Kurt A. Buhlmann

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.

A Global Analysis of Tortoise and Freshwater Turtle Distributions with Identification of Priority Conservation Areas

Abstract There are currently ca. 317 recognized species of turtles and tortoises in the world. Of those that have been assessed on the IUCN Red List, 63% are considered threatened, and 10% are critically endangered, with ca. 42% of all known turtle species threatened. Without directed strategic conservation planning, a significant portion of turtle diversity could be lost over the next century. Toward that conservation effort, we compiled museum and literature occurrence records for all of the worlds tortoises and freshwater turtle species to determine their distributions and identify priority regions for conservation. We constructed projected range maps for each species by selecting geographic information system–defined hydrologic unit compartments (HUCs) with verified locality points, and then added HUCs that connected known point localities in the same watershed or physiographic region and that had similar habitats and elevations as the verified HUCs. We analyzed a total of 305 turtle species and assigned each to 1 of 7 geographic regions of the world. Patterns of global turtle species distributions were determined and regional areas of turtle species richness identified. In only 2 areas of the world did as many as 18 or 19 species occur together in individual HUCs. We then compared species distributions with existing global conservation strategies (GCSs) and established biodiversity priority areas. Presence of a species in a GCS was defined as ≥ 5% its range. Of the 34 biodiversity hotspots, 28 collectively contain the projected ranges of 192 turtle species, with 74 endemic; the 5 high-biodiversity wilderness areas contain 72 species, with 17 endemic; and 16 other wilderness areas contain 52 species, with 1 endemic. However, 116 turtle species have either < 50% of their ranges in existing GCSs (57 species) or do not occur in them at all (59 species, 19.3%), thus potentially leaving many tortoises and freshwater turtles without any regional GCS. For each of these 116 species we identify a priority Ecoregion for further conservation consideration, and we identify 3 new global Turtle Priority Areas for conservation based on aggregated Ecoregions. These are the Southeastern United States, Lower Gangetic Plain, and Coastal Australia Turtle Priority Areas.

Translocation as a conservation tool: site fidelity and movement of repatriated gopher tortoises (Gopherus polyphemus)

Efforts to evaluate the efficacy of translocation as a conservation tool have mostly been inadequate, particularly for reptiles and amphibians, leading many biologists to discount translocation as a viable management option. Nevertheless, with two-thirds of the worlds tortoise and freshwater turtle species at risk, translocation may be one of the few remaining options for re-establishing extirpated populations and reconnecting fragmented ones. We translocated 106 gopher tortoises (Gopherus polyphemus) to a protected area within the historical range but with no resident tortoises and tested the effects of penning on site fidelity and activity area size. We assigned 38 adults and subadults to one of three penning treatments (9 months, 12 months and no penning) and radio-tracked them for 2 years. Penning significantly increased site fidelity and resulted in smaller activity areas. Our data suggest that translocation coupled with penning will improve the likelihood of establishing self-sustaining tortoise populations.

Maternal transfer of contaminants and reduced reproductive success of southern toads (Bufo [Anaxyrus] terrestris) exposed to coal combustion waste

Bioaccumulation of contaminants and subsequent maternal transfer to offspring are important factors that affect the reproductive success of wildlife. However, maternal transfer of contaminants has rarely been investigated in amphibians. We examined maternal transfer of trace elements in southern toads ( Bufo[Anaxyrus] terrestris) residing in two locations: (1) an active coal combustion waste (CCW) disposal basin and adjacent 40-ha floodplain contaminated with CCW over 35 years ago and (2) an uncontaminated reference site. Our study is among the few to document tissue concentration-dependent maternal transfer of contaminants and associated adverse effects in amphibians. We found that females collected from the CCW-contaminated area had elevated concentrations of Ni, Se, and Sr; these females also transferred elevated levels of Cu, Pb, Se, and Sr to their eggs compared to females from the reference site. Overall reproductive success, estimated as a function of clutch size and offspring viability, was reduced by 27% in clutches collected from parents from the contaminated site compared to the reference site. Offspring viability negatively correlated with female and/or egg concentrations of Se and Ni. Reproductive success negatively correlated with Se and Cu concentrations in females, and Se concentrations in eggs. Our study highlights how exposure to CCW can negatively affect amphibian reproduction.

Interactive effects of maternal and environmental exposure to coal combustion wastes decrease survival of larval southern toads (Bufo terrestris)

We conducted a mesocosm study to assess the individual and interactive effects of previous maternal exposure and larval exposure to trace element-laden sediments on southern toads (Bufo terrestris). Previous maternal exposure to coal combustion wastes (CCW) reduced larval survival to metamorphosis up to 57% compared to larvae of unexposed females. Larvae reared on CCW accumulated significant concentrations of trace elements resulting in extended larval periods, reduced growth rates, and reduced mass at metamorphosis. However, the effects were dependent on age of sediments, suggesting the effects of contaminants from CCW may be partially ameliorated over time through the reduced bioavailability of trace elements in aged CCW. Most importantly, maternal exposure to contaminants coupled with larval exposure to fresh CCW interacted to reduce survival to metamorphosis by 85% compared to reference conditions. Our study yields further evidence that disposal of CCW in aquatic basins potentially creates ecological traps for some amphibian populations.

Mitochondrial DNA Phylogeography and Subspecies Issues in the Monotypic Freshwater Turtle Sternotherus odoratus

Phylogeographic variation in mitochondrial (mt) DNA restriction sites is described for populations of the monotypic stinkpot turtle (Sternotherus odoratus) from the southeastern United States. Stinkpots display pronounced and hierarchical mtDNA phylogeographic differentiation, ranging from genetically shallow differences among local populations to genetically deep distinctions among regional assemblages of haplotypes. Both magnitude and general pattern of intraspecific mtDNA phylogeography in S. odoratus are remarkably similar to those in a related species (Sternotherus minor) that traditionally has been considered ditypic based on morphological and genetic appraisals. The pronounced phylogeographic population structure in S. odoratus effectively falsifies prior hypotheses that extensive dispersal and gene flow account for the morphometric conservatism among geographic populations. These findings also raise broader issues concerning the significance of subspecies designations in testudine systematics.

Ecology of Chicken Turtles (Deirochelys reticularia) in a Seasonal Wetland Ecosystem: Exploiting Resource and Refuge Environments

Abstract Chicken turtles (Deirochelys reticularia) were studied at Dry Bay, a Carolina bay wetland in South Carolina, USA, between 1994 and 2005. A total of 461 individual turtles was marked from 1993–1998. Minimum ages at maturity for males and females were 2 and 5 yr, respectively. All females reproduced each year, and 60% of reproductive females produced two clutches per season. Clutch size averaged 9.8 eggs, and both clutch and egg size increased with body size. Hatchlings averaged 29.2 mm PL, and body sizes were similar among years. Yearling survivorship varied from 7.0–43.0% (mean = 20.4%) among years. The highest survivorship of a hatchling cohort to age 5 was 0.21. Survivorships of juveniles and adults while in terrestrial refugia were higher than survivorships while in aquatic habitats. No adult females survived a 2-yr drought (2001–2003), and the bay was repopulated by mature males and juvenile females (most from the 1998 hatchling cohort) that had survived the extended drought in terrestrial refugia. Three of those juvenile females matured and produced eggs in 2004. The traits of early maturity, high susceptibility to predation, and shortened longevity characteristic of chicken turtles are consistent with predictions for species that live in seasonally fluctuating and highly unpredictable aquatic habitats.

Hematology of the Pascagoula map turtle (Graptemys gibbonsi) and the southeast Asian box turtle (Cuora amboinensis).

Abstract Turtle populations are decreasing dramatically due to habitat loss and collection for the food and pet market. This study sought to determine hematologic values in two species of turtles to help assess health status of captive and wild populations. Blood samples were collected from 12 individuals of the Pascagoula map turtle (Graptemys gibbonsi) and seven individuals of the southeast Asian box turtle (Cuora amboinensis) from the Savannah River Ecology Laboratory (South Carolina, USA). The hematologic data included hematocrit, total solids, erythrocyte count, leukocyte count, and differential and percentage leukocyte counts. Low hematocrit values and high basophil counts were found in both species. The basophil was the most abundant leukocyte in the Pascagoula map turtle (median = 0.80 × 109/L), whereas in the Southeast Asian box turtle the most abundant leukocyte was the heterophil (median = 2.06 × 109/L).

Overwintering of Gopher Tortoises (Gopherus polyphemus) Translocated to the Northern Limit of Their Geographic Range: Temperatures, Timing, and Survival

Abstract We examined overwintering behavior in gopher tortoises (Gopherus polyphemus) translocated to the northern periphery of their geographic range by using miniature temperature data loggers during 2 winters. All adult and juvenile tortoises monitored with temperature loggers survived overwintering; however, during the course of the study 2 translocated juvenile tortoises without temperature loggers died during winter months. Onset and termination of overwintering were not different between the 2 yrs and were not correlated with mean above-ground air temperature. Mean overwinter duration was 127 ± 9 d SD and 128 ± 13 d SD during 2002–2003 and 2004–2005, respectively. Tortoises experienced temperatures as low as 7°C and as high as 31°C while overwintering; however, most (12 of 15) tortoises experienced very little (< 1°C) mean daily temperature fluctuation despite air temperatures regularly dropping below 0°C and exceeding 20°C. The overall mean temperature of overwintering tortoises was 12.4° ± 0.8°C (2002–2003) and 12.6° ± 1.2°C (2004–2005). Large fluctuations in temperature occurred when tortoises actively basked, and half of the monitored tortoises did, particularly juveniles, which accounted for 42% of winter basking events. Our results suggest that, given timely access to suitable refugia at recipient sites, overwinter mortality of translocated adult individuals may be minimal.

Effects of Vegetation Structure and Artificial Nesting Habitats on Hatchling Sex Determination and Nest Survival of Diamondback Terrapins

Abstract It is often the case that multiple factors contribute to wildlife population declines such that management will require simultaneous, integrated interventions to stabilize and recover populations. Diamondback terrapins Malaclemys terrapin are a species of high conservation priority, and local populations can be threatened by multiple factors, including bycatch in commercial and recreational crab pots, vehicle strikes on coastal roads, nest depredation from subsidized and introduced predators, and terrestrial habitat alteration. Mitigation of just one of these factors will often be insufficient for recovering at-risk populations; thus, information to manage multiple threats is needed. We measured the effects of natural vegetation structure and constructed (artificial) nesting habitat on hatchling sex ratios and nest depredation for a declining terrapin population on Jekyll Island, Georgia. Nest temperatures were highest on constructed nesting mounds, intermediate in open grass areas, and coolest u...