urgent

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The Global Decline of Reptiles, Déjà Vu Amphibians J. WHITFIELD GIBBONS, DAVID E. SCOTT, T R AVIS J. RYA N , KURT A. B U H L M A N N , T R ACEY D. TUBERV I L L E , BRIAN S. METTS, JUDITH L. GREENE, TONY MILLS, YALE LEIDEN, SEAN POPPY, AND CHRISTOPHER T. WINNE

A s a group [reptiles] are nei t h er ‘good ’n or ‘b ad ,’ butia re intere s ting and unu su a l , a l t h o u gh of m i n ori 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 inter- changeable. For example,the Boy Scout merit badge pam- phlet 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, John- son et al. 1999, Sessions et al. 1999), which have been the subject of numerous, well-documented scientific studies.

Because amphibians are distributed worldwide, but her- petologists who document amphibian declines are not, it is difficult to accurately assess what p ortion of amphibian populations are experiencing significant declines or have already disappeared. Furthermore, the means of deter- mining 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

prob l em , as it has come to be known, has garne red sig- nificant attention not only among scientists but also in the popular media and in political circles.

The reptile probl em Despite the fact that reptiles and amphibians are often considered collectively, reptile declines deserve spotlight- ing and elucidating in their own right. The differences between the two groups are substantial. Modern amphib- ians and reptiles are products of independent lineages that have been separate for the past 300 million years (Pough et al. 1998). Many of the differences between the groups are obvious and considerable. For example,the integument of reptiles is covered with scales, whereas amphibians have a highly permeable, glandular skin,a feature often touted as enhancing the environmental sensitivity of amphibians to

“

J. Whitfield Gibbons (e-mail: [email protected]) is a professor of

e c o l o gy at Savannah River Ecology Laboratory (SREL), U n i v e rsity of

G e o r g i a ,A i ke n , SC 29802. David E. Scott, Tr avis J. Rya n , Tr a c ey D.

Tu b e rv i l l e , Brian S. Metts, Judith L. Greene, To ny Mills, Yale Leiden,

Sean Po p py, and Christopher T. Winne are researchers at SREL.

Ku rt A. Buhlmann is coordinator for amphibian and chelonian con-

s e r vation at Conser vation Intern a t i o n a l , Center for Applied

B i o d i v e rsity Science, Wa s h i n g t o n , DC 20037.

RE P T I L E S PE C I E S A R E D E C L I N I N G O N A

G LO BA L S C A L E. SI X S I G N I F I C A N T T H R E ATS

TO R E P T I L E P O P U LAT I O N S A R E H A B I TAT

LO S S A N D D E G RA DAT I O N, I N T RO D U C E D

I N VA S I V E S PE C I E S, E N V I RO N M E N TA L

P O L LU T I O N, D I S E A S E, U N S U S TA I NA B L E

U S E, A N D G LO BA L C L I M AT E C H A N G E

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toxic chemicals in both terrestrial and aquatic situations (Vitt et al. 1990). Additionally, reptile e ggs possess a cal- careous shell, whereas amphibian eggs are enclosed by simple gelatinous membranes, making the eggs more sus- ceptible to uptake of environmental contaminants (but see Pechmann and Wilbur 1994). The differences between amphibians and reptiles are not limited to morphology and reproductive biology; they also include ecological and behavioral traits. Most amphibians rarely travel more than a few hundred meters over the course of their lives (Seml- itsch and Ryan 1998); many reptiles may move several kilometers both terrestrially and aquatically and have home ranges encompassing tens or hundreds of square kilometers (Brown 1993), and individual sea turtles may cover half the globe annually (Ernst and Bar bour 1989).

Nonetheless, the similarities between the ectothermic tetra pod s — a m ph i bians and reptiles—link them inex- orably. Species of both classes occupy similar habitats and are equally vulne rable to habitat degradation. Thus, syn- topic sp ecies o f amphibians and reptiles are correspond- ingly defenseless against the global threats of deforesta- tion,draining of wetlands,and pollution from agricultural runoff. Although the amphibian decline problem is a seri- ous threat, reptiles appear to be in even greater dang er of extinction worldwide (Table 1).

Population declines can be difficult to detect; hence, long-term studies of natural populations and communi- ties are generally regarded as indispensable for under- standing normal population trends and fluctuations (Ti n- kle 1979). Lon g - term studies of a m ph i bians and repti l e s doc u m ent tem poral va ri a ti on attri but a ble to natu ral causes (Cody 1996). For example, Shine (1991) reported dramat- ic declines in Au s tralia of the com m on bl ack s n a ke

(Pseudechis porphyriacus),a large frog-eating snake, due to food shortages during extended drought conditions. Only the smaller snakes survived, suggesting that large snakes may be relatively more susceptible to declines caused by food shortages.Gibbons (1990) reported a natural decline for an isolated population of slider turtles (Trachemys scripta) on a coastal island. The turtle population had no juvenile recruitment, presumably because of constant pre- dation on smaller individuals by alligators (Alligator mis - sissippiensis) that had become established on the island; only large adult turtles survived. Natural fluctuations and l ocal ex ti n cti ons are com m on in both reptiles and amphibians (Pechmann et al. 1991, Blaustein et al. 1994c) and generally are no cause for alarm. However, not all declines are natural.

In this article, we c onsider the vulnerability o f reptiles within the context of the factors known or suspected to be associated with amphibian declines, using the six cate- gories of concern established by Partners in Amphibian and Reptile Conservation (PARC; Gibbons and Stangel 1999): habitat loss and degradation, introduced invasive species, environmental pollution, disease and parasitism, unsustainable use, and global climate change. An addi- tional category comprises unexplained declines for both reptiles and amphibians, wherein the disappearance of populations or a d ecline in numbers is a c ertainty but the cause is unknown. Of course, decline of a species may often be a cumulative effect of more than one of the potential causes,as proposed for the documented declines of the Milos viper (Microvipera schweizeri) of Greece (Nil- son et al. 1999) and the asp viper (Vipera aspis) of the Swiss Jura mountains (Moser et al. 1984, Jaggi and Baur 1999).

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Ta ble 1. Co n serva tion status of reptiles and amphibi a n s ,a cco rding to the US Fish and Wi l dlife Servi ce (FWS ) , Co nven tion on In tern a tional Trade in En d a n gered Spe cies (CITES), and The Wo rld Co n serva tion Union (IUCN).

A p p r o x i m a t e number of F W Sb C I T E Sc I U C Nd

Ta x o n s p e c i e sa E n d a n g e r e d T h r e a t e n e d Appendix I Appendix II Appendix III E x t i n c t E n d a n g e r e d Vu l n e r a b l e A m p h i b i a n s 4 6 8 0 1 7 9 1 3 6 8 0 5 4 9 7 5 Frogs and toads 4 1 0 0 9 5 1 1 6 6 0 5 3 8 5 0 S a l a m a n d e rs 4 1 5 8 4 2 2 0 0 1 1 2 5 C a e c i l i a n s 1 6 5 0 0 0 0 0 0 0 0 R e p t i l e s 7 1 5 0 7 0 1 8 7 0 3 8 3 1 9 2 0 1 0 0 1 5 3 Tu rt l e s 2 6 0 3 3 4 2 5 4 9 6 6 3 8 5 8 C r o c o d i l i a n s 2 2 1 5 3 1 6 8 0 0 7 3 Tu a t a r a 2 2 0 2 0 0 0 0 1 L i z a r d s 5 0 6 6 1 4 8 1 6 2 3 8 0 1 1 3 0 6 6 S n a ke s 1 8 0 0 6 3 1 1 8 8 1 3 3 2 5 2 5

aThe approx i m a te nu m ber of s pecies for each taxon is from Po u gh et al. ( 1 9 9 8 ) . The nu m bers in the table ref l ect worl dwi de esti m a tes of s pecies on ly ( excluding su b s pecies and pop u l a ti ons) listed by each or ga n i z a ti on under sel ected con s erva ti on ra n k i n gs .

bData from FWS (2000). cAppendix I species are thre a ten ed with ex ti n cti on and are , or may be ,a f fected by trade ; Appendix II species are not curren t ly thre a ten ed but are likely to

become so unless trade is re s tri cted ; Appendix III species are listed to prevent or re s tri ct ex p l oi t a ti on . Data from CITES (2000). d“ Ex ti n ct” refers to com p l ete taxon omic ex ti n cti on , ra t h er than the IUCN category “ex ti n ct in wi l d ” ; “en d a n gered ”i n clu des those species listed by IUCN

as “c ri ti c a lly en d a n gered ” ;“ vu l n era bl e” i n d i c a tes that species are likely to become ex ti n ct if c u rrent trends con ti nu e . Data from IUCN–World Con s erva- ti on Un i on (2000).

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Our account is not exhaustive; rather, we provide docu- m en ted examples of reptile pop u l a ti ons in peril and decline. The aggregate of examples of amphibians and reptiles indicates that the world’s herpetofauna face stres- sors from both known and unknown origins that, without remediation,can only lead to c ontinuing declines, extirpa- tions, and extinctions.

Di s tinguishing natu ral declines fro m a n t h ropogenic ones Amphibian declines are indisputably real and disquieting on a global scale. Yet providing unequivocal supporting documentation for the decline of any par ticular popula- tion or species can be an one rous task, and some expecta- tions of scientific rigor may be unable to be met (Pech- mann et al. 1991). One persistent incertitude regarding amphibian declines is whether a decline is simply within the natural range of variability for a population or is instead a consequence of anthropogenic causes that could portend an unrecoverable situation.

One difficulty in dem on s tra ting wh et h er ob s erved trends in esti m a ted pop u l a ti on sizes con s ti tute norm a l f lu ctu a ti ons or “u n n a tu ra l ” declines is that most fiel d s tudies of a m ph i bians or reptiles have not had the du ra- ti on or con s i s tency to make su ch determ i n a ti ons con- vi n c i n gly (Pechmann and Wi l bur 1994). “Sn a p s h o t s” ( i . e . , s h ort - term mon i toring) of pop u l a ti on size and s tru ctu re may dem on s tra te current status but do not reve a l l on g -term t rends in population size or health. For example, Petranka et al. (1993), who used short-term monitoring, and Ash (1997), who did long-term monitor- ing, came to diff erent conclusions regarding the eff ects of clearcutting on recovery time of terrestrial salamander populations. To be sure,the st rongest support for a decline

is a long-t erm data set that has registered p opulation lev- els for particular sp ecies in par ticular locations. However, the accumulation of numerous accounts from shorter- term studies of a varie ty o f amphibian sp ecies in diverse

habitats and geographic regions lends credence to pleas for concern about declines.

Studies of decline among reptiles, like those c onducted for amphibians,have not always been carried out as rigor- ously as scientists would prefer. Nonetheless, the ever- increasing number of perceived declines among reptiles and the documentation of adverse impacts on individuals that pre su m a bly can be proj ected into dem ogra ph i c changes are harbingers of a crisis situation.Our int ent is to show the phylogenetic and geographic breadth of per- ceived problems with many reptiles, on the premise that they foreshadow a more intense and widespread problem.

Ha bitat loss and degra d a ti o n Many scientists consider loss of suitable habitat to be the largest single factor contributing to declines of amphib- ians (Al ford and Ri ch a rds 1999). For ex a m p l e , s om e regions of the Unit ed States retain less than 20% of the wetland acreage they once had (Leja 1998), and conse- quent d eclines in associated amphibian populations ha ve been d ocumented (Lannoo et al. 1994). Numerous semi - aquatic reptiles rely on those very same wetlands. In South Carolina, the elimination or alteration of more than 90% of Coastal Plain Carolina bay wetlands (Bennett and Nel- son 1991) has reduced essential habitat for black swamp snakes (Seminatrix pygaea), eastern green water snakes (Nerodia floridana),and chicken turtles ( Deirochelys retic - ularia), all of whose distribution patterns are restricted primarily to seasonal wetlands (Buhlmann 1995, Dorcas et al. 1998). Likewise, as bogs disappear in the eastern Unit- ed States, so too do bog turtles (Clemmys muhlenbergii), and as st reams and rivers are polluted, dammed, or chan- n el i zed , riverine map tu rtles (Gra ptemys) decl i n e (Buhlmann and Gibbons 1997). Even if the jurisdictional

wetland itself is protected, in many cases the surrounding terrestrial habitat needed by semiaquatic reptiles for nests, hibernation sites,and other refugia is not (Burke and Gib- bons 1995).

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Am eri c a n cro cod i l e . Li ke many cro cod i l i a n s ,t h i s s pe cies has su f f ered fro m co m m erci a l overexpl o i t a ti o n and habi t a t d e s tru cti o n .

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Just as habitat alterations may affect terrestrial salaman- ders (deMaynadier and Hunter 1995),they may also cause declines in terrestrial reptiles. The loss of 97% of the southeastern longleaf pine habitat (Ware et al. 1993), which has contributed to the decline of the flatwoods sala- mander (Ambystoma cingulatum; Means et al. 1996), has also redu ced su i t a ble habitat for goph er tortoi s e s (Gopherus polyphemus), eastern indigo snakes (Drymar - chon corais), and east ern diamondba ck rattlesnakes (Cro - talus adamanteus; Guyer and Bailey 1993,Stephen H. Ben- nett, South Carolina Natural Heritage, Columbia, SC, personal communication).

Cu l tiva ted pine plantati ons in sout h e a s tern So ut h Africa ha ve been implicated in the endangerment of the rare short-headed legless skink (Acontias breviceps) and the disappearance of another lizard (Eastwood’s long- tailed seps, Tetradactylus eastwoodae; Branch 1998). In the Chiricahua mountains of southeastern Arizona,the elimi- nation o f native bunchg rasses by cattle grazing was con- sidered to be the primary cause of a detectable decline in the bu n ch grass lizard (S cel opo rus sc a l a ri s) , wh i ch use bunchgrasses for cover from predators and f or protection from harsh winter conditions (Ballinger and Congdon 1996). Habitat loss is the biggest problem in the decline of snakes in Australia (Shine 1991). The link between intact habitat and species persistence and well-being is a basic tenet of ecology and conservation biology (Meffe and Car- roll 1994, Mittermeier et al. 1999) and needs no further discussion.

The mere presence of humans may constitute an insid- ious f orm o f habitat d egradation in some instances, even

if the habitat itself remains intact. Based on a 20-year study, a wood turtle (Clemmys insculpta) population of more than 130 animals in a forested watershed in New Haven County, Connecticut, has been virtually eliminated since the area became open to the public (Garber and Burger 1995). The possible mechanisms of decline includ- ed removal, road kill, handling by recreationists,increased number of predators attracted by food waste, and distur- bance by dogs.

In trodu ced inva s ive spe ci e s Introduced species have been cited as a problem for many amphibians (Stolzenburg 1999). For example, the distrib- ution and abundance of several western US frog species have been severely reduced by non-nat ive fishes and bul l- frogs ( Rana catesb eiana), which w ere and continue to be introduced to wetland “island”habitats of low- and high- elevation lakes (Fisher and Shaffer 1996). The collapse of endemic reptile faunas on true islands aft er the int roduc- tion of exotic species is similarly well documented and pervasive;non-native rats,cats,and mongooses have extir- pated numerous lizard species on many islands (Case and Bolger 1991). The tuatara (Sphenodon punctatus), a prim- itive reptile,historically inhabited the two main islands of New Zealand and at least 40 of the offshore islands (Daugherty et al. 1990). The tuatara became extinct on the main islands in the nineteenth century and on 10 offshore islands within the last few decades, and is experiencing population declines on many of the other islands as a result of introduced mammals, primarily rats. Feral pigs in the Galapagos Islands, first not ed by Darwin in 1835, are just one of the non-native species that have caused the near extinction of the Galapagos tortoise (Geochelone ele - phantopus; Thornton 1971). Introduced rats are suspected to have dest royed both the eggs and young of the tortois- e s , but the initial cause of decline was 18th-cen tu ry mariners who stopped at the islands and stocked their ships with live tortoises as food f or the sailors (Pritchard 1967).

Even the introduction of non-native reptiles can disrupt indigenous reptile communities. For example, Losos et al. (1993) showed that the invasion of Grand Cayman by exotic brown anoles (Anolis sagrei) caused behavioral changes and shifts in habitat use by the native species, Anolis conspersus. Likewise, the introduction of the brown tree snake (Boiga irregularis) has been implicated in the ex ti rp a ti on of the gecko (Na ctus pel a gi c u s) from the islands of Guam and Tinian; the brown tree snake is also considered responsible for dramatic declines in other species of native lizards on 13 of the Marianas Islands (Rodda 1992).

Although island faunas are most susceptible to disrup- tion, the detrimental effects of invasives on nat ive reptiles are not limited to islands. In the continental United States, i m ported fire ants (S ol en opsis invi ct a) , i n trodu ced in Mobile, Alabama, as early as 1918 (Wilson 1950), have

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B l a ck swamp snake . Loss of Ca rolina bay wetlands has re du ced habitat for bl a ck swamp snakes and ot h er sem i - a q u a tic reptile spe cies that are re s tri cte d pri m a ri ly to sea sonal wet l a n d s .

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been reported to prey on both eggs (Moulis 1997) and young (Allen et al.1997) of reptiles.Fire ants are implicat- ed as a primary cause of extirpation of the Texas horned lizard (Phrynosoma cornutum) from part of its geographic range (Goin 1992).

Invasive species need not be other animals. Both the desert tortoise (Gopherus agassizii) and the gopher tortoise are threatened by the introduction of non-native plant species (Stewart et al. 1993, Lovich 1995) that alter habitat structure, native plant community composition, and even fire frequency. The black legless lizard (Anniella pulchra nigra) was considered for federal endangered status, in part because of the negative impact of non-native Hotten- tot fig plants on the lizards’ prey base in disturbed sand- dune habitat (Rutherford and Rorabaugh 1995); nonethe- less, an official decision was made not to list the species after viable lizard populations were found in undisturbed habitat with native vegetation (Morey 1998). In Idaho, reptile sp ecies richness decreased an average o f 5% fr om 1978 to 1998 at 24 sample sites in the Snake River Birds of Prey Area (John Cossel Jr. and Charles R. Peterson, Idaho State University, Pocatello ID, personal communication). According to Cossel and Peterson, the changes in reptile populations may have been influenced by a decrease in native shrub habitat caused by the prevalence of exotic annual grasses and the effects of wildfires that have burned over 50% of the area since the 1970s.

Envi ro n m ental poll u ti o n Numerous environmental contaminants—metals, pesti- cides and herbicides,and radioactive waste, for example— have direct and indirect effects on both amphibians and reptiles (e.g., Hinton and Scott 1990, Hall and Henry 1992). Amphibians have been the subject of numerous ecotoxicological studies,including assessment of the direct effects of contaminants such as fertilizers (Marco et al. 1999) or the more subtle effects of steroid-mimicking con- taminants (Hayes 1997). Reptiles are studied far less than amphibians with respect to the fate and effects of contam- inants (Hopkins et al. 1999), but they ha ve received suffi- cient toxicological study to provide convincing evidence that some individual reptiles are adversely affected by many contaminants (Hall 1980, Fontenot et al. 1994). For example,slider turtles (Trachemys scripta) exposed to met- al and radioisotope contaminants incur genetic damage (Lamb et al. 1995). The degree to which contaminants cause population-level effects remains largely unknown, both for amphibians and f or reptiles.

Contaminant effects in reptiles are known mainly from turtles and crocodilians. Many turtles and crocodilians, because they have environmental sex determination and large eggs that can incorporate high levels of environmen- tal pollutants, are especially sensitive to endocrine-dis- rupting chemicals (Guillette and Crain 1996). At som e con t a m i n a ted site s , tu rtles acc u mu l a te PCBs (po lych l ori n a t- ed bi ph enyl s ) , d i el d ri n , and other contaminants in ti s su e s

and e ggs (Bishop et al. 1994, Cobb and Wood 1997); sex reversal and abnormal gonads have been found in turtles exposed to PCBs (Bergeron et al. 1994, Guillette et al. 1995). Male American alligators (Alligator mississippiensis) inhabiting Lake Apopka, a chemically contaminated lake in Florida, had significantly reduced plasma testosterone levels and permanent gonadal alt erations (Guillette et al. 1994).

Even nonlethal effects o f endocrine disrup ters on rep- tiles may result in demographic shifts whose consequences for p opulations are presumably d etrimental. Population- level effects might also occur through changes to patterns of individual energy allocation. For example, in coal-ash polluted wetlands, water snakes (Nerodia fasciata) with high body burdens of metal contaminants exhibit elevated metabolic rates, which may result in less energy being devoted to reproduction, growth, and storage (Hopkins et al. 1999).

Di sea se and pa ra s i ti s m Parasites and disease have been documented or suspected as causes for d eclines in some amphibian species (Daszak et al. 1999). In some cases, sublethal environmental stres- sors may suppress immune systems (Carey 1993) and allow disease agents to kill weak ened animals (Alf ord and Richards 1999). Recently, however, a spreading “extinction wave” of chytrid fungus is thought to be causing the decline of anurans in Central America and Australia (Berger et al. 1998, Lips 1999); moreover, researchers believe that the fungus is killing otherwise healthy animals (Daszak et al. 1999). An iridovirus may be the primary cause of the periodic population crashes in the Sonora

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Ha bitat loss and degra d a tion are pri m a ry threats to bot h a m p h i bian and reptile popu l a ti o n s . Co nversion of wet l a n d s , e s pe ci a lly sea sonal wet l a n d s , and su rrou n d i n g terre s trial habitat to agri c u l tu ral (ill u s tra ted here) and ot h er uses have re su l ted in wetland losses exceeding 80% in many state s .

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ti ger salamander, Am bys toma ti gri num stebbi n s i (Ja n- covi ch et al. 1 9 9 7 ) . Some amph i bian bi o l ogists now believe that disease may rival habitat destruction as the largest single cause o f the decline of amphibians.

Among reptiles, the widespread upper respiratory tract disease, a contagious respiratory ailment caused by the bacterium Mycoplasma agassizii, is a potential cause of population declines in desert tortoises in the US South- west and gopher tortoises in the Southeast (Jacobson 1993, Smith et al. 1998).Shell diseases have been implicat- ed in the decline of turtles (e.g., shell lesions on sliders, Lovich et al. 1996; cutaneous dyskeratosis affecting the shell and thickened forelimb scutes of desert tortoises, Jacobson 1994; and emaciation and lesions of the plastron of federally listed flattened musk turtles, Sternotherus depressus, Dodd 1988). Individuals in many green sea tur- tle p opulations are severely aff ected by viral fibropapillo- mas, resulting in g rowths that can impair vision, locomo- tion,and feeding ability (Herbst 1994). As is often the case in amphibians,diseases that are debilitating to wild popu- lations of reptiles are most likely secondary expressions in individuals with impaired resistance caused by one or more primary environmental stressors, such as habitat degradation, invasive species, or pollution.

Un su s t a i n a ble use Human use of animals,including reptiles and amphibians, is an integral part of many cultures. Harvesting must be bi o l ogi c a lly su s t a i n a bl e , h owever, i f pop u l a ti ons and species are to persist (Pough et al. 1998). Overcollection for food, the pet trade, and biological supply houses has been suggested as having had an impact on some amphib- ian p opulations (D odd 1997). In the Unit ed States, note- worthy examples for amphibians occurred in the late 1800s to early 1900s, when commercial collectors harvest- ed for the frog legs market. Hundreds of thousands of

red - l eg ged fro gs (R ana auro ra d ray to n i i) were collect- ed from wetlands in California (Jennings and Hayes 1985), and over 20 million leopard frogs (Rana pipiens) were tak- en annually in northwestern Iowa (Lannoo et al. 1994). Midwestern wetlands today harbor fewer frogs,although it is difficult to apportion the relative losses among the caus- es of wetland habitat destruction and degradation, intro- duction of predators, and previous commercial impacts (Lannoo et al.1994). In India,the fr og-leg trade has result- ed in severe population declines of the Indian bullfrog (Rana tig rina) and the green pond frog (Rana hexadacty - la); an estimated 70 million frogs are exported illegally each year (Oza 1990).

Human use of a species is su s t a i n a ble if it can be con- ti nu ed indef i n i tely wi t h o ut adverse ef fects on pop u l a ti on su rvival (Ross 1998). Mu ch of the use of reptiles is cl e a r- ly unsu s t a i n a bl e . Com m ercial impacts on reptiles have been more perva s ive and severe than on amph i bians (e.g. , s ee Wi lliams 1999). The severi ty of the tu rtle crisis on a gl obal scale was em ph a s i zed by Rh odin (1999), wh o reported that of the approx i m a tely 293 taxa (mainly s pec i e s , but including some su b s pecies) of f re s hw a ter tu r- t l e s , tortoi s e s , and sea tu rtles known to be extant over the last few cen tu ri e s , 3% (9 taxa) are alre ady ex ti n ct in the wi l d . An ad d i ti onal 4% (12 taxa) are cri ti c a lly en d a n- gered , 11% (32 taxa) are en d a n gered , and 21% (61 taxa) a re vu l n era bl e .

The crisis is particularly acute for Asian freshwater tur- tles and tortoises, which are harvested as a local food source. Moreover, the international trade in turtles— which are eaten, sold as pets, or used in traditional Chi - nese medicinal remedies—is both extensive and unregu- lated (Sharma 1999). A recent report indicated that most turtle sp ecies in Vietnam and southern China are endan- gered and that turtles can no longer be found in the wild in Vietnam (Kiester and Juvik 1997). China is the biggest consumer of turtles in the food trade. Because the trade in turtles is not regulated, few records have been kept, but existing records indicate that the trade in live turtles to China is thousands of tons per year (Mockenhaupt 1999). The commercial trade in freshwater turtles exceeds any possible sustainable le vels, and extinction of some species in the wild can be expected within the next d ecade.

Most species of sea turtles continue to decline in all warm oceans of the world. The leatherback sea turtle (Dermochelys coriacea) was recently reported to be “on the road to extinction and further p opulation declines can be expected”unless appropriate measures are taken to reduce mortality rates in adults, hatchlings, and eggs (Spotila et a l . 1 9 9 6 ) . The esti m a ted worl dwi de pop u l a ti on of leatherbacks nesting on beaches in 1980 was 115,000, com p a red with just 34,500 in 1995. Ex p l oi t a ti on of leatherbacks in the Atlantic Ocean, through illegal har- vesting of both adults and eggs,is considered to be a major contributor to the decline of the species (Spotila et al. 1996). Likewise, for Kemp’s Ridley sea turtle ( Lepidochelys

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Ea s tern box tu rt l e . The pet trade appea rs espe ci a lly h a z a rd ous for some tu rtle spe ci e s , su ch as the ea s tern box tu rt l e .

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kempii), harvests of nesting females and their eggs on the largest known nesting site contributed to declines from 42,000 nesting females in 1947 to only a few hundr ed b y 1975 (Hildebrand 1982).

Among North American turtles, the diamondback t er- rapin (Ma l a cl emys terra p i n) , a small , e s tu a rine tu rt l e species with a geographic range from Cape Cod to Texas, decl i n ed severely fo ll owing heavy ex p l oi t a ti on as a gourmet food item from the late 1800s to the early 1900s (Carr 1952). With forced r eductions in harvesting, many populations were able to recover, but the terrapin now faces significant new threats, including highway mortality (Wood and Herlands 1997) and drowning in commercial and recreational crab traps (Bishop 1983, Roosenburg 1991). Renewed c ommercial har vest of the diamondba ck terrapin has also been documented (Garber 1988).

Commercial turtle trappers for the restaurant trade stepped up harvests of one of the largest freshwater turtles in the world, the alligator snapper (Macroclemys tem - minckii), from the 1960s through the 1980s (Roman et al. 1999). Consequently, as evidence from survey efforts sug- gests, the species has b een drastically reduced in numb ers in some of the southeastern US rivers it once inhabited (Moler 1992, Jensen 1998).

The enormous and once common populations of the arrau (Podocnemis expansa), a communally nesting turtle of the Orinoco and Amazon Rivers in South America, are now g reatly reduced in size because o f human c onsump- tion of eggs and nesting females (Pritchard and Trebbau 1984), an overexploitation problem identified almost two centuries ago (Humboldt 1814, from Pritchard and Treb- bau 1984). Declines from similar causes have befallen the terecay (Podocnemis unifilis) in tropical lowlands of South America (Thorbjarnarson et al. 1993) and the river ter- rapin (Batagur baska) in India (Bhupathy 1997).

Overharvesting for food is a problem not just for turtles but also for lizards,having contributed to declines in green iguanas (Iguana iguana) and spiny - t a i l ed iguanas (Ctenosaura similis) in tropical America (Fitch et al.1982).

The pet trade appears especially hazardous for some turtle sp ecies. In 1994, population d eclines were reported in box turtles (Terrapene carolina) in 16 states, ranging from Massachusetts to Florida and Oklahoma t o Wiscon- sin (Lieberman 1994). Doc u m en t a ti on of box tu rt l e decl i n e s — i n cluding records showing that, s i n ce 1995, 29,896 box turtles had been collected for the pet trade and shipped fr om Louisiana—resulted in unanimous passage of Act 81 by the Louisiana Senate and House of Represen- tatives in 1999;the act prohibits the commercial harvest of the state’s native box turtle populations. Overcollection for export is a serious factor in much of the box turtle decline and may exacerbate the eff ects of habitat loss (Lieberman 1994). Habitat destruction and illegal collecting for the pet trade are the primary threats to bog turtles (Clemmys muhlenbergii); Copeyon 1997). The number of northern populations has been reduced by 50%, with most of the

decline occurring over the last 20 years. Of the 191 remaining bog turtle habitats known in 1996,33 w ere clas- sified as in good c ondition, 67 as fair, and 76 as poor; the status of 15 was unknown.

Overcollecting is also a problem for some snake species. The ocellated mountain vip er (Vipera wagneri) in east ern Turkey has been sought by the pet trade and removed from the wild in large numbers, posing “a serious threat to survival of the species” (Nilson et al. 1990). Populations of several boa and python species have declined because of harvesting of wild snakes for their skins (Pough et al. 1998). Rapid d eclines o f large-bodied snakes, which tend to have a suite of life-history traits that make them more susceptible to population declines than smaller species (e.g., Dodd 1993),have been documented throughout the world in recent years (e.g.,Shine and Fitzgerald 1996). For example, females of the increasingly rare timber rat- tlesnake (Crotalus horridus), which may exceed a meter in length and typically take 9 years to reach maturity, pro- duce fewer than a dozen young every 3 years (Brown 1993).Large-bodied species such as rattlesnakes (Crotalus) have long generation times, a life-history t rait that, when com bi n ed with habitat loss, human pers ec uti on , a n d i n ten s ive overco ll ecti on (e.g. , “ra t t l e s n a ke ro u n du p s” ; Brown 1993),has led to dramatic declines of some species and ma de ap proximately one-third of rattlesnake sp ecies vulnerable to extinction (Greene 1997). High harvest rates of snakes with low reproductive frequencies, such as the f i l e s n a ke (Acro ch o rdus ara f u ra e) in Au s tra l i a , wo u l d almost certainly be unsustainable (Shine et al. 1995).

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Sn a pping tu rtle eggs and hatch l i n gs . Most co n t a m i n a n t s tudies on reptiles have be en co n du cted on snapp i n g tu rtles and all i ga to rs , in wh i ch sex reversal and abn o rm a l gonads have be en note d .

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These examples demonstrate that sustainable use of some long-lived reptile species is problematic. Because longevity in reptiles is associated with delayed sexual m a tu ri ty, h i gh adult su rvivors h i p, and low fec u n d i ty (Pough et al.1998), populations of long-lived species can- not r emain stable (or grow) when adults and older juve- niles are harvested at high rates (Congdon et al. 1993, 1994). This is not to say, however, that all such long-lived species should be c ommercially off-limits. The key to sus- tainability is having species- and population-specific man- agement plans and tightly controlled use (Ross 1998).

For example, three decades ago, several species of croc- odilians were on the verge of extinction because of a com- bination of threats, including habitat destruction (Ross 1998) and unsustainable harvest o f adults f or the leather trade (Brazaitis 1989). After years of total protection, sev- eral sp ecies ha ve r ecovered; a f ew are farmed or ranched commercially (King 1989). In some crocodile species, adult females are protected and only small numbers of eggs, small juveniles, and larger males are removed from the wild (King 1989). In contrast, 7–8% of all alligators more than 1.2 m in length are har vested annually in some Florida populations (David et al.1996). In addition,a 50% annual harvest rate of alligator eggs or hatchlings is allowed because removal at these life stages does not reduce recruitment into adult-size classes (Rice et al. 1999). Closely monit ored alligator populations, and pre- sumably populations of other long-lived species of rep- tiles, can sustain the legal, regulated har vest o f some pro- porti on of eggs , h a tch l i n gs , or adults with negl i gi bl e effects.

G l obal cl i m a te ch a n ge Few ecologists will dispute the link between increases in greenhouse gases and gl obal tem pera tu re . However, whether the current rate of climate change reflects natural variation or has an anthropogenic cause is hotly debated. For the purposes of this article, we accept the argument that the earth is undergoing unprecedented rapid climatic change (Schneider and Root 1998) that includes alter- ations in climate variables such as temperature and rain- fall patterns, storm severity, and storm frequency. If one accepts that human-induced climate change is occurring (e.g., Vinnikov et al.1999),then the consequences for her- petofaunal diversity can be addressed.

The obvious effects of climate change on biodiversity are mediated through changes in habitat. For example, global warming may further diminish prairie wetland habitat in the United States (Poiani and Johnson 1991). Future wetland acreage in the United States may be g reat- ly reduced under a variety of climate circulation models (Halpin 1997), and aquatic and semiaquatic species will suffer declines as habitat disappears. Although many habi- tats are ex pected to under go dra m a tic ch a n ge (e.g. , Guertin et al.1997,Still et al. 1999), predictions of species habitat shifts in response to global warming cannot be

based solely on analyses of climate–space changes, because species distributions are also a function of dispersal abili- ty and biotic interactions (Davis et al. 1998). Existing nature reserves will be inadequate to preserve current bio- diversity, because an already fragmented landscape will i m pede the abi l i ty of s pecies to re s pond to cl i m a te - induced habitat changes (Halpin 1997). Because of their limited dispersal abilities, reptiles and amphibians are especially vulnerable to rapid habitat changes and may suffer many more extinctions than birds as a result of a rapid rate of climate change (Schneider and Root 1998).

In discussions of observed amphibian declines, little mention has been ma de o f climate change (Dodd 1997), with two notable e xceptions. First, the famed golden toad (Bufo p eriglenes) extinc tion in Costa Rica may have b een caused,at least in part, by global warming effects on mon- tane dry-season mist frequencies (Pounds et al. 1999). Fauna in tropical montane cloud forests may be particu- larly susceptible to rapid climate shifts that may change patterns of cloud formation and thereby the availability of water (Still et al. 1999). Second, Blaustein et al. (1994a) have suggested that ultraviolet B (UVB) radiation has adverse effects on some amphibians, including reduced hatching success and decreased sur vival to metamorpho- sis. However, an increase in the level of UVB caused by depletion of the ozone layer probably does not pose an i m m ed i a te threat to reptile eggs , wh i ch are sel dom exposed to UVB radiation.

As with the amphibian studies, few researchers have directly assessed effects of climate change on r eptiles. It is nonetheless reasonable to expect that climate changes could re sult in con d i ti ons that el i m i n a te or severely restrict sp ecies with limited dist ributions (Schneider and Root 1998), as has been suggested for some Australian lizards (Brereton et al.1995) and crotaline snakes of North America and the neotropics (Greene and Campbell 1993). Additional effects of warming on some reptiles, based on em p i rical evi den ce with fre s hw a ter tu rt l e s , i n clu de enhanced juvenile growth rates, earlier ages at maturity, and shifts in functional sex ratios (Frazer et al. 1993). Global warming may have the greatest impact on those reptiles (crocodilians and some turtles) that have temper- ature-dependent sex determination (Janzen 1994), where- by the sex ratio of the hatchlings is determined by nest temperatures during incubation. Unless shifts occur in the pivotal temperatures at which sex is determined, or female nest-site choices (i.e., shade versus sun) evolve to keep pace with rising temperatures, altered sex ratios could affect population demographics and persistence.

En i gm a tic decl i n e s Finally, in addition to the many cases of declines that have s ome re a s on a bly unders tood causes, s ome amph i bi a n populations have declined, and even gone extinct, without any discernible causes. One well-known example is the gastric brooding frog (Rheobatrachus silus) of Australia.

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S h ort ly after the discovery of its unu sual sys tem of parental care, in which the young develop in the safety of the mother’s stomach (Tyler and Car ter 1981), the gastric brooding frog ceased to be found in nature. Disjunct pop- ulations o f the g reen salamand er ( Aneides aeneus ) in the s o ut h ern App a l achians have app a ren t ly decl i n ed , but without similar declines in other portions of its range (Jeff Corser, USGS-BRD, Twin Creeks Resource C enter, GSM- NP, Gatlinburg, TN, personal communication).

Similar cases exist for reptiles. For example, no living specimen of the Round Island burrowing boa (Bolyeria multocarinata) in the Indian Ocean has been seen since 1975 (Bullock 1986); the species may have become extinct in recent decades (Greene 1997). Although all species of reptiles native to North America in precolonial times per- sist in some regions, the current ranges of many are but a remnant of the much larger areas formerly occupied. Nat- ural populations of indigo snakes have not b een found in some regions of their historic range in more than 40 years (Mount 1975, Conant and Collins 1998),and the species is “declining in abundance and distribution throughout its U.S. geographic range” (Hallam et al. 1998). Likewise, s i gh ti n gs of the sout h ern hognose snake (Heterod o n simus) h ave not been reported from ei t h er Alabama or Mi s- s i s s i ppi in more than 18 ye a rs (Tu bervi lle et al. 2 0 0 0 ) , even in large pro tected areas with rel a tively pri s tine habi t a t s .

Do c u m en ting decl i n e s Regrettably, many amphibian populations and species that are thought to be declining have not been monitored over long periods of time, making short-term changes in pop- ulation size difficult to evaluate critically. The best long- term studies of amphibian populations that allow for crit- ical evaluation of population trends share a common characteristic: The subjects of these studies occur in high density either spatially (e.g., Jordan’s salamander, Plethod - on jordanii; Hairston 1987) or temporally (e.g., mole sala- manders, Ambystoma talpoideum; Pechmann et al. 1991; and natterjack toads, Bufo calamita; Banks et al. 1994).

Many of the sp ecies that have b ecome symbols for the declining amphibian phenomenon are seasonally active anurans that arrive over restricted periods of time at breeding sites where they congregate in greater densities than at any other time of the year. Researchers sit ready to record their ar rival and abundance, and if the animals fail to show up when expected,a problem is suspected; if such absences are protracted, then the change is presumably real (Blaustein et al. 1994c). The phenology of these amphibians permits d etection of breeding activity; there- fore, determination of whether the absence of breeding adults is a short-term aberration or an indication of a real decline becomes a matter of accumulating the data ne ces- sary to demonstrate a statistically significant trend (for discussion, see Blaustein et al. 1994c, Pechmann and Wilbur 1994, Reed and Blaustein 1995).

Among r eptiles, declines in sea turtles are perhaps the

best documented because, like many amphibians, they engage in an annual reproductive event (in this case, oviposition) with a predictable site and time. A few snake species in colder temperate regions are known to hiber- nate communally, and numbers can be assessed upon

emergence (Parker and Brown 1973). But what of the majority of reptile species that do not congregate to breed or hibernate and do not occur in particularly high densi- ties? F or example, the r acer ( Coluber const rictor), a c om- mon North American snake, is found in a wide variety of terrestrial habitats. Like most other e ctotherms, racers are more active, and therefore more commonly encountered, in the warmer months. However, aside from some regions where communal hib ernation o ccurs (Par ker and Brown 1973), determining the abundance of racers is difficult because of their stochastic patterns of activity. Herpetolo- gists would be hard-pressed to describe densities accurate- ly du ring any season over a wi de geogra phic ra n ge . Because r acers do not congregate at a breeding site, how could we take a census to know when and if racer popula- tions were declining at a substantial rate on a widespread

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Sou t h ern hogn o se snake . This spe cies has not be en re co rded from regions of its histo ric ra n ge in Al a ba m a and Mi s s i s s i ppi for more than 18 yea rs . Its disappea ra n ce is so m ewhat mys teri ou s , as the rea sons for its decline are n ot well unders tood .

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basis without mounting an intensive, long-term sampling program? The clandestine nature of many r eptiles, often combined with comparatively large home ranges, low pop u l a ti on den s i ti e s , and ra reness of con grega ti on a l behavior, makes documenting population trends very dif- ficult. As a result, populations may wither with little notice.Once an unmonitored species or population is rec- ognized as b eing unexpectedly depauperate or absent, the cause of decline may be unknown and unknowable.

Based on the accumulated evidence that many if not most declines reported for amphibians are indeed real,the proper course for conservation initiatives is to assume the worst for all herpetofauna, and therefore to implement abatement measures while gathering more data. Although the lack of long-term data often may preclude the id enti- fication of the cause of a decline, or even in some cases the corroboration o f a d ecline, the absence of that data does not rule out the exist ence of a correctable problem.

Co n clusion and re co m m en d a ti o n s The declines of m a ny reptile pop u l a ti ons are similar to those ex peri en ced by amph i bians in terms of t a xon om- ic bre ad t h , geogra phic scope , and severi ty. As wi t h a m ph i bi a n s , the causes are known with cert a i n ty in s ome instance s , su s pected in many, and unknown in o t h ers . Some ex ti rp a ti ons are local wh ereas others are m ore wi de s pre ad . The difficulty in doc u m en ting the s cope and source of e ach reptile (or amph i bian) pop u- l a ti on decline should not be undere s ti m a ted .

Biologists must be pragmatic in assessing which causes of pop u l a ti on declines can be obvi a ted direct ly. Th e i m p act of h a bitat degrad a ti on ,i n trodu ced inva s ive spec i e s , and unsu s t a i n a ble use can be con tro ll ed immed i a tely and

proximally through legislation and cultural shifts in envi- ronmental attitudes. Minimally, society must place a pre- mium on maintaining habitats of sufficient size and qual- ity not only for imperiled taxa but for herpetofauna in general (Beebee 1992, Semlitsch 1998). For example, pro- tecting the basins of wetlands is pointless if the surround- ing terrestrial zone that is fundamentally linked to the wet- land is allowed to be destroyed. Second, the release of invasive non-native species that could be harmful to rep- tile populations must be proscribed. Third, restricting trade in sensitive reptile species for which sustainable removal cannot be demonstrated will require the passage or strengthening and enforcement of legislation. In the case of Asian turtles, legislative remedies could be too lit- tle, too late—a stopgap remedy is necessary. The only way to p revent the imminent extinction o f a large number of the more than 80 species of turtles native to southern Asia will be to maintain populations in ex situ captive breeding and genetic reserve programs. With changes in cultural attitudes,strengthening of international trade regulations, and increased habitat protection, the reintroduction of these species into the wild may be possible.

Much o f today’s commercial exploitation of reptiles in the Unit ed States and elsewhere requires urgent govern- mental a ction to implement internationally a ccepted and enforced controls. Despite the fact that conservation mea- sures can be implemented effectively through legislation (as happened with legislation for protection of Louisiana box turtles and American alligators), the political pres- sures against accomplishing such goals cannot be overstat- ed. The lack of support by the World Trade Organization for recommendations to curtail sea turtle exploitation (WTO 1998) brings the problem into perspective on an international scale.

Direct and indirect eff ects o f environmental pol lution, disease and parasitism, and global climate change are more difficult to quantify in many instances and will be more difficult to change in the short term. Nonetheless, we must endeavor to understand these potential factors to ameliorate their impact on natural p opulations of reptiles and their habitats.

Finally, long-term monitoring o f reptile p opulations is essential and must be aided by the establishment of stan- dard methods and techniques. It is equally important that the aca demic community, land managers, and conserva- tion organizations recognize that rigorous field programs focusing on the distri buti on , a bu n d a n ce , s t a tu s , a n d trends o f populations and species are critical and worth- while. Herpetofaunal inventories should become a stan- dard part of environmental assessment programs, and the publication of field survey efforts that document potential or susp ected d eclines should be encouraged. When long- term and widespread monitoring becomes the norm, declines are likely to become less equivocal (in terms of protracted declines versus natural fluctuations) and the causes less mysterious.

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Sand monitor (Va ra nus go u l d i ). Al t h ou gh sand m o n i to rs (genus Va ra nu s, wh i ch includes the wo rl d ' s l a rgest lizards) appear to be thriving in many pa rts of t h eir natu ral habitats in Au s tra l i a , ot h er spe cies of t h e genus in As i a , Afri c a , and the East Indies are threa ten e d by exten s ive habitat destru cti o n .

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The disappearance of reptiles from the natural world is genuine and should be a matter of concern not simply because of reptiles’ perceived associations with amphib- ians, but because reptile declines,like those o f amphibians, are growing and serious in their own right. Current evi- dence suggests that amphibian and r eptile declines, which are exa cerbated by burgeoning human populations, con- stitute a worldwide crisis.

Ack n owl e d gm en t s Manuscript preparation was aided by Financial Assistance Aw a rd Nu m ber DE-FC09-96SR18546 from the US Dep a rtm ent of E n er gy to the Un ivers i ty of G eor gi a Research Foundation. We thank Ab Abercrombie, Justin Congdon, William Hopkins, Laura Janecek, Christopher Romanek, and Joseph Pechmann for discussion and com- ments on the manuscript. We also appreciate the help of Stephen H. Bennett, John Cossel Jr., Charles R. Peterson, Paul Moler, Woody Woodward,and Jeff Corser for provid- ing information on the status of particular species. This paper supports the PARC (Partners in Amphibian and Reptile C onservation) eff ort to promote education abou t reptiles and amphibians.

Ref eren ces ci te d Al ford RA , Ri ch a rds SJ. 1 9 9 9 . G l obal amph i bian decl i n e s : A probl em in

a pp l i ed eco l ogy. An nual Revi ew of E co l ogy and Sys tem a tics 30: 1 3 3 – 1 6 5 . All en CR, Ri ce KG , Wojcik DP, Perc ival HF. 1 9 9 7 . E f fect of red imported

f i re ant enven om i z a ti on on neonatal Am erican all i ga tors . Jo u rnal of Herpeto l ogy 31: 3 1 8 – 3 2 1 .

Ash A N .1 9 9 7 . Di s a ppe a ra n ce and retu rn of s a l a m a n ders to cl e a rc ut plots in the sout h ern Blue Ri d ge mountains. Con s erva ti on Bi o l ogy 11: 9 8 3 – 9 8 9 .

Ba ll i n ger RE, Con gdon JD. 1 9 9 6 . S t a tus of the bu n ch grass lizard , S cel o - po rus sc a l a ri s, in the Ch i ri c a hua mountains of s o ut h e a s tern Ari zon a . Bu ll etin of the Ma ryland Herpeto l ogical Soc i ety 32: 6 7 – 6 9 .

Banks B, Beebee TJC, Coo ke KS. 1 9 9 4 . Con s erva ti on of the natter jack toad B u fo calamita in Britain over the peri od 1976–1990 in rel a ti on to site pro tecti on and other factors . Bi o l ogical Con s erva ti on 67: 1 1 – 1 1 8 .

Beebee TJC. 1 9 9 2 . Am ph i bian decline? Na tu re 355: 1 2 0 . Ben n ett SH, Nel s on JB. 1 9 9 1 . Di s tri buti on and status of Ca rolina bays in

So uth Ca ro l i n a . Co lu m bia (SC): Non game and Heri t a ge Trust Pu bl i- c a ti on 1. Ava i l a ble from : So uth Ca rolina Wi l dl i fe and Ma ri n e Re s o u rces Dep a rtm en t , Co lu m bi a ,S C .

Ber ger L, et al. 1 9 9 8 . Chytri d i omycosis causes amph i bian mort a l i ty assoc i- a ted with pop u l a ti on declines in the ra i n forests of Au s tralia and Cen- tral Am eri c a . Proceed i n gs of the Na ti onal Ac ademy of S c i en ces of t h e Un i ted States of Am erica 95: 9 0 3 1 – 9 0 3 6 .

Ber geron JM, Crews D, Mc L achlan JA .1 9 9 4 . PCBs as envi ron m ental estro- gen s : Tu rtle sex determ i n a ti on as a bi om a rker of envi ron m ental con t- a m i n a ti on .E nvi ron m ental Health Pers pectives 102: 7 8 0 – 7 8 1 .

Bhu p a t hy S. 1 9 9 7 . Con s erva ti on of the en d a n gered river terrapin Ba t a g u r ba s k a in the Su n derban of West Ben ga l , In d i a . Jo u rnal of the Bom b ay Na tu ral Hi s tory Soc i ety 94: 2 7 – 3 5 .

Bi s h op CA, Brown GP, Brooks RJ, Lean DRS, Ca rey JH. 1 9 9 4 .O ra n och l o- rine contaminant con cen tra ti ons in eggs and their rel a ti onship to body s i ze and clutch ch a racteri s tics of the female com m on snapping tu rt l e (C h elyd ra serpen tina serpen ti n a) in Lake Ontari o, Ca n ad a . Arch ives of E nvi ron m ental Con t a m i n a ti on Tox i co l ogy 27: 8 2 – 8 7 .

Bi s h op JM. 1 9 8 3 . In c i dental captu re of d i a m on d b ack terrapin by crab po t s . E s tu a ries 6: 4 2 6 – 4 3 0 .

Bl a u s tein A R , Hoffman PD, Hokit DG , Ki e s ecker JM, Wa lls SC, Hays JB. 1 9 9 4 a . UV repair and re s i s t a n ce to solar UV-B in amph i bian eggs : A link to pop u l a ti on declines? Proceed i n gs of the Na ti onal Ac ademy of S c i en ce of the Un i ted States of Am erica 91: 1 7 9 1 – 1 7 9 5 .

Bl a u s tein A R , Hokit DG , O’ Ha ra RK, Holt RA .1 9 9 4 b. Pa t h ogenic fungus con tri butes to amph i bian losses in the Pacific Nort hwe s t . Bi o l ogi c a l Con s erva ti on 67: 2 5 1 – 2 5 4 .

Bl a u s tein A R , Wa ke DB, Sousa W P. 1 9 9 4 c . Am ph i bian decl i n e s : Ju d gi n g s t a bi l i ty, pers i s ten ce , and su s cepti bi l i ty of pop u l a ti ons to local and gl obal ex ti n cti on s . Con s erva ti on Bi o l ogy 8: 6 0 – 7 1 .

Bra n ch B. 1 9 9 8 .F i eld Gu i de to Sn a kes and Ot h er Reptiles of So uth Af ri c a . Sa n i bel Island (FL): Ra l ph Cu rtis Boo k s .

Bra z a i tis P. 1 9 8 9 . The trade in crocod i l i a n s . Pa ges 196–201 in Ross CA, ed . Crocodiles and All i ga tors . New York : Facts on File.

Brereton R, Ben n ett S, Ma n s er gh I. 1 9 9 5 . E n h a n ced greenhouse cl i m a te ch a n ge and its po ten tial ef fect on sel ected fauna of s o ut h e a s tern Au s- tra l i a : A trend analys i s . Bi o l o l ogical Con s erva ti on 72: 3 3 9 – 3 5 4 .

Brown WS . 1 9 9 3 . Bi o l ogy, s t a tu s , and managem ent of the ti m ber ra t- t l e s n a ke (Crotalus horri du s) : A guide for con s erva ti on . Soc i ety for the S tu dy of Am ph i bians and Repti l e s . Herpeto l ogy Ci rc u l a ti on 22: 1 – 7 2 .

Buhlmann KA .1 9 9 5 . Ha bitat use, terre s trial movem ents and con s erva ti on of the tu rtle Di ero ch elys reti c u l a ri a in Vi r gi n i a . Jo u rnal of Herpeto l ogy 2 9 :1 7 3 – 1 8 1 .

Buhlmann KA ,G i bbons JW. 1 9 9 7 . Im peri l ed aqu a tic reptiles of the sout h- e a s tern Un i ted State s : Hi s torical revi ew and current con s erva ti on sta- tu s . Pa ges 201–232 in Benz G, Co llins DE, ed s . Aqu a tic Fauna in Peri l : the So ut h e a s tern Pers pective . Dec a tur (GA): Lenz De s i gn & Com mu- n i c a ti on s .

Bu ll ock DJ. 1 9 8 6 . The eco l ogy and con s erva ti on of reptiles on Ro u n d Island and Gu n n er ’s Quoi n , Ma u ri tiu s . Bi o l ogical Con s erva ti on 37: 1 3 5 ,1 5 6 .

Bu rke V J, G i bbons JW. 1 9 9 5 . Terre s trial bu f fer zones and wetland con s er- va ti on : A case stu dy of f re s hw a ter tu rtles in a Ca rolina Bay. Con s erva- ti on Bi o l ogy 9: 1 3 6 5 – 1 3 6 9 .

Ca rey C. 1 9 9 3 . Hypothesis con cerning the causes of the disappe a ra n ce of boreal toads from the mountains of Co l orado. Con s erva ti on Bi o l ogy 7: 3 5 5 – 3 6 2 .

Ca rr A F. 1 9 5 2 . Ha n d book of Tu rt l e s . The Tu rtles of the Un i ted State s , Ca n ad a , and Ba ja Ca l i forn i a . It h aca (NY) : Com s tock Pu bl i s h ers As s o- c i a ti on , Corn ell Un ivers i ty Pre s s .

Case TJ, Bo l ger DT. 1 9 9 1 . The role of i n trodu ced species in shaping the dis- tri buti on and abu n d a n ce of island repti l e s . Evo luti on a ry Eco l ogy 5: 2 7 2 – 2 9 0 .

Cobb GP, Wood PD. 1 9 9 7 . PCB con cen tra ti ons in eggs and ch ori oa ll a n to- ic mem branes of l oggerh e ad sea tu rtles (C a retta caret t a) from Ca pe Romain Na ti onal Wi l dl i fe Ref u ge . Ch em o s ph ere 34: 5 3 9 – 5 4 9 .

Cody ML. 1 9 9 6 . In trodu cti on to lon g - term com mu n i ty eco l ogical stu d i e s . Pa ges 1–15 in Cody ML, Sm a llwood JA , ed s . Lon g - term Studies of Ver- tebra te Com mu n i ti e s . San Di ego : Ac ademic Pre s s .

Conant R. 1 9 7 2 . Reptile Stu dy. Official boo k l et for Merit Bad ge Seri e s . Irv- ing (T X ) : Boy Sco uts of Am eri c a .

Conant R, Co llins JT. 1 9 9 8 . Reptiles and Am ph i bians of North Am eri c a . 4th ed . New York : Ho u gh ton Mi f f l i n .

Con gdon JD, Dunham A E , van Loben Seals RC . 1 9 9 3 . Del ayed sex u a l m a tu ri ty and dem ogra phics of Bl a n d i n g’s tu rtles (Emyd o i d e a bl a n d i n gi i) : Im p l i c a ti ons for con s erva ti on and managem ent of l on g - l ived or ga n i s m s . Con s erva ti on Bi o l ogy 7: 8 2 6 – 8 3 3 .

_ _ _ _ _ _ .1 9 9 4 . Dem ogra phics of com m on snapping tu rtles (C h elyd ra ser - pen ti n a) : Im p l i c a ti ons for con s erva ti on and managem ent of l on g - l ived or ga n i s m s . Am erican Zoo l ogist 34: 3 9 7 – 4 0 8 .

[CITES] Conven ti on on In tern a ti onal Trade in Endangered Species of Wild Fauna and Flora . 2 0 0 0 . < w w w. c i te s . or g / C I T E S / en g / a ppen d / s pec i e s . s h tml> (7 Jan 2000).

Copeyon CK. 1 9 9 7 . E n d a n gered and thre a ten ed wi l dl i fe and plants: F i n a l rule to list the nort h ern pop u l a ti on of the bog tu rtle as thre a ten ed and the sout h ern pop u l a ti on as thre a ten ed due to similari ty of a ppe a ra n ce . Federal Regi s ter 62: 5 9 6 0 5 – 5 9 6 2 3 .

August 2000 / Vol. 50 No. 8 • BioScience 663

Articles

Downloaded from https://academic.oup.com/bioscience/article-abstract/50/8/653/243214 by Central Washington University user on 12 April 2018

Daszak P, Ber ger L, Cu n n i n gham A A , Hyatt A D, Green DE, S pe a re R. 1 9 9 9 . E m er ging infectious diseases and amph i bian pop u l a ti on decl i n e s . < w w w. cdc . gov / n c i dod / E I D / vo l 5 n o 6 / d a s z a k . h tm> (15 Nov 1999).

D a u gh erty CH, Cree A , Hay JM, Th om p s on MB. 1 9 9 0 . Negl ected taxon o- my and con ti nuing ex ti n cti ons of tu a t a ra (Sp h en od o n) . Na tu re 347: 1 7 7 – 1 7 9 .

D avid D, Bru n ell D, Ca rbonneau D, Dut ton H, Hord L, Wi l ey N, Wood- w a rd A . 1 9 9 6 . F l ori d a’s all i ga tor managem ent progra m , an update 1 9 8 7 – 1 9 9 5 . Pa ges 410–428 in Crocod i l e s , Proceed i n gs of the 13th Working Meeting of the Crocodile Specialist Gro u p, I U C N – The Worl d Con s erva ti on Un i on ; 11–17 May 1996; Gland (Swi t zerl a n d ) .

D avis A J, Jen k i n s on LS, L awton JH, S h orrocks B, Wood S. 1 9 9 8 . Ma k i n g m i s t a kes wh en pred i cting shifts in species ra n ge in re s ponse to gl ob a l w a rm i n g. Na tu re 391: 7 8 3 – 7 8 6 .

De May n ad i er PG, Hu n ter ML Jr. 1 9 9 5 . The rel a ti onship bet ween fore s t m a n a gem ent and amph i bian eco l ogy: A revi ew of the North Am eri c a n l i tera tu re .E nvi ron m ental Revi ews 3: 2 3 0 – 2 6 1 .

Dodd CK Jr. 1 9 8 8 . Disease and pop u l a ti on declines in the flatten ed mu s k tu rt l e , Stern ot h erus depre s su s. Am erican Mi dlands Na tu ralist 119: 3 9 4 – 4 0 1 .

_ _ _ _ _ _ . 1 9 9 3 . S tra tegies for snake con s erva ti on . Pa ges 363–394 in Sei gel RA , Co llins JT, ed s . Sn a ke s :E co l ogy and Beh avi or. New York : Mc Graw - Hi ll .

_ _ _ _ _ _ . 1 9 9 7 . Im peri l ed amph i bi a n s : A historical pers pective . Pa ge s 165–200 in Benz GW, Co llins DE, ed s . Aqu a tic Fauna in Peri l : t h e So ut h e a s tern Pers pective . Dec a tur (GA): Lenz De s i gn and Com mu n i- c a ti on s .

Dorcas ME, G i bbons JW, Dowling HG. 1 9 9 8 . S em i n a tri x Cope . Bl ack swamp snake . Pa ges 679.1–679.5 in Ca t a l ogue of Am erican Am ph i b- ians and Repti l e s .S t . Louis (MO): Soc i ety for the Stu dy of Am ph i bi a n s and Repti l e s .

E rnst CH, Ba rbour RW. 1 9 8 9 . Tu rtles of the Worl d . Wa s h i n g ton (DC ) : Sm i t h s onian In s ti tute Pre s s .

E rnst CH, Lovi ch JE, Ba rbour RW. 1 9 9 4 . Tu rtles of the Un i ted States and Ca n ad a . Wa s h i n g ton (DC ) : Sm i t h s onian In s ti tuti on Pre s s .

F i s h er RN, S h a f fer HB. 1 9 9 6 . The decline of a m ph i bians in Ca l i forn i a’s Great Cen tral Va ll ey. Con s erva ti on Bi o l ogy 10: 1 3 8 7 – 1 3 9 7 .

F i tch HS, Hen ders on RW, Hi llis DM. 1 9 8 2 . Ex p l oi t a ti on of iguanas in Cen- tral Am eri c a . Pa ges 397–417 in Bu r gh a rdt GM, Rand A S , ed s . Ig u a n a s of the Worl d . Pa rk Ri d ge (NJ): Noye s .

Fon tenot LW, Nobl et GP, Platt SG. 1 9 9 4 . Ro ten one hazards to amph i bi a n s and repti l e s . Herpeto l ogical Revi ew 25: 1 5 0 – 1 5 3 .

Fra zer NB, Greene JL, G i bbons JW. 1 9 9 3 . Tem poral va ri a ti on in growt h ra te and age at matu ri ty of male painted tu rt l e s , C h rysemys pict a. Am erican Mi dlands Na tu ralist 130: 3 1 4 – 3 2 4 .

G a rber SD. 1 9 8 8 . Di a m on d b ack terrapin ex p l oi t a ti on .P l a s tron Pa pers 17: 1 8 – 2 2 .

G a rber SD, Bu r ger J. 1 9 9 5 . A 20-yr stu dy doc u m en ting the rel a ti on s h i p bet ween tu rtle decline and human rec re a ti on .E co l ogical App l i c a ti on s 5 :1 1 5 1 – 1 1 6 2 .

G i bbons JW. 1 9 9 0 . Sex ra tios and their sign i f i c a n ce among tu rtle pop u l a- ti on s . Pa ges 171–182 in Gibbons JW, ed . L i fe Hi s tory and Eco l ogy of the Sl i der Tu rt l e . Wa s h i n g ton (DC ) : Sm i t h s onian In s ti tuti on Pre s s .

_ _ _ _ _ _ . 1 9 9 3 . Reptile and Am ph i bian Stu dy. Official boo k l et for Meri t Bad ge Seri e s . Irving (T X ) : Boy Sco uts of Am eri c a .

G i bbons JW, S t a n gel PW, ed s .1 9 9 9 . Con s erving Am ph i bians and Repti l e s in the New Mi ll en iu m . Proceed i n gs of the Pa rtn ers in Am ph i bian and Reptile Con s erva ti on (PA RC) Con feren ce ; 2–4 June 1999; At l a n t a ( G A ) . Ai ken (SC): Savannah River Eco l ogy Labora tory. Herp Outre ach Pu bl i c a ti on #2.

G oin JW. 1 9 9 2 . Requ i em or recovery? Texas Pa rks Wi l dl i fe (Au g u s t ) :2 8 – 3 5 . Greene HW. 1 9 9 7 . Sn a ke s : The Evo luti on and Mys tery in Na tu re . Lo s

An geles (CA): Un ivers i ty of Ca l i fornia Pre s s . Greene HW, Ca m pbell JA .1 9 9 3 . The futu re of p i t vi pers . Pa ges 421–427 in

Ca m pbell JA , Brodie ED Jr, ed s . Bi o l ogy of the Pitvi pers . L a n e s boro ( M N ) : Serpen t’s Tale Na tu ral Hi s tory Book Di s tri butors .

Gu ertin DS, E a s terling W E , Bra n dle JR. 1 9 9 7 . Cl i m a te ch a n ge and fore s t s in the Great Plains. Bi o S c i en ce 47: 2 8 7 – 2 9 5 .

Gu i ll et te LJ Jr, Crain DA . 1 9 9 6 . E n doc ri n e - d i s ru pting contaminants and reprodu ctive abn orm a l i ties in repti l e s . Com m ents in Tox i co l ogy 5: 3 8 1 – 3 9 9 .

Gu i ll et te LJ Jr, Gross TS , Ma s s on GR, Ma t ter JM, Perc ival HF, Woodw a rd A R . 1 9 9 4 . Devel opm ental abn orm a l i ties of the gon ad and abn orm a l s ex horm one con cen tra ti ons in juvenile all i ga tors from con t a m i n a ted and con trol lakes in Flori d a . E nvi ron m ental Health Pers pectives 102: 6 8 0 – 6 8 8 .

Gu i ll et te LJ Jr, Crain DA , Roon ey A A ,P i ck ford DB. 1 9 9 5 .O r ga n i z a ti on ver- sus activa ti on : The role of en doc ri n e - d i s ru pting contaminants (EDC s ) du ring em bryonic devel opm ent in wi l dl i fe .E nvi ron m ental Health Per- s pectives 103 (Su pp l em ent 7): 1 5 7 – 1 6 4 .

Guyer C, Ba i l ey MA. 1 9 9 3 . Am ph i bians and reptiles of l on gl e a f pine com- mu n i ti e s . Pa ges 139–158 in Hermann SM, ed . The Lon gl e a f P i n e E co s ys tem :E co l ogy, Re s tora ti on , and Ma n a gem en t . Proceed i n gs of t h e Ta ll Ti m bers Fire Eco l ogy Con feren ce , Nu m ber 18. Ta ll a h a s s ee (FL): Ta ll Ti m bers Re s e a rch Stati on .

Ha i rs ton NG Sr. 1 9 8 7 . Com mu n i ty Eco l ogy and Sa l a m a n der Gu i l d s . New York : Ca m bri d ge Un ivers i ty Pre s s .

Ha ll RJ. 1 9 8 0 .E f fects of envi ron m ental contaminant on repti l e s : A revi ew. US Fish and Wi l dl i fe Servi ce Special Scien ce Report on Wi l dl i fe 228: 1 – 1 2 .

Ha ll RJ, Hen ry PFP. 1 9 9 2 . Assessing ef fects of pe s ti c i des on amph i bians and repti l e s . Herpeto l ogy Jo u rnal 2: 6 5 – 7 1 .

Ha llam CO, Wh e a ton K, F i s ch er RA .1 9 9 8 . S pecies Prof i l e : E a s tern In d i go Sn a ke (Drym a rchon co rais cou peri) on Mi l i t a ry In s t a ll a ti ons in the So ut h e a s tern Un i ted State s . Wa s h i n g ton (DC ) : US Army Corps of E n gi n eers . Technical Report SERDP- 9 8 - 2 . Ava i l a ble from the US Army Corps of E n gi n eers , Wa s h i n g ton (DC ) .

Halpin PN. 1 9 9 7 .G l obal cl i m a te ch a n ge and natu ral area pro tecti on :m a n- a gem ent re s ponses and re s e a rch directi on s .E co l ogical App l i c a ti ons 7: 8 2 8 – 8 4 3 .

Hayes TB. 1 9 9 7 . S teroi d - m i m i cking envi ron m ental con t a m i n a n t s : Th ei r po ten tial role in amph i bian decl i n e s . Pa ges 145–149 in Bohme W, Bi s ch of f W, Zi egl er T, ed s . Herpeto l ogia Bon n en s i s : Proceed i n gs of t h e 8th Ord i n a ry Gen eral Meeting of the Soc i etas Eu rop aea Herpeto l ogi- c a ; 23–27 Aug 1995; Bon n ,G erm a ny.

Herbst LH. 1 9 9 4 .F i brop a p i ll om a tosis of m a rine tu rt l e s . An nual Revi ew of Fish Disease 4: 3 8 9 – 4 2 5 .

Hi l debrand HH. 1 9 8 2 . A historical revi ew of the status of sea tu rtle pop u- l a ti ons in the we s tern Gu l f of Mex i co. Pa ges 447–453 in Bjorndal KA , ed . Bi o l ogy and Con s erva ti on of Sea Tu rt l e s . Wa s h i n g ton (DC ) : Sm i t h- s onian In s ti tuti on Pre s s .

Hi n ton TG , S cott DE. 1 9 9 0 . Rad i oeco l ogical tech n i ques for herpeto l ogy, with an em phasis on fre s hw a ter tu rt l e s . Pa ges 267–287 in Gibbons JW, ed . L i fe Hi s tory and Eco l ogy of the Sl i der Tu rt l e . Wa s h i n g ton (DC ) : Sm i t h s onian In s ti tuti on Pre s s .

Hopkins WA , Rowe CL, Con gdon JD. 1 9 9 9 . E l eva ted trace el em ent con- cen tra ti ons and standard met a bolic ra te in banded water snakes (Nero - dia fasci a t a) ex po s ed to coal com bu s ti on waste s .E nvi ron m ental Tox i- co l ogy and Ch em i s try 18: 1 2 5 8 – 1 2 6 3 .

Hu m boldt AV. 1 8 1 4 . Rel a ti on histori qu e . In Hu m boldt A , Bonpland A , ed s . Voya ge aux Regi ons Equ i n oxiales du No uveau Con ti n en t , fait en 1 7 9 9 – 1 8 0 4 . Pt .1 . Pa ri s :S ch oell .

I U C N – World Con s erva ti on Un i on . 2 0 0 0 . < w w w. iu c n . or g / t h em e s / s s c / 9 6 a n rl / d t a bl e 1 . h tm> (7 Jan 2000).

Jacob s on ER. 1 9 9 3 . Im p l i c a ti ons of i n fectious diseases for captive prop a ga- ti on and introdu cti on programs of t h re a ten ed / en d a n gered repti l e s . Jo u rnal of Zoo and Wi l dl i fe Medicine 24: 2 4 5 – 2 5 5 .

_ _ _ _ _ _ .1 9 9 4 . Causes of m ort a l i ty and disease in tortoi s e s : A revi ew. Jo u r- nal of Zoo and Wi l dl i fe Medicine 25: 2 – 1 7 .

Ja ggi C, Baur B. 1 9 9 9 . Over growing forest as a po s s i ble cause for the loc a l ex ti n cti on of Vi pera aspis in the nort h ern Swiss Ju ra mountains. Am ph i bi a - Reptilia 20: 2 5 – 3 4 .

Ja n covi ch JK, D avi d s on EW, Morado JF, Jacobs BL, Co llins JP. 1 9 9 7 . Is o l a- ti on of a lethal vi rus from the en d a n gered ti ger salamander Am bys to m a ti gri num stebbi n s i. Diseases of Aqu a tic Organisms 31:161–167.

664 BioScience • August 2000 / Vol. 50 No. 8

Articles

Downloaded from https://academic.oup.com/bioscience/article-abstract/50/8/653/243214 by Central Washington University user on 12 April 2018

Ja n zen FJ. 1 9 9 4 . Cl i m a te ch a n ge and tem pera tu re depen dent sex determ i- n a ti on in repti l e s . Proceed i n gs of the Na ti onal Ac ademy of S c i en ces of the Un i ted States of Am erica 91: 7 4 8 7 – 7 4 9 0 .

Jen n i n gs MR, Hayes MP. 1 9 8 5 . Pre-1900 overh a rvest of Ca l i fornia red - l egged frogs (Rana auro ra drayto n i i) : The indu cem ent for bu ll f rog (Rana cate s bei a n a) introdu cti on . Herpeto l ogica 41: 9 4 – 1 0 3 .

Jen s en JB. 1 9 9 8 . Di s tri buti on and status of the all i ga tor snapping tu rt l e (Ma cro cl emys tem m i n ck i i) in Geor gi a . Pa per pre s en ted at the 78th An nual Meeting of the Am erican Soc i ety of Ich t hyo l ogists and Her- peto l ogi s t s ; 16–22 Jul 1998; Un ivers i ty of Gu el ph ,O n t a ri o, Ca n ad a .

Jo h n s on PTJ, Lu n de KB, Ri tchie EG. 1 9 9 9 . The ef fect of trem a tode infec- ti on on amph i bian limb devel opm ent and su rvivors h i p. S c i en ce 284: 8 0 2 – 8 0 4 .

Kell ert SR, Wi l s on EO. 1 9 9 3 . The Bi ophilia Hypo t h e s i s . Wa s h i n g ton (DC ) : Island Pre s s .

Ki e s ter A R , Juvik JO. 1 9 9 7 . Con s erva ti on ch a ll en ges of the tu rtle trade in Vi etnam and Ch i n a . Pa per pre s en ted at the Joint Meeting of Am eri c a n Soc i ety of Ich t hyo l ogists and Herpeto l ogi s t s , Herpeto l ogi s t s’ Le a g u e , and Soc i ety for the Stu dy of Am ph i bians and Repti l e s ; 26 June–2 Ju ly 1 9 9 7 ; Se a t t l e , WA .

King FW. 1 9 8 9 . Con s erva ti on and managem en t . Pa ges 216–229 in CA Ro s s , ed . Crocodiles and All i ga tors . New York : Facts on File.

Lamb T, Bi ckham JW, Lyne TB, G i bbons JW. 1 9 9 5 . The slider tu rtle as an envi ron m ental sen ti n el : Mu l tiple ti s sue assays using flow cytom etri c a n a lys i s .E co tox i co l ogy 4: 5 – 1 3 .

L a n n oo MJ, Lang K, Waltz T, P h i llips GS. 1 9 9 4 . An altered amph i bi a n a s s em bl a ge : Di ck i n s on Co u n ty, Iow a ,s even ty ye a rs after Frank Bl a n- ch a rd ’s su rvey. Am erican Mi dlands Na tu ralist 131: 3 1 1 – 3 1 9 .

Leja WT. 1 9 9 8 . Aqu a tic habitats in the Mi dwe s t : Wa i ting for amph i bi a n con s erva ti on initi a tive s . Pa ges 345–353 in Lannoo MJ, ed .S t a tus and Con s erva ti on of Mi dwe s tern Am ph i bi a n s . Iowa Ci ty (IA): Un ivers i ty of Iowa Pre s s .

L i eberman S. 1 9 9 4 . Can CITES Save the Box Tu rtle? Endangered Spec i e s Technical Bu ll eti n . US Dep a rtm ent of the In teri or Fish and Wi l dl i fe Servi ce . Federal Regi s ter 19 (5): 1 5 – 1 7 .

Lips KR. 1 9 9 9 . Mass mort a l i ty and pop u l a ti on declines of a nu rans at an upland site in we s tern Pa n a m a . Con s erva ti on Bi o l ogy 13: 1 1 7 – 1 2 5 .

Losos JB, Ma rks JC, S ch oen er TW. 1 9 9 3 . Ha bitat use and eco l ogical inter- acti ons of an introdu ced and a native species of An ol i s l i z a rd on Gra n d Caym a n , with a revi ew of the outcomes of anole introdu cti on s . O eco l ogia 95: 5 2 5 – 5 3 2 .

Lovi ch JE. 1 9 9 5 . Wi l dl i fe and weed s :L i fe in an alien landscape . News l et ter of the Ca l i fornia Exo tic Pest Plant Council 3: 4 – 5 .

Lovi ch JE, G o t te SW, E rnst CH, Ha rs h b a r ger JC, L aem m erzahl A F, G i b- bons JW. 1 9 9 6 . Preva l en ce and histop a t h o l ogy of s h ell disease in tu rt l e s f rom Lake Bl ack s h e a r, G eor gi a . Jo u rnal of Wi l dl i fe Diseases 32: 2 5 9 – 2 6 5 .

Ma rco M, Q u i l chano C, Bl a u s tein A R . 1 9 9 9 . Sen s i tivi ty to nitra te and n i tri te in pon d - breeding amph i bians from the Pacific Nort hwe s t ,U S A . E nvi ron m ental Tox i co l ogy and Ch em i s try 18: 2 8 3 6 – 2 8 3 9 .

Means DB, Palis JG, Ba ggett M. 1 9 9 6 .E f fects of slash pine silvi c u l tu re on a F l orida pop u l a ti on of f l a t woods salamander. Con s erva ti on Bi o l ogy 10: 4 2 6 – 4 3 7 .

Mef fe GK, Ca rro ll CR. 1 9 9 4 . Principles of Con s erva ti on Bi o l ogy. Su n der- land (MA): Si n a u er As s oc i a te s .

Mi t term ei er RA , Myers N, Gil PR, Mi t term ei er CG. 1 9 9 9 . Ho t s po t s :E a rt h’s Bi o l ogi c a lly Ri chest and Most Endangered Terre s trial Ecoregi on s . Ja p a n : Toppan Pri n ti n g.

Mocken h a u pt B. 7 Dec 1999. Tu rtles can’t hide from hu n gry hu m a n s . Ca m bodian Daily: 1 – 2 .

Mo l er PE .1 9 9 2 . Ra re and Endangered Biota of F l ori d a , Vo l .I I I . Am ph i b- ians and Repti l e s .G a i n e s vi lle (FL): Un ivers i ty of F l orida Pre s s .

Morey S. 1 9 9 8 .E n d a n gered and thre a ten ed wi l dl i fe and plants: Wi t h d raw- al of propo s ed rul to list the bl ack legless lizard as en d a n gered . Federa l Regi s ter 63: 4 3 1 2 9 – 4 3 1 3 5 .

Mo s er A , Gra ber C, Frey vogel TA . 1 9 8 4 . Ob s erva ti ons sur 1’et h o l ogie et 1 ’ evo luti on d’une pop u l a ti on de Vi pera aspis (L.) au nord du Ju ra Su i s s e . Am ph i bi a - Reptilia 5: 3 7 3 – 3 9 3 .

Moulis RA 1997. Pred a ti on of the imported fire ant (S ol en opsis invi ct a) on l oggerh e ad sea tu rtle (C a retta caret t a) nests on Wa s s aw Na ti on a l Wi l dl i fe Ref u ge , G eor gi a . Ch el onian Con s erva ti on and Bi o l ogy 2: 4 3 3 – 4 3 6 .

Mount RH. 1 9 7 5 . The Reptiles and Am ph i bians of Al a b a m a . Au bu rn (AL): Au bu rn Un ivers i ty, Alabama Agri c u l tu ral Ex peri m ental Stati on .

Ni l s on G, An d ren C, F l a rdh B. 1 9 9 0 . Vi pera albi zo n a, a new mountain vi per f rom cen tral Tu rkey, with com m ents on isolating ef fects of the An a to- lian Di a gon a l . Am ph i bi a - Reptilia 11: 2 8 5 – 2 9 4 .

Ni l s on G, An d ren C, Ioannidis Y, Dimaki M. 1 9 9 9 .E co l ogy and con s erva- ti on of the Milos vi per, Ma crovi pera schwei zeri (Wern er, 1 9 3 5 ) . Am ph i bi a - Reptilia 20: 3 5 5 – 3 7 5 .

Oza GM. 1 9 9 0 . E co l ogical ef fects of the frog’s leg trade .E nvi ron m en t a l i s t 1 0 : 3 9 – 4 1 .

Pa rker WS , Brown WS .1 9 7 3 .S pecies com po s i ti on and pop u l a ti on ch a n ge s in two com p l exes of s n a ke hibern acula in nort h ern Ut a h . Herpeto l og- ica 29: 3 1 9 – 3 2 6 .

Pechmann JHK, Wi l bur HM. 1 9 9 4 . Put ting declining amph i bian pop u l a- ti ons in pers pective : Na tu ral flu ctu a ti ons and human impact s . Her- peto l ogica 50: 6 5 – 8 4 .

Pechmann JHK, S cott DE, Sem l i t s ch RD, Ca l dwell JP, Vitt LJ, G i bbons JW. 1 9 9 1 . Declining amph i bian pop u l a ti on s : The probl em of s ep a ra ti n g human impact from natu ral flu ctu a ti on s .S c i en ce 253: 8 9 2 – 8 9 5 .

Poiani KA , Jo h n s on WC .1 9 9 1 .G l obal warming and pra i rie wet l a n d s . Bi o- S c i en ce 41: 6 1 1 – 6 1 8 .

Po u gh FH, An d rews RM, Cadle JE, Crump ML, Savi t z ky A H , Wells KD. 1 9 9 8 . Herpeto l ogy. New Jers ey: Pren ti ce - Ha ll .

Pounds JA , Fogden MPL, Ca m pbell JH. 1 9 9 9 . Bi o l ogical re s ponse to cl i- m a te ch a n ge on a tropical mountain. Na tu re 398: 6 1 1 – 6 1 5 .

Pri tch a rd PCH. 1 9 6 7 . L iving Tu rtles of the Worl d . Neptune (NJ): T F H Pu bl i c a ti on s .

Pri tch a rd PCH, Trebbau T. 1 9 8 4 . The Tu rtles of Ven e z u el a . Soc i ety for the S tu dy of Am ph i bians and Repti l e s , Con tri buti ons to Herpeto l ogy, Vo l . 2 . Ox ford (OH): Miami Un ivers i ty.

Reed JM, Bl a u s tein A R . 1 9 9 5 . As s e s s m ent of “n on decl i n i n g” a m ph i bi a n pop u l a ti ons using power analys i s . Con s erva ti on Bi o l ogy 9: 1 2 9 9 – 1 3 0 0 .

Rh odin A . 1 9 9 9 . Cel ebra te the tu rt l e : Percepti on and pre s erva ti on . Pa per pre s en ted at Powderm i ll 1999, 4th Occ a s i onal Fre s hw a ter Tu rtle Con- feren ce ; 13–16 Aug 1999; L a u gh l i n ,N V.

Ri ce KG , Perc ival HF, Woodw a rd A R , Jen n i n gs ML. 1 9 9 9 .E f fects of egg and h a tchling harvest on Am erican all i ga tors in Flori d a . Jo u rnal of Wi l dl i fe Ma n a gem ent 63: 1 1 9 3 – 1 2 0 0 .

Rodda GH. 1 9 9 2 . Loss of n a tive reptiles assoc i a ted with introdu cti ons of exo tics in the Ma riana Is l a n d s . Pacific Scien ce 46: 3 9 9 – 4 0 0 .

Roman J, Sa n t hu f f S D, Mo l er PE , Bowen BW. 1 9 9 9 . Pop u l a ti on stru ctu re and cryptic evo luti on a ry units in the all i ga tor snapping tu rt l e . Con s er- va ti on Bi o l ogy 13: 1 3 5 – 1 4 2 .

Roo s en burg W M .1 9 9 1 . The diamon d b ack terra p i n : Pop u l a ti on dy n a m i c s , h a bitat requ i rem en t s , and opportu n i ties for con s erva ti on . Pa ge s 227–234 in Mi hu rs ky JA , Ch a n ey A , ed s . New Pers pectives in the Ch e s a pe a ke Sys tem : A Re s e a rch and Ma n a gem ent Pa rtn ers h i p. Ba l ti- m ore (MD): Ch e s a pe a ke Re s e a rch Con s ortiu m .

Ross JP, ed .1 9 9 8 . Crocod i l e s :S t a tus Su rvey and Con s erva ti on Acti on Plan. 2nd ed . < w w w. f l m n h . u f l . edu / n a t s c i / h erpeto l ogy / act - p l a n / p l a n 1 9 9 8 a . h tm> (6 Jul 1998).

Rut h erford C, Rora b a u gh J. 1 9 9 5 .E n d a n gered and thre a ten ed wi l dl i fe and p l a n t s : Propo s ed rule to determine five plants and a lizard from Mon- terey Co u n ty, Ca l i forn i a , as en d a n gered or thre a ten ed . Federal Regi s ter 6 0 :3 9 3 2 6 – 3 9 3 3 7 .

S ch n ei der SH, Root TL. 1 9 9 8 . Cl i m a te ch a n ge . Pa ges 89–116 in Mac MJ, Op l er PA , Haecker CEP, Doran PD, ed s . S t a tus and Trends of t h e Na ti on’s Bi o l ogical Re s o u rce s , Vo l .1 . Re s ton (VA ) : US Dep a rtm ent of In teri or, US Geo l ogical Su rvey.

August 2000 / Vol. 50 No. 8 • BioScience 665

Articles

Downloaded from https://academic.oup.com/bioscience/article-abstract/50/8/653/243214 by Central Washington University user on 12 April 2018

Sem l i t s ch RD. 1 9 9 8 . Bi o l ogical del i n e a ti on of terre s trial bu f fer zones for pon d - breeding salamanders . Con s erva ti on Bi o l ogy 12:1113–1119.

Sem l i t s ch RD, Ryan TJ. 1 9 9 8 . Mi gra ti on , a m ph i bi a n . Pa ges 221–227 in Kn obil E, Nei ll JD, ed s . The Encycl opedia of Reprodu cti on , Vo l .3 . New York : Ac ademic Pre s s .

Se s s i ons SK, Fra n s s en RA , Horn er V L . 1 9 9 9 . Morph o l ogical clues from mu l ti l egged frogs : Are reti n oids to blame? Scien ce 284: 8 0 0 – 8 0 2 .

S h a rma DSK. 1 9 9 9 . Tortoise and Fre s hw a ter Tu rtle Trade and Uti l i s a ti on in Pen i n sular Ma l ays i a . A TRAFFIC So utheast Asia Report . Petaling Jaya , Sel a n gor (Ma l ays i a ) .

Shine R. 1 9 9 1 . Au s tralian Sn a ke s : A Na tu ral Hi s tory. It h aca (NY) : Corn ell Un ivers i ty Pre s s .

Shine R, F i t z gerald M. 1 9 9 6 .L a r ge snakes in a mosaic ru ral landscape : Th e eco l ogy of c a rpet pyt h ons Mo relia spilot a ( Serpen te s : Pyt h on i d ae) in Coastal Eastern Au s tra l i a . Bi o l ogical Con s erva ti on 76: 1 1 3 – 1 2 2 .

Shine R, Ha rl ow P, Keogh JS, Boe ad i . 1 9 9 5 . Bi o l ogy and com m ercial uti- l i z a ti on of ac roch ordid snake s , with special referen ce to karung (Acro - ch o rdus java n i c u s) . Jo u rnal of Herpeto l ogy 29: 3 5 2 – 3 6 0 .

Smith RB, Sei gel RA , Smith KR. 1 9 9 8 . O cc u rren ce of Upper Re s p i ra tory Tract Disease in goph er tortoise pop u l a ti ons in Florida and Mi s s i s s i p- p i . Jo u rnal of Herpeto l ogy 32: 4 2 6 – 4 3 0 .

S po tila JR, Dunham A E , Leslie A J, S teyerm a rk AC , Plotkin PT, Pa l adino FV. 1 9 9 6 . Worl dwi de pop u l a ti on decline of Derm o ch elys co ri a ce a: Are l e a t h erb ack tu rtles going ex ti n ct? Ch el onian Con s erva ti on and Bi o l o- gy 2: 2 0 9 – 2 2 2 .

S tew a rt MC, Au s tin DF, Bo u rne GR. 1 9 9 3 . Ha bitat stru ctu re and the dis- pers i on of goph er tortoises on a natu re pre s erve .F l orida Scien tist 56: 7 0 – 8 1 .

S ti ll CJ, Fo s ter PN, S ch n ei der SH. 1 9 9 9 . Si mu l a ting the ef fects of cl i m a te ch a n ge on tropical montane cloud fore s t s . Na tu re 398: 6 0 8 – 6 1 0 .

S to l zen burg W. 1 9 9 9 . Do u ble agen t s . Na tu re Con s ervancy 49: 1 8 – 2 4 . Th orbja rn a rs on JB, Perez N, E s c a l ona T. 1 9 9 3 . Ne s ting of Pod o cn em i s

u n i f i l i s in the Ca p a n a p a ro River Ven e z u el a . Jo u rnal of Herpeto l ogy 27: 3 4 4 – 3 4 7 .

Th orn ton I. 1 9 7 1 . D a rwi n’s Is l a n d s : A Na tu ral Hi s tory of the Galapago s . G a rden Ci ty (NY) : The Na tu ral Hi s tory Pre s s .

Tinkle DW. 1 9 7 9 . Lon g - term field stu d i e s . Bi o S c i en ce 29: 7 1 7 . Tu bervi lle TD, Bodie JR, Jen s en JB, L a Cl a i re LV, G i bbons JW. 2 0 0 0 . App a r-

ent decline of the So ut h ern Hognose Sn a ke (Heterodon simu s) . Jo u rn a l of Elisha Mi tch ell Scien tific Soc i ety 116(1): 1 9 – 4 0 .

Tyl er MJ, Ca rter DB. 1 9 8 1 .O ral bi rth of the young of the ga s tric brood i n g f rog Rh e oba tra chus silus. Animal Beh avi or 29: 2 8 0 – 2 8 2 .

[ F WS] US Fish and Wi l dl i fe Servi ce .2 0 0 0 . Box score , en d a n gered spec i e s . < en d a n gered . f ws . gov / box s core . h tml> (7 Jan 2000).

Vi n n i kov KY, Robock A ,S to u f fer RJ, Wals JE, Pa rk i n s on CL, Cava l i eri DJ, Mi tch ell JFB, G a rrett D, Za k h a rov V F. 1 9 9 9 . G l obal warming and n ort h ern hem i s ph ere sea ice ex ten t .S c i en ce 286: 1 9 3 4 – 1 9 3 7 .

Vitt LJ, Ca l dwell JP, Wi l bur HM, Smith DC .1 9 9 0 . Am ph i bians as harbi n- gers of dec ay. Bi o S c i en ce 40: 4 1 8 .

Wa re S, Frost C, Doerr PD. 1 9 9 3 . So ut h ern mixed hardwood fore s t : Th e form er lon gl e a f pine fore s t . Pa ges 447–493 in Ma rtin W H , Boyce SG, E ch tern acht AC , ed s . Bi od ivers i ty of the So ut h e a s tern Un i ted State s . New York : John Wi l ey & Son s .

Wi lliams T. 1 9 9 9 . The terri ble tu rtle trade . Au du bon Ma gazine 101: 4 4 – 5 1 . Wi l s on EO Jr. 1 9 5 0 . Va ri a ti on and ad a pt a ti on in the imported fire ant

S ol en opsis saevissima ri ch teri ( Forel) in the Gu l f S t a te s . Ma s ter ’s thesis, Un ivers i ty of Al a b a m a , Tu s c a l oo s a ,A L .

Wood RC , Herlands R. 1 9 9 7 . Tu rtles and ti re s : The impact of road k i lls on Nort h ern Di a m on d b ack Terra p i n , Ma l a cl emys terrapin terra p i n, pop u- l a ti ons on the Ca pe May Pen i n su l a , So ut h ern New Jers ey, U S A . Pa ge s 46–53 in Abbema JV, Pri tch a rd PCH, ed s . Proceed i n gs : Con s erva ti on , Re s tora ti on , and Ma n a gem ent of Tortoises and Tu rt l e s — An In tern a- ti onal Con feren ce . New York : New York Tu rtle and Tortoise Soc i ety.

[ WTO] World Trade Orga n i z a ti on . 1 9 9 8 . Report of the Appell a te Body, WT / D S 5 8 / A B / R , 12 October 1998. New York : World Trade Orga n i z a- ti on .

Zim HS, Smith HM.1953. Reptiles and Am ph i bi a n s : A Gu i de to Fa m i l i a r Am erican Spec i e s . New York :G o l den Pre s s .

666 BioScience • August 2000 / Vol. 50 No. 8

Articles

Downloaded from https://academic.oup.com/bioscience/article-abstract/50/8/653/243214 by Central Washington University user on 12 April 2018