Articles The Global Decline of Reptiles,Dé jà 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
s a group [reptiles] are neit h er ‘good ’n or ‘bad , ’ but “ ia re intere s ting and unu sua l , a lt h o u gh of mi nor A i m porta n ce . If th ey should all disappe ar , it wou l d REP TI L E SPE CI E S AR E DE CL I N IN G ON A not make mu ch difference one way or the other ”( Zim and Smith 1953,p. 9) . Fortu n a tely,this op i n i on from the Golden GLO BA L SC A L E. SI XS I G N I F IC A N T TH R E ATS Gu ide Series does not persist tod ay;most people have com e TOR E P T I L EPO P ULA T I O N SAR E H A BI T AT to recogn i ze the va lue ofboth reptiles and amphi bians as an in tegral part ofn a tu ral eco sys tems and as heralds of LO SS A N DD E G RADA TI O N , I N T RO D U C E D environ m ental qu a l ity (Gibbons and Stangel 1999). In recent ye ars ,as overa ll environ m ental aw a reness among the IN VA S I V E SPE C I E S , EN VI RO N M E N TA L p u blic has increa s ed, con cerns have come to include intere st in the eco logical state ofreptile and amph i bian spec i e s PO L LUT I O N , DI S E A SE , UN S U S TA I NA B L E th ems elves and oft heir habit a ts . Inc re a s ed awa reness may US E , A N D GLO BA L CL I M AT E C H A N G E stem from bet ter edu ca ti on abo ut threats to biod ivers ity in genera l , and to reptiles and amph ibians in parti c ul a r, a nd po s s ibly even from an innate attracti on to these taxa (Kell ert and Wil s on 1993). probl em ,as it has come to be known,has garnered sig- From the perspective ofmany nonscientists, the two nificant attention not only among scientists but also in the vertebrate classes comprising reptiles and amphibians, popular media and in political circles. collectively referred to as the herpetofauna, are inter- changeable.For example,the Boy Scout merit badge pam- The reptile problem phlet for herpetology was called simply Reptile Study from Despite the fact that reptiles and amphibians are often 1926 to 1993 (Conant 1972, Gibbons 1993), and major considered collectively,reptile declines deserve spotlight- zoos (e.g., National Zoo in Washington, DC;Zoo Atlanta; ing and elucidating in their own right. The differences and San Diego Zoo) use only the name “reptile”to refer to between the two groups are substantial. Modern amphib- the facility that houses both amphibians and reptiles. ians and reptiles are products ofindependent lineages that Thus, public attitudes about the need for conservation of have been separate for the past 300 million years (Pough et reptiles are probably linked to concern about amphibian al. 1998). Many ofthe differences between the groups are declines and deformities (Alford and Richards 1999,John- obvious and considerable.For example,the integument of son et al.1999, Sessions et al.1999), which have been the reptiles is covered with scales, whereas amphibians have a subject ofnumerous,well-documented scientific studies. highly permeable,glandular skin,a feature often touted as Because amphibians are distributed worldwide, but her- enhancing the environmental sensitivity ofamphibians to petologists who document amphibian declines are not,it is difficult to accurately assess what portion ofamphibian J. Whitfield Gibbons (e-mail: [email protected]) is a professor of populations are experiencing significant declines or have ec o l o gy at Savannah River Ecology Laboratory (SREL), Un iv ers ity of already disappeared. Furthermore,the means of deter- G e o r g i a ,A i ke n ,SC 29802. David E. Scott,Tr avis J. Rya n ,Tr a cey D. mining a species’ conservation status is a rigorous and Tu be rv i l l e ,Brian S. Metts,Judith L. Greene,To ny Mills,Yale Leiden, time-intensive process, and therefore counts of“ officially” Sean Po p py,and Christopher T . Winne are researchers at SREL. recognized endangered and threatened species are likely to Kur t A. Buhlmann is coordinator for amphibian and chelonian con- grossly underestimate the actual number of imperiled s e rvation at Conser vation Intern a t i o n a l ,Center for Applied s pecies (Ta ble 1). The worl dwi de amph i bian decl i n e Bi o d i v e rsity Science, Wa s h in g t o n ,DC 20037.
August 2000 / Vol. 50 No. 8 BioScience653 Articles
Table 1. Con serva tion status ofreptiles and amphibi a n s ,a cco rding to the US Fish and Wi l dlife Service (FWS ) , Conven tion on Intern a tional Trade in En da n gered Species (CITES), and The Wo rld Con serva tion Union (IUCN).
Ap p r ox i ma t e number of F WS b CI T ES c IU C N d Tax on s p e c i es a E nd a n ge r e d Th r ea t e n e dAppendix IAppendix IIAppendix III E x t i nc t En da n g e r ed Vul n er ab l e A mp hi b ia n s 46 80 1 7 9 13 6 8 0 5 4 9 75 Frogs and toads4 1 00 9 5 1 1 6 6 0 5 3 8 5 0 S al a m an de rs 41 5 8 4 2 2 0 0 1 1 2 5 C ae c i l i an s 16 5 0 0 0 0 0 0 0 0 Re p ti l e s 7 15 0 70 1 8 70 38 3 1 9 2 0 1 00 15 3 Turt l es 26 0 33 4 2 5 4 9 6 6 3 8 5 8 C ro c o d i l i an s 22 1 5 3 1 6 8 0 0 7 3 Tua t a r a 2 2 0 2 0 0 0 0 1 L i z a r ds 5 06 6 14 8 1 6 2 38 0 1 1 30 66 S na ke s 1 8 00 6 3 1 1 8 8 1 3 3 2 5 2 5
aThe approxi m a te nu m ber of s pecies for each taxon is from Po u gh et al.( 19 9 8) . The num bers in the table refl ect worldwi de esti m ates of s pecies on ly ( excluding su bs pecies and pop ul a ti ons) listed by each orga n i z a ti on under sel ected cons ervati on ran k i ngs . bData from FWS (2000). cAppendix I species are threa ten ed with ex tin cti on and are ,or may be ,a f fected by trade; Appendix II species are not current ly thre aten ed but are likely to become so unless trade is re stri cted ;Appendix III species are listed to prevent or re stri ct exp l oi t a ti on .Data from CITES (2000). d“Ex ti n ct” refers to com p l ete taxonomic ex tin cti on ,ra t h er than the IUCN category “ex ti n ct in wild ” ; “end a n gered ”i n clu des those species listed by IUCN as “cri tic a lly en d a n gered ” ;“ vu l n era ble” in d i c a tes that species are likely to become ex ti n ct if c urrent trends conti nue .Data from IUCN–W orld Cons erva- ti on Un ion (2000). toxic chemicals in both terrestrial and aquatic situations (Pseudechis porphyriacus ),a large frog-eating snake, due to (Vitt et al.1990). Additionally,reptile eggs possess a cal- food shortages during extended drought conditions. Only careous shell, whereas amphibian eggs are enclosed by the smaller snakes survived, suggesting that large snakes simple gelatinous membranes, making the eggs more sus- may be relatively more susceptible to declines caused by ceptible to uptake ofenvironmental contaminants (but see food shortages.Gibbons (1990) reported a natural decline Pechmann and Wilbur 1994). The differences between for an isolated population of slider turtles ( Trachemys amphibians and reptiles are not limited to morphology scripta) on a coastal island. The turtle population had no and reproductive biology;they also include ecological and juvenile recruitment, presumably because ofconstant pre- behavioral traits. Most amphibians rarely travel more than dation on smaller individuals by alligators ( Alligator mis- a few hundred meters over the course oftheir lives (Seml- sissippiensis ) that had become established on the island; itsch and Ryan 1998); many reptiles may move several only large adult turtles survived. Natural fluctuations and kilometers both terrestrially and aquatically and have l ocal ex ti n cti ons are com m on in both re ptiles and home ranges encompassing tens or hundreds ofsquare amphibians (Pechmann et al.1991, Blaustein et al.1994c) kilometers (Brown 1993), and individual sea turtles may and generally are no cause for alarm. However,not all cover halfthe globe annually (Ernst and Barbour 1989). declines are natural. Nonetheless,the similarities between the ectothermic In this article, we consider the vulnerability ofreptiles tetra pod s — a m ph i bians and reptiles— link them inex- within the context ofthe factors known or suspected to be orably.Species ofboth classes occupy similar habitats and associated with amphibian declines,using the six cate- are equally vulnerable to habitat degradation. Thus, syn- gories ofconcern established by Partners in Amphibian topic species ofamphibians and reptiles are correspond- and Reptile Conservation (PARC; Gibbons and Stangel ingly defenseless against the global threats ofdeforesta- 1999): habitat loss and degradation, introduced invasive tion,draining of wetlands,and pollution from agricultural species, environmental pollution,disease and parasitism, runoff.Although the amphibian decline problem is a seri- unsustainable use, and global climate change. An addi- ous threat, reptiles appear to be in even greater danger of tional category comprises unexplained declines for both extinction worldwide (Table 1). reptiles and amphibians, wherein the disappearance of Population declines can be difficult to detect; hence, populations or a decline in numbers is a certainty but the long-term studies ofnatural populations and communi- cause is unknown.Of course,decline of a species may ties are generally regarded as indispensable for under- often be a cumulative effect of more than one of the standing normal population trends and fluctuations (Ti n- potential causes,as proposed for the documented declines kle 1979). Long -term studies ofa mph i bians and repti l e s ofthe Milos viper ( Microvipera schweizeri ) ofGreece (Nil- docu m ent tem poral vari ati on attri but able to natural causes son et al. 1999) and the asp viper ( Vipera aspis ) of the (Cody 1996). For example,Shine (1991) reported dramat- Swiss Jura mountains (Moser et al.1984, Jaggi and Baur ic declin es in Au s tralia of the com m on bl ack s n a ke 1999).
654 BioScience August 2000 / Vol. 50 No. 8 Articles
Our account is not exhaustive; rather,we provide docu- habitats and geographic regions lends credence to pleas m en ted examples of reptile pop u l a ti ons in peril and for concern about declines. decline.The aggregate ofexamples of amphibians and Studies ofdecline among reptiles, like those conducted reptiles indicates that the world’s herpetofauna face stres- for amphibians,have not always been carried out as rigor- sors from both known and unknown origins that, without ously as scientists would prefer. Nonetheless, the ever- remediation,can only lead to continuing declines,extirpa- increasing number of perceived declines among reptiles tions, and extinctions. and the documentation ofadverse impacts on individuals that pre su m a bly can be proj ected into dem ogra ph i c Dis tinguishing natural declines from changes are harbingers ofa crisis situation.Our intent is to a n th ropogenic ones show the phylogenetic and geographic breadth ofper- Amphibian declines are indisputably real and disquieting ceived problems with many reptiles, on the premise that on a global scale. Yet providing unequivocal supporting they foreshadow a more intense and widespread problem. documentation for the decline ofany particular popula- tion or species can be an onerous task, and some expecta- Ha bitat loss and degra d ati o n tions of scientific rigor may be unable to be met (Pech- Many scientists consider loss ofsuitable habitat to be the mann et al. 1991). One persistent incertitude regarding largest single factor contributing to declines of amphib- amphibian declines is whether a decline is simply within ians (Al ford and Ri ch a rds 1999). For ex a m p l e ,s om e the natural range of variability for a population or is regions of the United States retain less than 20% ofthe instead a consequence ofanthropogenic causes that could wetland acreage they once had (Leja 1998), and conse- portend an unrecoverable situation. quent declines in associated amphibian populations have One difficulty in dem on s tra ting wh et h er ob s erved been documented (Lannoo et al.1994). Numerous semi- trends in esti m a ted pop u l a ti on sizes con s ti tute norm a l aquatic reptiles rely on those very same wetlands. In South f lu ctu a ti ons or “ u n n a tu ra l ”declines is that most fiel d Carolina,the elimination or alteration ofmore than 90% s tudies ofa m ph i bians or reptiles have not had the du ra- ofCoastal Plain Carolina bay wetlands (Bennett and Nel- ti on or con s i s tency to make su ch determ i n a ti ons con- son 1991) has reduced essential habitat for black swamp vi n c i n gly (Pechmann and Wi l bur 1994). “Sn a p s h o t s” snakes (Seminatrix pygaea ),eastern green water snakes ( i . e . ,s h ort - term mon i toring) of pop u l a ti on size and (Nerodia floridana ),and chicken turtles ( Deirochelys retic- s tru ctu re may dem on s tra te curren t status but do not ularia),all of whose distribution patterns are restricted reve a ll on g -term trends in population size or health. For primarily to seasonal wetlands (Buhlmann 1995,Dorcas et example,Petranka et al. (1993), who used short-term al. 1998). Likewise, as bogs disappear in the eastern Unit- monitoring, and Ash (1997), who did long-term monitor- ed States, so too do bog turtles ( Clemmys muhlenbergii ), ing, came to different conclusions regarding the effects of and as streams and rivers are polluted, dammed, or chan- clearcutting on recovery time ofterrestrial salamander n el i zed ,riverine map tu rtles ( Gra ptemys) decl i n e populations. To be sure,the strongest support for a decline (Buhlmann and Gibbons 1997). Even if the jurisdictional
Ameri c a n crocod i l e . Like many crocod i l i a n s ,t h i s s pe cies has su f f ered from com m erci a l overexpl o i t a tio n and habit a t d e s tru ctio n .
is a long-term data set that has registered population lev- wetland itself is protected, in many cases the surrounding els for particular species in particular locations. However, terrestrial habitat needed by semiaquatic reptiles for nests, the accumulation of numerous accounts from shorter- hibernation sites,and other refugia is not (Burke and Gib- term studies ofa variety ofamphibian species in diverse bons 1995).
August 2000 / Vol. 50 No. 8 BioScience655 Articles
Just as habitat alterations may affect terrestrial salaman- if the habitat itself remains intact. Based on a 20-year ders (deMaynadier and Hunter 1995),they may also cause study, a wood turtle ( Clemmys insculpta ) population of declines in terrestrial reptiles. The loss of 97% ofthe more than 130 animals in a forested watershed in New southeastern longleafpine habitat (Ware et al. 1993), Haven County,Connecticut, has been virtually eliminated which has contributed to the decline ofthe flatwoods sala- since the area became open to the public (Garber and mander (Ambystoma cingulatum ;Means et al.1996), has Burger 1995). The possible mechanisms ofdecline includ- also redu ced su i t a ble ha bitat for goph er tortoi s e s ed removal, road kill,handling by recreationists,increased (Gopherus polyphemus ),eastern indigo snakes ( Drymar - number ofpredators attracted by food waste, and distur- chon corais ),and eastern diamondback rattlesnakes ( Cro - bance by dogs. talus adamanteus ;Guyer and Bailey 1993,Stephen H.Ben- nett, South Carolina Natural Heritage, Columbia,SC, Introdu ced invas ive spe ci e s personal communication). Introduced species have been cited as a problem for many amphibians (Stolzenburg 1999). For example,the distrib- ution and abundance ofseveral western US frog species have been severely reduced by non-native fishes and bull- frogs (Rana catesbeiana ),which were and continue to be introduced to wetland “island”habitats oflow- and high- elevation lakes (Fisher and Shaffer 1996). The collapse of endemic reptile faunas on true islands after the introduc- 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 ofthe 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 ofintroduced mammals, primarily rats. Feral pigs in the Galapagos Islands, first noted by Darwin in 1835, are just one of the non-native species that have caused the Bl a ck swamp snake .Loss ofCa rolina bay wetlands has near extinction ofthe Galapagos tortoise ( Geochelone ele - redu ced habitat for bl a ck swamp snakes and oth er phantopus;Thornton 1971). Introduced rats are suspected sem i - a q ua tic reptile species that are res tri cte d to have destroyed both the eggs and young ofthe tortois- pri m a ri ly to sea sonal wetl a n ds . e s ,but the initial cause of decline was 18th-cen tu ry mariners who stopped at the islands and stocked their Cu l tiva ted pine plantati ons in sout h e a s tern So ut h ships with live tortoises as food for the sailors (Pritchard Africa have been implicated in the endangerment of the 1967). rare short-headed legless skink ( Acontias breviceps ) and Even the introduction ofnon-native reptiles can disrupt the disappearance ofanother lizard (Eastwood’ s long- indigenous reptile communities. For example,Losos et al. tailed seps, Tetradactylus eastwoodae ;Branch 1998). In the (1993) showed that the invasion of Grand Cayman by Chiricahua mountains ofsoutheastern Arizona,the elimi- exotic brown anoles ( Anolis sagrei ) caused behavioral nation ofnative bunchgrasses by cattle grazing was con- changes and shifts in habitat use by the native species, sidered to be the primary cause ofa detectable decline in Anolis conspersus .Likewise, the introduction ofthe brown the bu n ch grass lizard ( S cel opo rus sc a l a ri s) ,wh i ch use tree snake ( Boiga irregularis ) has been implicated in the bunchgrasses for cover from predators and for protection ex ti rp a ti on of the gecko ( Na ctus pel a gi c u s ) from the from harsh winter conditions (Ballinger and Congdon islands ofGuam and Tinian;the brown tree snake is also 1996). Habitat loss is the biggest problem in the decline of considered responsible for dramatic declines in other snakes in Australia (Shine 1991). The link between intact species ofnative lizards on 13 ofthe Marianas Islands habitat and species persistence and well-being is a basic (Rodda 1992). tenet ofecology and conservation biology (Meffe and Car- Although island faunas are most susceptible to disrup- roll 1994, Mittermeier et al. 1999) and needs no further tion, the detrimental effects ofinvasives on native reptiles discussion. are not limited to islands. In the continental United States, The mere presence ofhumans may constitute an insid- i m ported fire ants ( S ol en opsis invi ct a ) ,i n trodu ced in ious form ofhabitat degradation in some instances, even Mobile,Alabama, as early as 1918 (Wilson 1950), have
656 BioScience August 2000 / Vol. 50 No. 8 Articles been reported to prey on both eggs (Moulis 1997) and young (Allen et al.1997) ofreptiles.Fire ants are implicat- ed as a primary cause ofextirpation ofthe Texas horned lizard (Phrynosoma cornutum ) from part ofits 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 ofthe negative impact ofnon-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, Habitat loss and degrad a tion are prim a ry threats to both reptile species richness decreased an average of5% from am p h i bian and reptile popu l a tio n s .Co nversion of 1978 to 1998 at 24 sample sites in the Snake River Birds of wetl a n ds , es pe ci a lly sea sonal wet l a nd s, and surrou n di n g PreyArea (John Cossel Jr. and Charles R.Peterson, Idaho terres trial habitat to agric u l tu ral (ill us tra ted here) and State University, Pocatello ID, personal communication). oth er uses have re sul ted in wetland losses exceeding 80% According to Cossel and Peterson,the changes in reptile in many states . populations may have been influenced by a decrease in native shrub habitat caused by the prevalence of exotic and eggs (Bishop et al.1994, Cobb and Wood 1997); sex annual grasses and the effects ofwildfires that have burned reversal and abnormal gonads have been found in turtles over 50% ofthe area since the 1970s. exposed to PCBs (Bergeron et al. 1994, Guillette et al. 1995). Male American alligators ( Alligator mississippiensis ) Enviro n m ental poll u ti o n inhabiting Lake Apopka, a chemically contaminated lake Numerous environmental contaminants— metals, pesti- in Florida, had significantly reduced plasma testosterone cides and herbicides,and radioactive waste, for example— levels and permanent gonadal alterations (Guillette et al. have direct and indirect effects on both amphibians and 1994). reptiles (e.g., Hinton and Scott 1990, Hall and Henry Even nonlethal effects ofendocrine disrupters on rep- 1992). Amphibians have been the subject of numerous tiles may result in demographic shifts whose consequences ecotoxicological studies,including assessment ofthe direct for populations are presumably detrimental. Population- effects of contaminants such as fertilizers (Marco et al. level effects might also occur through changes to patterns 1999) or the more subtle effects ofsteroid-mimicking con- ofindividual energy allocation.For example,in coal-ash taminants (Hayes 1997). Reptiles are studied far less than polluted wetlands, water snakes ( Nerodia fasciata ) with amphibians with respect to the fate and effects ofcontam- high body burdens ofmetal contaminants exhibit elevated inants (Hopkins et al.1999), but they have received suffi- metabolic rates, which may result in less energy being cient toxicological study to provide convincing evidence devoted to reproduction, growth, and storage (Hopkins et that some individual reptiles are adversely affected by al. 1999). many contaminants (Hall 1980, Fontenot et al.1994). For example,slider turtles ( Trachemys scripta ) exposed to met- Disea se and pa ra si ti s m al and radioisotope contaminants incur genetic damage Parasites and disease have been documented or suspected (Lamb et al. 1995). The degree to which contaminants as causes for declines in some amphibian species (Daszak cause population-level effects remains largely unknown, et al.1999). In some cases, sublethal environmental stres- both for amphibians and for reptiles. sors may suppress immune systems (Carey 1993) and Contaminant effects in reptiles are known mainly from allow disease agents to kill weakened animals (Alford and turtles and crocodilians. Many turtles and crocodilians, Richards 1999). Recently,however ,a spreading “extinction because they have environmental sex determination and wave”of chytrid fungus is thought to be causing the large eggs that can incorporate high levels ofenvironmen- decline of anurans in Central America and Australia tal pollutants, are especially sensitive to endocrine-dis- (Berger et al. 1998, Lips 1999); moreover,researchers rupting chemicals (Guillette and Crain 1996). At som e believe that the fungus is killing otherwise healthy animals cont am i n a ted site s, turtles acc umu l a te PCBs (polych l ori n a t- (Daszak et al. 1999). An iridovirus may be the primary ed biph enyl s ) , di eld ri n , and other contaminants in ti ssu es cause of the periodic population crashes in the Sonora
August 2000 / Vol. 50 No. 8 BioScience657 Articles ti ger salamander, Am bys toma ti gri num stebbi n s i (Ja n- red - l egged frogs ( Rana auro ra drayto n i i ) were collect- covi ch et al. 1 9 9 7 ) .Some amph i bian bi o l ogists now ed from wetlands in California (Jennings and Hayes 1985), believe that disease may rival habitat destruction as the and over 20 million leopard frogs ( Rana pipiens ) were tak- largest single cause ofthe decline ofamphibians. 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 ofwetland habitat destruction and degradation, intro- duction of predators, and previous commercial impacts (Lannoo et al.1994). In India,the frog-leg trade has result- ed in severe population declines of the Indian bullfrog (Rana tigrina ) and the green pond frog ( Rana hexadacty- la);an estimated 70 million frogs are exported illegally each year (Oza 1990). Human use ofa species is su s t a i n a ble ifit 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 ofthe use ofreptiles 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 ofthe tu rtle crisis on a gl obal scale was em ph a s i zed by Rh odin (1999), wh o reported that ofthe approx i m a tely 293 taxa (mainly Ea s tern box turt l e . The pet trade appears especi a lly s pec i e s ,but including some su b s pecies) off re s hw a ter tu r- h az ard ous for some turtle speci e s ,su ch as the eas tern box t l e s ,tortoi s e s ,and sea tu rtles known to be extant over the tu rt l e . last few cen tu ri e s ,3% (9 taxa) are alre ady ex ti n ct in the Among reptiles, the widespread upper respiratory tract wi l d .An ad d i ti onal 4% (12 taxa) are cri ti c a lly en d a n- disease, a contagious respirator y ailment caused by the gered ,11% (32 taxa) are en d a n gered ,and 21% (61 taxa) bacterium Mycoplasma agassizii ,is a potential cause of a re vu l n era bl e . population declines in desert tortoises in the US South- The crisis is particularly acute forAsian freshwater tur- west and gopher tortoises in the Southeast (Jacobson tles and tortoises, which are harvested as a local food 1993, Smith et al.1998).Shell diseases have been implicat- source.Moreover, the international trade in turtles— ed in the decline of turtles (e.g., shell lesions on sliders, which are eaten,sold as pets, or used in traditional Chi- Lovich et al. 1996; cutaneous dyskeratosis affecting the nese medicinal remedies—is both extensive and unregu- shell and thickened forelimb scutes ofdesert tortoises, lated (Sharma 1999). A recent report indicated that most Jacobson 1994; and emaciation and lesions ofthe plastron turtle species in Vietnam and southern China are endan- offederally listed flattened musk turtles, Sternotherus gered and that turtles can no longer be found in the wild depressus,Dodd 1988). Individuals in many green sea tur- in Vietnam (Kiester and Juvik 1997). China is the biggest tle populations are severely affected by viral fibropapillo- consumer ofturtles in the food trade. Because the trade in mas, resulting in growths that can impair vision, locomo- turtles is not regulated, few records have been kept, but tion,and feeding ability (Herbst 1994). As is often the case existing records indicate that the trade in live turtles to in amphibians,diseases that are debilitating to wild popu- China is thousands oftons per year (Mockenhaupt 1999). lations ofreptiles are most likely secondary expressions in The commercial trade in freshwater turtles exceeds any individuals with impaired resistance caused by one or possible sustainable levels, and extinction ofsome species more primary environmental stressors, such as habitat in the wild can be expected within the next decade. degradation, invasive species, or pollution. Most species ofsea turtles continue to decline in all warm oceans of the world. The leatherback sea turtle Un su s t a i na ble use (Dermochelys coriacea ) was recently reported to be“on the Human use ofanimals,includin g reptiles and amphibians, road to extinction and further population declines can be is an integral part ofmany cultures. Harvesting must be expected”unless appropriate measures are taken to reduce bi o l ogi c a lly su s t a i n a bl e ,h owever, i fpop u l a ti ons and mortality rates in adults, hatchlings, and eggs (Spotila et species are to persist (Pough et al.1998). Overcollection a l .1 9 9 6 ) .The esti m a ted worl dwi de pop u l a ti on of for food, the pet trade, and biological supply houses has leatherbacks nesting on beaches in 1980 was 115,000, been suggested as having had an impact on some amphib- com p a red w ith just 34,500 in 1995. Ex p l oi t a ti on of ian populations (Dodd 1997). In the United States, note- leatherbacks in the Atlantic Ocean, through illegal har- worthy examples for amphibians occurred in the late vesting ofboth adults and eggs,is considered to be a major 1800s to early 1900s, when commercial collectors harvest- contributor to the decline of the species (Spotila et al. ed for the frog legs market. Hundreds of thousands of 1996). Likewise, for Kemp’s Ridley sea turtle ( Lepidochelys
658 BioScience August 2000 / Vol. 50 No. 8 Articles kempii),harvests ofnesting females and their eggs on the decline occurring over the last 20 years. Of the 191 largest known nesting site contributed to declines from remaining bog turtle habitats known in 1996,33 were clas- 42,000 nesting females in 1947 to only a few hundred by sified as in good condition,67 as fair, and 76 as poor; the 1975 (Hildebrand 1982). status of15 was unknown. Among North American turtles, the diamondback ter- rapin (Ma l a cl emys terrap 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 reductions 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 commercial harvest ofthe diamondback terrapin has also been documented (Garber 1988). Commercial turtle trappers for the restaurant trade stepped up harvests ofone ofthe 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 been drastically reduced in numbers in some of the southeastern US rivers it once inhabited (Moler 1992, Jensen 1998). The enormous and once common populations ofthe arrau (Podocnemis expansa ),a communally nesting turtle ofthe Orinoco and Amazon Rivers in South America,are Sn a pping turtle eggs and hatchl i n gs .Most con t a m i na n t now greatly reduced in size because ofhuman consump- s tudies on reptiles have been con du cted on snappi n g tion of eggs and nesting females (Pritchard and Trebbau turtles and all i gato rs ,in wh i ch sex reversal and abn o rm a l 1984), an overexploitation problem identified almost two gonads have be en note d . centuries ago (Humboldt 1814, from Pritchard and Treb- Overcollecting is also a problem for some snake species. bau 1984). Declines from similar causes have befallen the The ocellated mountain viper ( Vipera wagneri ) in eastern terecay (Podocnemis unifilis ) in tropical lowlands ofSouth Turkey has been sought by the pet trade and removed America (Thorbjarnarson et al. 1993) and the river ter- from the wild in large numbers,posing “a serious threat to rapin (Batagur baska ) in India (Bhupathy 1997). survival ofthe species”(Nilson et al.1990). Populations of Overharvesting for food is a problem not just for turtles several boa and python species have declined because of but also for lizards,having contributed to declines in green harvesting ofwild snakes for their skins (Pough et al. iguanas (Iguana iguana ) a nd spiny - t a i l ed iguanas 1998). Rapid declines oflarge-bodied snakes, which tend (Ctenosaura similis ) in tropical America (Fitch et al.1982). to have a suite oflife-history traits that make them more The pet trade appears especially hazardous for some susceptible to population declines than smaller species turtle species. In 1994, population declines were reported (e.g., Dodd 1993),have been documented throughout the in box turtles ( Terrapene carolina ) in 16 states, ranging world in recent years (e.g.,Shine and Fitzgerald 1996). For from Massachusetts to Florida and Oklahoma toWiscon- example,females of the increasingly rare timber rat- sin (Lieberman 1994). Doc u m en t a ti on of box tu rt l e tlesnake (Crotalus horridus ),which may exceed a meter in decl i n e s — i n cluding records showing that, s i n ce 1995, length and ty pically take 9 years to reach maturity, pro- 29,896 box turtles had been collected for the pet trade and duce fewer than a dozen young every 3 years (Brown shipped from Louisiana—resulted in unanimous passage 1993).Large-bodied species such as rattlesnakes ( Crotalus) ofAct 81 by the Louisiana Senate and House ofRepresen- have long generation times, a life-history trait that, when tatives in 1999;the act prohibits the commercial harvest of com bi n ed with habitat loss, human pers ec uti on ,a n d the state’s native box turtle populations. Overcollection for 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” ; export is a serious factor in much ofthe box turtle decline Brown 1993),has led to dramatic declines ofsome species and may exacerbate the effects ofhabitat loss (Lieberman and made approximately one-third ofrattlesnake species 1994). Habitat destruction and illegal collecting for the pet vulnerable to extinction (Greene 1997). High harvest rates trade are the primary threats to bog turtles ( Clemmys ofsnakes with low reproductive frequencies,such as the muhlenbergii );Copeyon 1997). The number ofnorthern 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 populations has been reduced by 50%, with most ofthe almost certainly be unsustainable (Shine et al.1995).
August 2000 / Vol. 50 No. 8 BioScience659 Articles
These examples demonstrate that sustainable use of based solely on analyses ofclimate– space changes, because some long-lived reptile species is problematic. Because species distributions are also a function ofdispersal abili- longevity in reptiles is associated with delayed sexual ty and biotic interactions (Davis et al. 1998). Existing m a tu ri ty, h i gh adult su rvivors h i p, and low fec u n d i ty nature reserves will be inadequate to preserve current bio- (Pough et al.1998), populations oflong-lived species can- diversity, because an already fragmented landscape will not remain stable (or grow) when adults and older juve- i m pede the abi l i ty of s pecies to re s pond to cl i m a te - niles are harvested at high rates (Congdon et al. 1993, induced habitat changes (Halpin 1997). Because oftheir 1994). This is not to say, however, that all such long-lived limited dispersal abilities, reptiles and amphibians are species should be commercially off-limits. The key to sus- especially vulnerable to rapid habitat changes and may tainability is having species- and population-specific man- suffer many more extinctions than birds as a result ofa agement plans and tightly controlled use (Ross 1998). rapid rate ofclimate change (Schneider and Root 1998). For example,three decades ago, several species ofcroc- In discussions ofobserved amphibian declines,little odilians were on the verge ofextinction because ofa com- mention has been made ofclimate change (Dodd 1997), bination of threats, including habitat destruction (Ross with two notable exceptions. First, the famed golden toad 1998) and unsustainable harvest ofadults for the leather (Bufo periglenes ) extinction in Costa Rica may have been trade (Brazaitis 1989). After years oftotal protection, sev- caused,at least in part, by global warming effects on mon- eral species have recovered;a few are farmed or ranched tane dry-season mist frequencies (Pounds et al. 1999). commercially (King 1989). In some crocodile species, Fauna in tropical montane cloud forests may be particu- adult females are protected and only small numbers of larly susceptible to rapid climate shifts that may change eggs, small juveniles,and larger males are removed from patterns ofcloud formation and thereby the availability of the wild (King 1989). In contrast, 7–8% ofall alligators water (Still et al. 1999). Second, Blaustein et al. (1994a) more than 1.2 m in length are harvested annually in some have suggested that ultraviolet B (UVB) radiation has Florida populations (David et al.1996). In addition,a 50% adverse effects on some amphibians, including reduced annual harvest rate of alligator eggs or hatchlings is hatching success and decreased survival to metamorpho- allowed because removal at these life stages does not sis. However,an increase in the level of UVB caused by reduce recruitment into adult-size classes (Rice et al. depletion of the ozone layer probably does not pose an 1999). Closely monitored alligator populations, and pre- i m m ed i a te threat to reptile eggs ,wh i ch are sel dom sumably populations ofother long-lived species ofrep- exposed to UVB radiation. tiles, can sustain the legal,regulated harvest ofsome pro- As with the amphibian studies, few researchers have porti on of eggs ,h a tch l i n gs ,or adults with negl i gi bl e directly assessed effects ofclimate change on reptiles. It is effects. 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 Gl obal cl i m ate ch a n ge restrict species with limited distributions (Schneider and Few ecologists will dispute the link between increases in Root 1998), as has been suggested for some Australian greenhouse gases and gl obal tem pera tu re .However, lizards (Brereton et al.1995) and crotaline snakes ofNorth whether the current rate ofclimate change reflects natural America and the neotropics (Greene and Campbell 1993). variation or has an anthropogenic cause is hotly debated. Additional effects ofwarming on some reptiles, based on For the purposes ofthis article, we accept the argument em p i rical evi den ce with fre s hw a ter tu rt l e s ,i n clu de that the earth is undergoing unprecedented rapid climatic enhanced juvenile growth rates, earlier ages at maturity, change (Schneider and Root 1998) that includes alter- and shifts in functional sex ratios (Frazer et al. 1993). ations in climate variables such as temperature and rain- Global warming may have the greatest impact on those fall patterns, storm severity, and storm frequency.If one reptiles (crocodilians and some turtles) that have temper- accepts that human-induced climate change is occurring ature-dependent sex determination (Janzen 1994), where- (e.g., Vinnikov et al.1999),then the consequences for her- by the sex ratio of the hatchlings is determined by nest petofaunal diversity can be addressed. temperatures during incubation.Unless shifts occur in the The obvious effects of climate change on biodiversity pivotal temperatures at which sex is determined, or female are mediated through changes in habitat. For example, nest-site choices (i.e., shade versus sun) evolve to keep global warming may further diminish prairie wetland pace with rising temperatures, altered sex ratios could habitat in the United States (Poiani and Johnson 1991). affect population demographics and persistence. Future wetland acreage in the United States may be great- ly reduced under a variety ofclimate circulation models En igm a tic decl i ne s (Halpin 1997), and aquatic and semiaquatic species will Finally,in addition to the many cases ofdeclines that have suffer declines as habitat disappears. Although many habi- s ome re a s on a bly unders tood causes, s ome amph i bi a n tats are ex pected to under go dra m a tic ch a n ge (e.g. , populations have declined,and even gone extinct, without Guertin et al.1997,Still et al. 1999), predictions ofspecies any discernible causes. One well-known example is the habitat shifts in response to global warming cannot be gastric brooding frog ( Rheobatrachus silus ) of Australia.
660 BioScience August 2000 / Vol. 50 No. 8 Articles
S h ort ly after the discovery of its unu sual sys tem of best documented because, like many amphibians, they parental care,in which the young develop in the safety of engage in an annual reproductive event (in this case, the mother’s stomach (Tyler and Carter 1981), the gastric oviposition) with a predictable site and time. A few snake brooding frog ceased to be found in nature.Disjunct pop- species in colder temperate regions are known to hiber- ulations ofthe green salamander ( Aneides aeneus ) in the nate communally ,and numbers can be assessed upon 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 ofits range (Jeff Corser, USGS-BRD, Twin Creeks Resource Center,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 ofmany are but a remnant ofthe much larger areas formerly occupied. Nat- ural populations ofindigo snakes have not been found in some regions oftheir 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 ofthe sout h ern hognose snake ( Heterod o n simus)h ave not been reported from ei t her Alabama or Mi s- s i s si ppi in more than 18 yea rs (Tu bervi lle et al.2 0 0 0) , even in large pro tected areas with rel a tively pri s tine habit a ts . Doc u men ting decl in es Regrettably, many amphibian populations and species that are thought to be declining have not been monitored over long periods oftime, making short-term changes in pop- ulation size difficult to evaluate critically.The best long- term studies ofamphibian populations that allow for crit- ical evaluation of population trends share a common characteristic: The subjects ofthese studies occur in high Sou t h ern hogn o se snake. This spe cies has not been density either spatially (e.g., Jordan’s salamander, Plethod - reco rded from regions ofits histo ric ra n ge in Ala ba m a on jordanii ;Hairston 1987) or temporally (e.g., mole sala- and Mi s si s s i ppi for more than 18 years . Its disappeara nce manders, Ambystoma talpoideum ;Pechmann et al. 1991; is so m ewhat mys teri ou s ,as the reasons for its decline are and natterjack toads, Bufo calamita ;Banks et al.1994). n ot well unders tood . Many ofthe species that have become symbols for the declining amphibian phenomenon are seasonally active emergence (Parker and Brown 1973). But what ofthe anurans that arrive over restricted periods oftime at majority ofreptile species that do not congregate to breed breeding sites where they congregate in greater densities or hibernate and do not occur in particularly high densi- than at any other time ofthe year.Researchers sit ready to ties? For example,the racer ( Coluber constrictor ), a com- record their arrival and abundance,and if the animals fail mon North American snake, is found in a wide variety of to show up when expected,a problem is suspected; if such terrestrial habitats. Like most other ectotherms, racers are absences are protracted, then the change is presumably more active, and therefore more commonly encountered, real (Blaustein et al. 1994c). The phenology of these in the warmer months. However,aside from some regions amphibians permits detection ofbreeding activity; there- where communal hibernation occurs (Parker and Brown fore,determination of whether the absence of breeding 1973), determining the abundance of racers is difficult adults is a short-term aberration or an indication ofa real because oftheir stochastic patterns ofactivity. Herpetolo- decline becomes a matter ofaccumulating the data neces- gists would be hard-pressed to describe densities accurate- sary to demonstrate a statistically significant trend (for ly du ring any season over a wi de geogra phic ra n ge . discussion, see Blaustein et al. 1994c, Pechmann and Because racers do not congregate at a breeding site, how Wilbur 1994, Reed and Blaustein 1995). could we take a census to know when and if racer popula- Among reptiles, declines in sea turtles are perhaps the tions were declining at a substantial rate on a widespread
August 2000 / Vol. 50 No. 8 BioScience661 Articles
proximally through legislation and cultural shifts in envi- ronmental attitudes. Minimally,society must place a pre- mium on maintaining habitats ofsufficient size and qual- ity not only for imperiled taxa but for herpetofauna in general (Beebee 1992, Semlitsch 1998). For example,pro- tecting the basins ofwetlands 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 ofAsian turtles, legislative remedies could be too lit- tle,too late—a stopgap remedy is necessary. The only way to prevent the imminent extinction ofa large number of the more than 80 species ofturtles native to southernAsia (Va ranus go u l di ) Sand monitor .Al t h ou gh sand will be to maintain populations in ex situ captive breeding Va ranu s m on ito rs (genus , whi ch includes the wo rl d’ s and genetic reser ve programs. With changes in cultural la rgest lizards) appear to be thriving in many parts of attitudes,strengthening ofinternational trade regulations, t h eir natural habitats in Aus tra l i a ,ot h er spe cies oft h e and increased habitat protection, the reintroduction of genus in As i a ,Afri c a ,and the East Indies are threaten e d these species into the wild may be possible. by exten sive habitat destructi o n . Much oftoday’s commercial exploitation ofreptiles in basis without mounting an intensive, long-term sampling the United States and elsewhere requires urgent govern- program? The clandestine nature ofmany reptiles, often mental action to implement internationally accepted and combined with comparatively large home ranges, low enforced controls.Despite the fact that conservation mea- pop u l a ti on den s i ti e s ,and ra reness of con grega ti on a l sures can be implemented effectively through legislation behavior,makes documenting population trends very dif- (as happened with legislation for protection ofLouisiana ficult.As a result, populations may wither with little box turtles and American alligators), the political pres- notice.Once an unmonitored species or population is rec- sures against accomplishing such goals cannot be overstat- ognized as being unexpectedly depauperate or absent, the ed. The lack ofsupport by the World Trade Organization cause ofdecline may be unknown and unknowable. for recommendations to curtail sea turtle exploitation Based on the accumulated evidence that many if not (WTO 1998) brings the problem into perspective on an most declines reported for amphibians are indeed real,the international scale. proper course for conservation initiatives is to assume the Direct and indirect effects ofenvironmental pollution, worst for all herpetofauna, and therefore to implement disease and parasitism, and global climate change are abatement measures while gathering more data. Although more difficult to quantify in many instances and will be the lack oflong-term data often may preclude the identi- more difficult to change in the short term. Nonetheless,we fication ofthe cause ofa decline,or even in some cases the must endeavor to understand these potential factors to corroboration ofa decline,the absence ofthat data does ameliorate their impact on natural populations ofreptiles not rule out the existence ofa correctable problem. and their habitats. Finally,long-term monitoring ofreptile populations is Co n clusion and re com m en d ati o n s essential and must be aided by the establishment ofstan- The declines ofm a ny reptile pop u l a ti ons are similar to dard methods and techniques.It is equally important that those ex peri en ced by amph i bians in terms oft a xon om- the academic community ,land managers, and conserva- ic bre ad t h ,geogra phic scope ,and se veri ty. As wi t h tion organizations recognize that rigorous field programs a m ph i bi a n s ,the causes are known with cert a i n ty in focusing on the distri buti on ,a bu n d a n ce ,s t a tu s ,a n d s ome instance s ,su s pected in many,and un known in trends ofpopulations and species are critical and worth- o t h ers .Some ex ti rp a ti ons are local wh ereas others are while. Herpetofaunal inventories should become a stan- m ore wi de s pre ad .The diff iculty in doc u m en ting the dard part ofenvironmental assessment programs, and the s cope and source ofe ach reptile (or amph i bian) pop u- publication offield survey efforts that document potential l a ti on decline should not be undere s ti m a ted . or suspected declines should be encouraged.When long- Biologists must be pragmatic in assessing which causes term and widespread monitoring becomes the norm, ofpop u l a ti on declines can be obvi a ted direct ly.Th e declines are likely to become less equivocal (in terms of i mp act of ha bitat degrad a ti on ,i n trodu ced inva s ive speci e s , protracted declines versus natural fluctuations) and the and unsu st a i na ble use can be con tro ll ed immed i a tely and causes less mysterious.
662 BioScience August 2000 / Vol. 50 No. 8 Articles
The disappearance ofreptiles from the natural world is Bl a u s tein A R ,Hoffman PD,Hokit DG, Ki e secker JM,Wa lls SC, Hays JB. genuine and should be a matter ofconcern not simply 1 9 9 4a . UV repair and re si st a n ce to solar UV-B in amph i bian eggs: A link to popu la ti on declines? Proceed in gs of the Nati onal Ac ademy of because of reptiles’ perceived associations with amphib- S ci en ce of the Uni ted States of Am erica 91: 17 9 1 – 1 79 5 . ians, but because reptile declines,like those ofamphibians, Bla u s tein A R ,Hokit DG, O’Ha ra RK, Holt RA .1 9 9 4 b. Pat h ogenic fungus are growing and serious in their own right. Current evi- con tri butes to amph i bian losses in the Pacific Nort hwe st . Bio l ogi c al dence suggests that amphibian and reptile declines,which Con s erva ti on 67: 2 51 –2 5 4 . are exacerbated by burgeoning human populations, con- Bla u stein AR ,Wa ke DB,Sousa W P.1 99 4 c. Amph i bian decl i n e s :Ju dgi ng s ta bi l i ty, persi sten ce , and su scepti bi li ty of pop ul a ti ons to local and stitute a worldwide crisis. gl obal exti n cti on s. Cons ervati on Bio l ogy 8: 6 0 – 7 1. Bra n ch B.1 9 9 8 .F i eld Gu ide to Sna kes and Ot her Reptiles ofSouth Afri c a . Ackn owl e d gm ent s San i bel Island (FL): Ral ph Cu rtis Book s . Manuscript preparation was aided by Financial Assistance Braz a i tis P.19 8 9. The trade in crocod il i an s . Pages 196–201 in Ross CA, ed . Aw a rd Nu m ber DE-FC09- 96SR18546 from the US Crocodiles and All i ga tors .New York :Facts on File. Brereton R, Ben n ett S,Man s er gh I.1 99 5 .E n ha n ced greenhouse cl i ma te Dep a rtm ent of E n er gy to the Un ivers i ty of G eor gi a cha n ge and its poten tial ef fect on sel ected fauna of s o ut he as tern Au s- Research Foundation.W e thank Ab Abercrombie, Justin tra l i a :A trend analys i s .Bio l o l ogical Con serva ti on 72: 3 39 –3 5 4. Congdon,William Hopkins, Laura Janecek, Christopher Brown WS .19 9 3. Bi o l ogy,s t a tu s ,and managem ent of the ti m ber rat- Romanek, and Joseph Pechmann for discussion and com- tl e sn a ke (Crotalus horri dus ) :A guide for cons ervati on. Soci ety for the S tudy of Amph i bians and Repti l e s. Herpeto l ogy Circ u l a ti on 22: 1 – 7 2. ments on the manuscript. We also appreciate the help of Buhlmann KA .1 9 9 5 .Habitat use, terres trial movem ents and cons ervati on Stephen H.Bennett,John Cossel Jr., Charles R.Peterson, of the tu rtle Di ero ch elys retic u l a ri a in Vir gi n i a .Jo urnal of Herpeto l ogy Paul Moler,WoodyWoodward,and Jeff Corser for provid- 2 9 :1 7 3 – 1 8 1 . ing information on the status ofparticular species. This Buhlmann KA ,G i bbons JW. 1 99 7 .Im peril ed aqu a tic reptiles of the sout h- paper supports the PARC (Partners in Amphibian and e as tern Uni ted State s: His torical revi ew and current con s erva ti on sta- tus . Pa ges 201–232 in Benz G,Co llins DE,ed s .Aqua tic Fauna in Peri l : Reptile Conservation) effort to promote education about the So ut h ea s tern Perspective .Dec a tur (GA):Lenz De si gn & Commu- reptiles and amphibians. ni c ati on s . Bu ll ock DJ. 1 98 6 .The eco l ogy and con s erva ti on of reptiles on Ro un d Ref eren ces cite d Island and Gu n ner ’ s Quoin , Mau ritiu s. Bi o l ogical Con s ervati on 37: Alford RA, Rich a rds SJ. 19 9 9 . Gl obal amphi bian decli n e s :A problem in 1 3 5 ,1 5 6 . app l i ed ecol ogy . Annu al Review of Eco l ogy and System a tics 30: 13 3– 16 5 . Bu rke V J, G i bbons JW.1 9 95 . Terres trial bu f fer zones and wetland cons er- Allen CR, Rice KG ,Wojcik DP,Percival HF. 19 9 7. Ef fect of red imported va ti on :A case stu dy of f res hwa ter turtles in a Ca rolina Bay.Con s erva- f i re ant enven om i z a ti on on neonatal American alli ga tors .Jo u rnal of tion Bio l ogy 9: 13 6 5– 13 6 9. Herpeto l ogy 31: 3 18 –3 2 1. Carey C.1 9 93 .Hypothesis concerning the causes of the disappea ran ce of boreal toads from the mountains of Co l orado.Con serva ti on Bi o l ogy 7: Ash A N .1 9 9 7 .Di sa ppe a ra n ce and return of sa l a m a n ders to cle a rc ut plots 3 55 –3 6 2. in the south ern Blue Rid ge mountains.Con s erva tion Bi o l ogy 11: Ca rr A F.1 9 52 . Han d book of Turt l e s .The Tu rtles of the Un ited States , 9 8 3– 98 9 . Can ad a , and Ba ja Ca l i forn i a. It h aca (NY): Com s tock Pu bl is h ers Ass o- Ball i nger RE, Con gdon JD. 1 9 9 6. S ta tus of the bu n ch grass lizard, Scel o - c ia ti on ,Corn ell Un iversi ty Pre s s . porus sca la ri s,in the Chi ri ca hua mountains of so ut h e as tern Ari zona . Case TJ, Bol ger DT.1 99 1 .The role of in trodu ced species in shaping the dis- Bu ll etin of the Maryland Herpetol ogical Soci ety 32: 6 7– 69 . tri buti on and abu nd a n ce of island repti l es .Evo luti ona ry Ecol ogy 5: Banks B,Beebee TJC, Cooke KS. 1 9 94 .Con s erva ti on of the natter jack toad 27 2 –2 9 0. B u fo calamita in Britain over the peri od 1976–1990 in rel a ti on to site Cobb GP,Wood PD.1 9 97 .PCB con cen trati ons in eggs and ch orioa ll a n to- pro tecti on and other factors. Bi o l ogical Cons ervati on 67: 1 1 – 1 18 . ic mem branes of l oggerh e ad sea tu rtles ( Ca retta caret ta ) from Ca pe Beebee TJC. 1 9 92 . Amph i bian decline? Na tu re 355: 1 2 0. Romain Na ti onal Wil dl i fe Refu ge . Chem o s ph ere 34: 5 39 –5 4 9. Benn ett SH, Nel son JB.1 9 91 . Di stri buti on and status of Carolina bays in Cody ML.1 99 6 .In trodu ction to lon g - term commu n i ty ecol ogical stu d i es . So uth Caro l i na . Colu m bia (SC): Non game and Heri t age Trust Publ i- Pa ges 1–15 in Cody ML, Sm allwood JA, ed s .Lon g - term Studies ofVer- 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 tebra te Commu n i ti es .San Di ego :Ac ademic Pres s. Res ou rces Depa rtm en t , Co lu m bi a ,S C . Conant R.1 97 2 .Reptile Stu dy.Official book l et for Merit Badge Serie s . Irv- Ber ger L, et al.1 9 9 8. Chytri di omycosis causes amph ibian morta l i ty assoc i- ing (TX ) : Boy Scouts of Am eri c a. a ted with popu l a ti on declines in the ra i n forests of Au stralia and Cen- Conant R,Co llins JT.19 9 8. Reptiles and Amph i bians of North Am eri ca . tral Am eri c a. Proceed i n gs of the Nati onal Academy of Sc i ences of th e 4th ed .New York :Ho u gh ton Mif fl i n. Uni ted States of Am erica 95: 9 0 31 –9 0 36 . Congdon JD, Dunham A E, van Loben Seals RC. 19 9 3. Delay ed sex u a l Ber geron JM,Crews D, Mc Lachlan JA .1 9 9 4 .PCBs as envi ron m ental estro- 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 gen s: Turtle sex determ i n a ti on as a biom a rker of envi ron m ental con t- bla n d i n gii ): Imp l i ca ti ons for con s ervati on and management of l on g - a m i n a ti on .E nvi ron m ental Health Pers pectives 102: 7 8 0– 7 81 . lived or ga n is m s .Con serva ti on Bi o l ogy 7: 82 6 – 8 3 3. Bhu pa t hy S. 19 9 7. Cons ervati on of the end a n gered river terrapin Ba t a g ur ______.1 9 9 4 .Demogra phics of com mon snapping tu rtles ( C h elyd ra ser - bas ka in the Sun derban of West Benga l ,In di a .Jo u rnal of the Bom b ay penti n a ): Imp l i c a ti ons for cons ervati on and management of lon g - l ived Na tu ral Hi story Soc i ety 94: 27 –3 5 . orga n i s m s. Am erican Zool ogist 34: 3 9 7– 40 8 . Bi s h op CA, Brown GP,Brooks RJ, Lean DRS, Ca rey JH.1 9 9 4 .O ra n och l o- [CITES] Conventi on on In terna ti onal T rade in Endangered Species of rine contaminant concen tra ti ons in eggs and their rela ti onship to body Wild Fauna and Flora .2 00 0 .
August 2000 / Vol. 50 No. 8 BioScience663 Articles
Daszak P,Ber ger L,Cun n i ngham A A ,Hyatt AD, Green DE,S pe a re R.19 9 9. Gu ill et te LJ Jr,Crain DA .1 9 96 . En doc ri n e -d i s ru pting contaminants and E m er ging infectious diseases and amph ibian pop ul a ti on decli ne s . reproductive abn orm a l ities in repti l es .Com m ents in Toxi co l ogy 5:
664 BioScience August 2000 / Vol. 50 No. 8 Articles
Jan zen FJ. 1 99 4 . Cli m a te ch a n ge and tem pera tu re depen dent sex determ i- Mos er A ,Gra ber C,Frey vogel TA .1 9 84 . Ob serva ti ons sur 1’et h o l ogie et na ti on in repti l e s. Proceed i n gs of the Nati onal Ac ademy of S c i en ces of 1’ evo lution d’une popu la ti on de Vi pera aspis (L.) au nord du Ju ra the Uni ted States of Am erica 91: 7 48 7 – 7 49 0 . Sui ss e. Amph i bia - Reptilia 5: 3 7 3– 39 3 . Jen ni n gs MR, Hayes MP.1 98 5 .Pre-1900 overh a rvest of Ca l i fornia red - Moulis RA 1997. Preda ti on ofthe imported fire ant ( S ol en opsis invict a ) on legged frogs ( Rana aurora drayto n ii ): The indu cem ent for bu ll f rog loggerh ead sea tu rtle ( Ca retta carett a) nests on Wa s s aw Na ti on a l (Rana cates bei an a ) introdu ction . Herpetol ogica 41: 9 4– 10 3 . Wi ldl i fe Ref uge , G eor gi a .Ch el onian Con serva ti on and Bi o l ogy 2: Jen s en JB.1 9 9 8. Dis tri buti on and status of the alli ga tor snapping tu rt l e 4 33 –4 3 6 . (Macro cl emys temm i n ck ii ) in Geor gia .Pa per pre s ented at the 78th Mount RH. 1 97 5 .The Reptiles and Am ph ibians of Ala b a m a .Au bu rn (AL): Annual Meeting of the Am erican Soc iety of Icht hyo l ogists and Her- Aubu rn Un ivers i ty, Alabama Agric u l tu ral Ex perim ental Stati on . peto l ogi s t s ;16–22 Jul 1998; Univers ity ofGu el ph ,O n t a ri o, Can ad a . Nil s on G, And ren C, Fl a rdh B.1 9 90 . Vipera albi zo n a ,a new mountain vi per Joh n s on PTJ,Lu n de KB, Ritchie EG.1 99 9 .The ef fect of trem a tode infec- f rom cen tral Tu rkey, with comm ents on isolating ef fects of the Ana to- tion on amph ibian limb devel opm ent and survivors hi p. S c ien ce 284: lian Di agon a l .Am ph i bi a - Reptilia 11: 28 5 – 2 94 . 8 02 –8 0 4. Nil s on G, And ren C, Ioannidis Y,Dimaki M.1 9 9 9 .E co l ogy and cons erva- Kell ert SR, Wi l s on EO.19 9 3. The Bi ophilia Hypo th e s i s. Was h in g ton (DC) : ti on of the Milos vi per, Ma crovi pera schwei zeri (Wern er, 1 93 5 ). Island Pres s. Amph i bi a - Reptilia 20: 3 5 5– 37 5 . Kie s ter A R, Juvik JO.1 9 9 7. Cons ervati on cha ll en ges of the tu rtle trade in Oza GM.1 99 0 .E co l ogical ef fects of the frog’s leg trade .E nviron m en t a l i s t Vi etnam and Chi n a .Pa per pres en ted at the Joint Meeting of Am eri ca n 10 : 39 –4 1 . Soc iety of Ich t hyol ogists and Herpeto l ogi st s ,Herpeto l ogi s t s’Le a g u e, Pa rker WS, Brown WS .1 9 7 3 .S pecies com po s i ti on and popu la ti on cha n ge s and Soc i ety for the Stu dy of Am phi bians and Reptil e s ;26 June–2 Ju ly in two com pl exes of s n a ke hibern acula in nort hern Ut a h. Herpeto l og- 1 9 97 ;Se a t t l e ,WA. ica 29: 3 19 –3 2 6. King FW. 19 8 9. Con serva ti on and managem en t .Pa ges 216–229 in CA Pechmann JHK, Wil bur HM.1 99 4 .Put ting declining amphi bian popu la- Ros s ,ed .Crocodiles and All i ga tors .New York :Facts on File. ti ons in pers pective: Na tu ral fluctu ati ons and human impact s. Her- Lamb T, Bickham JW,Lyne TB,G ibbons JW.1 99 5 .The slider tu rtle as an peto l ogica 50: 6 5 – 8 4. envi ron m ental sen ti n el : Mul tiple ti ssue assays using flow cytom etri c Pechmann JHK, Scott DE,Sem l it s ch RD,Cal dwell JP,Vitt LJ, G i bbons JW. an a lys i s .E co tox ico logy 4: 5– 13 . 19 9 1 .Declining amphi bian popu la ti on s :The probl em of sep a ra ti n g L a n n oo MJ,Lang K,Waltz T, P h i llips GS.1 99 4 .An altered amphi bi an human impact from natu ral fluctu a ti on s .S c i en ce 253: 8 9 2– 89 5 . as sem bl a ge :Di cki ns on Co un ty, Iow a ,s even ty ye a rs after Frank Bl a n- Poiani KA ,Jo hn s on WC .1 9 9 1 .G l obal warming and prai rie wet l an d s . Bio- ch ard ’s su rvey.Am erican Mi dlands Na turalist 131: 3 1 1– 31 9 . Sc i ence 41: 6 11 –6 1 8. Leja WT. 19 9 8. Aqu a tic habitats in the Midwe s t :Wai ting for amphi bia n Po u gh FH,An d rews RM,Cadle JE,Crump ML, Savi t z ky A H, Wells KD. con s erva ti on initi a tive s. Pages 345–353 in Lannoo MJ,ed .S t a tus and 19 9 8. Herpeto l ogy. New Jers ey: Prenti ce -Ha ll . Con s erva tion of Midwe s tern Amph i bi a n s. Iowa Ci ty (IA):Un iversi ty Pounds JA, Fogden MPL,Ca m pbell JH.1 9 99 . Bio l ogical re sponse to cl i- ofIowa Pres s. ma te ch a n ge on a tropical mountain.Na tu re 398: 6 11 –6 1 5. Li eberman S. 1 9 94 .Can CITES Save the Box Tu rtle? Endangered Spec i es Pritch a rd PCH. 1 9 6 7. L iving Tu rtles of the World .Neptune (NJ): T F H Technical Bu lleti n .US Dep a rtment of the In teri or Fish and Wi l dl i fe Publ i c ati ons . Service . Federal Regi s ter 19 (5):1 5 – 1 7. Pritch ard PCH,T rebbau T.1 98 4 .The Tu rtles of Ven e z u el a .Soci ety for the Lips KR. 19 9 9. Mass mort a li ty and pop ul a ti on declines of a nurans at an Stu dy of Am ph i bians and Repti l e s, Con tri butions to Herpeto l ogy,Vo l. upland site in we stern Pan a m a . Con serva ti on Bi o l ogy 13: 11 7 –1 2 5. 2. Ox ford (OH):Miami Univers i ty. Losos JB,Ma rks JC, S choen er TW. 1 99 3 . Habitat use and ecol ogical inter- Reed JM,Bl au stein A R .1 9 95 . Ass e s s m ent of “n on decl i n i n g”a mph i bi an actions of an introdu ced and a native species of Anol i s li z a rd on Gra n d popu l a ti ons using power analysi s. Con s erva tion Bio l ogy 9: 1 2 9 9– 13 0 0. Cayma n , with a revi ew of the outcomes of anole introdu ction s . Rh odin A. 19 9 9. Cel ebra te the tu rt l e :Percepti on and pres ervati on . Paper O eco l ogia 95: 5 2 5– 5 32 . pres ented at Powdermi ll 1999, 4th Occa s i onal Fres hwa ter Tu rtle Con- Lovi ch JE.1 99 5 .Wi l dl i fe and weed s :L i fe in an alien landscape. News l et ter ference ; 13–16 Aug 1999; L a u gh l i n ,N V. of the Ca l ifornia Exo tic Pest Plant Council 3: 4 –5 . Ri ce KG, Perc ival HF,Woodw a rd AR ,Jen n i n gs ML. 1 9 9 9 .E f fects of egg and Lovi ch JE,G o t te SW,Ernst CH, Hars hb a r ger JC, L aem m erzahl A F,G i b- ha tchling harvest on American alli ga tors in Flori d a .Jo u rnal of Wi l dl i fe bons JW.1 9 96 .Preva l ence and histopa t h o l ogy of s h ell disease in tu rtle s Man a gem ent 63: 11 9 3– 12 0 0 . 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: Rodda GH.1 9 9 2. Loss of na tive reptiles assoc i a ted with introducti ons of 2 5 9– 26 5 . exo tics in the Ma riana Isl a n d s .Pacific Scien ce 46: 3 9 9– 40 0 . Ma rco M,Q u i l chano C,Bl au stein A R .19 9 9. Sens itivi ty to nitrate and Roman J, Sa n t huf f SD, Mol er PE ,Bowen BW.19 9 9. Popu la ti on structu re n i tri te in pon d - breeding amphi bians from the Pacific Nort hwe s t ,U S A . and cryptic evo luti on a ry units in the alli ga tor snapping turt l e . Con s er- Envi ron m ental Tox ico logy and Ch em is try 18: 2 83 6 – 2 83 9 . vati on Bi o l ogy 13: 1 3 5– 14 2 . Means DB,Palis JG,Baggett M.1 9 9 6 .E f fects of slash pine silvi c u l tu re on a Roo s en burg W M .1 9 9 1 .The diamon d b ack terra p i n :Popu la ti on dyn a m i c s, F l orida pop ul a ti on of fl a t woods salamander.Con s erva ti on Bio l ogy 10: h a bitat requ i rem en t s ,and opportu n i ties for con s erva ti on .Pa ge s 42 6 – 4 37 . 227–234 in Mi hu rsky JA, Ch an ey A ,ed s. New Perspectives in the Meffe GK, Ca rro ll CR. 1 9 94 .Principles of Con s erva tion Bio l ogy. Sun der- Che s a pe ake System :A Re s e a rch and Ma na gem ent Pa rtn ers h i p.Ba lti- land (MA):Si n a u er As s oci a te s . m ore (MD):Ch e s a pe ake Res e a rch Con s ortiu m . Mit term ei er RA ,Myers N,Gil PR, Mi t term ei er CG. 1 9 99 .Ho t s po t s :E a rt h’s Ross JP,ed .1 9 9 8 .Crocod i l e s :S t a tus Su rvey and Cons ervati on Action Plan. Bi o l ogi ca lly Richest and Most Endangered T erres trial Ecoregi on s . 2nd ed.
August 2000 / Vol. 50 No.8 BioScience665 Articles
Seml i t s ch RD.1 99 8 .Bi o l ogical del i ne a ti on of terres trial bu ffer zones for Thorn ton I.1 9 7 1. Da rwi n’ s Is l a n d s :A Na tu ral Hi s tory of the Galapagos . pon d - breeding salamanders. Cons ervati on Bio l ogy 12:1113–1119. G a rden Ci ty (NY): The Na tu ral Hi story Pre ss . Sem l i t s ch RD, Ryan TJ. 19 9 8. Migra ti on, am ph i bi a n .Pa ges 221–227 in Tinkle DW.1 97 9 .Lon g -term field stu d i es .Bi o S c i en ce 29: 7 17 . Kn obil E,Nei ll JD, ed s. The Encyclopedia of Reprodu cti on ,Vo l .3 .New Tu bervi lle TD, Bodie JR, Jen s en JB,L a Cl a i re LV,G i bbons JW.2 00 0 . Appa r- York :Ac ademic Pre ss . ent decline of the Sout h ern Hognose Sn ake (Heterodon simu s ). Jou rna l Se s s i ons SK, Fran s sen RA ,Horn er V L. 1 99 9 .Morph o l ogical clues from of Elisha Mi tch ell Scientific Soci ety 116(1): 1 9 – 4 0. mul ti l egged frogs :Are reti n oids to blame? Scien ce 284: 8 0 0– 80 2 . Tyl er MJ,Ca rter DB.1 9 8 1 .O ral bi rth of the young of the gas tric brood in g S h arma DSK.1 99 9 .Tortoise and Fre s hw a ter Turtle Trade and Util i s a ti on in frog Rh e oba tra chus silus .Animal Beh avi or 29: 2 8 0– 28 2 . Peni n sular Ma l ays ia .A TRAFFIC So utheast Asia Report .Petaling Jaya, [ F WS] US Fish and Wi l dli fe Servi ce .2 0 0 0 .Box score ,en d an gered spec i e s. Sel a n gor (Mal ays i a ) .
666 BioScience August 2000 / Vol. 50 No. 8