |
orange, round |
|
AS3--D |
South Bay |
bacillus |
white, irregular |
|
AS3-E |
South Bay |
bacillus |
ivory, small, irregular |
|
AS3-F |
LMT-050 |
bacillus |
clear, small, irregular |
|
AS3-G |
LMT-050 |
bacillus |
light yellow-orange, small, round |
|
AS3-H |
LMT-050 |
bacillus |
light yellow, small, round |
|
AS3-I |
LMT-050 |
bacillus |
pink, small, round |
|
AS3-J |
ABC |
bacillus |
peach, small, round |
|
AS3-K |
South Bay |
coccus |
transparent, small, round |
|
AS3-L |
South Bay |
coccus |
white, small, round |
|
AS3-M |
South Bay |
bacillus |
yellow/orange, small, round |
|
AS3-N |
LMT-050 |
bacillus |
ivory, small, round |
|
AS3-0 |
LMT-051 |
bacillus |
white, small, round |
|
AS3-P |
ABC |
bacillus |
white, small, round |
|
AS3-Q |
South Bay |
bacillus |
white, small, round |
|
AS3-R |
South Bay |
bacillus |
white, small , irregular |
|
AS3-S |
South Bay |
cocco-bacillus |
white, small, round |
|
AS3-T |
ABC |
bacillus |
orange, small, round |
|
AS3-U |
ABC |
bacillus |
orange, small, round |
|
AS3-V |
LMT-051 |
bacillus |
pink/orange, small, round |
|
AS3-W |
LMT-050 |
bacillus |
ivory, small, round |
|
AS3-X |
LMT-051 |
bacillus |
peach, small, round |
|
AS3- Y |
ABC |
bacillus |
ivory, tiny, round |
|
AS3-Z |
ABC |
bacillus |
orange, small, round |
The high percentage of Gram-positive bacteria may reflect the toxicity of arsenic, which may result in high selection pressure for Gram-positive organisms. Once inside a cell, As(III) disrupts protein folding and protein-DNA interactions (Norman 1998). Gram-positive cells have a thicker cell wall compared to Gram¬ negative cells. The thicker cell wall might make it more difficult for As(III) to enter the cell. The isolates enriched in As(III) medium were rod-shaped or bacillus (23/26), cocci (2/26) and
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THE TEXAS JOURNAL OF SCIENCE-VOL. 61, NO. 4, 2009
Table 2. Morphology of Laguna Madre bacteria isolated from As(V)-containmg media. As(V)-tolerant bacteria were isolated from the Laguna Madre from different sites. Isolates were streaked onto minimal media supplemented with 2 mM As(V) and incubated anaerobically for 30 d. Cells were Gram-stained and the colony morphology was visually observed and recorded.
|
Isolate |
Sediment Source |
Gram Stain |
Shape |
Colony Appearance |
|
ASS - A |
LMT-050 |
+ |
bacillus |
transparent, small, round, smooth |
|
AS5-B |
ABC |
+ |
bacillus |
transparent, small, round, smooth |
|
AS5-C |
South Bay |
+ |
bacillus |
ivory, small, irregular, smooth |
|
AS5-D |
LMT-051 |
- |
cocco-bacillus |
ivory, small, irregular smooth |
|
AS5-E |
LMT-050 |
- |
coccus |
transparent, small, round, smooth |
|
AS5-F |
LMT-050 |
+ |
coccus |
ivory, round with filaments, smooth |
|
AS5-G |
LMT-050 |
- |
cocco-bacillus |
ivory clear, small, irregular, smooth |
|
AS5-H |
LMT-051 |
+ |
coccus |
white, small,, round, smooth |
|
ASS -I |
LMT-050 |
- |
cocco-bacillus |
white, small, irregular, smooth, |
|
AS5-J |
LMT-050 |
- |
bacillus |
transparent, small, round, smooth |
|
ASS -K |
LMT-050 |
+ |
coccus |
ivory, small, irregular, filamentous |
|
ASS-L |
LMT-050 |
coccus |
transparent, small, round, smooth |
cocco-bacillus (1/26) [Table 1]. The typical colony morphology of the As(III) isolates was smooth and round but varied in color and shape. The morphologies observed ranged from small, white punctiform colonies to irregular-shaped, colored colonies. Colony colors included pink and orange [Table 1].
The isolates cultured in As(V) were either Gram-positive (7/12) or Gram-negative bacteria (5/12) and were bacillus (4/12), cocci (5/12), and cocco-bacillus (3/12) [Table 2].
The colony morphologies also varied for the As(V) isolates. Colonies were mostly irregular and white, or almost transparent [Table 2]. Two of the As(V) isolates, AS5-F and AS5-K, were filamentous; both were isolated from LMT-050 [Table 2]. In general, isolates from the As(V) enrichments displayed slower growth rates than those isolated from As(III) media (data not shown). However, this was most likely due to incubation conditions - anaerobic for As(V) versus aerobic conditions for As(III) - and not arsenic toxicity.
BERLANGA, ET AL.
269
For the As(III) isolates {n = 26) tested with API 20E® strips, three of the isolates were positive for P-galactosidase and six were positive for gelatinase; two were positive for mannitol and saccharose oxidation; one was positive for melibiose utilization. The remaining seventeen tests were negative for all As(III) isolates [Table 3].
Among the As(V) isolates {n= 12) tested with API 20E® strips, five were positive for p~galactosidase, two were positive for arginine dihydrolase, and seven were positive for gelatinase. In addition, three were positive for glucose, mannitol, rhamnose, saccharose, amygdalin, or arabinose oxidation. The remaining thirteen tests were negative for all As(V) isolates [Table 4].
The high number of negative tests made putative identification of the isolates difficult; however, the isolates from the anaerobic As(V) enrichment cultures appeared more metabolically diverse than those cultured in the aerobic As(III) enrichment cultures. The enzymatic flexibility that some As(V)-tolerant bacteria displayed may be due to the lower toxicity of As(V) relative to that of As(III) or As(III) may select for characteristics that were not included on the test strips and not observed.
There were a low number of positive API tests from the microorganisms isolated from As(III) enrichments [Table 3]. Among the As(III)-tolerant isolates tested, isolates AS3-J from site ABC and isolate AS3-K from South Bay each displayed only three positive tests which was the highest number of positive tests [Table 3], Isolates AS3-J and AS3-K are likely to be different microorganisms because their morphology was different and their API profiles displayed two tests in common but differed in one [Table 3], AS3-J and AS3-K were both able to oxidize mannitol and saccharose; however, only AS3-J was able to metabolize melibiose while AS3-K produced p-galactosidase indicating lactose utilization [Table 3]. Isolates AS3-G, AS3-H, AS3-T, AS3-U, AS3-W and AS3-Z tested positive for gelatinase [Table 3];
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Table 3. Biochemical profiles of As(III)-tolerant bacteria. Twenty-six (26) As(III)- tolerant bacteria were isolated from the Laguna Madre sediment. The isolates’ metabolic activities were tested using API 20E® strips. A plus sign (+) indicates that the isolate was positive for the test; a negative sign (-) indicates a negative reaction
|
for the test. Only isolates that displayed at least one positive test are shown. |
|||
|
Isolate |
|||
|
AS3- AS3- AS3- AS3- |
AS3- AS3- AS3- AS3- AS3- |
AS3- |
|
|
E G H J |
K M T U W |
Z |
|
|
ONPG |
+ - - - |
+ + - - - |
_ |
|
ADH |
_ _ _ _ |
_____ |
- |
|
LDC |
- _ - - |
_____ |
- |
|
ODC |
- - - - |
_____ |
- |
|
CIT |
- - - - |
_____ |
- |
|
H2S |
_ _ _ _ |
_____ |
- |
|
URE |
_ _ _ _ |
_____ |
- |
|
TDA |
- - - - |
_____ |
- |
|
IND |
- - - - |
_____ |
- |
|
VP |
_ _ _ _ |
_____ |
- |
|
GEL |
- + + - |
- - + + + |
+ |
|
GLU |
_ _ _ _ |
_____ |
- |
|
MAN |
- - - + |
+ _ _ _ _ |
- |
|
INO |
- - - - |
_____ |
- |
|
SOR |
_ _ _ _ |
_____ |
- |
|
RHA |
_ _ _ _ |
_____ |
- |
|
SAC |
- - - + |
+ _ _ _ _ |
- |
|
MEL |
- - - + |
_____ |
- |
|
AMY |
- - - - |
_____ |
- |
|
ARA |
- - - - |
_____ |
- |
|
N02 |
- - - - |
_____ |
- |
|
N2 |
- - - - |
_____ |
- |
Tests: ONPG, |3-galactosidase activity; ADH, arginine dihydrolase; LDC, lysine decarboxylase; ODC, ornithine decarboxylase; CIT, citrate utilization; H2S, hydrogen sulfide production; URE, urease; TDA, tryptophan deaminase; IND, indole production; VP, acetoin production (Voges-Proskaur); GEL, gelatinase; GLU, glucose; MAN, mannitol; INO, inositol; SOR, sorbitol; RHA, rhamnose; SAC, sucrose; MEL, melibiose; AMY, amygdalin; ARA, arabinose; N02, nitrate reduction to nitrite; N2, nitrate reduction to nitrogen gas.
moreover, AS3-T, AS3-U and AS3-Z all showed similar colony morphologies and are potentially the same organism despite being isolated from different locations in the Laguna Madre [Table 1].
The As(V) isolates from the sediment samples collected at LMT- 050 had the highest number of positive API tests for all isolates tested [Table 4]. The LMT-050 population included AS5-A, ASS-
BERLANGA, ET AL.
271
Table 4. Biochemical profiles of As(V)-tolerant bacteria. Twelve (12) As(V)-tolerant bacteria were isolated from the Laguna Madre sediment. The isolates’ metabolic activities were tested using API 20E® strips. A plus sign (+) indicates that the isolate was positive for the test; a negative sign (-) indicates a negative reaction for the test.
Isolate
|
ASS |
ASS |
ASS |
ASS |
ASS |
ASS |
ASS |
ASS |
ASS |
ASS |
ASS |
ASS |
|
|
-A |
-B |
-C |
= D |
= E |
-F |
-G |
-H |
-I |
- J |
-K |
-L |
|
|
ONPG |
+ |
+ |
- |
- |
+ |
- |
- |
_ |
- |
+ |
- |
+ |
|
ADH |
+ |
- |
- |
- |
- |
- |
- |
- |
- |
+ |
- |
- |
|
LDC |
||||||||||||
|
ODC |
||||||||||||
|
CIT |
||||||||||||
|
H2S |
||||||||||||
|
URE |
||||||||||||
|
TDA |
||||||||||||
|
IND |
||||||||||||
|
VP |
||||||||||||
|
GEL |
- |
- |
+ |
+ |
- |
- |
+ |
+ |
+ |
- |
+ |
+ |
|
GLU |
+ |
- |
- |
- |
+ |
- |
- |
- |
- |
+ |
- |
- |
|
MAN |
+ |
- |
- |
- |
+ |
- |
- |
- |
- |
+ |
- |
- |
|
INO |
||||||||||||
|
SOR |
||||||||||||
|
RHA |
+ |
- |
- |
- |
+ |
- |
- |
- |
- |
+ |
- |
- |
|
SAC |
+ |
- |
- |
- |
+ |
- |
- |
- |
- |
+ |
- |
- |
|
MEL AMY |
+ |
+ |
||||||||||
|
ARA |
+ |
- |
- |
- |
- |
- |
- |
- |
- |
+ |
- |
- |
|
N02 |
||||||||||||
|
N2 |
Tests: ONPG, P-galactosidase activity; ADH, arginine dihydrolase; LDC, lysine decarboxylase; ODC, ornithine decarboxylase; CIT, citrate utilization; H2S, hydrogen sulfide production; URE, urease; TDA, tryptophan deaminase; IND, indole production; VP, acetoin production (Voges-Proskaur); GEL, gelatinase; GLU, glucose; MAN, mannitol; INO, inositol; SOR, sorbitol; RHA, rhamnose; SAC, sucrose; MEL, melibiose; AMY, amygdalin; ARA, arabmose; N02, nitrate reduction to nitrite; N2, nitrate reduction to nitrogen gas.
E, and AS 5-1, which were all isolated from the same sediment sample and have similar morphologies; however, they varied slightly in their biochemical profiles. The three isolates all tested positive for P-galactosidase and utilization of glucose, mannitol and rhamnose, but only AS5-A and AS5-J tested positive for arginine dihydrolase and arabinose metabolism, and AS5-E and AS5-J tested positive for amygdalin utilization [Table 4]. Even though AS5-A, AS5-E, and AS5-J isolates from LMT-050 were the most metabolically diverse, they all tested negative for gelatinase, which
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THE TEXAS JOURNAL OF SCIENCE-VOL. 61, NO. 4, 2009
overall had the highest number of positive reactions [Table 4]. The highest number of gelatinase-positive isolates were obtained in the anaerobically-grown As(V) isolates compared to the aerobic As(III) isolates. Only 6/26 As(III) isolates were positive for gelatinase whereas 7/12 of the As(V) isolates were gelatinase positive [Table 3 and 4], Gelatinase is a digestive enzyme necessary to break down gelatin, a protein found in animal connective tissue, which is sometimes degraded by bacteria during biofilm formation (McNamara et ah 1997). The production of gelatinase is also used to differentiate and identify anaerobes (Whaley et ah 1982). The overall high number of positive gelatinase tests suggests that some of these organisms may be anaerobic decomposers of organic matter (McNamara et al. 1997).
Isolates (5/12) from the As(V) enrichments were positive for fJ- galactosidase activity which indicates that some As(V)-tolerant bacteria from the Laguna Madre can use lactose as a carbon source [Table 4]. This was unexpected because lactose is not a commonly used carbon source in marine environments as it does not easily absorb to sediment particles (Sansone et al. 1987). Acetate is more easily absorbed to sediment particles and is more readily available to sediment bacteria; thus, it was used as the principle carbon source in the isolation medium. No isolate was capable of nitrate reduction [Table 3 and 4] which was also unexpected because many facultative and anaerobic sediment bacteria are able reduce NO3". NOs' is a better electron acceptor energetically compared to As(V) (Dowdle et ah 1996).
Results from the 16S rRNA gene sequencing showed an array of positive matches. Table 5 shows the top BLASTN result for the As(III) and As(V) isolates that were successMly sequenced. The top similarity match (% Match) is shown. Isolate AS3-E displayed high similarity to Mycoplasma hyopneumoniae. Isolate AS3-K showed good similarity to Salinispora tropica CNB-440, a marine Gram-positive bacterium with a high percentage of G+C bases in the DNA (Maldonado et al. 2005; Williams et al. 2005). Isolate
BERLANGA, ET AL.
273
Table 5. As(III)-tolerant and As(V)-tolerant bacteria isolated from the Laguna Madre sediment. The 16S rRNA genes from the isolates were amplified by PCR, sequenced, and compared to other known bacteria using the BLASTN search engine and data-base. The isolates were matched to the highest percentage match. The top BLASTN matches and the percent sequence match are shown.
|
Isolate |
Sediment Source |
Best Match |
Percent Match |
|
AS3-E |
South Bay |
Mycoplasma hyopneumoniae |
100 |
|
AS3-K |
South Bay |
Salinispora tropica CNB-440 |
92 |
|
AS5-B |
ABC |
Frankia alni ACN14A |
100 |
|
AS5-E |
LMT-050 |
Pelodictyon luteolum |
95 |
AS5-B had high similarity with Frankia alni strain ACN14A which is a Gram-positive, nitrogen-fixing bacterium that can live symbiotically with some non-legume plants (Atlas & Bartha 1998; Normand et al. 2007.). Isolate AS5-E showed similarity with Pelodictyon luteolum, a photosynthetic, green-sulfur bacterium (Overmann & Tuschak 1997).
Although the 16S rRNA gene sequencing resulted in a variety of potential matches, the identity of the organisms is yet to be conclusively determined. This is because the sequencing results do not agree with the morphological and physiological data for the isolates. For example, isolate AS3-E was observed to be a Gram¬ positive, rod-shaped bacterium [Table 3] and showed high identity with M. hyopneumoniae. Mycoplasma hyopneumoniae is related to low G+C Gram-positive organisms, it lacks a cell wall and is associated with a mild, chronic form of pneumonia that affects pigs (Atlas & Bartha 1998; Minion et al. 2004). However, mycoplasma cells are typically small, coccus-shaped cells with a convex dense region in the center sometimes referred to a “fried egg” appearance (see Madigan & Martinko 2005). Thus, the observed morphology of this isolate does not agree with what would be expected for a mycoplasma cell and it is unclear why a swine pathogen would be present in Laguna Madre sediments. Recent research has involved inserting arsenic resistance genes as genetic markers for the
274
THE TEXAS JOURNAL OF SCIENCE-VOL. 61, NO. 4, 2009
development of genetically-modified vaccines against Mycoplasma hyopneumoniae in infected swine (Matic 2008). What role this may play in arsenic tolerance is not yet known, especially for environmental strains of the bacterium.
Isolates AS5-B and AS3-K showed high similarity to F. alni and S. tropica, respectively. Organisms are Gram-positive, aerobic bacteria, which does agree with these observations [Table 3 & 4] yet these bacteria are typically filamentous and produce hyphae/mycelia when grown in laboratory media (Benson & Silvester 1993; Maldonado et ah 2005). This morphology was not observed for either isolate. The lack of agreement between the morphology and sequencing data may be due to PCR amplification of extraneous sequences or limited sequence information in the BLASTN database that did not allow for an ideal match. Thus, As(III)“tolerant and As(V)-tolerant isolates from the Laguna Madre appear to be diverse groups of yet unidentified microorganisms.
The results of this investigation provide insights into the potential for arsenic mobilization in the Lower Laguna Madre. Arsenic is carcinogenic and toxic, especially As(III); thus it is advantageous to have information into possible arsenic cycling in the Lower Laguna Madre due to recreational use of the lagoon and fisheries that occupy regions adjacent to the lagoon. The Laguna Madre is a rare hypersaline estuarine ecosystem, and it is important to ascertain whether arsenic and other contaminants are potentially harmful to the ecosystem. Arsenic was used as a pesticide for several decades and cannot be degraded like an organic pollutant; it can only be converted to different forms. Thus, once in the ecosystem, it will stay there in some manner. It is likely that the shallow water levels, low water flow, high evaporation rates, high salinity and pH of the Laguna Madre affect the concentration and speciation of the arsenic. To what extent is not yet known.
These results suggest that there is the potential for arsenic mobilization (i.e., reduction of As(V) to As(III)) in the Laguna
BERLANGA, ET AL.
275
Madre due to the presence of several different arsenic-tolerant bacterial types isolated under arsenic-reducing (As(V)) conditions. These organisms displayed different metabolic abilities and different biochemical profiles, suggesting that they are not the same species. Results of the 16S rRNA gene sequencing experiments support this. Furthermore, these organisms were isolated from several locations in the Lower Laguna Madre with varying environmental conditions, which suggests that they might be widespread in the ecosystem.
If there is the potential for As(V) reduction to As(III), it is important to consider how this may affect the arsenic toxicity in the Laguna Madre and how this in turn will affect the biota in the ecosystem. One would think that bacterial cells reducing As(V) to As(III) would be making a toxic environment for themselves and be affected by their own metabolic products. Why this does not appear to affect the bacterial cells is not known but it necessitates the involvement of some type of arsenic tolerance. It is possible that the produced As(III) may re-oxidize by chemical or biological means, or that the cells may have some mechanism of resisting the produced As(III). Some bacterial cells have arsenic resistance mechanisms such as efflux pumps that keep arsenic out of the cell (Newman et al. 1998). Such mechanisms were not tested for in the current study.
The presence of As(III)-tolerant bacteria in the lagoon implies a possible mechanism for counteracting the mobilization of arsenic if these As(III)-tolerant organisms can also oxidize As(III) to As(V). Future studies will include the determination of the relative abundance and density of As(III)-oxidizing and As(V)-reducing bacteria in the Laguna Madre, comparing arsenic oxidation and reduction at different sites, conducting seasonal studies on arsenic transformations in the Laguna Madre, and the detection of genes associated with arsenic oxidation and arsenic reduction (Saltikov & Newman 2003; Murphy & Saltikov 2007). Additionally arsenic
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THE TEXAS JOURNAL OF SCIENCE-VOL. 61, NO. 4, 2009
reduction rates can be conducted in the future to conclusively demonstrate arsenic mobilization in the Laguna Madre.
Acknowledgements
We wish to thank Hudson DeYoe, Thomas Whelan III and the UTPA Coastal Studies Lab for assistance in sample collection. Funding was supplied by the Howard Hughes Medical Institute Undergraduate Science Education Program Grant (#520006321), the NSF-Collaborative Research at Undergraduate Institutions (CRUI) Program, the Guerra Honors Program, and the Faculty Research Council at UTPA.
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Smedley, P. L. & D. G. Kinniburgh. 2002. A review of the source, behaviour and distribution of arsenic in natural waters. Appl Geochem., 17:517-568.
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KLL at: klowe@utpa.edu
TEXAS J. OF SCI. 61(4):279-294
NOVEMBER, 2009
DIVERSITY AND ABUNDANCE OF UNIONID MUSSELS IN THREE SANCTUARIES ON THE SABINE RIVER IN NORTHEAST TEXAS
NeD B. Ford, Jessica Gullett and Marsha E. May*
Department of Biology, University of Texas at Tyler Tyler, Texas 75799 and
^Wildlife Diversity Branch, Texas Parks and Wildlife Department 4200 Smith School Road, Austin, Texas 78744
Abstract.-Populations of freshwater mussels (Bivalvia: Unionidae) are declining for reasons that are primarily anthropogenic. The Texas Administrative Code lists 18 freshwater mussel sanctuaries (“no-take” areas) within Texas stream segments and reservoirs with three being on the Sabine River in northeast Texas. Visits to each Sabine River sanctuary were made multiple times between April and September 2007 with two goals: to establish species richness by locating rarer species not found in earlier surveys and to collect unionid data that could be used to evaluate abundances among the sanctuaries. Using timed and density surveys (0.25 meter square quadrats) 1596 individuals of 18 unionid species were recorded. Densities ranged from means of over 21 per meter square in one sanctuary to 3.6 per meter square in the sanctuary nearest the dam at Lake Tawakoni. Because a range of sizes were found for several species at the two downstream sanctuaries, recruitment evidently occurs. One of the healthiest unionid populations in these areas was Fusconaia askewi, which is a species of concern in the Texas Wildlife Action Plan. The mussel beds were found only in small, isolated patches in any sanctuary and silting over of beds with sand from bankfalls was evident throughout the river. Whether these sanctuaries will sustain all species within the upper Sabine River is questionable and it will be important to continue to monitor them.
It is increasingly evident that freshwater mussels (Bivalvia: Unionidae) are important components of riverine ecosystems (Christian & Berg 2000; Vaughn & Hakenkamp 2001; Howard & Cuffey 2006; Vaughn & Spooner 2006). Unionids have historically dominated lotic environments of the southeastern United States in terms of benthic biomass (Parmalee & Bogan 1998) and in undisturbed rivers may exceed other assemblages by an order of magnitude (Stray er et al. 1994). With the greatest diversity in the world, the continental United States supported nearly 300 species of unionid mussels (Neves 1993; Turgeon et al. 1998). However, their sedentary, slow-growing and long-lived (many > 25 years) life histories plus early parasitic phase usually requiring a host fish (Kat
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THE TEXAS JOURNAL OF SCIENCE-VOL. 61, NO. 4, 2009
1984; Watters 1994; Vaughn & Taylor 2000) has made them highly susceptible to human impacts such as wetland drainage, channeli¬ zation, sedimentation, dredging, pollution, invasive species and impoundments (Vaughn & Taylor 1999; Howells et al. 2000; Lydeard et al. 2004). The decline of North American unionid populations has been occurring for over a century (Neves et al. 1997; Vaughn 1997) with the extinction of at least 35 species and up to 65% imperiled to some degree (Turgeon et al. 1998). For many states, including Texas, the extent of freshwater mussel decline is simply not known (Bogan 1993; Layzer et al. 1993; Neves 1993).
At least 52 species of unionids occur in Texas and yet our understanding of their conservation status is quite limited (Howells et al. 1996; 1997). Although specific data are not available, it seems likely that East Texas unionid populations have declined at least equivalent to unionids in the other regions (Neck 1986; Howells 1997; Bordelon & Harrel 2004; Ford & Nicholson 2006). The human population of the region has been growing rapidly with dramatically increasing demands on its water resources, as illustrated by the 31 large reservoirs on its rivers (Ford & Nicholson 2006). Most of the rivers of eastern Texas are isolated from each other and many drain independently into the Gulf of Mexico. For example, the Sabine River begins in North-Central Texas in Hunt, Rains and Van Zandt counties and flows southeasterly first to a large reservoir on the border with Louisiana, Toledo Bend Lake, then ends in Sabine Lake, an estuary of the Gulf of Mexico. Additionally, one reservoir was built at the headwaters of the river. Lake Tawakoni, and a second, Lake Fork, is located in Wood, Rains and Hopkins counties and contributes much initial flow to the river through Lake Fork Creek. These two reservoirs have likely changed the river downstream both in flow patterns and geomorphology (Ford & Nicholson 2007). The only recent published surveys of mussels from the Sabine River drainage are for Lake Tawakoni (Neck 1986), a study on the Old Sabine Bottom Wildlife Management Area, which has the Sabine River as its
FORD, GULLETT & MAY
281
northern border (Ford & Nicholson 2006) and a number of unpublished Texas Parks and Wildlife Department (TPWD) surveys
(summarized in Howells 1997; 2006).
Mussel harvesting in Texas has occurred for over one hundred years, however, the intense overharvesting that occurred in the Mississippi Valley apparently did not occur in Texas (Howells et al. 1996). Although harvesting permits were required, little effort to monitor the mussel-harvesting was implemented until the increasing demand from the cultured pearl industry for American mussel shell begin in the late 1970s. In 1992, the Texas Administrative Code listed 28 freshwater mussel sanctuaries within Texas stream segments and reservoirs, but in 2006, Rule 57.157 reduced the number to 18 (Fig. 1). Harvesting is not permitted in these "no-take" areas with the intention that they will provide adult unionids producing glochidia for dispersal by fish hosts to non¬ protected areas.
Three of the sanctuaries occur on the Sabine River in Northeast Texas. Texas Parks and Wildlife Department conducted some limited surveys at the bridge crossings of these sanctuaries in 1993 (Howells 1995) and 1994 (Howells 1995; 1996a; 1996b) and again in 2005 and 2006 (Howells 2006). The goal of this study was to survey unionid mussels throughout the full extent of each sanctuary to establish total species richness for each and to collect data that could be used to evaluate densities of mussels within each sanctuary.
Materials and Methods
Study areas first sanctuary directly below Lake Tawakoni (hereafter called Lake Tawakoni Sanctuary) begins at the dam at Lake Tawakoni and ends downstream at State Highway 19 in Rains and Van Zandt counties. The riverbed from the dam to Highway 19 was obviously heavily impacted by scouring that occurred during high water releases. Daily discharges in this section of the river ranged from lows of 5 cfs (cubic feet per second) to high releases of
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THE TEXAS JOURNAL OF SCIENCE-VOL. 61, NO. 4, 2009
Fig. 1. Texas Mussel Sanctuaries (Texas Administrative Code Title 31, part 2, Ch. 57, subch. B, rule 57.157); A. Big Cypress Creek in Camp County; Bl. Sabine River in Rains and Van Zandt counties; B2. Sabine River in Smith, Upshur and Wood counties; B3. Sabine River in Harrison and Panola counties; C. Angelina River in Angelina, Cherokee, Jasper, Nacogdoches, Rusk, San Augustine, and Tyler counties; D. Neches River in Hardin, Jasper, Orange and Tyler counties; E. Trinity River in Houston, Leon Madison, Trinity and Walker counties; F. Live Oak Creek in Gillespie County; G. Brazos River in Palo Pinto and Parker counties; H. Guadalupe River in Kerr County; 1. Concho River in Concho County; J. San Saba River in Menard County; K. Guadalupe River in Gonzales County; L. San Marcos River in Hays, Guadalupe and Gonzales counties; M. Pine Creek in Lamar and Red River counties; N. Sanders Creek in Fannin and Lamar counties; O. Elm Creek in Runnels and Taylor counties; P. Rio Grande in Webb County.
FORD, GULLET! & MAY
283
over 7000 cfs in just one day (United States Geological Survey [USGS] 2007). The initial first km is channelized and deep. The rest consists of mud and silty substratum with large amounts of detritus and nonorganic trash (plastic and styrofoam).
The second sanctuary below the bridge at Highway 14 (hereafter called Highway 14 Sanctuary) is located from Farm to Market Road 14 to State Highway 155 in Smith, Upshur and Wood counties. In this section, the river was relatively wide (20-30 m at low water) and so a number of shallow sites with mussels and shells were evident. Some exposure of rocky outcrops of Cretaceous origin occurred with areas of small cobble. However, a large percentage of the sanctuary had severe erosion of the steep riverbanks, including numerous bankfalls. Daily discharges in this section of the river ranged from a low of 45 cfs to a high of 18,500 cfs in the year of the study (USGS 2007). This part of the river normally experiences flooding several times in the winter but during the year of the survey the high flows occurred during midsummer.
The third sanctuary below the bridge at Highway 43 (hereafter Highway 43 Sanctuary) is located from State Highway 43 down¬ stream to U. S. Highway 59 in Harrison and Panola counties. The river in this section was also relatively shallow and wide. However, daily discharges in this section of the river were more dramatic and ranged from lows of 1 1 cfs to high releases of 20,400 cfs (USGS 2007). It also had some areas of bedrock and extremely large boulders. Few reaches of any length with smaller rocks and cobble were evident.
Sampling techniques sanctuary was surveyed multiple times between April and September 2007 using two methods. The total extent of each sanctuary was initially explored by kayaking during low water with reconnaissance for shells and stream characteristics appropriate for mussels such as current and the presence of cobble (Vaughn et al. 1997; Strayer et al. 1997; Strayer & Smith 2003). Five to seven sites spaced throughout the length of
284
THE TEXAS JOURNAL OF SCIENCE-VOL. 61, NO. 4, 2009
each sanctuary were sampled. At selected sites, timed surveys were conducted and in areas with adequate mussel numbers, density surveys were performed. Both methods are necessary as timed surveys are useM for locating rare species but cannot be used for statistical comparison between areas (Strayer & Smith 2003).
Timed surveys -VimQ searches were conducted by surveying a 100m stretch of the river visually and tactilely for live and recently dead mussels in shallow areas and along the banks. Each site was sampled for a total of one-person hour. All live unionids and shells that were complete with both valves were collected, identified and counted. Live specimens were returned to the river. One voucher of each species was retained in the University of Texas at Tyler collection and any questionable specimens were collected and sent to Robert Howells of TPWD for identification.
Density surveys -In timed survey sites where unionids were abundant (at least 12 per 1 person hour), nearby areas were sampled using 0.25 meter square quadrats to estimate density (expressed as mussels per square meter). A random plot design was used with three starting points (k) and a sample total of 10 quadrats (n) (Strayer & Smith 2003). An approximate width of river of 20 m (W) and 100 m for the reach sampled (L) was used. This produced a distance of three meters between samples. Two surveyors searched the substratum by hand and excavated all mussels to a depth of 15 cm until no more specimens were found. Both live and recently dead (complete with both valves) were identified and counted. Measurements of length, width and height were taken only on living unionids.
Data analysis -Ml individuals counted in the timed surveys were used to calculate a Shannon-Wiener species diversity (H* base e) and evenness (J') indices. Rank abundance was determined for unionids for both methods. A Jaccard’s Coefficient of Community was used to compare species similarity between sanctuaries for the timed surveys (Brower et al. 1997). Richness and densities were
FORD, GULLET! & MAY
285
m
0)
Q
CD
Q.
(f)
Quadrula verrucosa Fusconaia askewi Quadrula apiculata Lampsilis teres Truncilla truncata Potamilus purpuratus Quadrula mortoni Obliquaria reflexa Plectomerus dombeyanus Leptodea fragilis Megalonaias nervosa Pyganodon grandis Potamilus amphichaenus Arcidens confragosus Amblema plicata Lampsilis hydiana Lampsilis satura Anodonta suborbiculata
|
L. L L L ■ |
||||
|
□ Density ■ Timed |
||||
0 100 200 300 400 500 600
Number
Figure 2. Comparison of the number of unionid mussels collected at the three sanctuaries of the Sabine River by sampling technique. The species are ranked by their abundances in the timed surveys.
compared for the density surveys using a single classification nested ANOVA with the sanctuary and sites nested with sanctuary as effects to be tested (SYSTAT® 1 1 2004).
Results
Eighteen unionid species totaling 1596 individuals were found in the survey of 19 sites in the three sanctuaries on the Sabine River (Figure 2). Only one species, Anodonta suborbiculata, was found in this study that was not recorded in Howells' surveys of these sanctuaries (Table 1). In the timed survey all 18 unionid species were found (Table 2) whereas in the density survey only 15 were recorded (Table 3). Four species were abundant in both timed and density surveys (Fig. 2). These species were Quadrula verrucosa, Fusconaia askewi, Q. apiculata and Truncilla truncata. Several other species were abundant in the time surveys, but less so in the
286
THE TEXAS JOURNAL OF SCIENCE-VOL. 61, NO. 4, 2009
Table 1. Totals of unionids collected by various methods including visual examination, wading and snorkeling with hand collection recorded by the Texas Parks and Wildlife Department at three sanctuaries in the Sabine River. Collections occurred in 1993 and 1994 at the Lake Tawakoni sanctuary, in 1994 also at the Highway 14 sanctuary and in 1994, 1995 and twice in 2005 at the highway 43 sanctuary (Howells 1995; 1996a; 1996b; 2006).
|
Lake Tawakoni |
Highway 14 |
Highway 43 |
Total |
|
|
Fusconaia askewi |
0 |
0 |
88 |
88 |
|
Quadrula verrucosa |
0 |
0 |
74 |
74 |
|
Lamps il is teres |
3 |
0 |
63 |
66 |
|
Leptodea fragilis |
28 |
1 |
19 |
48 |
|
Quadrula mortoni |
0 |
0 |
47 |
47 |
|
Obliquaria reflexa |
0 |
0 |
37 |
37 |
|
Quadrula apiculata |
4 |
0 |
24 |
28 |
|
Potamilus purpuratus |
17 |
0 |
10 |
27 |
|
Potamilus amphichaenus |
1 |
0 |
11 |
12 |
|
Amblema plicata |
3 |
0 |
8 |
11 |
|
Plectomerus dombeyanus |
0 |
0 |
10 |
10 |
|
Truncilla truncata |
2 |
0 |
7 |
9 |
|
Lamps ills satura |
0 |
0 |
6 |
6 |
|
Pyganodon grandis |
6 |
0 |
0 |
6 |
|
Lamps ills hydiana |
0 |
0 |
5 |
5 |
|
Megalonaias nervosa |
1 |
0 |
4 |
5 |
|
Utterbackia imbecillis |
0 |
0 |
3 |
3 |
|
Arcidens confragosus |
0 |
1 |
1 |
2 |
|
Toxolasma texasiensis |
2 |
0 |
0 |
2 |
|
Total Number |
67 |
2 |
417 |
486 |
|
Species Richness |
10 |
2 |
17 |
19 |
density surveys. Timed surveys are generally more successful at locating rare species but tend to record more of the large species (Stray er et al. 1997; Vaughn et ah 1997). Seven species were relatively rare in both methods (Table 2 & 3). Measurements of live specimens found during the density survey are shown in Table 4. A few species, including Fusconaia askewi, exhibited a wide range of sizes in the Highway 14 and 43 Sanctuaries.
Jaccard's Coefficient of Community index indicated fewer species in common between the Lake Tawakoni Sanctuary and the other sanctuaries (CCj 14 vs. Tawakoni = 0.44%; CCj 43 vs.
FORD, GULLETT & MAY
287
Table 2. Totals of the species collected by the timed method at the three sanctuaries in the Sabine River.
|
Lake Tawakoni |
Hwy 14 |
Hwy 43 |
Total |
|
|
Quadrula verrucosa |
0 |
397 |
129 |
526 |
|
Fusconaia askewi |
0 |
169 |
154 |
323 |
|
Quadrula apiculata |
24 |
117 |
41 |
182 |
|
Lamp sills teres |
1 |
24 |
76 |
101 |
|
Truncilla truncata |
2 |
66 |
27 |
95 |
|
Potamilus purpuratus |
6 |
32 |
32 |
70 |
|
Quadrula mortoni |
0 |
11 |
56 |
67 |
|
Obliquaria reflexa |
0 |
39 |
26 |
65 |
|
Plectomerus dombeyanus |
0 |
17 |
22 |
39 |
|
Leptodea fragilis |
2 |
15 |
17 |
34 |
|
Megalonaias nervosa |
0 |
22 |
9 |
31 |
|
Pyganodon grandis |
13 |
1 |
1 |
15 |
|
Potamilus amphichaenus |
6 |
3 |
5 |
14 |
|
Arcidens confragosus |
0 |
8 |
4 |
12 |
|
Amblema plicata |
1 |
0 |
7 |
8 |
|
Lampsilis hydiana |
0 |
0 |
5 |
5 |
|
Lampsilis satura |
0 |
0 |
5 |
5 |
|
Anodonta suborbiculata |
1 |
0 |
3 |
4 |
|
Total number |
56 |
921 |
619 |
1596 |
|
Species richness |
9 |
14 |
18 |
18 |
|
Shannon diversity |
1.63 |
1.82 |
2.27 |
2.13 |
|
Evenness |
0.74 |
0.69 |
0.78 |
0.73 |
Tawakoni = 0.50%; CCj 14 vs. 43 = 0.78%). Lake Tawakoni Sanctuary had the fewest individuals and lowest species richness (Table 2). The highway 14 had the greatest number of individuals but the highway 43 sanctuary had the greatest richness (Table 2).
Densities of unionids were significantly different among all three sanctuaries (F = 7.93; df = 7,102; P < 0.0001). The density for Lake Tawakoni Sanctuary was the lowest, Highway 43 sanctuary a little higher and the Highway 14 sanctuary was the highest (Table 3).
Discussion
The Sabine River historically supported approximately 33 unionid species (Howells et al. 1996). Recent surveys have
288
THE TEXAS JOURNAL OF SCIENCE-VOL. 61, NO. 4, 2009
Table 3. Totals of the species collected by quadrate sampling method (for density measurement) at all three sanctuaries in the Sabine River.
|
Lake Tawakoni |
Hwy 14 |
Hwy 43 |
Total |
|
|
Truncilla truncata |
0 |
81 |
8 |
89 |
|
Quadrula apiculata |
5 |
61 |
11 |
77 |
|
Quadrula verrucosa |
0 |
51 |
7 |
58 |
|
Fusconaia askewi |
0 |
28 |
24 |
52 |
|
Obliquaria reflexa |
0 |
22 |
9 |
31 |
|
Quadrula mortoni |
0 |
2 |
12 |
14 |
|
Lampsilis teres |
0 |
2 |
9 |
11 |
|
Potamilus purpuratus |
1 |
7 |
1 |
9 |
|
Leptodea fragilis |
1 |
3 |
1 |
5 |
|
Plectomerus dombeyanus |
0 |
4 |
0 |
4 |
|
Pyganodon grandis |
1 |
2 |
0 |
3 |
|
Arcidens confragosus |
0 |
2 |
0 |
2 |
|
Megalonaias nervosa |
0 |
2 |
0 |
2 |
|
Potamilus amphichaenus |
1 |
0 |
1 |
2 |
|
Amblema plicata |
0 |
1 |
0 |
1 |
|
Number |
9 |
268 |
83 |
360 |
|
Mean per square meter |
3.60 |
21.44 |
7.60 |
|
|
Standard error |
1.64 |
3.56 |
1.08 |
|
|
Species richness |
5 |
14 |
10 |
15 |
recorded only a portion of those (Neck 1986; Ford & Nicholson 2006; Howells 1997; 2006). Ford & Nicholson's (2006) study on the Old Sabine Bottom Wildlife Management Area (OSBWMA) used timed searches and found 13 unionid species in that limited section of the Sabine River. The major substratum was sand and clay, neither of which are stable habitats for unionids and may explain the lower richness at the OSBWMA. The TPWD surveys involved visual, tactile and some snorkeling searches at the bridges bordering these sanctuaries in 1993 (Howells 1995) and 1994 (Howells 1995; 1996a; 1996b) and again in 2005 and 2006 (Howells 2006). In those surveys, TPWD found 486 live and recently dead individuals of 19 species (Table 1). Nearly all these specimens were from the sanctuary furthest downstream at the bridges on Highways 43 and 59. The addition to the current survey of the two species (Utterbackia imbecillis and Toxolasma texasiensis) that TPWD recorded in their surveys means that the
FORD, GULLETT & MAY
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Table 4. Measurements on live unionids collected during density surveys in the three sanctuaries in the Sabine River. Mean Length and Standard Deviation given with the Range in parenthesis.
LakeTawakoni Hwy 14 Hw>'43
290
THE TEXAS JOURNAL OF SCIENCE-VOL. 61, NO. 4, 2009
mussel fauna of the sanctuaries of the Sabine River currently exhibits 69.7% of the total species that historically occurred in the Sabine River.
It appears that, as in other east Texas rivers, anthropogenic impacts are likely reducing unionid diversity and abundance in the upper Sabine River. Near the dam at Lake Tawakoni the scouring impact of high water releases on the river substrate was very evident. The substrate was silt and sand, with only one very small site (30 m) of cobble where a few unionids were found. Further downstream, the riverbanks were relatively low and erosion was not evident but debris from the reservoir was abundant. The most apparent factor that could be impacting the mussels in other two sanctuaries was erosion. The Highway 14 Sanctuary had a number of shallow reaches with cobble, which produced riffles where live unionids were abundant. This sanctuary also had steep banks and surrounding agricultural land often came adjacent to the river. A number of recent bankfalls, which released large amounts of sand downstream were evident. Highway 43 Sanctuary was also shallow and wide, but had areas with extremely large boulders and little cobble. Mussels were not found in reaches with solid bedrock. The greatest densities were found just downstream of the bridge at Highway 43, which had stable geomorphology but where smaller rocks and cobble were present. During the time of this survey, construction was occurring near the bridge that released sand into the river. Then a rare summer flood occurred, which shifted the sand downstream covering much of one of the study sites.
Timed surveys can be used to examine species richness and ranked species abundances and the unionids in the sanctuaries were comparable to recent surveys in other east Texas rivers (Howells et al 2000; Bordelon & Harrel 2004). As is typical of unionid diversity studies, the rank abundance curve exhibited a few very abundant species with several intermediately abundant species and a large number of rare species (Fig. 2). The highest density of unionids of over 21 per square meter was found in the Highway 14
FORD, GULLETT & MAY
291
Sanctuary (Table 2). This density compares favorably to those in Little River (17 unionids per square meter) and the Kiamichi river (20 unionids per square meter) in southeastern Oklahoma (Vaughn & Spooner 2004). However, it is important to point out that these sites in the Sabine River were chosen particularly due to the presence of abundant unionids. Observations made during this study were that such optimal sites were relatively limited in each sanctuary. Indeed, there was significant variation among sanctuary mussel density. The Highway 43 Sanctuary had a mean density of only 7.6 unionids per square meter and the Lake Tawakoni Sanctuary had a much lower mean density of 3.6 unionids per square meter.
It does appear that recruitment of young is occurring in both Highway 14 and Highway 43 Sanctuaries since a range of sizes were found for several species (Table 4). One of the healthiest populations was Fusconaia askewi, which is a species of concern in the Texas Wildlife Action Plan (TPWD 2006). This population had very large individuals as well as very small specimens.
Unionid beds were found only in the sanctuaries below Highway 14 and 43 with only one very small area in the Lake Tawakoni Sanctuary with enough mussels to do a density survey. Although some of these beds in the downstream sanctuaries appeared to have significant numbers of unionids, it is evident that the beds do not extend for any length but rather are very sporadic. From limited observations made elsewhere and the literature (Neck 1986; Ford & Nicholson 2006; Howells 1997; 2006), it is likely that this pattern is true throughout the extent of the upper Sabine River. To understand the species composition as is exists today in the sanctuaries would require a landscape level approach detailing the various habitats that support the different species of unionids.
The impact of high water releases on erosion of the banks and covering of beds with sand was obviously a problem for these unionid populations. This was most evident by the lowest density
292
THE TEXAS JOURNAL OF SCIENCE-VOL. 61, NO. 4, 2009
of mussel occurring in the sanctuary near the dam. Even though this area had less erosion of banks (probably because bank-fiill level was relatively low and water likely spread over the surrounding wetlands), there were no mussels in most of the samples. The scouring effect of high water releases is known to impact mussels near reservoirs. Recruitment of mussels from this sanctuary is probably limited and it is unlikely that the small areas of dense mussels in the other sanctuaries will sustain all species within the upper Sabine River. It will be important to monitor these sanctuaries in the future.
Acknowledgements
We thank TPWD for the State Wildlife Grant supporting this research. We thank David Kimberly and Daymon Hail for field assistance. We also thank Robert G. Howells (TPWD - currently BioStudies, Kerrville, Texas) and Lyubov E. Burlakova for confirming species identifications, and Robert Howells and Matt Troia for reviewing a draft of this paper. Voucher specimens have been deposited at the University of Texas at Tyler invertebrate collection.
Literature Cited
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Howells, R. G. 1997. Status of freshwater mussels (Bivalvia: Unionidae) of the Big Thicket Region of eastern Texas. Texas J. Sci., 49 supplement:21-34.
Howells, R. G. 2006. Statewide freshwater mussel survey. Final report as required by State Wildlife Grants Program Texas Federal Aid Project. Inland Fisheries Division, Texas Parks and Wildlife Department, Austin, 107 pp.
Howells, R. G., C. M. Mather & J. A. M. Bergmann. 1997. Conservation status of selected freshwater mussels in Texas. Pp. 117-127, in K. W. Cummings, A. C. Buchanan, C. A. Mayer & T. J. Naimo (ed.). Conservation and Management of Freshwater Mussels II, Proceedings of a UMRC Symposium, Rock Island, Illinois, 293 pp.
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Howells, R. G., R. W. Neck & H. D. Murray. 1996. Freshwater mussels of Texas.
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Layzer, J. B., M. E. Gordon & R. M Anderson. 1993. Mussels: the forgotten fauna of regulated rivers: a case study of the Caney Fork River. Regul. River, 8:63-71. Lydeard, C., R. H. Cowie, W. F. Ponder, A. E. Bogan, P. Bouchet, S. A. Clark, K. S. Cummings, T. J. Frest, O. Gargominy, D. G. Herbert, R. Hershler, K. E. Perez, B. Roth, M. Seddon, E. E. Strong & F. G. Thompson. 2004. The global decline of nonmarine mollusks. Biol. Sci., 54:321-330.
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Turgeon, D. D., J. F. Quinn, Jr., A. E. Bogan, E. V. Coan, F. G. Hochberg, W. G. Lyons, P. M. Mikkelsen, R. J. Neves, C. F. E. Roper, G. Rosenberg, B. Roth, A. Scheltema, F. G. Thompson, M. Vecchione & J. D. Williams. 1998. Common and Scientific Names of Aquatic Invertebrates from the United States and Canada: Mollusks, 2"^ Edition. American Fisheries Society, Special Publication 26, Bethseda, Maryland, 526 pp.
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NBF at: Neil_Ford@uttyler.edu
TEXAS J. OF SCI. 61(4):295-310
NOVEMBER, 2009
MORNING AND EVENING DENSITIES OF WHITE- WINGED AND MOURNING DOVES IN THE LOWER RIO GRANDE VALLEY, TEXAS
Michael F. Small, Margaret L. Collins, John T. Baccus and Steven J. Benn*
Department of Biology, Wildlife Ecology Program Texas State University-San Marcos, San Marcos, Texas 78666 and ^Texas Parks and Wildlife Department,
Weslaco, Texas 78596
Abstract.-This study evaluated post-nesting, pre-hunting season densities of eastern white-winged (Zenaida asiatica asiatica) and mourning doves (Z macrourd) based on morning versus evening distance sampling in south Texas. Probability of detection curves did not differ by diel period within species. White-winged dove density estimates were significantly greater in the evening compared to the morning (0.97 doves/ha, 95% Cl: 0.65-1.44 morning and 2.09 doves/ha, 95% Cl: 1.53-2.86 evening). Morning dove densities did not differ by diel period. Analysis of the raw data suggests the disparity in white-winged dove density estimates is most likely attributable to pre-sunrise activity by white-winged doves causing lower morning counts.
Historically, the lower Rio Grande Valley (LRGV) of Texas was the only area in Texas where eastern white- winged doves {Zenaida asiatica asiatica) and mourning doves (Z. macroura) exhibited sympatry. Although mourning doves are generally cosmopolitan in Texas (Haskett & Sayre 1993), the breeding range of eastern white¬ winged doves was originally restricted to the LRGV at the southern tip of the state (Schwertner et al. 2002; Small et al. 2006). However, beginning about 1920, industrialized farming and municipal development led to an estimated overall loss of white¬ winged dove breeding habitat exceeding 90% (Purdy & Tomlinson 1991; Tremblay et al. 2005).
Following this habitat loss, and possibly associated with it, white-winged doves began expanding northward, forming urban populations. This range expansion continued, peaking sometime in the late 1970s to present (Small et al. 2006). As of 1990, more breeding white-winged doves occurred outside the LRGV than within it (George et al. 1990). During this same period, mourning
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dove distribution remained essentially unchanged in Texas (Otis et al 2008).
Because both dove species are migratory game birds, they are monitored annually. Mourning doves are monitored as part of national call-count and breeding bird surveys. The Texas Parks and Wildlife Department (TPWD) has monitored white- winged doves in the LRGV since about 1949 using an auditory-count index. This auditory-count index involves counting calling white-winged doves and using a conversion table to estimate the breeding-pair density (Rappole & Waggerman 1986). However, how and when the conversion table was developed is unknown; rendering the results spurious, except to establish trends (Sepulveda et al. 2006).
To remedy this, and following pilot studies in 2004 and 2005, TPWD implemented distance sampling to estimate the size of urban white-winged dove populations statewide. However, the remaining traditional rural, nesting habitat in south Texas is still occupied by white-winged doves, but monitoring of these populations has been suspended by TPWD. Distance sampling of urban white-winged dove populations in Texas is conducted only in the early morning, when it is believed detection rates are highest. Yet Small (2006) found evenings were just as effective as mornings in sampling white-winged dove populations in Mason, (Mason County) Texas.
Monitoring of urban white- winged dove populations in Texas is conducted annually between 15 May and 15 June. Therefore, these densities effectively estimate potentially breeding adults. To estimate individuals available for harvest during the hunting season, some measure of productivity is needed in addition to the number of potentially breeding adults.
The objectives of this study were to determine: (1) if using point transects in distance sampling are effective for simultaneously estimating white-winged and mourning dove densities in native brush of the LRGV during the post-breeding/pre-hunting season; and (2) if morning and evening distance sampling yielded the same
SMALL ET AL.
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density estimates for either white-winged or mourning doves or both.
The reasoning for these objectives was to evaluate whether using the covariate “species” in the multiple covariate distance sampling (MCDS) engine of Program DISTANCE (Thomas et al. 2006) would provide similar probability of detection curves from a single model for each diel sampling period by species. Also, if the probability of detection curves proved to be similar, as was anticipated, would density estimates derived for each diel period be similar; thus, indicating populations sampled in mornings versus evenings were sufficiently closed to produce reliable population estimates.
Methods
Study area -This study was conducted at the Anacua Unit of the Las Palomas Wildlife Management Area (Lat 26°03T7.2", Long 97°50'46.15") between Santa Maria, Texas and the U.S. -Mexico border (Cameron County). The Anacua Unit consists of 92.1 ha of riparian and upland native brush habitat interspersed with three fallow fields from north to south. Vegetation is dominated by Texas ebony (Pithecellobium ebano), anacua (Ehretia anacua), retama {Parkinsonia aculeate), and mesquite {Prosopis glandulosa) (Jahrsdoerfer & Leslie 1988). It is bordered by agricultural fields separated by dirt roads and bisected from east to west by a flood control levee.
Assumptions of distance sampling-Voini transect distance sampling requires that three primary assumptions be met to obtain unbiased density estimates (Buckland et al. 2001). These assumptions are: (1) objects on the point are detected with certainty (i.e., g(0) =1); (2) objects are detected at their initial location; and (3) measurements of distances to objects are exact. Protocol for this study emphasized visually scanning each point upon approach and then scanning outward from the point. Consequently, individuals on the point did not go undetected. In instances when a dove was observed on or near the point but moved in response to
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the approach of the observer, the distance from the point to the location of the dove prior to movement was recorded. All points were clearly marked and visible to the observer from a distance sufficient to determine the position of doves prior to movement in response to observer approach. Thus, assumption one was not violated.
For assumption two, movements prior to or during the observation period were random with respect to the observer and assumption two was considered met (Tumock & Quinn 1991; Buckland & Tumock 1992; Buckland et al. 2001). Lastly, assumption three, requiring accurate measurement of distances to detected doves, was not violated. All observers used laser range finders which recorded distances to the nearest meter. No guesses of distance were made for any observations.
Sampling protocol -A satellite photograph of the study area was imported into ArcGIS version 9.2 (Environmental Systems Research Institute, Inc., Redlands, CA, USA). A polyline layer was drawn along dirt roads surrounding the Anacua Unit, the outside edge of fallow fields, and along the levee traversing the area. Five sets of 20 points (100 total points) were randomly generated along the polyline. A random number generator was then used to shuffle each of the five sets of 20 points.
Two observers trained in distance sampling of doves conducted two sets of point transects from 31 My-4 August and 10- 14 August 2008. Each sampling period consisted of the 100 randomly chosen points. Because an entire sampling period of 100 points could not be completely sampled within a morning or evening period (2 h), each transect was conducted on five consecutive days (20 points/day). Previous experience indicated that 20 points could be sampled within < 2 h. Because of heavy precipitation during the second sampling period on the evening of 13 August, only 4 points could be accessed per observer. As a result, the first survey consisted of 100 points and the second survey consisted of 88 points.
SMALL ET AL.
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On each day, the 20-point subsets were divided between the two observers, with each observer surveying the same points in the morning and evening. One observer surveyed the first 10 points, while the second observer simultaneously surveyed the remaining 10 points. The sequence of the points was randomized each day to avoid points in close proximity being sampled consecutively. The same 100 points were used for both 5-day sampling periods but observers switched points between transects; i.e., observer one for transect one became observer two for transect two and vice versa. Consequently, neither observer visited the same points while conducting the second sampling period that they surveyed during the first sampling period.
Observers conducted surveys concurrently beginning about 15 min after official sunrise and completing surveys no later than 2 h post-sunrise. Each day, transect surveys were duplicated in the evenings beginning no earlier than 2 h pre-sunset and completed no later than 15 min pre-sunset. Transect points were visited in the same sequence in the evening as in the morning. Survey protocol followed Schwertner & Johnson (2005). Each point was visited for a 2-min period and distances to all white-winged and mourning doves observed were recorded to the nearest meter using a Bushnell™ Yardage Pro Legend laser range-finder (Bushnell, Inc., Overland Park, KS, USA). For this study, only visual detections were used; auditory detections were not recorded.
Data analysis were analyzed in program DISTANCE (Thomas et al. 2006) using the MCDS engine because two covariates were of interest; time of day (morning and evening) at the stratum level and species (white-winged dove and mourning dove) as an added covariate. The two trials were pooled to ensure adequate numbers of observations were available for analysis at the covariate levels (Marquez & Buckland 2004; Marquez et al. 2007). Data were combined for both observers because Program DISTANCE uses detection models that are pooling robust and because the covariates of interest were time of day (morning versus evening) and species (white- winged dove versus mourning dove).
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The two sample periods were pooled into a single point transect to maximize numbers of observations available for analysis at the covariate levels (Marquez & Buckland 2004; Marquez et al. 2007). Although the conventional distance sampling (CDS) engine allows for a single covariate (at the stratum level), separate runs would have to be made for the additional covariate (Buckland et al. 2001). Probability of detection fiinction curves within species was compared using a Kolmogorov-Smimov test.
The advantage of the MCDS engine over the CDS engine for this study was that a single truncation point and a single detection model could be used. This affords greater precision in density estimates via smaller 95% confidence intervals (CIs), In addition, use of the MCDS engine provides output data that allows calculation of a scaling parameter (5) which is then used to plot the probability of detection curves at the co variate level. Evaluation of these curves in relation to each other allows assessment of the validity of the covariates (Marquez et al. 2007).
Initially, five candidate models from the MCDS engine were run using all data (no truncation) with no covariates and restricted to no more than two adjustment terms. The Akaike Information Criterion (AIC) was used to select the most parsimonious model for estimating population density (Burnham & Anderson 2003), Using the most parsimonious model, a likely truncation point was chosen based on diagnostic output from Program DISTANCE. Once identified, data were run again with a single covariate (species) and using various truncation points around the original choice until the data satisfactorily fit the probability of detection curve both visually and statistically; using the Komolgorov-Smimov test P-value calculated by DISTANCE.
Output from Program DISTANCE, using the most parsimonious model (that with the lowest AIC value), was then used to determine scale parameters (s) which were used to model probability of detection curves for each species by morning and evening. Program DISTANCE was then run to calculate population density
SMALL ET AL.
301
estimates for each species by time of day with corresponding 95% confidence intervals.
As a further evaluation of morning versus evening sampling, raw data obtained from each sampling period were examined. Paired t- tests were used to compare daily differences in number of individuals, number of observations (clusters), and mean cluster size between morning and evening sampling for each species. Also, scatter plots of number of doves seen each minute post¬ sunrise and pre-sunset were generated for each species. If any plot showed a pattern of increasing values at either end of the plot, these data were grouped into 10 min intervals and regressed against number of individuals seen.
Results
From the pool of 100 randomly placed points, 188 point surveys were conducted. A total of 105 and 108 individual mourning doves were recorded across 78 and 84 observations made during morning and evening sampling, respectively; this compared to 815 and 1,346 individual white- winged doves across 207 and 357 observations, respectively.
The most parsimonious model selected by Program DISTANCE was a half-normal with a cosine key function and one expansion term of order two {D = 0.03, P = 0.74) with data truncated at 160 m. Probability of detection functions constructed from these data were extremely similar between species and nearly identical within species for morning and evening sample periods (D = 0.12, P = 0.16 for both species. Fig. 1). However, the density estimate was significantly higher for evening sampling than for morning sampling for white-winged doves (0.97 doves/ha, 95% Cl: 0.65- 1.44 morning and 2.09 doves/ha, 95% Cl: 1.53-2.86 evening. Fig. 2), Estimates did not differ for mourning doves (0.38 doves/ha, 95% Cl: 0.24-0.59 morning and 0.53 doves/ha, 95% Cl: 0.35-0.80 evening. Fig. 2).
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THE TEXAS JOURNAL OF SCIENCE, VOL. 61, NO. 4, 2009
a.
Distance (m)
-WWD-M
-WWD-E
b.
-MODaM
-MODO-E
Figure 1. Probability of detection curves for (a) white- winged doves sampled in the morning (WWD-M) and the evening (WWD-E) and for (b) mourning doves sampled in the morning (MODO-M) and the evening (MODO-E).
For white- winged doves, total number of doves observed and total number of observations (clusters) were higher during evening sampling = -2.62, P = 0.03 and = -5.36, P < 0.01, respective¬ ly). Mean white- winged dove cluster size per day did not differ between morning and evening sampling (fg = 0.04, P = 0.97). For mourning doves, total number of doves observed, total number of
SMALL ET AL.
303
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Figure 2. Density estimates and 95% confidence intervals for white-winged and mourning doves sampled in mornings and evenings.
observations (clusters), and mean cluster size per day did not differ between morning and evening sampling (tg = -0.23, P = 0.82, /g = - 0.72, P = 0.49, and tg = 0.24, P = 0.81, respectively). Evaluation of scatter plots showed only white-winged doves sampled in the morning had substantially more individuals seen closer to sunrise. Regression of number of white- winged doves over 10 min intervals (the last interval was only 8 min) post-sunrise showed a strongly
'j
significant negative relationship (r = 0.81, P < 0.01, Fig. 3).
These results are consistent with counts of daily data. White¬ winged doves had higher counts during evenings than mornings for number of individuals (7 of 10 days) and number of clusters observed (9 of 10 days, 1 equal). Mean daily cluster size differ-
304 THE TEXAS JOURNAL OF SCIENCE, VOL. 61, NO. 4, 2009
a.
Minutes post-siinrise
Figure 3. (a) Scatter plot of white- winged doves seen by minute post-surrise and (b) regression of white-winged doves seen over 10 min intervals.
ences were equal, each diel period having 5 days with higher values. For mourning doves, number of individuals and number of
SMALL ET AL.
305
clusters was similar in the mornings and evenings with evenings having higher values on 4 of 10 days, 2 equal and 5 of 10 days, respectively. Evening counts of mean cluster size were higher on 6 of 10 days (Fig. 4).
Discussion
This study had a narrow time window for completion. Because doves commonly nest more than once (often late in the breeding season), initiate fall feeding flights, and exhibit some variability in migration, there was only about a four-week, post-nesting, pre¬ hunting season period of time to complete this study. Also, on 23 July, category III Hurricane Dolly hit the Texas coast about 90 km east of the study site. Doves may have scattered, or left the area entirely, as a result of effects of Hurricane Dolly, resulting in lower than normal density estimates
Significantly different density estimates by diel period for white¬ winged doves, specifically, a higher evening density estimate compared to morning, suggest morning and evening populations were not comprised of the same individuals; the population was not closed. Although some of the individuals present may have remained constant, the proportion is unclear. Further, these results do not preclude the use of morning and evening distance sampling for determining white-winged dove density during other times of the year.
The most plausible explanation for this discrepancy is that white-winged doves began leaving roosts prior to or at sunrise and were consequently unavailable for counting because of lack of available daylight. This conclusion is supported by the number of white-winged doves seen relative to time (Fig. 3). White-winged doves are considered diurnal (Schwertner et al. 2002); thus, individuals moving between roosts at night seems highly improbable. However, they do exhibit some degree of crepuscular activity (Cottam & Trefethen 1968). It is assumed that, under this scenario, white-winged doves in the morning do not leave roosts at
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Figure 4. Daily values for (a) number of individuals, (b) number of observations, and (c) mean cluster size for white-winged doves sampled in die morning (WWD-Ld) and the evening (WWD-E) and for mourning doves sampled in the morning (MODO-M) and the evening (MODO-E).
the same time, but do so in a streaming fashion, beginning earlier than 15 min post-sunrise. If so, this count bias would account for
SMALL ET AL.
307
the differences in the number of white-winged doves seen in morning and evening samples. For evenings, white- winged doves returning to roosts may be more time-structured (i.e., occurs within a shorter time-frame and more consistently on a daily basis). A study of morning distance sampling with a starting time of 15 min pre-sunrise may alleviate differences found in this study between diel periods provided visibility is sufficient to count doves.
White-winged doves monitored by radio-telemetry in urban areas exhibited high site fidelity and structured home ranges centered on their nest (Small et al. 2005), Because this study was conducted during the post-breeding period and pre-hunting season, it is conceivable that white- winged doves do not retain the same site fidelity associated with nesting. Generally, post-nesting white¬ winged doves become gregarious in roosting, aggregate into large feeding flocks, and forage together to build energy reserves for the fall migration (Cottam & Trefethen 1968; Schwertner et al. 2002). Roosting in proximity to changing available food and water resources may contribute to a lack of site fidelity in white-winged doves and may also, at least partially, explain the high variation in daily morning and evening counts (Fig. 3).
Mourning doves, conversely, exhibited nearly identical density estimates for morning and evening surveys (Fig. 2) and very low daily variation in number of individuals, number of observations, and mean cluster size (Fig. 3). While this result does not definitively prove that the mourning dove population being sampled was closed, it provides strong support for this hypothesis. It also suggests that, pending further research, mourning doves can be sampled as reliably in the evening as in the morning.
This study indicates distinctly different behavior in post-nesting white-winged and mourning doves. Should fiirther study indicate these differences to be consistent over time, it may be beneficial to monitor the two species differently. Mourning doves are currently monitored annually as part of the federal mourning dove call-count
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survey conducted in late May and early June (Dolton 1993). The purpose of the call-count survey is to monitor relative abundance and population trends which are used to determine hunting seasons. However, this method is retroactive as opposed to adaptive. Analysis of previous trends elicits a response in future regulations as opposed to regulations influencing trends by using adaptive management models. Also, productivity, which is highly variable in mourning doves (Hayslette et al. 1996; 2000), is not measured. Only estimates of breeding adults are quantified, which may not be reflective of numbers of individuals available for harvest in a given year.
Based on this study, and pending future research, several recommendations can be made. First, the monitoring of urban white-winged doves using distance sampling should continue to occur at the onset of the breeding season in mid-May. However, white-winged dove monitoring should be expanded to include rural nesting populations and a nesting productivity monitoring initiative should be implemented to more accurately estimate doves available for harvest.
Secondly, further evaluation of post-nesting distance sampling of mourning doves should be implemented. If late summer sampling of mourning doves proves to provide accurate estimates of individuals available for harvest, consideration should be given to shifting the monitoring of mourning doves from late spring to late fall. Both of these suggestions have the potential for providing more precision in estimating population trends for both these game species while improving efficiency of human resources required for conducting these surveys.
Acknowledgments
Thanks to J. Veech for reviewing earlier drafts of this manuscript. J. Timmons was instrumental in data collection. This study was funded by the Texas Parks and Wildlife Department white-winged dove stamp fund.
SMALL ET AL.
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Dolton, D. D. 1993. The call-count survey: historic development and current procedures. Pp. 233-252, in Ecology and Management of the Mourning Dove (T. S. Baskett, M. W. Sayre, R. E. Tomlinson, & R. E. Mirarchi, eds.), Stackpole Books, Harrisburg, 608 pp.
George, R. R., E. Tomlinson, R. W. Engel-Wilson, G. L. Waggerman & A. G. Spratt. 1994. White-winged dove. Pp. 29-50, in Migratory, Shore and Upland Game Bird Management in North America (T. C. Tacha & C. E. Braun, eds.), Allen Press, Lawrence, 233 pp.
Hayslette, S. E., T. C. Tacha & G. L. Waggerman. 1996. Changes in white-winged dove reproduction in Southern Texas, 1954-93. J Wildl Manage, 60(2):298-301.
Hayslette, S. E., T. C. Tacha & G. L. Waggerman. 2000. Factors affecting white¬ winged, white-tipped, and mourning dove reproduction in Lower Rio Grande Valley. J Wildl Manage, 64(l):286-295.
Jahrsdoerfer, S. E. & D. M. Leslie. 1988. Tamaulipan brushland of the Lower Rio Grande Valley of South Texas: description, human impacts, and management options. United States Fish and Wildlife Service, Biological Report, 88:1-62.
Marques, T. A., L. Thomas, S. G. Fancy & S. T. Buckland. 2007. Improving estimates of bird density using multiple-covariate distance sampling. Auk, 124(4): 1229- 1243.
Marques, F. F. C. & S. T. Buckland. 2004. Covariate models for the detection function. Pages 31-47, in Advanced Distance Sampling (S. T. Buckland, D. R. Anderson, K. P. Burnham, J. L. Laake, D, L. Borchers, & L. Thomas., eds.), Oxford University Press, Oxford, 434 pp.
Otis, D. L., J. H. Schulz, D. Miller, R. E. Mirarchi & T. S. Baskett. 2008. Mourning dove (Zenaida macroura). The Birds of North America Online (A. Poole, ed.). Ithaca: Cornell Lab of Ornithology; Retrieved from the Birds of North America Online: http://bna.birds.comell.edU/bna/species/l 17. doi:10.2173/bna.l 17
Purdy, P. C. & R. E. Tomlinson. 1991. The eastern white-winged dove: factors influencing use and continuity of the resource. Pp. 225-265, in Neotropical Wildlife Use and Conservation. (J. G. Robinson & K. H. Redford, eds.). University of Chicago Press, Chicago, 538 pp.
Rappole, J. H. & G. L. Waggerman. 1986. Calling males as an index of density for breeding white-winged doves. Wildl Soc Bull, 14(1):151-155.
Schwertner, T. W. & K, Johnson. 2005. Using land cover to predict white-winged dove occurrence and relative density in the Edwards Plateau. Pp. 98-102, in Managing
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Wildlife in the Southwest: New Challenges for the 21st Century (J. W. Cain III & P. R. Krausman, eds.), Southwest Section of The Wildlife Society, Alpine, 142 pp.
Schwertner, T. W., H. A. Mathewson, J. A, Roberson, M. Small, & G. L. Waggerman. 2002. White-winged dove (Zenaida asiatica). in The Birds of North America. No. 710 (A. Poole & F. Gill, eds.). The Birds of North America, Inc., Philadelphia.
Sepulveda, M., F. Hernandez, D. G. Hewitt, W. P. Kuvlesky, G. Waggerman & R. L. Bingham. 2006. Evaluation of auditory counts for estimating breeding populations of white-winged doves. J Wildl Manage, 70(5): 1393-1402.
Small, M. F. 2007. Flow alteration of the lower Rio Grande and white-winged dove range expansion and monitoring techniques. Unpublished Ph.D. dissertation, Texas State University- San Marcos, San Marcos, 148 pp.
Small, M. F., J. T. Baccus & T. W. Schwertner. 2006. Historic and current distribution and abundance of white-winged doves {Zenaida asiatica) in the United States. Texas Omith Soc, Occasional Publ, 6:1-23 pp.
Small, M. F., C. L. Schaefer, J. T. Baccus & J. A. Roberson. 2005. Breeding ecology of white-winged doves in a recently colonized urban environment. Wilson Bull, 117(2):172-176.
Thomas, L., J. L. Laake, S. Strindberg, F. F. C. Marques, S. T. Buckland, D. L. Borchers, D. R. Anderson, K. P. Burnham, S. L. Hedley, J. H. Pollard, J. R. B. Bishop & T. A. Marques. 2006. Distance 5.0. Release 5, version 2. Research Unit for Wildlife Population Assessment, University of St. Andrews, UK. http://www.ruwpa.st- and.ac.uk/distance/
Tremblay, T. A., W. A. White & J. A. Raney. 2005. Native woodland loss during the mid 1900s in Cameron County, Texas. Southwest Nat, 50(4):479-482.
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MFS at: ms81@txstate.edu
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GENERAL NOTES
PREVALENCE OF HEMATOZOAN PARASITES (APICOMPLEXA) IN SOME COMMON PASSERINE BIRDS (PASSERIFORMES) FROM EAST-CENTRAL OKLAHOMA
Michael D. Bay and Kenneth D. Andrews
Department of Biology, East Central University Ada, Oklahoma 74820
Blood parasites (hematozoa) occur in the plasma {Trypanosoma) and within the blood cells {Plasmodium^ Leucocytozoon and Haemoproteus) of a number of avian species. Most of these infections are likely benign in wild birds (Bennett et al 1988; Weatherhead & Bennett 1991; 1992), and occasionally pathogenic during stressful times (Atkinson & Van Riper 1991; Weatherhead & Bennett 1991). Furthermore, parasites may have some influence on sexual selection (Hamilton & Zuk 1982; Zuk 1991); however, this has yet to be resolved (Weatherhead 1 990; Weatherhead et al 1991; Seutin 1994; Scheuerlein & Ricklefs 2004).
The distribution of blood parasites has been studied in many regions (e.g., Bernard & Bair 1 986 in Vermont; Rodriguez & Matta 2001 in Colombia), while other areas have been less well studied or not at all. Parasitism of Oklahoma birds has been investigated in only one previous instance (Janovy 1963), and few data exist concerning the levels of infection or types of parasites involved. In this study, the incidence of infection is detailed for four common passeriform species, and also the types of blood parasites involved and their intensities.
Methods and Materials
This study was conducted in Pontotoc, Murray and Okfiiskee counties of Oklahoma from May 2002 through August 2005. Since most hemosporidian infections are patent by early to mid-summer.
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this time frame is optimal in sampling infected hosts (Valkiunas 2001). All birds were captured using 30- and 38- mm mesh mist nets, and banded with U.S. Bird Banding Laboratory aluminum bands. All captured individuals were sexed and aged where possible, as well as measured and weighed. Blood samples were obtained from toenail clippings and smeared on slides. These samples were air dried, fixed with 100% methanol and then stained with Giemsa (Bennett 1970). All slides were examined at 400- lOOOX. Parasites were quantified by counting the number per 10,000 blood cells to obtain an estimate of parasite intensity (Godfrey et al. 1987). All blood smears were submitted as voucher specimens to the U.S. National Parasite Collection (accession numbers 100814- 100835), Beltsville Agricultural Research Center, 10300 Baltimore Avenue, Beltsville, Maryland 20705.
Results and Discussion
A total of 175 birds representing four species (49 Carolina Chickadees, Parus carolinensis, 55 House Sparrows, Passer domesticus, 37 Northern Cardinals, Cardinalis cardinalis and 34 House Finches, Carpodacus mexicanus) were examined. No significant difference (x, df= 3, P>0.05) between years in the prevalence of infection, was noted, permitting data to be pooled across years for each species. Overall prevalence of blood parasite infections was 12.5% for the total sample. Four blood parasites (identified to genus) were found ranging from a prevalence of 1.8 to 13.5% for the host species (Table 1), with Haemoproteus sp. being the most common (54.5% of those infected). Though the prevalence of parasites was low in the species sampled, they were significantly different (x^=17.3, df=3, P<0.001), possibly indicating some degree of susceptibility to vectors and/or differences in host resistance to infection. Although prevalence tends to vary from region to region, and from species to species, most studies report a low percentage of infection in passerine birds. For instance, Williams & Bennett (1978) found that 10.5% of Northern Cardinals
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Table L Prevalence (number infected / number examined, %) of blood parasites in four common bird species from east-central Oklahoma. HP= Haemoproteus; PL= Plasmodium', HG= Haemogregarina', LK= Leukocytozoon.
|
Parasite |
|||||
|
Host |
n |
HP |
PL |
HG |
LK |
|
Cardinalis cardinalis (Northern Cardinal) |
37 |
13.5% |
5.4% |
- |
2.7% |
|
Passer domesticus (House Sparrow) |
55 |
9.1% |
1.8% |
1.8% |
- |
|
Carpodacus mexicanus (House Finch) |
34 |
2.9% |
2.9% |
2.9% |
2.9% |
|
Parus caroUnensis (Carolina Chickadee) |
49 |
2.0% |
- |
2.0% |
2.0% |
(«=180) and 15,2% of House Sparrows {n=\ll), in New Jersey were infected, compared to 21% of cardinals and 12.7% of House Sparrows in this study. In contrast, Greiner et al (1975) found a higher percentage of cardinals were infected (42.9%), though prevalence findings for the House Finch and Carolina Chickadee were similar to this study (14.8% and 6.8% respectively). Studies by Bernard & Bair ( 1 986), Stabler & Kitzmiller (1970) and Al-Dabagh ( 1 964), also report a low infection prevalence in the House Sparrow, comparable to this study. The only other study conducted in Oklahoma (Janovy 1963) reported that only 5.8% of passerine birds («=102) were infected, although only the House Sparrow was common to this study.
Haemoproteus was the most frequent occurring parasite in this study as well as in the studies of passeriform birds in other regions (e.g., Williams & Bennett 1978 in New Jersey and Maryland; Bennett et al. 1991 in Mexico; Scheuerlein & Ricklefs 2004 in Europe), while Leucocytozoon was most prevalent in the studies of Stabler & Kitzmiller (1970) in Colorado, Bernard & Bair (1986) in Vermont, and Merino et al. (1997) in Spain. Janovy’s (1963) study in Oklahoma reports Haemoproteus was the most frequent parasite encountered, though most were from a non-passeriform bird, the Mourning Dove {Zenaidura macroura).
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The level of intensity (parasites per 10,000 blood cells) was low for all infected individuals, so it was not possible to determine if any pattern existed for each host species relative to the sampling period. Of the four parasites, Plasmodium spp. had the highest mean intensity in the Northern Cardinal (9.9%) and the House Sparrow (1.2%), followed by Haemoproteus spp (1.5%) and Leukocytozoon spp. (0.84%) in the House Finch. Haemogregarina spp. was detected in three of the four bird species sampled (except the Northern Cardinal) but had the lowest intensity (0.03% to 0.28).
The interpretation of parasitemia levels can be difficult, since they tend to vary considerably both temporally and spatially and may often be associated with considerable error in comparison to prevalence (McCurdy et al. 1998). Although the intensity levels of this study were low and too infrequent for analysis, it is important to report them here for comparison to future studies. Also, since parasites might be metabolically costly to birds, the body weights of infected individuals were compared to those that were not infected in three of the four host species (excluding Carolina Chickadee because of low infection). Since there are no gender difference in the body weights of males and females, the weights were combined in the analysis. For the Northern Cardinal and House Finch there was no significant difference in the mean body weights of those infected compared to those that were not (t=0.07, P>0.05 and t=1.47, P>0.05, respectively), however, in the House Sparrow, infected individuals had a higher mean body weight (t=2.71,P<0.01) (Table 2).
Assessing the effects of blood parasites on wild hosts is a difficult process and there is even some debate as to whether these parasites are pathogenic or not (Atkinson & Van Riper 1991). It is possible that some species are more resistant than others to a buildup of high levels of parasitemia. Some studies show that high parasite levels could affect working adults (feeding nestlings) (Merino et al. 2000), or possibly early aged individuals (hatchlings) or first year adults (Weatherhead & Bennett 1 992). In this study, the level of parasitemia was relatively low, and any pathogenic effects might be minimal. This
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Table 2. Body weights (X ± SE) of bird species, comparing infected individuals to those not infected from east-central, Oklahoma 2002-2005.
|
Host Species |
Infected |
n |
Uninfected |
n |
t |
P |
|
Northern Cardinal |
40.9 ± 6.4% |
8 |
41.4 ± 1.4% |
29 |
.07 |
>0.05 |
|
House Sparrow |
30.4 ± 6.9% |
7 |
27.6 ± 0.72% |
48 |
2.71 |
<0.01 |
|
House Finch |
20.3 ± 5.8% |
4 |
20.7 ± 0.68% |
30 |
1.47 |
>0.05 |
may explain why there was no difference in body weights between infected and uninfected individuals in three of the four species, although it is interesting that infected House Sparrows had a higher mean body weight in comparison to uninfected individuals. While some studies report little if any difference in body condition of infected and uninfected birds (e.g., Weatherhead & Bennett 1992), some do report a higher mean body weight in infected individuals as Bennett et al. (1988) found in the Black and White Warbler {Mniotilta varia) and Fox Sparrow {Passerella iliaca). Bennett et al. (1988) suggests that it is possible that blood parasites simply do not cause a loss of body mass, even in individuals with a high parasitemia. Also, given the small body mass of passerine species, changes due to parasite infection may be too small to distinguish from other natural occurring effects on body weight, such as foraging and breeding activities (Bennett et al. 1988).
Acknowledgments
Many thanks to Rick Davis for helping mist net birds and Tiffany Howell for inspecting slides and counting infected blood cells. This research was aided by a Federal Bird Banding Permit (U.S. Department of the Interior, Bird Banding Laboratory, Laurel, Maryland) issued to the senior author.
Literature Cited
Al-Dabagh, M. A. 1964. The incidence of blood parasites in wild and domestic birds of Columbus, Ohio. Am. Midi. Nat., 72:148-150.
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Atkinson, C.T. & C. Van Riper IIL 1991. Pathogenicity and epizootiology of avian haematozoa: Plasmodium, Leucocytozoon, and Haemoproteus. Pp 19-48 in Bird- parasite interactions (J.E. Loye and M. Zuk, eds), Oxford Univ. Press, 406pp.
Bennett, G. F. 1970. Simple techniques for making avian blood smears. Can. J. Zook, 48:585-586.
Bennett, G. F., J. R. Caines & M. A. Bishop. 1988. Influence of blood parasites on the body mass of passeriform birds. J. Wildl. Dis., 24:339-343.
Bennett, G. F., Aguirre, A. & R. S. Cook. 1991. Blood parasites of some birds from northeastern Mexico. J. ParasitoL, 77:38-41.
Bernard, W. H. & R. D. Bair 1986. Prevalence of avian hematozoa in central Vermont. J. Wildl. Dis., 22:365-374.
Godfrey, R. D., Fedynich, A. M. & D. B. Pence. 1987. Quantification of hematozoa in blood smears. J. Wildl. Dis., 23:558-565.
Greiner, E. C., Bennett, G. F. E. M. White & R. F. Coombs. 1975. Distribution of the avian hematozoa of North America. Can J. Zook, 53:1762-1787.
Hamilton, W. D. & M. Zuk. 1982. Heritable true fitness and bright birds: a role for parasites. Science, 218:384-387.
Janovy, J. 1 963 . A preliminary survey of blood parasites of Oklahoma birds. Proc. Okla. Acad. Sck, 43:59-61.
McCurdy, D.G., D.Shtler, A. Mullie & M.R. Forbes. 1998. Sex- biased parasitsm of avian hosts: relations to blood parasite taxon and mating system. Oikos, 82:303-3 12.
Merino, S., Potti, J. & J. A. Fargallo. 1997. Blood parasites of passerine birds from central Spain. J. Wildl. Dis., 33:638-641.
Merino, S., Morreno, J., J. J. Sanz & E. Arriero. 2000. Are avian blood parasites pathogenic in the wild? A medication experiment in blue tits {Parus caeruleus). Proc. R. Soc. Lond., 267:2507-2510.
Rodriguez, O. A. & N. E. Matta. 2001 . Blood parasites in some birds from eastern plains of Colombia. Mem. Inst. Oswaldo Cruz, 96:1 173-1 176.
Scheuerlein, A. & R. E. Ricklefs. 2004. Prevalence of blood parasites in European passeriform birds. Proc. R. Soc. Lond., B 271.
Seutin, G. 1994. Plumage redness in redpoll finches does not affect hemoparasitic infection. Oikos, 70:280-286.
Stabler, R. M. & N. Kitzmiller. 1970. Hematozoa from Colorado birds. III. Passeriformes. J. Parasit., 56:12-16.
Valkiunas, G. 2001. Blood parasites of birds: some obstacles in their use in ecological and evolutionary biology studies. Avian Ecok Behav., 7:87-100.
Weatherhead, P. J. 1 990. Secondary sexual traits, parasites and polygyny in Red winged Blackbirds. Behav. Ecok, 1:125-130.
Weatherhead, P. J. & G. F. Bennett. 1991. Ecology of Red winged Blackbird parasitism by haematozoa. Can. J. Zook, 69:2352-2359.
Weatherhead, P. J. Bennett, G. F., & D. Shutler. 1991 . Sexual selection and parasites in wood warblers. Auk, 108:147-152.
Weatherhead, P. J. & G. F. Bennett. 1992. Ecology of parasitism of Brown headed Cowbirds by haematozoa. Can J. Zook, 70:1-7.
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Williams, N. A. & G. F. Bennett. 1978. Hematozoa of some birds of New Jersey and Maryland. Can. J. Zool., 56:596-603.
Zuk, M. 1991. Parasites and bright birds: new data and a new prediction. Pp 3 1 7-327, in Bird-parasite interactions (J. E. Loye and M. Zuk, eds), Oxford Univ. Press, 406pp.
MDB at: mbay@ecok.edu
* * * * *
NOTES ON REPRODUCTION OF THE KNOB-SCALED LIZARD, XENOSAURUS GRANDIS (SQUAMATA: XENOSAURIDAE), FROM VERACRUZ, MEXICO
Stephen R. Goldberg
Department of Biology, Whittier College, PO Box 634 Whittier, California 90608
The knob-scaled lizard, Xenosaurus grandis is distributed as disjunct populations from west central Veracruz southward to Guerrero, Oaxaca and Chiapas, Mexico to Alta Verapaz, Guatemala (Ballinger et al. 2000a). It is viviparous (Ballinger et al. 2000b). Information on the reproduction of A. grandis is in Fritts (1966); Alvarez del Toro (1982); Ballinger et al. (2000b); Smith et al. (2000). The purpose of this note is to add information on the reproductive biology of X. grandis from the first histological examination of gonadal material from this species.
Eleven males (mean snout-vent length, SVL = 104.5 mm ± 12.5 SD, range = 83-120 mm); 27 females (mean SVL = 108.7 mm ± 12.3 SD, range = 87-133 mm); 3 juveniles (mean SVL 69.3 mm ± 8.1 SD, range = 62-78 mm) and one neonate (SVL = 42 mm) X. grandis collected from 1969 to 1983 at Cuautlapan (18°52’12”N, 97°r48”W), Veracruz, Mexico were examined from the herpetology collection of the Natural History Museum of Los
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Angeles County (LACM), Los Angeles, California.
The left testis, epididymis and left ovary were removed from males and females, respectively. Histology slides were prepared by conventional methods and stained by Harris hematoxylin and eosin (Presnell & Schreibman 1997). Oviductal eggs or enlarged ovarian follicles (> 4 mm length) were counted. Histology slides are deposited in LACM. An unpaired ^test was used to compare male and female mean body sizes, and linear regression analyses examined the relationship between female body size and clutch number (Instat vers. 3.0b, Graphpad Software, San Diego, CA).
The following Xenosaurus grandis specimens from Veracruz, Mexico were examined: LACM 5927, 10981, 75420, 75688, 75690, 75691,75694, 104942, 120049-120057, 120059, 120060, 120064, 120065, 120070, 120071, 120075-120077, 120080-120084, 120086, 120087, 121537, 135539, 135541, 135544, 135545, 135547, 136334-136336.
There was no significant size difference between mean male and female SVLs (unpaired t test, P = 0.34). Monthly stages in the testicular cycle are in Table 1. Three stages were present: (1) Regression: germinal epithelium of the seminiferous tubules is 1-2 layers thick and is composed mainly of spermatogonia with occasional Sertoli cells; (2) Recrudescence: there is an increase of cellularity in the seminiferous tubules due to a proliferation of germ cells; primary spermatocytes predominate. In late stage recrudescence, secondary spermatocytes may be abundant and occasional spermatids are noted; (3) Spermiogenesis: seminiferous tubules are lined by clusters of spermatozoa and groups of metamorphosing spermatids are present.
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Table 1. Monthly stages in testicular cycle of 11 Xenosaurus grandis from Veracruz, Mexico.
|
Month |
n |
Regression |
Recrudescence |
Spermiogenesis |
|
January |
4 |
4 |
0 |
0 |
|
May |
1 |
0 |
1 |
0 |
|
August |
5 |
0 |
0 |
5 |
|
September |
1 |
0 |
0 |
1 |
Regressed testes were present in January (Table 1). Recrudescence (= renewal) was in progress in the single male X. grandis from May. Testes from August and September were undergoing spermiogenesis (= sperm formation). The smallest reproductively active males (spermiogenesis in progress) both measured 83 mm SVL and were from August (LACM 120080, 121537). One apparently sub-adult male from March with a regressed testis (LACM 120065) measured 78 mm SVL. Two other subadults, (LACM 120054) SVL = 68 mm from January and (LACM 120087) SVL= 62 mm from July were not sexed.
Smith et al. (2000) reported that grandis males from Veracruz, Mexico mate in fall at which time testes are enlarged. Findings from this study confirm a late-summer fall period of sperm production for X. grandis, consistent with other fall/winter active viviparous lizards (Goldberg 1971; 2002; Smith et al. 2000).
Monthly stages in the ovarian cycle are in Table 2. Five stages were noted: (1) Quiescent: no yolk deposition; (2) Yolk deposition: early vitellogenesis in progress with basophilic yolk granules; (3) Enlarged follicles > 5 mm; yolk filled follicles are approaching ovulation; (4) Oviductal eggs: ovulation has occurred; (5) Embryos are developing within the oviducts.
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Table 2. Monthly stages in the ovarian cycle of 27 Xenosaurus grandis from Veracruz, Mexico.
|
Month |
n |
Quiescent |
Yolk deposition |
Enlarged follicles >5inni |
Oviductal eggs |
Embryos |
|
January |
6 |
3 |
0 |
2 |
0 |
1* |
|
April |
1 |
1 |
0 |
0 |
0 |
0 |
|
May |
5 |
2 |
0 |
2 |
1 |
0 |
|
June |
2 |
1 |
0 |
0 |
0 |
1 |
|
July |
4 |
3 |
0 |
0 |
0 |
1 |
|
August |
8 |
3 |
2 |
3 |
0 |
0 |
|
October |
1 |
1 |
0 |
0 |
0 |
0 |
* Reproductive organs were damaged making it impossible to count the number of embryos.
Embryos were observed in January, June and July suggesting parturition occurs in late summer. One neonate that measured 42 mm SVL was ‘‘prematurely” bom dead in captivity during May (LACM 135547). The presence of reproductively quiescent females during all months sampled indicates X. grandis do not produce young each year. Histological examination revealed none of these quiescent ovaries exhibited any trace of yolk deposition. Moreover, it is doubtful if two May A grandis females with enlarged follicles > 5 mm that had not yet ovulated would have produced young that summer, suggesting it may take some females more than two years to complete gestation. Ballinger et al. (2000b) reported X grandis females reproduce every other year. The smallest reproductively active X. grandis female (developing embryos) measured 90 mm SVL (LACM 10981). The correlation between female body size and litter size was not significant {P = 0.77). Mean clutch size for 10 gravid X. grandis was 5.7 ± 0.95 SD, range: 4-7. This mean litter size is larger than the 3.2 ± 0.2 SE reported for X. grandis
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agrenon from Oaxaca, Mexico (Lemos-Espinal et al. 2003) where the two smallest reproductively active females (embryos present) measured 97 mm SVL. It is however close to the mean litter size of 5.1 ± 0.2 SE, range 2-8 forX. grandis from Veracruz (Ballinger et al. 2000b). This suggests geographic variation occurs inX. grandis litter sizes. Fritts (1966) reported young ofX. grandis were bom in July which is consistent with Ballinger et al. (2000b) who reported parturition from June through August.
The factors responsible for only part of a female lizard population reproducing in a given year are unknown. It is typical for adult females of most species to be in various stages of the ovarian activity during the reproductive cycle in the temperate zone (see for example Goldberg 1973; 1975) or to exhibit some reproductive activity (often associated with moisture) throughout the year at low elevations in the tropics (Fitch 1982). Reports of female lizards with biennial production of young are more typical of those living in very harsh environments (Cree & Guillette 1995; Boretto & Ibarguengoytia 2006; Ibargiiengoytia & Casalins 2007). In addition to X. grandis, another lizard in which only parts of the adult female population reproduces each year is the xantusiid lizard, Xantusia riversiana (cf. Goldberg & Bezy 1974). In contrast toX. grandis, females of the viviparous congeners X. newmanorum and X. platyceps reproduce each year (Ballinger et al. 2000b). Additional study is needed to elucidate the factors responsible for only part of the X grandis female population reproducing in a given year.
Acknowledgments
I thank Christine Thacker (LACM) for permission to examine specimens.
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Literature Cited
Alvarez del Toro, M. 1982. Los Reptiles de Chiapas. Tercera Edic. Publicacion del Institute de Historia Natural, Tuxtla Gutierrez, Chiapas, Mexico, 248 pp.
Ballinger, R. E., J. A. Lemos-Espinal & G. R. Smith. 2000a. Xenosaurus grandis (Gray). Knob-scaled lizard. Catalog. Amer. Amphib. ReptiL, 713:1-4.
Ballinger, R. E., J. A. Lemos-Espinal & G.R. Smith. 2000b. Reproduction in females of three species of crevice-dwelling lizards (genus Xenosaurus) from Mexico. Stud. Neotrop. Fauna Environ., 35:179-183.
Boretto, J. M. & N. R. Ibarguengoytia. 2006. Asynchronous spermatogenesis and biennial female cycle of the viviparous lizard Phymaturus antofagastensis (Liolaemidae): reproductive responses to high altitudes and temperate climate of Catamarca, Argentina. Amphib.-Reptil., 27:25-36.
Cree, A. & L. L. Guillette, Jr. 1995. Biennial reproduction with a fourteen-month pregnancy in the gecko Hoplodactylus maculatus from Southern New Zealand. J. Herpetol., 29:163-173.
Fitch, H. S. 1982. Reproductive cycles in tropical reptiles. Occas. Pap. Mus. Nat. Hist. Univ. Kansas, 96:1-53.
Fritts, T. H. 1966. Notes on the reproduction of Xenosaurus grandis (Squamata: Xenosauridae). Copeia, 1966:598.
Goldberg, S. R. 1971. Reproductive cycle of the ovoviviparous iguanid lizard Sceloporus jarrovi Cope. Herpetologica, 27:123-131.
Goldberg, S. R. 1973. Ovarian cycle of the western fence lizard, Sceloporus occidentalis. Herpetologica, 29:284-289.
Goldberg, S. R. 1975. Reproduction in the sagebrush lizard, Sceloporus graciosus. Amer. Midi. Nat., 93:177-187.
Goldberg, S. R. 2002. Eumeces brevirostris (Short-nosed Skink). Reproduction. Herpetol. Rev., 33:134.
Goldberg, S. R. & R. L. Bezy. 1974. Reproduction in the island night lizard, Xantusia riversiana. Herpetologica, 30:350-360.
Ibarguengoytia, N. R. & L. M. Casalins. 2007. Reproductive biology of the southernmost gecko Homonota darwini: convergent life-history patterns among southern hemisphere reptiles living in harsh environments. J. Herpetol., 41 :72-80.
Lemos-Espinal, J, A., G. R. Smith & R. E. Ballinger. 2003. Ecology of Xenosaurus grandis agrenon, a knob-scaled lizard from Oaxaca, Mexico. J. Herpetol., 37:192- 196.
Presnell, J. K. & M. P. Schreibman. 1997. Humason’s Animal Tissue Techniques, 5*^ Edit., The Johns Hopkins University Press, Baltimore, MD. 572 pp.
Smith, G. R., R. E. Ballinger & J. A. Lemos-Espinal. 2000. Male reproductive cycle of the knob-scaled lizard, Xenosaurus grandis. Southwest. Nat., 45:356-357.
SRG at: sgoldberg@whittier.edu
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323
POPULATION DYNAMICS OF AN ESTABLISHED REPRODUCING POPULATION OF THE INVASIVE APPLE SNAIL (POMACEA INSULARUM) IN SUBURBAN SOUTHEAST HOUSTON, TEXAS
Colin H. Kyle, Matthew K. Trawick, James P. McDonough and Romi L, Burks
Department of Biology, 1001 East University Avenue Southwestern University, Georgetown, Texas 78626
Over the past 15 years in the United States, a rise in introductions of non-native gastropod species has prompted major concern from both the U.S. Department of Agriculture and aquatic ecologists (Robinson 1999; Levine & Antonio 2003). Due to their large size (i.e., mass and operculum width up to approximately 150 g and 55 mm, respectively; Youens & Burks 2008) and high rate of reproduction (i.e., up to 4000 eggs per clutch; Barnes et al. 2008), the freshwater gastropod family Ampullariidae contains a number of destructive invasive species (Rawlings et al. 2007) that alter ecosystem function and threaten native biodiversity (Carlsson et al. 2004; Carlsson & Bronmark 2006; Boland et al. 2008; Connors et al. 2008). Invading habitats worldwide, apple snails of the genus Pomacea now represent an increasing environmental problem in the U.S. Multiple introductions (Rawlings et al. 2007) of numerous species from multiple origins (Hayes et al. 2008) complicate this problem.
Native to temperate South America, the apple snail species now found in Texas (Karatayev et al. 2009), Pomacea insularum, possesses a round shell with a characteristic deep groove on the whorl (i.e., channeled) (Howells et al. 2006). Unlike most snails, P. insularum, and closely related P. canaliculata (another channeled species), consume macroscopic plants rather than algae (Carlsson & Lacoursiere 2005; Burlakova et al. 2008). Because molecular geneticists only recently identified P. insularum as a distinct species from its close relative, the mode of introduction, spread, and current distribution of this newly introduced species requires more attention
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from ecologists (Rawlings et al. 2007; Karatayev et al. 2009).
To address whether or not newly established populations of P. insularum now persist, this report analyzed size structure of P. insularum populations from 2006-2008. This study examined changes in proportions of juveniles and adults within sample populations. An increase in the proportion of juveniles between samples taken from 2006 to 2008 indicates changes in the size distributions of introduced populations of P. insularum.
Live snails were collected during five trips: May 2006 (^=100), May 2007 {n=2\\ September 2007 (n=ll\ May 2008 (/?=82) and August 2008 {n=\16). Each trip involved two sample sites in the Houston area: Horsepen Bay located within Armand Bayou and a drainage ditch in nearby Clear Lake. All snails taken from both sampling sites were pooled into one sampling event based on date. The same water system connects both sample sites, thus creating five population samples. To obtain a comprehensive population sample, teams explored the banks of sampling areas and pulled any observable snails using nets. This frequently involved traveling via canoe to areas inaccessible by foot. Bank sampling included careful exploration of emergent macrophyte stands and within dense patches of freely floating plants. For the Armand Bayou site, sampling days varied between 8-10 hours on the water, with a consistent traveling distance of approximately 2 km upstream. Researchers separated snails into two broad groups based upon their operculum widths: juveniles (< 40 mm) and adults (> 40 mm). Operculum width serves as a good indicator of snail size (Youens & Burks 2008) and suggestions for size at maturity for P. insularum currently do not exist in the literature. Cazzaniga ( 1 990) noted that an operculum size of 40 mm for larger P. insularum may be similar to the 25 mm threshold in operculum width that delineates smaller adult P. canaliculata. To test differences in proportions of juveniles over different sample populations, all five sample populations were compared against each other using a z-test of significance for two proportions (Baldi & Moore 1996).
Data analysis revealed significant differences between proportions
TEXAS J. SCI. 61(4), NOVEMBER, 2009
325
of juveniles across sample populations, with all samples occurring in a non-random distribution (all /^-values <0.05). According to pair-wise z-tests, the sample from August of 2008 exhibited a significantly higher proportion of juveniles than three of the other four samples, with the September 2007 sample not statistically different than any of the samples (Table 1). The largest difference between proportions existed between the earliest sample, May 2006, and the most recent, August 2008. The August 2008 sample showed a change in the size structure distribution, which indicates a larger proportion of juveniles.
The increase in the overall proportion of juveniles collected from 2006 to 2008 (Table 1) suggests that the total number of juvenile P. insularum present in the study sites increased over this period. Juvenile snails (<40 mm) were not observed in samples taken from the earliest sampling events. The use of consistent and comprehensive sampling methods suggests that research teams did not simply miss juveniles in earlier sampling events. The continued presence of egg clutches observed during field studies coupled with the change in proportion of juveniles indicates that invasive populations of P. insularum in the study sites are increasing in overall size distribution. An increasing number of juveniles may imply that exotic P. insularum populations are growing in the aquatic ecosystems of southeast Houston. For P. canaliculata, Carlsson & Bronmark (2006) demonstrated that smaller snails exhibited higher feeding rates. Therefore, an increase in the population size of non-native P. insularum could produce more damage to aquatic vegetation due to their higher rate of consumption (Boland et al. 2008; Burlakova et al. 2008). However, invasive ecologists need future research on population size per unit area and snail consumption rates of macroscopic plants to support these predictions.
For the first time, this study documents the presence of the growing size distributions of populations of invasive P. insularum in southeast Texas. However, scientists still know little about the ability of this species to damage local ecosystems. Due to their recent presence, only limited estimates on the reproductive ability of P. insularum exist
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Table 1: Individual percentages for each size class present with the total number of snails collected from each sampling event. Samples occur across six operculum uddth size classes with a threshold at 40 mm for adults. Different small letters denote statistical significance between sampling events in the total proportion of juveniles (10-40 mm) according to a z-test of significance for proportions.
|
Sampling Event |
N |
Juveniles |
Adults |
|||||
|
10-20 mm |
20-30 mm |
30-40 mm |
Significance |
40-50 mm |
50-60 mm |
>60 mm |
||
|
May-06 |
100 |
0% |
0% |
5% |
ab |
73% |
22% |
0% |
|
May-07 |
21 |
0% |
0% |
4.8% |
ab |
66.6% |
28.6% |
0% |
|
Sep-07 |
77 |
0% |
1.3% |
1.3% |
abc |
14.8% |
72.7% |
10.4% |
|
May-08 |
82 |
1.2% |
6.1% |
8.5% |
a |
43.9% |
40.3% |
0% |
|
Aug-08 |
176 |
16.5% |
18.8% |
2.8% |
c |
11.9% |
40.9% |
9.1% |
(Barnes et al. 2008). However, the potential population growth made possible by females routinely laying large egg clutches (each containing approximately 2000 eggs; Barnes et al. 2008) warrants serious concern. Without further investigation of the population size structure, invasive ecologists cannot accurately predict effects of P. insularum on aquatic Texas ecosystems. Ecologists must conduct future research, specifically density estimations and consumption rates, to understand fully the overall effect P. insularum will have in southeast Texas and possibly along the entire Gulf coast.
Acknowledgements
We thank the Texas Academy of Sciences, Southwestern University and H-E-B for providing the funds necessary for this study. Our gratitude also goes to Mark Kramer, George Regmond, Ann Brinly and the entire staff at Armand Bayou Nature Center for helping us with our data collection. We would also like to thank Rebecca Marfurt, Sarah Hensley, Matt Barnes, Abby Youens and Brandon Boland for providing initial life history data for P. insularum.
Literature Cited
Baldi, B. & D. S. Moore. 1996. The practice of statistics in the life sciences. W. H. Freeman and Company, New York, 516pp.
Barnes, M. A., R. K. Marfurt, J. J. Hand & R. L. Burks. 2008. Fecundity of the exotic applesnail, Pomacea insularum. Journal of the North American Benthological
TEXAS J. SCI. 61(4), NOVEMBER, 2009
327
Society, 27(3):738-745.
Boland, B., M. Meerhoff, C. Fosalba, N. Mazzeo, M. Barnes & R. Burks. 2008, Juvenile snails, adult appetites: Contrasting resource consumption between two species of applesnails (Pomacea). Journal of Molluscan Studies, 74(l):47-54.
Burlakova, L. E., A. Y. Karatayev, D. P. Padilla, L. D. Cartwright & D. N. Hollas. 2008. Wetland restoration and invasive species: Apple snail {Pomacea insularum) feeding on native and invasive aquatic plants. Restoration Ecology, 17(3): 433-440.
Cazzinga, N. J. 1990. Sexual dimorphism in Pomacea canaliculata. The Veliger, 33(4):384-388.
Carlsson, N. O. L., C. Bronmark & L. A. Hansson. 2004. Invading herbivory: The golden apple snail alters ecosystem tlmctioning in Asian wetlands. Ecology, 85(6):1575-1580.
Carlsson, N. O. L. & C. Bronmark. 2006. Size-dependent effects of an invasive herbivorous snail {Pomacea canaliculata) on macrophyte and periphyton in Asian wetlands. Freshwater Biology, 51:695-704.
Carlsson, N. O. L. & J. O. Lacoursiere. 2005. Herbivory on aquatic vascular plants by the introduced golden apple snail {Pomacea canaliculata) in Lao PDR. Biological Invasions, 7:233-241.
Conner, S. L,, C. M. Pomory & P. C, Darby. 2008. Density effects of native and exotic snails on growth in juvenile apple snails Pomacea paliidosa (Gastiopoda: Ampullariidae): A laboratory experiment. Jounial of Molluscan Studies, 74:355-362.
Hayes, K. A., R. C. Joshi, S. C. Thiengo & R. H. Cowie. 2008. Out of South America: Multiple origins of non-native apple snails in Asia. Diversity and Distributions, 14(4):701-712.
Howells, R. G., L. E. Burlakova, A. Y. Karatayev, R. K. Marfiirt & R. L. Burks. 2006. Native and introduced Ampullariidae in North America: History, status, and ecology, pp. 73-112, in Global advancements in ecology and management of golden apple snails (R. Joshi, & L. Sebastian eds). Philippine Rice Research Institute, 588pp.
Karatayev, A. Y., L. E. Burlakova, V. A. Karatayev & D. K. Padilla. 2009. Introduction, distribution, spread, and impacts of exotic freshwater gastropods in Texas. Hydrobiologia, 619:181-194.
Levine, J. M. & C. M. Antonio. 2003. Forecasting biological invasions with increaseing international trade. Conservation Biology, 17:322-326.
Rawlings, T. A., K. A. Hayes, R. H. Cowie & T. M. Collins. 2007. The identity, distribution, and impacts of non-native apple snails in the continental United States. BMC Evolutionary Biology, 7:97-1 1 1.
Robinson, D. G. 1999. Alien invasions: The effects of the global economy on nonmarine gastropod introductions into the United States. Malacologia, 41(2):413- 438.
Youens, A. K. & R. B. Burks. 2008. Comparing applesnails with oranges: The need to standardize measuring techniques when studying Pomacea. Aquatic Ecology, 42:679-684.
burksr@southwestem.edu
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IN RECOGNITION OF THEIR ADDITIONAL SUPPORT OF THE TEXAS ACADEMY OF SCIENCE DURING 2009
PATRON MEMBERS
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INDEX TO VOLUME 61 (2009) THE TEXAS JOURNAL OF SCIENCE
Rigel K. Rilling
Department of Biology, Angelo State University San Angelo, Texas 76909
This index has separate subject and author sections. Words, phrases, locations, proper names and the scientific names of organisms are followed by the initial page number of the articles in which they appeared. The author index includes the names of all authors followed by the initial page number of their respective article(s).
SUBJECT INDEX
A
Ambystomajeffersonianum 61 Ammotragus lervia 1 5 amphibians 3, 61 Andropogon glomeratus 83 Anguillidae 3 1 Anisoptera 157 anthropogenic effects 3, 279 aoudad 1 5 Apicomplexa 311 Araneidae 203 arboreal nesting 163 Arkansas 1 5 1
central and southern 3 1 endemic fauna of 203 Arkansas Counties Columbia County 3 1 arsenic-tolerant cultures 259 Atherinopsidae 3 1 avian taxonomy 195
B
bare ground 119,219 Bivalvia 203,279
brackish wetlands 83 Bromus japonicus 119
C
Caddell formation 181 Calidris minutilla 233 Catostomidae 3 1 Centrarchidae 3 1 Cephenemiya jellisoni 1 87 Cephenemiya phobifer 187 Cephenem iya pratti 187 Charadriiformes 233 chronic wasting disease 1 87 clutch size 1 3 1 Clypeasteroida 181 Coleoptera 203 Collembola 203 Costa Rica 147 cover board arrays 3 Cymbovula acicularis 67 Cyprinidae 3 1
330
THE TEXAS JOURNAL OF SCIENCE-VOL. 61, NO. 4, 2009
D
detoxification, arsenic 259 density 295 diel 295
Dipodomys elator 119 Diplopoda 151, 203 Diptera 187,203 distance sampling 295 diversity 3, 83, 279 domestic goat 1 5 domestic sheep 1 5
E
ectoparasites 131, 187 endemic species 203 Environmental Protection Agency (EPA) 259 Eocene, upper 1 8 1 Ephemeroptera 203 Erizathon dorsatum 65 escape terrain 1 5 Etheostoma asprigene 3 1 Etheostoma fusiforme 3 1 Eubacteria 259
F
facultative species 243 fatty acid profiles 45 fire 219
floodplain ecosystem 3 freshwater wetlands 83 reservoir 233 frugivory 97 Fuirena simplex 83 Fundulidae 3 1 Fungi 203
Fusconaia askewi 279
G
gas chromatography 45 gas exchange 243 Gastropoda 67, 203, 323 Gekko smithii 225 Geographic Information System (GIS) 15
global climate change 1 3 1 granivory 97 grazing intensity 1 19 grazing regime 119 ground coverage 119,219 Gulf Coast 67, 181
H
hatching success 131 Hematozoa 3 1 1 herpetofauna 3 Hiodon tergisus 3 1 Hiodontidae 3 1 Hirundo rustica erythrogaster 131
Hymenoptera 203
I
Icturalidae 3 1 Illinois 61 index fossil 181 infanticide 131 invasive species 323
J
Julida 151 K
karyotype 195
L
Laguna Madre 259 leaf litter 219
TEXAS J. SCI. 61(4), NOVEMBER, 2009
331
leaves 243 Leguminosae 243 Lertha extensa 45 limiting resource 163 lipid composition 45
M
Mabuya unimarginata 147 mass spectrometry 45 Mexico
Baja California 229 Coahuila 1 5
Sierra Maderas del Carmen 15 Sierra San Marcos y del Pino 15
Tamaulipas 67 Veracruz 317
minimum contaminant level 259 Mississippi 181 Muridae 97 Mussels 279 Mustela frenata 229 Mustelidae 229 Mycoplasma 259 Myxidium serotinum 61 Myxozoa 61
N
nasopharyngeal bots 187 Nemopteridae 45 nesting success 131 nestling success 131 Neuroptera 45 Notorus phaeus 3 1
O
Ochrotomys nuttalli 163 Odocoileus hemionus 1 87 Odocoileus virginianus 1 87 Oestridae 187
Oklahoma, east-central 311
Old Sabine Bottom Wildlife Management Area 3 omnivory 97 organic substrate 2 1 9 overwintering 233 Ovis canadensis 1 5 Ovulidae 67 oxidation 259
P
Parajulidae 151 parasites 131,187,311 Passeriformes 311 Pelodictyon 259 Percidae 3 1 Percina sp. 31 Periarch us lyel li 181 Peromyscus pectoral is 97 phospholipid 45 photosynthetic rate 243 pine slough 219 polymerase chain reaction (PCR) 259
Pomacea insularum 323 population dynamics 323 Program R 195 Pseudoscorpionida 203 Pteronotropis hubbsi 3 1
R
radio-tracking 163 recolonization 219 recruitment 279 reproductive cycle 147, 225, 317 reptiles 3, 147,219,225,317 Rio Grande Valley, lower 295
332
THE TEXAS JOURNAL OF SCIENCE-VOL. 61, NO. 4, 2009
s
Sabine River 279 Salinispora 259 sanctuaries, mussel 279 Schoenoplectus pungens 83 Scincella lateral is 219 Scincidae 147,219 Scutelliformes 1 8 1 seasonal flooding 1 63 seasonal leaf fall 219 seasonal trophic ecology 97 sediment samples 259 Sophora secundiflora 243 Spar tin a patens 83 species richness 3, 83 Squamata 147,219,225,317 Stephen F. Austin State Univ.
Experimental F orest 163 stomatal conductance 243 suburban habitat 323
T
Texas
central 97,157,243 eastern 3, 163 Edwards Plateau 65 northeast 131,279 south 259, 295 South Padre Island 83 west central Texas 233 Texas Cities Houston 323
Texas Counties
Angelina County 163 Jones County 157 Houston County 163, 323 Nacogdoches County 163 Smith County 3 San Augustine County 163 Taylor County 157 Witchita County 119 Texas Wildlife Action Plan 279 transpiration 243 transplant and restoration 15 triacylglycerol 45 Trichoptera 203 trophic opportunism 97
U
Unionidae 279 V
vegetation height 119
W
water potential, leaf 243 wetland habitat 3, 83
X
Xenosaurus grandis 3 1 7 Z
Zenaia asiatica asiatica 295 Zenaia macroura 295
TEXAS J. SCI. 61(4), NOVEMBER, 2009
333
AUTHORS
Alaniz-Garcia, J. 229 Andrews, K. D. 311
Baccus, J. T. 97, 195, 295 Baird, A. B. 65 Bashan, M. 45 Bay,M.D. 311 Benn, S. J. 295 Berlanga, G. A. 259 Bradstreet, A. P. 163 Burks, R.L. 323
Cakmak, O. 45 Collins, M.L. 295 Contreras-Balderas, A. J. 15 Correa-Sandoval, A. 67 Crawford, J. A. 61
Edwards, C.W. 163 Espinosa-T., A. 15 Eubanks, T. M. 259
Ford,N.B. 3,279 Forstner, M. R. J. 195 Furuya, M. 243
Garcia- A., M. A. 15 Goetze, J. R. 119 Goldberg, S. R. 147,225,317 Gonzalez-Guzman, S. 229 Gullett,J. 279
Hall,D. W. 65 Hardwick, J, M. 97 Herriman, K. 3 Huffman, D. G. 97 Hunkapiller, T. R. 3
Johnson, B. W. 157 Judd,F. W. 83 Kainer, M. A. 97 Kasner, A. C. 233
Kelley, S.W. 187 Kopachena, J. G. 131 Kuhns, A. R. 61 Kyle,C.H. 323
LaDuc, T. J. 65 Lee,T.E. 157 Lonard, R. I. 83 Lowe,K.L. 259
Martinez-Gallardo, R. 229
Maxwell, T. C. 233
May, M. E. 279
McAllister, C. T. 31, 61, 151, 203
McDonough, J. P. 323
Nelson, A. D. 119 Nelson, M. 119
Patel, A. J. 157 Pauly, G. B. 65 Persans, M. W. 259
Robison, H.W, 31,151,203 Ruddick,R.H. 233 Ruiz-Campos, G. 229
Sandoval, A. V. 15 Satar, A. 45 Slay,M.E. 203 Small, M.F. 195,295 Strenth, N. E. 67
Trawick, M. K. 323 Tumlinson, R. 31 Turner, K.T. 131
Van Auken, O. W. 243 Vogtsberger, R. C. 157
Watson, C. M. 219 Watson, E. 119
Zachos, L. G. 181
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REVIEWERS
The Editorial staff wishes to acknowledge the following individuals for serving as reviewers for those manuscripts considered for publication in Volume 61. Without your assistance it would not be possible to maintain the quality of research results published in this volume of the Texas Journal of Science.
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|
|
e Total Free or Nominal Rate Distribution (Sum of 15d(1), (2), (3) and (4)) |
0 |
. 0 . |
||
|
f. Total Distribution (Sum of f5c and ISe) ^ |
830 |
830 |
||
|
g Copies not Distributed (See fosfrucf/ons to PuW/sfters #4 (page #3j) ^ |
70 |
70 |
||
|
h. Total (Sum of 1 51 and g) ^ |
900 |
900 |
||
|
I Percent Paid w (IScdivided by 15f times 100) * |
100% |
100% |
16. Pubtication of Statement of Ownership
If the publication is a qeneral publication, publication of this statement is required. Will be printed Q Publication not required,
in the _ _ issue of this publication
17. Signature and TiUe of Editor, Publisher. Business Manager, or Owner
Date
4^
At
E'd: k.
25 Sept. 2009
I certify that all information furnished on this form is true and campiste. I understand that anyone who furnishes false or misleading information on this form or who omits material or information requested on the form may be subject to criminal sanctions (including fines and imprisonment) and/or civil sanctions (including civil penalties).
PS Form 3526, September 2007 (Page 2 of 3)
THE TEXAS ACADEMY OF SCIENCE, 2009-2010
OFFICERS
President President Elect: Vice-President:
Immediate Past President: Executive Secretary: Corresponding Secretary: Managing Editor:
Manuscript Editor:
Treasurer:
AAAS Council Representative: International Coordinator:
William J. Quinn, St. Edward’s University
Benjamin A. Pierce, Southwestern University
Romi L. Burks, Southwestern University
Raymond C. Mathews, Jr., Texas Water Dev. Board
Fred Stevens, Schreiner University
Diane B. Hyatt, Texas Water Development Board
Ned E. Strenth, Angelo State University
Frederick B. Stangl, Jr., Midwestern State University
John A. Ward, Brooke Army Medical Center
James W. Westgate, Lamar University
Armando J. Contreras, Universidad Autonoma de N.L.
DIRECTORS
2007 Renard L. Thomas, Texas Southern University Bob Murphy, Texas Parks and Wildlife Department
2008 Christopher M. Ritzi, Sul Ross State University Andrew C. Kasner, Audubon Texas
2009 Ana B. Christensen, Lamar University
Thomas L. Arsuffi, Texas Tech at Junction
SECTIONAL CHAIRPERSONS
Anthropology: Raymond Mauldin, University of Texas at San Antonio Biomedical: G. Scott Weston, University of the Incarnate Word Botany: David Lemke, Texas State University
Cell and Molecular Biology: Magaly Rincon-Zachary, Midwestern State University
Chemistry and Biochemistry: J. D. Lewis, St. Edward’s University
Computer Science: James McGuffee, St. Edward’s University
Conservation Ecology: Wendi Moran, Hardin-Simmons University
Environmental Science: Kenneth R. Summy, University of Texas-Pan American
Freshwater Sciences: Matt Chumchal, Texas Christion University
Geosciences: Chris Barken, Stephen F. Austin State University
Marine Sciences: Larry D. McKinney, Harte Research Institute
Mathematics: Elsie M. Campbell, Angelo State University
Physics: David L. Bixler, Angelo State University
Science Education: Patricia Ritschel-Trifilo, Harden-Simmons University
Systematics and Evolutionary Biology: Tara Maginnis, St. Edward’s University
Terrestrial Ecology and Management: Richard Patrock, St. Edward’s University
COUNSELORS
Collegiate Academy: David S. Marsh, Angelo State University Junior Academy: Vince Schielack, Texas A&M University
PERIODICALS
THE TEXAS JOURNAL OF SCIENCE Texas Academy of Science CMB 629
Wayland Baptist University Plainview, Texas 79072
SMITHSONIAN INSTITUTION LIBRARIES
3 9088 01558 5730