Christopher T. Winne

The Global Decline of Reptiles, Déjà Vu Amphibians

A s a group [reptiles] are nei t h er ‘good ’n or ‘b ad ,’ but ia re intere s ting and unu su a l , a l t h o u gh of m i n or i m port a n ce . If t h ey should all disappe a r, it wo u l d not make mu ch differen ce one way or the other ”( Zim and Smith 1953, p. 9 ) . Fortu n a tely, this op i n i on from the Golden Gu i de Series does not persist tod ay; most people have com e to recogn i ze the va lue of both reptiles and amph i bians as an i n tegral part of n a tu ral eco s ys tems and as heralds of envi ron m ental qu a l i ty (Gibbons and Stangel 1999). In recent ye a rs , as overa ll envi ron m ental aw a reness among the p u blic has incre a s ed , con cerns have come to inclu de intere s t in the eco l ogical state of reptile and amph i bian spec i e s t h em s elves and of t h eir habi t a t s . In c re a s ed aw a reness may s tem from bet ter edu c a ti on abo ut threats to bi od ivers i ty in gen era l , and to reptiles and amph i bians in parti c u l a r, a n d po s s i bly even from an innate attracti on to these taxa ( Kell ert and Wi l s on 1993). From the perspective of many nonscientists, the two vertebrate classes comprising reptiles and amphibians, collectively referred to as the herpetofauna, are interchangeable. For example,the Boy Scout merit badge pamphlet for herpetology was called simply Reptile Study from 1926 to 1993 (Conant 1972, Gibbons 1993), and major zoos (e.g., National Zoo in Washington, DC; Zoo Atlanta; and San Diego Zoo) use only the name “reptile” to refer to the facility that houses both amphibians and reptiles. Thus, public attitudes about the need for conservation of reptiles are probably linked to concern about amphibian declines and deformities (Alford and Richards 1999, Johnson et al. 1999, Sessions et al. 1999), which have been the subject of numerous, well-documented scientific studies. Because amphibians are distributed worldwide, but herpetologists who document amphibian declines are not, it is difficult to accurately assess what portion of amphibian populations are experiencing significant declines or have already disappeared. Furthermore, the means of determining a species’ conservation status is a rigorous and time-intensive process, and therefore counts of “officially” recognized endangered and threatened species are likely to grossly underestimate the actual number of imperiled s pecies (Ta ble 1). The worl dwi de amph i bian decl i n e probl em , as it has come to be known, has garnered significant attention not only among scientists but also in the popular media and in political circles.

Post-drought responses of semi-aquatic snakes inhabiting an isolated wetland: Insights on different strategies for persistence in a dynamic habitat

Most aquatic habitats are temporally dynamic, and selection has favored diverse strategies to persist in the face of fluctuating environmental conditions. Isolated wetlands in the southeastern United States harbor high diversities of aquatic and semi-aquatic organisms. However, drought may render these wetlands temporarily unsuitable for many species, sometimes for years at a time. We studied the movement patterns and demography of seven species of semi-aquatic snakes at Ellenton Bay, an isolated 10-ha freshwater wetland in the Upper Coastal Plain of South Carolina, following complete drying of the bay during a drought from 2000 to 2003. Behavioral and population responses varied markedly among species. Cottonmouths (Agkistrodon piscivorus) migrated to and from the wetland annually, fared well, and reproduced during the drought. Banded watersnakes (Nerodia fasciata) suffered a dramatic population decline and apparently did not reproduce, while eastern green watersnakes (N. floridand) were locally extirpated. Black swamp snakes (Seminatrix pygaea) aestivated within the wetland and were less affected by the drought than Nerodia. Interspecific differences in response to drought demonstrate that conservation measures may affect species differently and highlight the importance of terrestrial habitat around wetlands for semi-aquatic reptiles.

Getting the Drift: Examining the Effects of Timing, Trap Type and Taxon on Herpetofaunal Drift Fence Surveys

ABSTRACT The evaluation of appropriate sampling methodologies is critical for accurately determining the distribution and status of herpetofaunal populations. We report the results of a year-long drift fence study, using multiple trap types (large pitfall traps, small pitfall traps and funnel traps), of a species-rich herpetofaunal community (59 species) surrounding an isolated wetland in the southeastern United States. Specifically, we determined the effects that timing, trap type and taxon had on capture rates of herpetofauna. We found that funnel traps captured the greatest number of herpetofaunal species, but a combination of funnel traps and large pitfall traps yielded the greatest number of individual captures due to complementary biases in capture efficiencies among herpetofaunal taxa. With little exception, small pitfall traps were relatively ineffective for sampling herpetofauna. We also found that the timing of drift fence monitoring affected herpetofaunal species accumulation rates but that seasonal effects were taxon-specific. Our study affirms that drift fences are exceptional tools for inventorying and monitoring diverse species and large numbers of herpetofauna and also demonstrates the important effects that season and taxon can have on capture rates. Therefore, we recommend a priori delineation of project goals and the use of multiple trap types with careful attention to the timing of drift fence monitoring to maximize sampling efficiency and minimize biases associated with data collection.

Enigmatic Decline of a Protected Population of Eastern Kingsnakes, Lampropeltis Getula, in South Carolina

Abstract Although recent reports of global amphibian declines have received considerable attention, reptile declines have gone largely unreported. Among reptiles, snakes are particularly difficult to quantitatively sample, and thus, most reports of snake declines are based on qualitative or anecdotal evidence. Recently, several sources have suggested that Eastern Kingsnakes (Lampropeltis getula) have declined over a substantial portion of their range in the southeastern United States, particularly in Florida. However, published evidence for L. getula declines or their potential causes are limited. We monitored the status of a population of L. getula on the U.S. Department of Energys Savannah River Site (SRS) in Aiken, South Carolina, USA, from 1975 to 2006. Herpetofaunal populations on the Savannah River Site have been protected from the pressures of collecting and development since 1951 due to site access restrictions. Here, we document a decline in both abundance and body condition of L. getula inhabiting the vicinity of a large isolated wetland over the past three decades. Because this L. getula population was protected from anthropogenic habitat degradation, collection, and road mortality, we are able to exclude these factors as possible causes of the documented decline. Although the definitive cause of the decline remains enigmatic, natural succession of the surrounding uplands, periodic extreme droughts, shifts in community composition (e.g., increased Agkistrodon piscivorus abundance), introduced fire ants, or disease are all potential contributors to the decline.

Empirical Tests of Biased Body Size Distributions in Aquatic Snake Captures

Abstract Ecologists often rely on a suite of demographic parameters—such as age structure, body size distributions, population density, and sex ratios—to understand life history patterns, population dynamics, and community structure of snakes. Unfortunately, in many cases little consideration is given to how sampling techniques may influence the outcome of demographic studies. Herein, we use a combination of field capture techniques, an extensive database of field-captured snakes, and laboratory and field experiments to evaluate how capture methods may influence demographic assessments of several North American semi-aquatic snake species, including Agkistrodon piscivorus, Farancia abacura, Nerodia fasciata, N. floridana, N. rhombifer, N. taxispilota, Regina rigida, Seminatrix pygaea, and Thamnophis sauritus. We found that commercially available aquatic funnel traps (i.e., minnow traps) generally yielded biased assessments of population demography, but that the nature and magnitude of these biases varied predictably by species and trap type. Experimental manipulations of funnel opening diameter in aquatic funnel traps demonstrated that such modifications allowed for capture of larger snakes but that the size of funnel opening necessary to capture the largest individuals varied between species. Additionally, we found differences between snake species in their ability to escape from different types of traps at birth, suggesting that escape of neonates through trap mesh can lead to the lack of small snakes often observed in field samples. Overall, our results demonstrate that capture methods may bias assessments of snake population demography, but that careful design of sampling methodology, with consideration of potential biases, can yield meaningful data on snake biology.

Ecological and Methodological Factors Affecting Detectability and Population Estimation in Elusive Species

ABSTRACT Although mark-recapture methods are among the most powerful tools for monitoring wildlife populations, the secretive nature of some species requires a comprehensive understanding of the factors that affect capture probability to maximize accuracy and precision of population parameter estimates (e.g., population size and survivorship). Here, we used aquatic snakes as a case study in applying rigorous mark-recapture methods to estimate population parameters for secretive species. Specifically, we used intensive field sampling and robust design mark-recapture analyses in Program MARK to test specific hypotheses about ecological and methodological factors influencing detectability of two species of secretive aquatic snakes, the banded watersnake (Nerodia fasciata), and the black swamp snake (Seminatrix pygaea). We constructed a candidate set of a priori mark-recapture models incorporating various combinations of time- and sex-varying capture and recapture probabilities, behavioral responses to traps (i.e., trap-happiness or trap-shyness), and temporary emigration, and we ranked models for each species using Akaikes Information Criterion. For both banded watersnakes and black swamp snakes we found strong support for time-varying capture and recapture probabilities and strong trap-happy responses, factors that can bias population estimation if not accommodated in the models. We also found evidence of sex-dependent temporary emigration in black swamp snakes. Our study is among the first comprehensive assessments of factors affecting detectability in snakes and provides a framework for studies aimed at monitoring populations of other secretive species.

Influence of body size on swimming performance of four species of neonatal natricine snakes acutely exposed to a cholinesterase‐inhibiting pesticide

Locomotor performance is an important fitness-related trait in reptiles because of its potential influence on prey capture and predator avoidance. Because cholinesterase-inhibiting pesticides disrupt neuromuscular signaling, reduction in performance seems to be a logical translation of this biochemical disruption to the organism level. In the present study, we compared the swimming performance of four species of natricine snakes acutely exposed to a formulation of carbaryl to determine whether neonatal body size or skin permeability influences responsiveness. Exposure to high concentrations of carbaryl (2.5-5.0 mg/L) resulted in reduced swimming performance in all four species of snakes, and species responded similarly to the pesticide once body size was accounted for allometrically. Using traditional methods in physiological ecology to estimate skin permeability (a parameter that influences the dose of contaminant absorbed), we found that water flux across the integument also scaled allometrically with body surface area and, therefore, was similar among species after controlling for this relationship. We suggest that future studies examining the effects of repeated low-dose exposure to cholinesterase inhibitors on performance parameters will be useful in assessing the ecological significance of our findings.

Unveiling Escape and Capture Rates of Aquatic Snakes and Salamanders (Siren spp. and Amphiuma means) in Commercial Funnel Traps

ABSTRACT Aquatic funnel trapping with commercially available minnow traps has proven effective for sampling several aquatic snake species. However, the efficacy of this technique for sampling snakes has received little controlled evaluation. We investigated the ability of aquatic snakes to escape from three funnel trap varieties (cylindrical steel, cylindrical plastic, and rectangular collapsible nylon mesh). We found that when intentionally released into traps, the majority (74%) of snakes escaped within 24 hours. Snakes escaped most frequently from collapsible traps, and of the species tested, Seminatrix pygaea escaped most frequently. We found significant differences in capture rates among trap types for S. pygaea, Farancia abacura (both captured most in plastic traps), and Nerodia fasciata (captured most in steel traps). Additionally, as we captured many large aquatic salamanders (Siren spp. and Amphiuma means), we also report trapping efficacies of the funnel traps for these amphibians.

Does dispersal across an aquatic geographic barrier obscure phylogeographic structure in the diamond-backed watersnake (Nerodia rhombifer)?

The impact of barriers to dispersal and gene flow is often inferred to be the primary cause of lineage divergence and phylogeographic structure in terrestrial organisms. In particular, the Mississippi River has been implicated as a barrier to gene flow in many species, including aquatic taxa. However, if barriers are permeable to organisms, then phylogeographic structure may be difficult to detect due to gene flow between lineages. Using time-calibrated Bayesian phylogenetic analyses of mtDNA, and phylogeographic coalescent simulations, we determine if the Mississippi River operates as a barrier to gene flow in the aquatic diamond-backed watersnake (Nerodia rhombifer). The phylogenetic analyses support a basal division within N. rhombifer mtDNA lineages that coincides with populations generally east and west of the Mississippi River. These results, and that of the divergence dating analyses, therefore suggest that the river was a significant barrier to gene flow in the Pleistocene ∼ 1.4 million years ago, presumably during an interglacial period when the river was much wider. However, we also detect western haplotypes in the eastern clade, and vice versa, thereby indicating that this barrier has not been complete. Nonetheless, the coalescent simulations that account for limited migration suggest that the Mississippi River was an important feature that shaped the phylogeographic history of this aquatic snake in the USA despite limited gene flow.

Population Structure, Body Size, and Seasonal Activity of Black Swamp Snakes (Seminatrix pygaea)

Abstract We examined the ecology of a Black Swamp Snake (Seminatrix pygaea) population inhabiting an isolated wetland in the upper Coastal Plain of South Carolina. The observed population structure was skewed towards mature individuals, with neonates and juveniles underrepresented, perhaps due to trapping bias. The sex ratio was biased during May and June, with females outnumbering males, but no sex ratio bias was evident at other times of the year. Seminatrix pygaea showed sexual dimorphism in body size, with females being longer and heavier than males and males having relatively longer tails than females, but there was no difference in monthly growth rates. Approximately 76.3% of the mature females captured in May and June 1998 were pregnant. Therefore, most mature females in this population probably exhibit annual reproduction, while some undergo biennial reproduction. The majority of females gave birth in July or August, with a few births occurring in September and October, and perhaps even as early as May or June. Our mark-recapture estimates suggest a population density greater than 60 adult snakes per hectare, which indicates this small aquatic snake, endemic to the Southeast, may play a large role as both predator and prey within isolated wetland ecosystems.