August 2000 Vol 50 No 8 BioScience 653

Articles

The Global Declineof Reptiles Deacutejagrave VuAmphibians J WHITFIELD GIBBONS DAVID E SCOTT T R AVIS J RYA N KURT AB U H L M A N N T R ACEY D TUBERV I L L E BRIAN S METTS JUDITH L GREENETONY MILLS YALE LEIDEN SEAN POPPY AND CHRISTOPHER T WINNE

A s a group [reptiles] are nei t h er lsquogood rsquon or lsquob ad rsquo 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 rdquo( Zim andSmith 1953 p 9 ) Fortu n a tely this op i n i on from the GoldenGu i de Series does not persist tod ay most people have com eto recogn i ze the va lue of both reptiles and amph i bians as ani n tegral part of n a tu ral eco s ys tems and as heralds ofenvi ron m ental qu a l i ty (Gibbons and Stangel 1999) Inrecent ye a rs as overa ll envi ron m ental aw a reness among thep u blic has incre a s ed con cerns have come to inclu de intere s tin the eco l ogical state of reptile and amph i bian spec i e st h em s elves and of t h eir habi t a t s In c re a s ed aw a reness mays tem from bet ter edu c a ti on abo ut threats to bi od ivers i ty ingen era l and to reptiles and amph i bians in parti c u l a r a n dpo 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 twovertebrate classes comprising reptiles and amphibianscollectively referred to as the herpetofauna are inter-changeable For examplethe Boy Scout merit badge pam-phlet for herpetology was called simply Reptile Study from1926 to 1993 (Conant 1972 Gibbons 1993) and majorzoos (eg National Zoo in Washington DC Zoo Atlantaand San Diego Zoo) use only the name ldquoreptilerdquo to refer tothe facility that houses both amphibians and reptilesThus public attitudes about the need for conservation ofreptiles are probably linked to concern about amphibiandeclines and deformities (Alford and Richards 1999 John-son et al 1999 Sessions et al 1999) which have been thesubject of numerous well-documented scientific studies

Because amphibians are distributed worldwide but her-petologists who document amphibian declines are not itis difficult to accurately assess what portion of amphibianpopulations are experiencing significant declines or havealready disappeared Furthermore the means of deter-mining a speciesrsquo conservation status is a rigorous andtime-intensive process and therefore counts of ldquoofficiallyrdquorecognized endangered and threatened species are likely togrossly underestimate the actual number of imperileds pecies (Ta ble 1) The worl dwi de amph i bian decl i n e

probl em as it has come to be known has garnered sig-nificant attention not only among scientists but also in thepopular media and in political circles

The reptile probl emDespite the fact that reptiles and amphibians are oftenconsidered collectively reptile declines deserve spotlight-ing and elucidating in their own right The differencesbetween the two groups are substantial Modern amphib-ians and reptiles are products of independent lineages thathave been separate for the past 300 million years (Pough etal 1998) Many of the differences between the groups areobvious and considerable For examplethe integument ofreptiles is covered with scales whereas amphibians have ahighly permeable glandular skina feature often touted asenhancing the environmental sensitivity of amphibians to

ldquo

J Whitfield Gibbons (e-mail gibbonssreledu) 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 Conservation 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

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 bysimple gelatinous membranes making the eggs more sus-ceptible to uptake of environmental contaminants (but seePechmann and Wilbur 1994) The differences betweenamphibians and reptiles are not limited to morphologyand reproductive biology they also include ecological andbehavioral traits Most amphibians rarely travel more thana few hundred meters over the course of their lives (Seml-itsch and Ryan 1998) many reptiles may move severalkilometers both terrestrially and aquatically and havehome ranges encompassing tens or hundreds of squarekilometers (Brown 1993) and individual sea turtles maycover half the globe annually (Ernst and Barbour 1989)

Nonetheless the similarities between the ectothermictetra pod s mdash a m ph i bians and reptilesmdashlink them inex-orably Species of both classes occupy similar habitats andare equally vulnerable to habitat degradation Thus syn-topic sp ecies o f amphibians and reptiles are correspond-ingly defenseless against the global threats of deforesta-tiondraining of wetlandsand pollution from agriculturalrunoff Although the amphibian decline problem is a seri-ous threat reptiles appear to be in even greater danger ofextinction worldwide (Table 1)

Population declines can be difficult to detect hencelong-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 sdoc 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 tofood shortages during extended drought conditions Onlythe smaller snakes survived suggesting that large snakesmay be relatively more susceptible to declines caused byfood shortagesGibbons (1990) reported a natural declinefor an isolated population of slider turtles (Trachemysscripta) on a coastal island The turtle population had nojuvenile recruitment presumably because of constant pre-dation on smaller individuals by alligators (Alligator mis -sissippiensis) that had become established on the islandonly large adult turtles survived Natural fluctuations andl ocal ex ti n cti ons are com m on in both reptiles andamphibians (Pechmann et al 1991 Blaustein et al 1994c)and generally are no cause for alarm However not alldeclines are natural

In this article we consider the vulnerability of reptileswithin the context of the factors known or suspected to beassociated with amphibian declines using the six cate-gories of concern established by Partners in Amphibianand Reptile Conservation (PARC Gibbons and Stangel1999) habitat loss and degradation introduced invasivespecies environmental pollution disease and parasitismunsustainable use and global climate change An addi-tional category comprises unexplained declines for bothreptiles and amphibians wherein the disappearance ofpopulations or a decline in numbers is a certainty but thecause is unknown Of course decline of a species mayoften be a cumulative effect of more than one of thepotential causesas proposed for the documented declinesof the Milos viper (Microvipera schweizeri) of Greece (Nil-son et al 1999) and the asp viper (Vipera aspis) of theSwiss Jura mountains (Moser et al 1984 Jaggi and Baur1999)

654 BioScience August 2000 Vol 50 No 8

Articles

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 enumber 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 eA 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 5Frogs and toads 4 1 0 0 9 5 1 1 6 6 0 5 3 8 5 0S a l a m a n d e rs 4 1 5 8 4 2 2 0 0 1 1 2 5C a e c i l i a n s 1 6 5 0 0 0 0 0 0 0 0R 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 3Tu rt l e s 2 6 0 3 3 4 2 5 4 9 6 6 3 8 5 8C r o c o d i l i a n s 2 2 1 5 3 1 6 8 0 0 7 3Tu a t a r a 2 2 0 2 0 0 0 0 1L i z a r d s 5 0 6 6 1 4 8 1 6 2 3 8 0 1 1 3 0 6 6S 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)dldquo Ex ti n ctrdquo refers to com p l ete taxon omic ex ti n cti on ra t h er than the IUCN category ldquoex ti n ct in wi l d rdquo ldquoen d a n gered rdquoi n clu des those species listed by IUCN

as ldquoc ri ti c a lly en d a n gered rdquo ldquo vu l n era bl erdquo 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 IUCNndashWorld Con s erva-ti on Un i on (2000)

Our account is not exhaustive rather we provide docu-m en ted examples of reptile pop u l a ti ons in peril anddecline The aggregate of examples of amphibians andreptiles indicates that the worldrsquos herpetofauna face stres-sors from both known and unknown origins that withoutremediationcan only lead to continuing declines extirpa-tions and extinctions

Di s tinguishing natu ral declines fro ma n t h ropogenic ones Amphibian declines are indisputably real and disquietingon a global scale Yet providing unequivocal supportingdocumentation for the decline of any particular popula-tion or species can be an onerous task and some expecta-tions of scientific rigor may be unable to be met (Pech-mann et al 1991) One persistent incertitude regardingamphibian declines is whether a decline is simply withinthe natural range of variability for a population or isinstead a consequence of anthropogenic causes that couldportend an unrecoverable situation

One difficulty in dem on s tra ting wh et h er ob s ervedtrends in esti m a ted pop u l a ti on sizes con s ti tute norm a lf lu ctu a ti ons or ldquou n n a tu ra l rdquo declines is that most fiel ds 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) ldquoSn a p s h o t srdquo( i e s h ort - term mon i toring) of pop u l a ti on size ands tru ctu re may dem on s tra te current status but do notreve a l l on g -term trends in population size or health Forexample Petranka et al (1993) who used short-termmonitoring and Ash (1997) who did long-term monitor-ing came to different conclusions regarding the effects ofclearcutting on recovery time of terrestrial salamanderpopulations To be surethe st rongest support for a decline

is a long-term data set that has registered population lev-els for particular species in par ticular locations Howeverthe accumulation of numerous accounts from shorter-term studies of a varie ty of amphibian sp ecies in diverse

habitats and geographic regions lends credence to pleasfor concern about declines

Studies of decline among reptiles like those conductedfor amphibianshave not always been carried out as rigor-ously as scientists would prefer Nonetheless the ever-increasing number of perceived declines among reptilesand the documentation of adverse impacts on individualsthat pre su m a bly can be proj ected into dem ogra ph i cchanges are harbingers of a crisis situationOur intent is toshow the phylogenetic and geographic breadth of per-ceived problems with many reptiles on the premise thatthey foreshadow a more intense and widespread problem

Ha bitat loss and degra d a ti o nMany scientists consider loss of suitable habitat to be thelargest 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 eregions of the United States retain less than 20 of thewetland acreage they once had (Leja 1998) and conse-quent declines in associated amphibian populations havebeen documented (Lannoo et al 1994) Numerous semi-aquatic reptiles rely on those very same wetlands In SouthCarolina the elimination or alteration of more than 90of Coastal Plain Carolina bay wetlands (Bennett and Nel-son 1991) has reduced essential habitat for black swampsnakes (Seminatrix pygaea) eastern green water snakes(Nerodia floridana)and chicken turtles (Deirochelys retic -ularia) all of whose distribution patterns are restrictedprimarily to seasonal wetlands (Buhlmann 1995 Dorcas etal 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 pol luted 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 surroundingterrestrial habitat needed by semiaquatic reptiles for nestshibernation sitesand other refugia is not (Burke and Gib-bons 1995)

August 2000 Vol 50 No 8 BioScience 655

Articles

Am eri c a ncro cod i l e Li ke manycro cod i l i a n s t h i ss pe cies hassu f f ered fro mco m m erci a loverexpl o i t a ti o nand habi t a td e s tru cti o n

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

Cu l tiva ted pine plantati ons in sout h e a s tern So ut hAfrica have been implicated in the endangerment of therare short-headed legless skink (Acontias breviceps) andthe disappearance of another lizard (Eastwoodrsquos long-tailed seps Tetradactylus eastwoodae Branch 1998) In theChiricahua mountains of southeastern Arizonathe elimi-nation of native bunchgrasses by cattle grazing was con-sidered to be the primary cause of a detectable decline inthe bu n ch grass lizard (S cel opo rus sc a l a ri s) wh i ch usebunchgrasses for cover from predators and for protectionfrom harsh winter conditions (Ballinger and Congdon1996) Habitat loss is the biggest problem in the decline ofsnakes in Australia (Shine 1991) The link between intacthabitat and species persistence and well-being is a basictenet of ecology and conservation biology (Meffe and Car-roll 1994 Mittermeier et al 1999) and needs no furtherdiscussion

The mere presence of humans may constitute an insid-ious form o f habitat degradation in some instances even

if the habitat itself remains intact Based on a 20-yearstudy a wood turtle (Clemmys insculpta) population ofmore than 130 animals in a forested watershed in NewHaven County Connecticut has been virtually eliminatedsince the area became open to the public (Garber andBurger 1995) The possible mechanisms of decline includ-ed removal road kill handling by recreationistsincreasednumber of predators attracted by food waste and distur-bance by dogs

In trodu ced inva s ive spe ci e sIntroduced species have been cited as a problem for manyamphibians (Stolzenburg 1999) For example the distrib-ution and abundance of several western US frog specieshave been severely reduced by non-native fishes and bull-frogs (Rana catesbeiana) which were and continue to beintroduced to wetland ldquoislandrdquohabitats of low- and high-elevation lakes (Fisher and Shaffer 1996) The collapse ofendemic reptile faunas on true islands after the introduc-tion of exotic species is similarly well documented andpervasivenon-native ratscatsand mongooses have extir-pated numerous lizard species on many islands (Case andBolger 1991) The tuatara (Sphenodon punctatus) a prim-itive reptilehistorically inhabited the two main islands ofNew Zealand and at least 40 of the offshore islands(Daugherty et al 1990) The tuatara became extinct on themain islands in the nineteenth century and on 10 offshoreislands within the last few decades and is experiencingpopulation declines on many of the other islands as aresult of introduced mammals primarily rats Feral pigs inthe Galapagos Islands first noted by Darwin in 1835 arejust one of the non-native species that have caused thenear extinction of the Galapagos tortoise (Geochelone ele -phantopus Thornton 1971) Introduced rats are suspectedto have destroyed both the eggs and young of the tortois-e s but the initial cause of decline was 18th-cen tu rymariners who stopped at the islands and stocked theirships with live tortoises as food f or the sailors (Pritchard1967)

Even the introduction of non-native reptiles can disruptindigenous reptile communities For example Losos et al(1993) showed that the invasion of Grand Cayman byexotic brown anoles (Anolis sagrei) caused behavioralchanges and shifts in habitat use by the native speciesAnolis conspersus Likewise the introduction of the browntree snake (Boiga irregularis) has been implicated in theex ti rp a ti on of the gecko (Na ctus pel a gi c u s) from theislands of Guam and Tinian the brown tree snake is alsoconsidered responsible for dramatic declines in otherspecies 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 native reptilesare not limited to islands In the continental United Statesi m ported fire ants (S ol en opsis invi ct a) i n trodu ced inMobile Alabama as early as 1918 (Wilson 1950) have

656 BioScience August 2000 Vol 50 No 8

Articles

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

been reported to prey on both eggs (Moulis 1997) andyoung (Allen et al1997) of reptilesFire ants are implicat-ed as a primary cause of extirpation of the Texas hornedlizard (Phrynosoma cornutum) from part of its geographicrange (Goin 1992)

Invasive species need not be other animals Both thedesert tortoise (Gopherus agassizii) and the gopher tortoiseare threatened by the introduction of non-native plantspecies (Stewart et al 1993 Lovich 1995) that alter habitatstructure native plant community composition and evenfire frequency The black legless lizard (Anniella pulchranigra) was considered for federal endangered status inpart because of the negative impact of non-native Hotten-tot fig plants on the lizardsrsquo prey base in disturbed sand-dune habitat (Rutherford and Rorabaugh 1995) nonethe-less an official decision was made not to list the speciesafter viable lizard populations were found in undisturbedhabitat with native vegetation (Morey 1998) In Idahoreptile sp ecies richness decreased an average o f 5 from1978 to 1998 at 24 sample sites in the Snake River Birds ofPrey Area (John Cossel Jr and Charles R Peterson IdahoState University Pocatello ID personal communication)According to Cossel and Peterson the changes in reptilepopulations may have been influenced by a decrease innative shrub habitat caused by the prevalence of exoticannual grasses and the effects of wildfires that have burnedover 50 of the area since the 1970s

Envi ro n m ental poll u ti o nNumerous environmental contaminantsmdashmetals pesti-cides and herbicidesand radioactive waste for examplemdashhave direct and indirect effects on both amphibians andreptiles (eg Hinton and Scott 1990 Hall and Henry1992) Amphibians have been the subject of numerousecotoxicological studiesincluding assessment of the directeffects of contaminants such as fertilizers (Marco et al1999) or the more subtle effects of steroid-mimicking con-taminants (Hayes 1997) Reptiles are studied far less thanamphibians with respect to the fate and effects of contam-inants (Hopkins et al 1999) but they have received suffi-cient toxicological study to provide convincing evidencethat some individual reptiles are adversely affected bymany contaminants (Hall 1980 Fontenot et al 1994) Forexampleslider turtles (Trachemys scripta) exposed to met-al and radioisotope contaminants incur genetic damage(Lamb et al 1995) The degree to which contaminantscause population-level effects remains largely unknownboth for amphibians and for reptiles

Contaminant effects in reptiles are known mainly fromturtles and crocodilians Many turtles and crocodiliansbecause they have environmental sex determination andlarge eggs that can incorporate high levels of environmen-tal pollutants are especially sensitive to endocrine-dis-rupting chemicals (Guillette and Crain 1996) At som econ 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 eggs (Bishop et al 1994 Cobb and Wood 1997) sexreversal and abnormal gonads have been found in turtlesexposed to PCBs (Bergeron et al 1994 Guillette et al1995) Male American alligators (Alligator mississippiensis)inhabiting Lake Apopka a chemically contaminated lakein Florida had significantly reduced plasma testosteronelevels and permanent gonadal alterations (Guillette et al1994)

Even nonlethal effects o f endocrine disrup ters on rep-tiles may result in demographic shifts whose consequencesfor populations are presumably detrimental Population-level effects might also occur through changes to patternsof individual energy allocation For example in coal-ashpolluted wetlands water snakes (Nerodia fasciata) withhigh body burdens of metal contaminants exhibit elevatedmetabolic rates which may result in less energy beingdevoted to reproduction growth and storage (Hopkins etal 1999)

Di sea se and pa ra s i ti s mParasites and disease have been documented or suspectedas causes for declines in some amphibian species (Daszaket al 1999) In some cases sublethal environmental stres-sors may suppress immune systems (Carey 1993) andallow disease agents to kill weakened animals (Alford andRichards 1999) Recently however a spreading ldquoextinctionwaverdquo of chytrid fungus is thought to be causing thedecline of anurans in Central America and Australia(Berger et al 1998 Lips 1999) moreover researchersbelieve that the fungus is killing otherwise healthy animals(Daszak et al 1999) An iridovirus may be the primarycause of the periodic population crashes in the Sonora

August 2000 Vol 50 No 8 BioScience 657

Articles

Ha bitat loss and degra d a tion are pri m a ry threats to bot ha m p h i bian and reptile popu l a ti o n s Co nversion ofwet 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 gterre s trial habitat to agri c u l tu ral (ill u s tra ted here) andot h er uses have re su l ted in wetland losses exceeding 80in many state s

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 nowbelieve that disease may rival habitat destruction as thelargest single cause o f the decline of amphibians

Among reptiles the widespread upper respiratory tractdisease a contagious respiratory ailment caused by thebacterium Mycoplasma agassizii is a potential cause ofpopulation declines in desert tortoises in the US South-west and gopher tortoises in the Southeast (Jacobson1993 Smith et al 1998)Shell diseases have been implicat-ed in the decline of turtles (eg shell lesions on slidersLovich et al 1996 cutaneous dyskeratosis affecting theshell and thickened forelimb scutes of desert tortoisesJacobson 1994 and emaciation and lesions of the plastronof federally listed flattened musk turtles Sternotherusdepressus Dodd 1988) Individuals in many green sea tur-tle populations are severely affected by viral fibropapillo-mas resulting in growths that can impair vision locomo-tionand feeding ability (Herbst 1994) As is often the casein amphibiansdiseases that are debilitating to wild popu-lations of reptiles are most likely secondary expressions inindividuals with impaired resistance caused by one ormore primary environmental stressors such as habitatdegradation invasive species or pollution

Un su s t a i n a ble useHuman use of animalsincluding reptiles and amphibiansis an integral part of many cultures Harvesting must bebi 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 andspecies are to persist (Pough et al 1998) Overcollectionfor food the pet trade and biological supply houses hasbeen suggested as having had an impact on some amphib-ian populations (Dodd 1997) In the United States note-worthy examples for amphibians occurred in the late1800s to early 1900s when commercial collectors harvest-ed for the frog legs market Hundreds of thousands of

red - l egged frogs (Rana auro ra drayto 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 frogsalthough itis 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 al1994) In Indiathe 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 illegallyeach 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 onsu 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 havebeen more perva s ive and severe than on amph i bians (eg s ee Wi lliams 1999) The severi ty of the tu rtle crisis on agl obal scale was em ph a s i zed by Rh odin (1999) wh oreported that of the approx i m a tely 293 taxa (mainlys 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 thelast few cen tu ri e s 3 (9 taxa) are alre ady ex ti n ct in thewi 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 foodsource Moreover the international trade in turtlesmdashwhich are eaten sold as pets or used in traditional Chi-nese medicinal remediesmdashis both extensive and unregu-lated (Sharma 1999) A recent report indicated that mostturtle sp ecies in Vietnam and southern China are endan-gered and that turtles can no longer be found in the wildin Vietnam (Kiester and Juvik 1997) China is the biggestconsumer of turtles in the food trade Because the trade inturtles is not regulated few records have been kept butexisting records indicate that the trade in live turtles toChina is thousands of tons per year (Mockenhaupt 1999)The commercial trade in freshwater turtles exceeds anypossible sustainable levels and extinction of some speciesin the wild can be expected within the next decade

Most species of sea turtles continue to decline in allwarm oceans of the world The leatherback sea turtle(Dermochelys coriacea) was recently reported to be ldquoon theroad to extinction and further population declines can beexpectedrdquounless appropriate measures are taken to reducemortality rates in adults hatchlings and eggs (Spotila eta l 1 9 9 6 ) The esti m a ted worl dwi de pop u l a ti on ofleatherbacks nesting on beaches in 1980 was 115000com p a red with just 34500 in 1995 Ex p l oi t a ti on ofleatherbacks in the Atlantic Ocean through illegal har-vesting of both adults and eggsis considered to be a majorcontributor to the decline of the species (Spotila et al1996) Likewise for Kemprsquos Ridley sea turtle (Lepidochelys

658 BioScience August 2000 Vol 50 No 8

Articles

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

kempii) harvests of nesting females and their eggs on thelargest known nesting site contributed to declines from42000 nesting females in 1947 to only a few hundred by1975 (Hildebrand 1982)

Among North American turtles the diamondback ter-rapin (Ma l a cl emys terra p i n) a small e s tu a rine tu rt l especies with a geographic range from Cape Cod to Texasdecl i n ed severely fo ll owing heavy ex p l oi t a ti on as agourmet food item from the late 1800s to the early 1900s(Carr 1952) With forced reductions in harvesting manypopulations were able to recover but the terrapin nowfaces significant new threats including highway mortality(Wood and Herlands 1997) and drowning in commercialand recreational crab traps (Bishop 1983 Roosenburg1991) Renewed commercial har vest of the diamondbackterrapin has also been documented (Garber 1988)

Commercial turtle trappers for the restaurant tradestepped up harvests of one of the largest freshwater turtlesin the world the alligator snapper (Macroclemys tem -minckii) from the 1960s through the 1980s (Roman et al1999) Consequently as evidence from survey efforts sug-gests the species has b een drastical ly reduced in numbersin some of the southeastern US rivers it once inhabited(Moler 1992 Jensen 1998)

The enormous and once common populations of thearrau (Podocnemis expansa) a communally nesting turtleof the Orinoco and Amazon Rivers in South America arenow greatly reduced in size because of human consump-tion of eggs and nesting females (Pritchard and Trebbau1984) an overexploitation problem identified almost twocenturies ago (Humboldt 1814 from Pritchard and Treb-bau 1984) Declines from similar causes have befallen theterecay (Podocnemis unifilis) in tropical lowlands of SouthAmerica (Thorbjarnarson et al 1993) and the river ter-rapin (Batagur baska) in India (Bhupathy 1997)

Overharvesting for food is a problem not just for turtlesbut also for lizardshaving contributed to declines in greeniguanas (Iguana iguana) and spiny - t a i l ed iguanas(Ctenosaura similis) in tropical America (Fitch et al1982)

The pet trade appears especially hazardous for someturtle sp ecies In 1994 population declines were reportedin box turtles (Terrapene carolina) in 16 states rangingfrom Massachusetts to Florida and Oklahoma to Wiscon-sin (Lieberman 1994) Doc u m en t a ti on of box tu rt l edecl i n e s mdash i n cluding records showing that s i n ce 199529896 box turtles had been collected for the pet trade andshipped from Louisianamdashresulted in unanimous passageof Act 81 by the Louisiana Senate and House of Represen-tatives in 1999the act prohibits the commercial harvest ofthe statersquos native box turtle populations Overcollection forexport is a serious factor in much of the box turtle declineand may exacerbate the effects of habitat loss (Lieberman1994) Habitat destruction and illegal collecting for the pettrade are the primary threats to bog turtles (Clemmysmuhlenbergii) Copeyon 1997) The number of northernpopulations has been reduced by 50 with most of the

decline occurring over the last 20 years Of the 191remaining bog turtle habitats known in 199633 were clas-sified as in good condition 67 as fair and 76 as poor thestatus of 15 was unknown

Overcollecting is also a problem for some snake speciesThe ocellated mountain viper (Vipera wagneri) in easternTurkey has been sought by the pet trade and removedfrom the wild in large numbers posing ldquoa serious threat tosurvival of the speciesrdquo (Nilson et al 1990) Populations ofseveral boa and python species have declined because ofharvesting of wild snakes for their skins (Pough et al1998) Rapid declines o f large-bodied snakes which tendto have a suite of life-history traits that make them moresusceptible to population declines than smaller species(eg Dodd 1993)have been documented throughout theworld in recent years (egShine and Fitzgerald 1996) Forexample females of the increasingly rare timber rat-tlesnake (Crotalus horridus) which may exceed a meter inlength and typically take 9 years to reach maturity pro-duce fewer than a dozen young every 3 years (Brown1993)Large-bodied species such as rattlesnakes (Crotalus)have long generation times a life-history t rait that whencom bi n ed with habitat loss human pers ec uti on a n di n ten s ive overco ll ecti on (eg ldquora t t l e s n a ke ro u n du p srdquo Brown 1993)has led to dramatic declines of some speciesand ma de approximately one-third of rattlesnake sp eciesvulnerable to extinction (Greene 1997) High harvest ratesof snakes with low reproductive frequencies such as thef 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 dalmost certainly be unsustainable (Shine et al 1995)

August 2000 Vol 50 No 8 BioScience 659

Articles

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

These examples demonstrate that sustainable use ofsome long-lived reptile species is problematic Becauselongevity in reptiles is associated with delayed sexualm a tu ri ty h i gh adult su rvivors h i p and low fec u n d i ty(Pough et al1998) populations of long-lived species can-not remain stable (or grow) when adults and older juve-niles are harvested at high rates (Congdon et al 19931994) This is not to say however that all such long-livedspecies should be commercially 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 (Ross1998) and unsustainable harvest of adults for the leathertrade (Brazaitis 1989) After years of total protection sev-eral sp ecies have recovered a f ew are farmed or ranchedcommercially (King 1989) In some crocodile speciesadult females are protected and only small numbers ofeggs small juveniles and larger males are removed fromthe wild (King 1989) In contrast 7ndash8 of all alligatorsmore than 12 m in length are harvested annually in someFlorida populations (David et al1996) In additiona 50annual harvest rate of alligator eggs or hatchlings isallowed because removal at these life stages does notreduce recruitment into adult-size classes (Rice et al1999) Closely monitored alligator populations and pre-sumably populations of other long-lived species of rep-tiles can sustain the legal regulated harvest of some pro-porti on of eggs h a tch l i n gs or adults with negl i gi bl eeffects

G l obal cl i m a te ch a n geFew ecologists will dispute the link between increases ingreenhouse gases and gl obal tem pera tu re Howeverwhether the current rate of climate change reflects naturalvariation or has an anthropogenic cause is hotly debatedFor the purposes of this article we accept the argumentthat the earth is undergoing unprecedented rapid climaticchange (Schneider and Root 1998) that includes alter-ations in climate variables such as temperature and rain-fall patterns storm severity and storm frequency If oneaccepts that human-induced climate change is occurring(eg Vinnikov et al1999)then the consequences for her-petofaunal diversity can be addressed

The obvious effects of climate change on biodiversityare mediated through changes in habitat For exampleglobal warming may further diminish prairie wetlandhabitat in the United States (Poiani and Johnson 1991)Future wetland acreage in the United States may be great-ly reduced under a variety of climate circulation models(Halpin 1997) and aquatic and semiaquatic species willsuffer declines as habitat disappears Although many habi-tats are ex pected to under go dra m a tic ch a n ge (eg Guertin et al1997Still et al 1999) predictions of specieshabitat shifts in response to global warming cannot be

based solely on analyses of climatendashspace changes becausespecies distributions are also a function of dispersal abili-ty and biotic interactions (Davis et al 1998) Existingnature reserves will be inadequate to preserve current bio-diversity because an already fragmented landscape willi 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 theirlimited dispersal abilities reptiles and amphibians areespecially vulnerable to rapid habitat changes and maysuffer many more extinctions than birds as a result of arapid rate of climate change (Schneider and Root 1998)

In discussions of observed amphibian declines littlemention has been made of climate change (Dodd 1997)with two notable exceptions First the famed golden toad(Bufo periglenes) extinction in Costa Rica may have b eencausedat 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 changepatterns of cloud formation and thereby the availability ofwater (Still et al 1999) Second Blaustein et al (1994a)have suggested that ultraviolet B (UVB) radiation hasadverse effects on some amphibians including reducedhatching success and decreased survival to metamorpho-sis However an increase in the level of UVB caused bydepletion of the ozone layer probably does not pose ani m m ed i a te threat to reptile eggs wh i ch are sel domexposed to UVB radiation

As with the amphibian studies few researchers havedirectly assessed effects of climate change on r eptiles It isnonetheless reasonable to expect that climate changescould re sult in con d i ti ons that el i m i n a te or severelyrestrict sp ecies with limited dist ributions (Schneider andRoot 1998) as has been suggested for some Australianlizards (Brereton et al1995) and crotaline snakes of NorthAmerica and the neotropics (Greene and Campbell 1993)Additional effects of warming on some reptiles based onem p i rical evi den ce with fre s hw a ter tu rt l e s i n clu deenhanced juvenile growth rates earlier ages at maturityand shifts in functional sex ratios (Frazer et al 1993)Global warming may have the greatest impact on thosereptiles (crocodilians and some turtles) that have temper-ature-dependent sex determination (Janzen 1994) where-by the sex ratio of the hatchlings is determined by nesttemperatures during incubation Unless shifts occur in thepivotal temperatures at which sex is determined or femalenest-site choices (ie shade versus sun) evolve to keeppace with rising temperatures altered sex ratios couldaffect population demographics and persistence

En i gm a tic decl i n e sFinally in addition to the many cases of declines that haves ome re a s on a bly unders tood causes s ome amph i bi a npopulations have declined and even gone extinct withoutany discernible causes One well-known example is thegastric 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 ofparental care in which the young develop in the safety ofthe motherrsquos stomach (Tyler and Carter 1981) the gastricbrooding frog ceased to be found in nature Disjunct pop-ulations of the g reen salamand er (Aneides aeneus ) in thes o ut h ern App a l achians have app a ren t ly decl i n ed butwithout similar declines in other portions of its range (JeffCorser USGS-BRD Twin Creeks Resource Center GSM-NP Gatlinburg TN personal communication)

Similar cases exist for reptiles For example no livingspecimen of the Round Island burrowing boa (Bolyeriamultocarinata) in the Indian Ocean has been seen since1975 (Bullock 1986) the species may have become extinctin recent decades (Greene 1997) Although all species ofreptiles native to North America in precolonial times per-sist in some regions the current ranges of many are but aremnant of the much larger areas formerly occupied Nat-ural populations of indigo snakes have not been found insome regions of their historic range in more than 40 years(Mount 1975 Conant and Collins 1998)and the species isldquodeclining in abundance and distribution throughout itsUS geographic rangerdquo (Hallam et al 1998) Likewises i gh ti n gs of the sout h ern hognose snake (Heterod o nsimus) 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 ) evenin 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 sRegrettably many amphibian populations and species thatare thought to be declining have not been monitored overlong 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 commoncharacteristic The subjects of these studies occur in highdensity either spatially (eg Jordanrsquos salamander Plethod -on jordanii Hairston 1987) or temporally (eg mole sala-manders Ambystoma talpoideum Pechmann et al 1991and natterjack toads Bufo calamita Banks et al 1994)

Many of the species that have become symbols for thedeclining amphibian phenomenon are seasonally activeanurans that arrive over restricted periods of time atbreeding sites where they congregate in greater densitiesthan at any other time of the year Researchers sit ready torecord their arrival and abundance and if the animals failto show up when expecteda problem is suspected if suchabsences are protracted then the change is presumablyreal (Blaustein et al 1994c) The phenology of theseamphibians permits detection of breeding activity there-fore determination of whether the absence of breedingadults is a short-term aberration or an indication of a realdecline becomes a matter of accumulating the data neces-sary to demonstrate a statistically significant trend (fordiscussion see Blaustein et al 1994c Pechmann andWilbur 1994 Reed and Blaustein 1995)

Among reptiles declines in sea turtles are perhaps the

best documented because like many amphibians theyengage in an annual reproductive event (in this caseoviposition) with a predictable site and time A few snakespecies in colder temperate regions are known to hiber-nate communally and numbers can be assessed upon

emergence (Parker and Brown 1973) But what of themajority of reptile species that do not congregate to breedor hibernate and do not occur in particularly high densi-ties F or example the r acer (Coluber const rictor) a com-mon North American snake is found in a wide variety ofterrestrial habitats Like most other ectotherms racers aremore active and therefore more commonly encounteredin the warmer months However aside from some regionswhere communal hibernation occurs (Parker and Brown1973) determining the abundance of racers is difficultbecause 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 howcould we take a census to know when and if racer popula-tions were declining at a substantial rate on a widespread

August 2000 Vol 50 No 8 BioScience 661

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

basis without mounting an intensive long-term samplingprogram The clandestine nature of many reptiles oftencombined with comparatively large home ranges lowpop u l a ti on den s i ti e s and ra reness of con grega ti on a lbehavior makes documenting population trends very dif-ficult As a result populations may wither with littlenoticeOnce an unmonitored species or population is rec-ognized as being unexpectedly depauperate or absent thecause of decline may be unknown and unknowable

Based on the accumulated evidence that many if notmost declines reported for amphibians are indeed realtheproper course for conservation initiatives is to assume theworst for all herpetofauna and therefore to implementabatement measures while gathering more data Althoughthe lack of long-term data often may preclude the id enti-fication of the cause of a decline or even in some cases thecorroboration o f a decline the absence of that data doesnot rule out the existence of a correctable problem

Co n clusion and re co m m en d a ti o n sThe declines of m a ny reptile pop u l a ti ons are similar tothose 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 ha m ph i bi a n s the causes are known with cert a i n ty ins ome instance s su s pected in many and unknown ino t h ers Some ex ti rp a ti ons are local wh ereas others arem ore wi de s pre ad The difficulty in doc u m en ting thes 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 causesof pop u l a ti on declines can be obvi a ted direct ly Th ei 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 ingeneral (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 ofinvasive non-native species that could be harmful to rep-tile populations must be proscribed Third restrictingtrade in sensitive reptile species for which sustainableremoval cannot be demonstrated will require the passageor strengthening and enforcement of legislation In thecase of Asian turtles legislative remedies could be too lit-tle too latemdasha stopgap remedy is necessary The only wayto prevent the imminent extinction of a large number ofthe more than 80 species of turtles native to southern Asiawill be to maintain populations in ex situ captive breedingand genetic reserve programs With changes in culturalattitudesstrengthening of international trade regulationsand increased habitat protection the reintroduction ofthese species into the wild may be possible

Much of todayrsquos commercial exploitation of reptiles inthe United States and elsewhere requires urgent govern-mental action to implement internationally accepted andenforced controls Despite the fact that conservation mea-sures can be implemented effectively through legislation(as happened with legislation for protection of Louisianabox turtles and American alligators) the political pres-sures against accomplishing such goals cannot be overstat-ed The lack of support by the World Trade Organizationfor recommendations to curtail sea turtle exploitation(WTO 1998) brings the problem into perspective on aninternational scale

Direct and indirect effects of environmental pol lutiondisease and parasitism and global climate change aremore difficult to quantify in many instances and will bemore difficult to change in the short term Nonetheless wemust endeavor to understand these potential factors toameliorate their impact on natural populations of reptilesand their habitats

Finally long-term monitoring o f reptile populations isessential and must be aided by the establishment of stan-dard methods and techniques It is equally important thatthe academic community land managers and conserva-tion organizations recognize that rigorous field programsfocusing on the distri buti on a bu n d a n ce s t a tu s a n dtrends of populations and species are critical and worth-while Herpetofaunal inventories should become a stan-dard part of environmental assessment programs and thepublication of field survey efforts that document potentialor suspected declines should be encouraged When long-term and widespread monitoring becomes the normdeclines are likely to become less equivocal (in terms ofprotracted declines versus natural fluctuations) and thecauses less mysterious

662 BioScience August 2000 Vol 50 No 8

Articles

Sand monitor (Va ra nus go u l d i ) Al t h ou gh sandm o n i to rs (genus Va ra nu s wh i ch includes the wo rl d rsquo sl a rgest lizards) appear to be thriving in many pa rts oft h eir natu ral habitats in Au s tra l i a ot h er spe cies of t h egenus in As i a Afri c a and the East Indies are threa ten e dby exten s ive habitat destru cti o n

The disappearance of reptiles from the natural world isgenuine and should be a matter of concern not simplybecause of reptilesrsquo perceived associations with amphib-ians but because reptile declineslike those of amphibiansare growing and serious in their own right Current evi-dence suggests that amphibian and reptile declines whichare exacerbated by burgeoning human populations con-stitute a worldwide crisis

Ack n owl e d gm en t sManuscript preparation was aided by Financial AssistanceAw a rd Nu m ber DE-FC09-96SR18546 from the USDep a rtm ent of E n er gy to the Un ivers i ty of G eor gi aResearch Foundation We thank Ab Abercrombie JustinCongdon William Hopkins Laura Janecek ChristopherRomanek and Joseph Pechmann for discussion and com-ments on the manuscript We also appreciate the help ofStephen H Bennett John Cossel Jr Charles R PetersonPaul Moler Woody Woodwardand Jeff Corser for provid-ing information on the status of particular species Thispaper supports the PARC (Partners in Amphibian andReptile Conservation) effort to promote education aboutreptiles and amphibians

Ref eren ces ci te dAl 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 ndash 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 ndash 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 119 8 3 ndash 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 ndash 6 9

Banks B Beebee TJC Coo ke KS 1 9 9 4 Con s erva ti on of the natter jack toadB u fo calamita in Britain over the peri od 1976ndash1990 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 ndash 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 eRe 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 eUn i ted States of Am erica 95 9 0 3 1 ndash 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 ndash 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 rba 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 ndash 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 ofE nvi ron m ental Con t a m i n a ti on Tox i co l ogy 27 8 2 ndash 8 7

Bi s h op JM1 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 ndash 4 3 0

Bl a u s tein A R Hoffman PD Hokit DG Ki e s ecker JM Wa lls SC Hays JB1 9 9 4 a UV repair and re s i s t a n ce to solar UV-B in amph i bian eggs Alink to pop u l a ti on declines Proceed i n gs of the Na ti onal Ac ademy ofS c i en ce of the Un i ted States of Am erica 91 1 7 9 1 ndash 1 7 9 5

Bl a u s tein A R Hokit DG Orsquo Ha ra RK Holt RA 1 9 9 4 b Pa t h ogenic funguscon tri butes to amph i bian losses in the Pacific Nort hwe s t Bi o l ogi c a lCon s erva ti on 67 2 5 1 ndash 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 gs 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 andgl obal ex ti n cti on s Con s erva ti on Bi o l ogy 8 6 0 ndash 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 196ndash201 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 tech 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 ndash 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 theS tu dy of Am ph i bians and Repti l e s Herpeto l ogy Ci rc u l a ti on 22 1 ndash 7 2

Buhlmann KA 1 9 9 5 Ha bitat use terre s trial movem ents and con s erva ti onof 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 ogy2 9 1 7 3 ndash 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 201ndash232 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 amp 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 dIsland and Gu n n er rsquos Quoi n Ma u ri tiu s Bi o l ogical Con s erva ti on 371 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 ndash 1 3 6 9

Ca rey C 1 9 9 3 Hypothesis con cerning the causes of the disappe a ra n ce ofboreal toads from the mountains of Co l orado Con s erva ti on Bi o l ogy 73 5 5 ndash 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 52 7 2 ndash 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 peRomain Na ti onal Wi l dl i fe Ref u ge Ch em o s ph ere 34 5 3 9 ndash 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 1ndash15 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 lm a tu ri ty and dem ogra phics of Bl a n d i n grsquos tu rtles (Emyd o i d e abl 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 ndash 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 ivedor ga n i s m s Am erican Zoo l ogist 34 3 9 7 ndash 4 0 8

[CITES] Conven ti on on In tern a ti onal Trade in Endangered Species ofWild Fauna and Flora 2 0 0 0 lt 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 tmlgt (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 lrule to list the nort h ern pop u l a ti on of the bog tu rtle as thre a ten ed andthe 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 ndash 5 9 6 2 3

August 2000 Vol 50 No 8 BioScience 663

Articles

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 bysimple gelatinous membranes making the eggs more sus-ceptible to uptake of environmental contaminants (but seePechmann and Wilbur 1994) The differences betweenamphibians and reptiles are not limited to morphologyand reproductive biology they also include ecological andbehavioral traits Most amphibians rarely travel more thana few hundred meters over the course of their lives (Seml-itsch and Ryan 1998) many reptiles may move severalkilometers both terrestrially and aquatically and havehome ranges encompassing tens or hundreds of squarekilometers (Brown 1993) and individual sea turtles maycover half the globe annually (Ernst and Barbour 1989)

Nonetheless the similarities between the ectothermictetra pod s mdash a m ph i bians and reptilesmdashlink them inex-orably Species of both classes occupy similar habitats andare equally vulnerable to habitat degradation Thus syn-topic sp ecies o f amphibians and reptiles are correspond-ingly defenseless against the global threats of deforesta-tiondraining of wetlandsand pollution from agriculturalrunoff Although the amphibian decline problem is a seri-ous threat reptiles appear to be in even greater danger ofextinction worldwide (Table 1)

Population declines can be difficult to detect hencelong-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 sdoc 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 tofood shortages during extended drought conditions Onlythe smaller snakes survived suggesting that large snakesmay be relatively more susceptible to declines caused byfood shortagesGibbons (1990) reported a natural declinefor an isolated population of slider turtles (Trachemysscripta) on a coastal island The turtle population had nojuvenile recruitment presumably because of constant pre-dation on smaller individuals by alligators (Alligator mis -sissippiensis) that had become established on the islandonly large adult turtles survived Natural fluctuations andl ocal ex ti n cti ons are com m on in both reptiles andamphibians (Pechmann et al 1991 Blaustein et al 1994c)and generally are no cause for alarm However not alldeclines are natural

In this article we consider the vulnerability of reptileswithin the context of the factors known or suspected to beassociated with amphibian declines using the six cate-gories of concern established by Partners in Amphibianand Reptile Conservation (PARC Gibbons and Stangel1999) habitat loss and degradation introduced invasivespecies environmental pollution disease and parasitismunsustainable use and global climate change An addi-tional category comprises unexplained declines for bothreptiles and amphibians wherein the disappearance ofpopulations or a decline in numbers is a certainty but thecause is unknown Of course decline of a species mayoften be a cumulative effect of more than one of thepotential causesas proposed for the documented declinesof the Milos viper (Microvipera schweizeri) of Greece (Nil-son et al 1999) and the asp viper (Vipera aspis) of theSwiss Jura mountains (Moser et al 1984 Jaggi and Baur1999)

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Articles

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 enumber 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 eA 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 5Frogs and toads 4 1 0 0 9 5 1 1 6 6 0 5 3 8 5 0S a l a m a n d e rs 4 1 5 8 4 2 2 0 0 1 1 2 5C a e c i l i a n s 1 6 5 0 0 0 0 0 0 0 0R 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 3Tu rt l e s 2 6 0 3 3 4 2 5 4 9 6 6 3 8 5 8C r o c o d i l i a n s 2 2 1 5 3 1 6 8 0 0 7 3Tu a t a r a 2 2 0 2 0 0 0 0 1L i z a r d s 5 0 6 6 1 4 8 1 6 2 3 8 0 1 1 3 0 6 6S 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)dldquo Ex ti n ctrdquo refers to com p l ete taxon omic ex ti n cti on ra t h er than the IUCN category ldquoex ti n ct in wi l d rdquo ldquoen d a n gered rdquoi n clu des those species listed by IUCN

as ldquoc ri ti c a lly en d a n gered rdquo ldquo vu l n era bl erdquo 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 IUCNndashWorld Con s erva-ti on Un i on (2000)

Our account is not exhaustive rather we provide docu-m en ted examples of reptile pop u l a ti ons in peril anddecline The aggregate of examples of amphibians andreptiles indicates that the worldrsquos herpetofauna face stres-sors from both known and unknown origins that withoutremediationcan only lead to continuing declines extirpa-tions and extinctions

Di s tinguishing natu ral declines fro ma n t h ropogenic ones Amphibian declines are indisputably real and disquietingon a global scale Yet providing unequivocal supportingdocumentation for the decline of any particular popula-tion or species can be an onerous task and some expecta-tions of scientific rigor may be unable to be met (Pech-mann et al 1991) One persistent incertitude regardingamphibian declines is whether a decline is simply withinthe natural range of variability for a population or isinstead a consequence of anthropogenic causes that couldportend an unrecoverable situation

One difficulty in dem on s tra ting wh et h er ob s ervedtrends in esti m a ted pop u l a ti on sizes con s ti tute norm a lf lu ctu a ti ons or ldquou n n a tu ra l rdquo declines is that most fiel ds 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) ldquoSn a p s h o t srdquo( i e s h ort - term mon i toring) of pop u l a ti on size ands tru ctu re may dem on s tra te current status but do notreve a l l on g -term trends in population size or health Forexample Petranka et al (1993) who used short-termmonitoring and Ash (1997) who did long-term monitor-ing came to different conclusions regarding the effects ofclearcutting on recovery time of terrestrial salamanderpopulations To be surethe st rongest support for a decline

is a long-term data set that has registered population lev-els for particular species in par ticular locations Howeverthe accumulation of numerous accounts from shorter-term studies of a varie ty of amphibian sp ecies in diverse

habitats and geographic regions lends credence to pleasfor concern about declines

Studies of decline among reptiles like those conductedfor amphibianshave not always been carried out as rigor-ously as scientists would prefer Nonetheless the ever-increasing number of perceived declines among reptilesand the documentation of adverse impacts on individualsthat pre su m a bly can be proj ected into dem ogra ph i cchanges are harbingers of a crisis situationOur intent is toshow the phylogenetic and geographic breadth of per-ceived problems with many reptiles on the premise thatthey foreshadow a more intense and widespread problem

Ha bitat loss and degra d a ti o nMany scientists consider loss of suitable habitat to be thelargest 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 eregions of the United States retain less than 20 of thewetland acreage they once had (Leja 1998) and conse-quent declines in associated amphibian populations havebeen documented (Lannoo et al 1994) Numerous semi-aquatic reptiles rely on those very same wetlands In SouthCarolina the elimination or alteration of more than 90of Coastal Plain Carolina bay wetlands (Bennett and Nel-son 1991) has reduced essential habitat for black swampsnakes (Seminatrix pygaea) eastern green water snakes(Nerodia floridana)and chicken turtles (Deirochelys retic -ularia) all of whose distribution patterns are restrictedprimarily to seasonal wetlands (Buhlmann 1995 Dorcas etal 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 pol luted 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 surroundingterrestrial habitat needed by semiaquatic reptiles for nestshibernation sitesand other refugia is not (Burke and Gib-bons 1995)

August 2000 Vol 50 No 8 BioScience 655

Articles

Am eri c a ncro cod i l e Li ke manycro cod i l i a n s t h i ss pe cies hassu f f ered fro mco m m erci a loverexpl o i t a ti o nand habi t a td e s tru cti o n

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

Cu l tiva ted pine plantati ons in sout h e a s tern So ut hAfrica have been implicated in the endangerment of therare short-headed legless skink (Acontias breviceps) andthe disappearance of another lizard (Eastwoodrsquos long-tailed seps Tetradactylus eastwoodae Branch 1998) In theChiricahua mountains of southeastern Arizonathe elimi-nation of native bunchgrasses by cattle grazing was con-sidered to be the primary cause of a detectable decline inthe bu n ch grass lizard (S cel opo rus sc a l a ri s) wh i ch usebunchgrasses for cover from predators and for protectionfrom harsh winter conditions (Ballinger and Congdon1996) Habitat loss is the biggest problem in the decline ofsnakes in Australia (Shine 1991) The link between intacthabitat and species persistence and well-being is a basictenet of ecology and conservation biology (Meffe and Car-roll 1994 Mittermeier et al 1999) and needs no furtherdiscussion

The mere presence of humans may constitute an insid-ious form o f habitat degradation in some instances even

if the habitat itself remains intact Based on a 20-yearstudy a wood turtle (Clemmys insculpta) population ofmore than 130 animals in a forested watershed in NewHaven County Connecticut has been virtually eliminatedsince the area became open to the public (Garber andBurger 1995) The possible mechanisms of decline includ-ed removal road kill handling by recreationistsincreasednumber of predators attracted by food waste and distur-bance by dogs

In trodu ced inva s ive spe ci e sIntroduced species have been cited as a problem for manyamphibians (Stolzenburg 1999) For example the distrib-ution and abundance of several western US frog specieshave been severely reduced by non-native fishes and bull-frogs (Rana catesbeiana) which were and continue to beintroduced to wetland ldquoislandrdquohabitats of low- and high-elevation lakes (Fisher and Shaffer 1996) The collapse ofendemic reptile faunas on true islands after the introduc-tion of exotic species is similarly well documented andpervasivenon-native ratscatsand mongooses have extir-pated numerous lizard species on many islands (Case andBolger 1991) The tuatara (Sphenodon punctatus) a prim-itive reptilehistorically inhabited the two main islands ofNew Zealand and at least 40 of the offshore islands(Daugherty et al 1990) The tuatara became extinct on themain islands in the nineteenth century and on 10 offshoreislands within the last few decades and is experiencingpopulation declines on many of the other islands as aresult of introduced mammals primarily rats Feral pigs inthe Galapagos Islands first noted by Darwin in 1835 arejust one of the non-native species that have caused thenear extinction of the Galapagos tortoise (Geochelone ele -phantopus Thornton 1971) Introduced rats are suspectedto have destroyed both the eggs and young of the tortois-e s but the initial cause of decline was 18th-cen tu rymariners who stopped at the islands and stocked theirships with live tortoises as food f or the sailors (Pritchard1967)

Even the introduction of non-native reptiles can disruptindigenous reptile communities For example Losos et al(1993) showed that the invasion of Grand Cayman byexotic brown anoles (Anolis sagrei) caused behavioralchanges and shifts in habitat use by the native speciesAnolis conspersus Likewise the introduction of the browntree snake (Boiga irregularis) has been implicated in theex ti rp a ti on of the gecko (Na ctus pel a gi c u s) from theislands of Guam and Tinian the brown tree snake is alsoconsidered responsible for dramatic declines in otherspecies 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 native reptilesare not limited to islands In the continental United Statesi m ported fire ants (S ol en opsis invi ct a) i n trodu ced inMobile Alabama as early as 1918 (Wilson 1950) have

656 BioScience August 2000 Vol 50 No 8

Articles

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

been reported to prey on both eggs (Moulis 1997) andyoung (Allen et al1997) of reptilesFire ants are implicat-ed as a primary cause of extirpation of the Texas hornedlizard (Phrynosoma cornutum) from part of its geographicrange (Goin 1992)

Invasive species need not be other animals Both thedesert tortoise (Gopherus agassizii) and the gopher tortoiseare threatened by the introduction of non-native plantspecies (Stewart et al 1993 Lovich 1995) that alter habitatstructure native plant community composition and evenfire frequency The black legless lizard (Anniella pulchranigra) was considered for federal endangered status inpart because of the negative impact of non-native Hotten-tot fig plants on the lizardsrsquo prey base in disturbed sand-dune habitat (Rutherford and Rorabaugh 1995) nonethe-less an official decision was made not to list the speciesafter viable lizard populations were found in undisturbedhabitat with native vegetation (Morey 1998) In Idahoreptile sp ecies richness decreased an average o f 5 from1978 to 1998 at 24 sample sites in the Snake River Birds ofPrey Area (John Cossel Jr and Charles R Peterson IdahoState University Pocatello ID personal communication)According to Cossel and Peterson the changes in reptilepopulations may have been influenced by a decrease innative shrub habitat caused by the prevalence of exoticannual grasses and the effects of wildfires that have burnedover 50 of the area since the 1970s

Envi ro n m ental poll u ti o nNumerous environmental contaminantsmdashmetals pesti-cides and herbicidesand radioactive waste for examplemdashhave direct and indirect effects on both amphibians andreptiles (eg Hinton and Scott 1990 Hall and Henry1992) Amphibians have been the subject of numerousecotoxicological studiesincluding assessment of the directeffects of contaminants such as fertilizers (Marco et al1999) or the more subtle effects of steroid-mimicking con-taminants (Hayes 1997) Reptiles are studied far less thanamphibians with respect to the fate and effects of contam-inants (Hopkins et al 1999) but they have received suffi-cient toxicological study to provide convincing evidencethat some individual reptiles are adversely affected bymany contaminants (Hall 1980 Fontenot et al 1994) Forexampleslider turtles (Trachemys scripta) exposed to met-al and radioisotope contaminants incur genetic damage(Lamb et al 1995) The degree to which contaminantscause population-level effects remains largely unknownboth for amphibians and for reptiles

Contaminant effects in reptiles are known mainly fromturtles and crocodilians Many turtles and crocodiliansbecause they have environmental sex determination andlarge eggs that can incorporate high levels of environmen-tal pollutants are especially sensitive to endocrine-dis-rupting chemicals (Guillette and Crain 1996) At som econ 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 eggs (Bishop et al 1994 Cobb and Wood 1997) sexreversal and abnormal gonads have been found in turtlesexposed to PCBs (Bergeron et al 1994 Guillette et al1995) Male American alligators (Alligator mississippiensis)inhabiting Lake Apopka a chemically contaminated lakein Florida had significantly reduced plasma testosteronelevels and permanent gonadal alterations (Guillette et al1994)

Even nonlethal effects o f endocrine disrup ters on rep-tiles may result in demographic shifts whose consequencesfor populations are presumably detrimental Population-level effects might also occur through changes to patternsof individual energy allocation For example in coal-ashpolluted wetlands water snakes (Nerodia fasciata) withhigh body burdens of metal contaminants exhibit elevatedmetabolic rates which may result in less energy beingdevoted to reproduction growth and storage (Hopkins etal 1999)

Di sea se and pa ra s i ti s mParasites and disease have been documented or suspectedas causes for declines in some amphibian species (Daszaket al 1999) In some cases sublethal environmental stres-sors may suppress immune systems (Carey 1993) andallow disease agents to kill weakened animals (Alford andRichards 1999) Recently however a spreading ldquoextinctionwaverdquo of chytrid fungus is thought to be causing thedecline of anurans in Central America and Australia(Berger et al 1998 Lips 1999) moreover researchersbelieve that the fungus is killing otherwise healthy animals(Daszak et al 1999) An iridovirus may be the primarycause of the periodic population crashes in the Sonora

August 2000 Vol 50 No 8 BioScience 657

Articles

Ha bitat loss and degra d a tion are pri m a ry threats to bot ha m p h i bian and reptile popu l a ti o n s Co nversion ofwet 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 gterre s trial habitat to agri c u l tu ral (ill u s tra ted here) andot h er uses have re su l ted in wetland losses exceeding 80in many state s

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 nowbelieve that disease may rival habitat destruction as thelargest single cause o f the decline of amphibians

Among reptiles the widespread upper respiratory tractdisease a contagious respiratory ailment caused by thebacterium Mycoplasma agassizii is a potential cause ofpopulation declines in desert tortoises in the US South-west and gopher tortoises in the Southeast (Jacobson1993 Smith et al 1998)Shell diseases have been implicat-ed in the decline of turtles (eg shell lesions on slidersLovich et al 1996 cutaneous dyskeratosis affecting theshell and thickened forelimb scutes of desert tortoisesJacobson 1994 and emaciation and lesions of the plastronof federally listed flattened musk turtles Sternotherusdepressus Dodd 1988) Individuals in many green sea tur-tle populations are severely affected by viral fibropapillo-mas resulting in growths that can impair vision locomo-tionand feeding ability (Herbst 1994) As is often the casein amphibiansdiseases that are debilitating to wild popu-lations of reptiles are most likely secondary expressions inindividuals with impaired resistance caused by one ormore primary environmental stressors such as habitatdegradation invasive species or pollution

Un su s t a i n a ble useHuman use of animalsincluding reptiles and amphibiansis an integral part of many cultures Harvesting must bebi 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 andspecies are to persist (Pough et al 1998) Overcollectionfor food the pet trade and biological supply houses hasbeen suggested as having had an impact on some amphib-ian populations (Dodd 1997) In the United States note-worthy examples for amphibians occurred in the late1800s to early 1900s when commercial collectors harvest-ed for the frog legs market Hundreds of thousands of

red - l egged frogs (Rana auro ra drayto 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 frogsalthough itis 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 al1994) In Indiathe 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 illegallyeach 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 onsu 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 havebeen more perva s ive and severe than on amph i bians (eg s ee Wi lliams 1999) The severi ty of the tu rtle crisis on agl obal scale was em ph a s i zed by Rh odin (1999) wh oreported that of the approx i m a tely 293 taxa (mainlys 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 thelast few cen tu ri e s 3 (9 taxa) are alre ady ex ti n ct in thewi 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 foodsource Moreover the international trade in turtlesmdashwhich are eaten sold as pets or used in traditional Chi-nese medicinal remediesmdashis both extensive and unregu-lated (Sharma 1999) A recent report indicated that mostturtle sp ecies in Vietnam and southern China are endan-gered and that turtles can no longer be found in the wildin Vietnam (Kiester and Juvik 1997) China is the biggestconsumer of turtles in the food trade Because the trade inturtles is not regulated few records have been kept butexisting records indicate that the trade in live turtles toChina is thousands of tons per year (Mockenhaupt 1999)The commercial trade in freshwater turtles exceeds anypossible sustainable levels and extinction of some speciesin the wild can be expected within the next decade

Most species of sea turtles continue to decline in allwarm oceans of the world The leatherback sea turtle(Dermochelys coriacea) was recently reported to be ldquoon theroad to extinction and further population declines can beexpectedrdquounless appropriate measures are taken to reducemortality rates in adults hatchlings and eggs (Spotila eta l 1 9 9 6 ) The esti m a ted worl dwi de pop u l a ti on ofleatherbacks nesting on beaches in 1980 was 115000com p a red with just 34500 in 1995 Ex p l oi t a ti on ofleatherbacks in the Atlantic Ocean through illegal har-vesting of both adults and eggsis considered to be a majorcontributor to the decline of the species (Spotila et al1996) Likewise for Kemprsquos Ridley sea turtle (Lepidochelys

658 BioScience August 2000 Vol 50 No 8

Articles

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

kempii) harvests of nesting females and their eggs on thelargest known nesting site contributed to declines from42000 nesting females in 1947 to only a few hundred by1975 (Hildebrand 1982)

Among North American turtles the diamondback ter-rapin (Ma l a cl emys terra p i n) a small e s tu a rine tu rt l especies with a geographic range from Cape Cod to Texasdecl i n ed severely fo ll owing heavy ex p l oi t a ti on as agourmet food item from the late 1800s to the early 1900s(Carr 1952) With forced reductions in harvesting manypopulations were able to recover but the terrapin nowfaces significant new threats including highway mortality(Wood and Herlands 1997) and drowning in commercialand recreational crab traps (Bishop 1983 Roosenburg1991) Renewed commercial har vest of the diamondbackterrapin has also been documented (Garber 1988)

Commercial turtle trappers for the restaurant tradestepped up harvests of one of the largest freshwater turtlesin the world the alligator snapper (Macroclemys tem -minckii) from the 1960s through the 1980s (Roman et al1999) Consequently as evidence from survey efforts sug-gests the species has b een drastical ly reduced in numbersin some of the southeastern US rivers it once inhabited(Moler 1992 Jensen 1998)

The enormous and once common populations of thearrau (Podocnemis expansa) a communally nesting turtleof the Orinoco and Amazon Rivers in South America arenow greatly reduced in size because of human consump-tion of eggs and nesting females (Pritchard and Trebbau1984) an overexploitation problem identified almost twocenturies ago (Humboldt 1814 from Pritchard and Treb-bau 1984) Declines from similar causes have befallen theterecay (Podocnemis unifilis) in tropical lowlands of SouthAmerica (Thorbjarnarson et al 1993) and the river ter-rapin (Batagur baska) in India (Bhupathy 1997)

Overharvesting for food is a problem not just for turtlesbut also for lizardshaving contributed to declines in greeniguanas (Iguana iguana) and spiny - t a i l ed iguanas(Ctenosaura similis) in tropical America (Fitch et al1982)

The pet trade appears especially hazardous for someturtle sp ecies In 1994 population declines were reportedin box turtles (Terrapene carolina) in 16 states rangingfrom Massachusetts to Florida and Oklahoma to Wiscon-sin (Lieberman 1994) Doc u m en t a ti on of box tu rt l edecl i n e s mdash i n cluding records showing that s i n ce 199529896 box turtles had been collected for the pet trade andshipped from Louisianamdashresulted in unanimous passageof Act 81 by the Louisiana Senate and House of Represen-tatives in 1999the act prohibits the commercial harvest ofthe statersquos native box turtle populations Overcollection forexport is a serious factor in much of the box turtle declineand may exacerbate the effects of habitat loss (Lieberman1994) Habitat destruction and illegal collecting for the pettrade are the primary threats to bog turtles (Clemmysmuhlenbergii) Copeyon 1997) The number of northernpopulations has been reduced by 50 with most of the

decline occurring over the last 20 years Of the 191remaining bog turtle habitats known in 199633 were clas-sified as in good condition 67 as fair and 76 as poor thestatus of 15 was unknown

Overcollecting is also a problem for some snake speciesThe ocellated mountain viper (Vipera wagneri) in easternTurkey has been sought by the pet trade and removedfrom the wild in large numbers posing ldquoa serious threat tosurvival of the speciesrdquo (Nilson et al 1990) Populations ofseveral boa and python species have declined because ofharvesting of wild snakes for their skins (Pough et al1998) Rapid declines o f large-bodied snakes which tendto have a suite of life-history traits that make them moresusceptible to population declines than smaller species(eg Dodd 1993)have been documented throughout theworld in recent years (egShine and Fitzgerald 1996) Forexample females of the increasingly rare timber rat-tlesnake (Crotalus horridus) which may exceed a meter inlength and typically take 9 years to reach maturity pro-duce fewer than a dozen young every 3 years (Brown1993)Large-bodied species such as rattlesnakes (Crotalus)have long generation times a life-history t rait that whencom bi n ed with habitat loss human pers ec uti on a n di n ten s ive overco ll ecti on (eg ldquora t t l e s n a ke ro u n du p srdquo Brown 1993)has led to dramatic declines of some speciesand ma de approximately one-third of rattlesnake sp eciesvulnerable to extinction (Greene 1997) High harvest ratesof snakes with low reproductive frequencies such as thef 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 dalmost certainly be unsustainable (Shine et al 1995)

August 2000 Vol 50 No 8 BioScience 659

Articles

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

These examples demonstrate that sustainable use ofsome long-lived reptile species is problematic Becauselongevity in reptiles is associated with delayed sexualm a tu ri ty h i gh adult su rvivors h i p and low fec u n d i ty(Pough et al1998) populations of long-lived species can-not remain stable (or grow) when adults and older juve-niles are harvested at high rates (Congdon et al 19931994) This is not to say however that all such long-livedspecies should be commercially 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 (Ross1998) and unsustainable harvest of adults for the leathertrade (Brazaitis 1989) After years of total protection sev-eral sp ecies have recovered a f ew are farmed or ranchedcommercially (King 1989) In some crocodile speciesadult females are protected and only small numbers ofeggs small juveniles and larger males are removed fromthe wild (King 1989) In contrast 7ndash8 of all alligatorsmore than 12 m in length are harvested annually in someFlorida populations (David et al1996) In additiona 50annual harvest rate of alligator eggs or hatchlings isallowed because removal at these life stages does notreduce recruitment into adult-size classes (Rice et al1999) Closely monitored alligator populations and pre-sumably populations of other long-lived species of rep-tiles can sustain the legal regulated harvest of some pro-porti on of eggs h a tch l i n gs or adults with negl i gi bl eeffects

G l obal cl i m a te ch a n geFew ecologists will dispute the link between increases ingreenhouse gases and gl obal tem pera tu re Howeverwhether the current rate of climate change reflects naturalvariation or has an anthropogenic cause is hotly debatedFor the purposes of this article we accept the argumentthat the earth is undergoing unprecedented rapid climaticchange (Schneider and Root 1998) that includes alter-ations in climate variables such as temperature and rain-fall patterns storm severity and storm frequency If oneaccepts that human-induced climate change is occurring(eg Vinnikov et al1999)then the consequences for her-petofaunal diversity can be addressed

The obvious effects of climate change on biodiversityare mediated through changes in habitat For exampleglobal warming may further diminish prairie wetlandhabitat in the United States (Poiani and Johnson 1991)Future wetland acreage in the United States may be great-ly reduced under a variety of climate circulation models(Halpin 1997) and aquatic and semiaquatic species willsuffer declines as habitat disappears Although many habi-tats are ex pected to under go dra m a tic ch a n ge (eg Guertin et al1997Still et al 1999) predictions of specieshabitat shifts in response to global warming cannot be

based solely on analyses of climatendashspace changes becausespecies distributions are also a function of dispersal abili-ty and biotic interactions (Davis et al 1998) Existingnature reserves will be inadequate to preserve current bio-diversity because an already fragmented landscape willi 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 theirlimited dispersal abilities reptiles and amphibians areespecially vulnerable to rapid habitat changes and maysuffer many more extinctions than birds as a result of arapid rate of climate change (Schneider and Root 1998)

In discussions of observed amphibian declines littlemention has been made of climate change (Dodd 1997)with two notable exceptions First the famed golden toad(Bufo periglenes) extinction in Costa Rica may have b eencausedat 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 changepatterns of cloud formation and thereby the availability ofwater (Still et al 1999) Second Blaustein et al (1994a)have suggested that ultraviolet B (UVB) radiation hasadverse effects on some amphibians including reducedhatching success and decreased survival to metamorpho-sis However an increase in the level of UVB caused bydepletion of the ozone layer probably does not pose ani m m ed i a te threat to reptile eggs wh i ch are sel domexposed to UVB radiation

As with the amphibian studies few researchers havedirectly assessed effects of climate change on r eptiles It isnonetheless reasonable to expect that climate changescould re sult in con d i ti ons that el i m i n a te or severelyrestrict sp ecies with limited dist ributions (Schneider andRoot 1998) as has been suggested for some Australianlizards (Brereton et al1995) and crotaline snakes of NorthAmerica and the neotropics (Greene and Campbell 1993)Additional effects of warming on some reptiles based onem p i rical evi den ce with fre s hw a ter tu rt l e s i n clu deenhanced juvenile growth rates earlier ages at maturityand shifts in functional sex ratios (Frazer et al 1993)Global warming may have the greatest impact on thosereptiles (crocodilians and some turtles) that have temper-ature-dependent sex determination (Janzen 1994) where-by the sex ratio of the hatchlings is determined by nesttemperatures during incubation Unless shifts occur in thepivotal temperatures at which sex is determined or femalenest-site choices (ie shade versus sun) evolve to keeppace with rising temperatures altered sex ratios couldaffect population demographics and persistence

En i gm a tic decl i n e sFinally in addition to the many cases of declines that haves ome re a s on a bly unders tood causes s ome amph i bi a npopulations have declined and even gone extinct withoutany discernible causes One well-known example is thegastric 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 ofparental care in which the young develop in the safety ofthe motherrsquos stomach (Tyler and Carter 1981) the gastricbrooding frog ceased to be found in nature Disjunct pop-ulations of the g reen salamand er (Aneides aeneus ) in thes o ut h ern App a l achians have app a ren t ly decl i n ed butwithout similar declines in other portions of its range (JeffCorser USGS-BRD Twin Creeks Resource Center GSM-NP Gatlinburg TN personal communication)

Similar cases exist for reptiles For example no livingspecimen of the Round Island burrowing boa (Bolyeriamultocarinata) in the Indian Ocean has been seen since1975 (Bullock 1986) the species may have become extinctin recent decades (Greene 1997) Although all species ofreptiles native to North America in precolonial times per-sist in some regions the current ranges of many are but aremnant of the much larger areas formerly occupied Nat-ural populations of indigo snakes have not been found insome regions of their historic range in more than 40 years(Mount 1975 Conant and Collins 1998)and the species isldquodeclining in abundance and distribution throughout itsUS geographic rangerdquo (Hallam et al 1998) Likewises i gh ti n gs of the sout h ern hognose snake (Heterod o nsimus) 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 ) evenin 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 sRegrettably many amphibian populations and species thatare thought to be declining have not been monitored overlong 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 commoncharacteristic The subjects of these studies occur in highdensity either spatially (eg Jordanrsquos salamander Plethod -on jordanii Hairston 1987) or temporally (eg mole sala-manders Ambystoma talpoideum Pechmann et al 1991and natterjack toads Bufo calamita Banks et al 1994)

Many of the species that have become symbols for thedeclining amphibian phenomenon are seasonally activeanurans that arrive over restricted periods of time atbreeding sites where they congregate in greater densitiesthan at any other time of the year Researchers sit ready torecord their arrival and abundance and if the animals failto show up when expecteda problem is suspected if suchabsences are protracted then the change is presumablyreal (Blaustein et al 1994c) The phenology of theseamphibians permits detection of breeding activity there-fore determination of whether the absence of breedingadults is a short-term aberration or an indication of a realdecline becomes a matter of accumulating the data neces-sary to demonstrate a statistically significant trend (fordiscussion see Blaustein et al 1994c Pechmann andWilbur 1994 Reed and Blaustein 1995)

Among reptiles declines in sea turtles are perhaps the

best documented because like many amphibians theyengage in an annual reproductive event (in this caseoviposition) with a predictable site and time A few snakespecies in colder temperate regions are known to hiber-nate communally and numbers can be assessed upon

emergence (Parker and Brown 1973) But what of themajority of reptile species that do not congregate to breedor hibernate and do not occur in particularly high densi-ties F or example the r acer (Coluber const rictor) a com-mon North American snake is found in a wide variety ofterrestrial habitats Like most other ectotherms racers aremore active and therefore more commonly encounteredin the warmer months However aside from some regionswhere communal hibernation occurs (Parker and Brown1973) determining the abundance of racers is difficultbecause 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 howcould we take a census to know when and if racer popula-tions were declining at a substantial rate on a widespread

August 2000 Vol 50 No 8 BioScience 661

Articles

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

basis without mounting an intensive long-term samplingprogram The clandestine nature of many reptiles oftencombined with comparatively large home ranges lowpop u l a ti on den s i ti e s and ra reness of con grega ti on a lbehavior makes documenting population trends very dif-ficult As a result populations may wither with littlenoticeOnce an unmonitored species or population is rec-ognized as being unexpectedly depauperate or absent thecause of decline may be unknown and unknowable

Based on the accumulated evidence that many if notmost declines reported for amphibians are indeed realtheproper course for conservation initiatives is to assume theworst for all herpetofauna and therefore to implementabatement measures while gathering more data Althoughthe lack of long-term data often may preclude the id enti-fication of the cause of a decline or even in some cases thecorroboration o f a decline the absence of that data doesnot rule out the existence of a correctable problem

Co n clusion and re co m m en d a ti o n sThe declines of m a ny reptile pop u l a ti ons are similar tothose 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 ha m ph i bi a n s the causes are known with cert a i n ty ins ome instance s su s pected in many and unknown ino t h ers Some ex ti rp a ti ons are local wh ereas others arem ore wi de s pre ad The difficulty in doc u m en ting thes 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 causesof pop u l a ti on declines can be obvi a ted direct ly Th ei 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 ingeneral (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 ofinvasive non-native species that could be harmful to rep-tile populations must be proscribed Third restrictingtrade in sensitive reptile species for which sustainableremoval cannot be demonstrated will require the passageor strengthening and enforcement of legislation In thecase of Asian turtles legislative remedies could be too lit-tle too latemdasha stopgap remedy is necessary The only wayto prevent the imminent extinction of a large number ofthe more than 80 species of turtles native to southern Asiawill be to maintain populations in ex situ captive breedingand genetic reserve programs With changes in culturalattitudesstrengthening of international trade regulationsand increased habitat protection the reintroduction ofthese species into the wild may be possible

Much of todayrsquos commercial exploitation of reptiles inthe United States and elsewhere requires urgent govern-mental action to implement internationally accepted andenforced controls Despite the fact that conservation mea-sures can be implemented effectively through legislation(as happened with legislation for protection of Louisianabox turtles and American alligators) the political pres-sures against accomplishing such goals cannot be overstat-ed The lack of support by the World Trade Organizationfor recommendations to curtail sea turtle exploitation(WTO 1998) brings the problem into perspective on aninternational scale

Direct and indirect effects of environmental pol lutiondisease and parasitism and global climate change aremore difficult to quantify in many instances and will bemore difficult to change in the short term Nonetheless wemust endeavor to understand these potential factors toameliorate their impact on natural populations of reptilesand their habitats

Finally long-term monitoring o f reptile populations isessential and must be aided by the establishment of stan-dard methods and techniques It is equally important thatthe academic community land managers and conserva-tion organizations recognize that rigorous field programsfocusing on the distri buti on a bu n d a n ce s t a tu s a n dtrends of populations and species are critical and worth-while Herpetofaunal inventories should become a stan-dard part of environmental assessment programs and thepublication of field survey efforts that document potentialor suspected declines should be encouraged When long-term and widespread monitoring becomes the normdeclines are likely to become less equivocal (in terms ofprotracted declines versus natural fluctuations) and thecauses less mysterious

662 BioScience August 2000 Vol 50 No 8

Articles

Sand monitor (Va ra nus go u l d i ) Al t h ou gh sandm o n i to rs (genus Va ra nu s wh i ch includes the wo rl d rsquo sl a rgest lizards) appear to be thriving in many pa rts oft h eir natu ral habitats in Au s tra l i a ot h er spe cies of t h egenus in As i a Afri c a and the East Indies are threa ten e dby exten s ive habitat destru cti o n

The disappearance of reptiles from the natural world isgenuine and should be a matter of concern not simplybecause of reptilesrsquo perceived associations with amphib-ians but because reptile declineslike those of amphibiansare growing and serious in their own right Current evi-dence suggests that amphibian and reptile declines whichare exacerbated by burgeoning human populations con-stitute a worldwide crisis

Ack n owl e d gm en t sManuscript preparation was aided by Financial AssistanceAw a rd Nu m ber DE-FC09-96SR18546 from the USDep a rtm ent of E n er gy to the Un ivers i ty of G eor gi aResearch Foundation We thank Ab Abercrombie JustinCongdon William Hopkins Laura Janecek ChristopherRomanek and Joseph Pechmann for discussion and com-ments on the manuscript We also appreciate the help ofStephen H Bennett John Cossel Jr Charles R PetersonPaul Moler Woody Woodwardand Jeff Corser for provid-ing information on the status of particular species Thispaper supports the PARC (Partners in Amphibian andReptile Conservation) effort to promote education aboutreptiles and amphibians

Ref eren ces ci te dAl 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 ndash 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 ndash 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 119 8 3 ndash 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 ndash 6 9

Banks B Beebee TJC Coo ke KS 1 9 9 4 Con s erva ti on of the natter jack toadB u fo calamita in Britain over the peri od 1976ndash1990 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 ndash 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 eRe 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 eUn i ted States of Am erica 95 9 0 3 1 ndash 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 ndash 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 rba 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 ndash 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 ofE nvi ron m ental Con t a m i n a ti on Tox i co l ogy 27 8 2 ndash 8 7

Bi s h op JM1 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 ndash 4 3 0

Bl a u s tein A R Hoffman PD Hokit DG Ki e s ecker JM Wa lls SC Hays JB1 9 9 4 a UV repair and re s i s t a n ce to solar UV-B in amph i bian eggs Alink to pop u l a ti on declines Proceed i n gs of the Na ti onal Ac ademy ofS c i en ce of the Un i ted States of Am erica 91 1 7 9 1 ndash 1 7 9 5

Bl a u s tein A R Hokit DG Orsquo Ha ra RK Holt RA 1 9 9 4 b Pa t h ogenic funguscon tri butes to amph i bian losses in the Pacific Nort hwe s t Bi o l ogi c a lCon s erva ti on 67 2 5 1 ndash 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 gs 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 andgl obal ex ti n cti on s Con s erva ti on Bi o l ogy 8 6 0 ndash 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 196ndash201 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 tech 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 ndash 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 theS tu dy of Am ph i bians and Repti l e s Herpeto l ogy Ci rc u l a ti on 22 1 ndash 7 2

Buhlmann KA 1 9 9 5 Ha bitat use terre s trial movem ents and con s erva ti onof 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 ogy2 9 1 7 3 ndash 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 201ndash232 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 amp 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 dIsland and Gu n n er rsquos Quoi n Ma u ri tiu s Bi o l ogical Con s erva ti on 371 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 ndash 1 3 6 9

Ca rey C 1 9 9 3 Hypothesis con cerning the causes of the disappe a ra n ce ofboreal toads from the mountains of Co l orado Con s erva ti on Bi o l ogy 73 5 5 ndash 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 52 7 2 ndash 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 peRomain Na ti onal Wi l dl i fe Ref u ge Ch em o s ph ere 34 5 3 9 ndash 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 1ndash15 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 lm a tu ri ty and dem ogra phics of Bl a n d i n grsquos tu rtles (Emyd o i d e abl 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 ndash 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 ivedor ga n i s m s Am erican Zoo l ogist 34 3 9 7 ndash 4 0 8

[CITES] Conven ti on on In tern a ti onal Trade in Endangered Species ofWild Fauna and Flora 2 0 0 0 lt 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 tmlgt (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 lrule to list the nort h ern pop u l a ti on of the bog tu rtle as thre a ten ed andthe 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 ndash 5 9 6 2 3

August 2000 Vol 50 No 8 BioScience 663

Articles

Our account is not exhaustive rather we provide docu-m en ted examples of reptile pop u l a ti ons in peril anddecline The aggregate of examples of amphibians andreptiles indicates that the worldrsquos herpetofauna face stres-sors from both known and unknown origins that withoutremediationcan only lead to continuing declines extirpa-tions and extinctions

Di s tinguishing natu ral declines fro ma n t h ropogenic ones Amphibian declines are indisputably real and disquietingon a global scale Yet providing unequivocal supportingdocumentation for the decline of any particular popula-tion or species can be an onerous task and some expecta-tions of scientific rigor may be unable to be met (Pech-mann et al 1991) One persistent incertitude regardingamphibian declines is whether a decline is simply withinthe natural range of variability for a population or isinstead a consequence of anthropogenic causes that couldportend an unrecoverable situation

One difficulty in dem on s tra ting wh et h er ob s ervedtrends in esti m a ted pop u l a ti on sizes con s ti tute norm a lf lu ctu a ti ons or ldquou n n a tu ra l rdquo declines is that most fiel ds 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) ldquoSn a p s h o t srdquo( i e s h ort - term mon i toring) of pop u l a ti on size ands tru ctu re may dem on s tra te current status but do notreve a l l on g -term trends in population size or health Forexample Petranka et al (1993) who used short-termmonitoring and Ash (1997) who did long-term monitor-ing came to different conclusions regarding the effects ofclearcutting on recovery time of terrestrial salamanderpopulations To be surethe st rongest support for a decline

is a long-term data set that has registered population lev-els for particular species in par ticular locations Howeverthe accumulation of numerous accounts from shorter-term studies of a varie ty of amphibian sp ecies in diverse

habitats and geographic regions lends credence to pleasfor concern about declines

Studies of decline among reptiles like those conductedfor amphibianshave not always been carried out as rigor-ously as scientists would prefer Nonetheless the ever-increasing number of perceived declines among reptilesand the documentation of adverse impacts on individualsthat pre su m a bly can be proj ected into dem ogra ph i cchanges are harbingers of a crisis situationOur intent is toshow the phylogenetic and geographic breadth of per-ceived problems with many reptiles on the premise thatthey foreshadow a more intense and widespread problem

Ha bitat loss and degra d a ti o nMany scientists consider loss of suitable habitat to be thelargest 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 eregions of the United States retain less than 20 of thewetland acreage they once had (Leja 1998) and conse-quent declines in associated amphibian populations havebeen documented (Lannoo et al 1994) Numerous semi-aquatic reptiles rely on those very same wetlands In SouthCarolina the elimination or alteration of more than 90of Coastal Plain Carolina bay wetlands (Bennett and Nel-son 1991) has reduced essential habitat for black swampsnakes (Seminatrix pygaea) eastern green water snakes(Nerodia floridana)and chicken turtles (Deirochelys retic -ularia) all of whose distribution patterns are restrictedprimarily to seasonal wetlands (Buhlmann 1995 Dorcas etal 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 pol luted 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 surroundingterrestrial habitat needed by semiaquatic reptiles for nestshibernation sitesand other refugia is not (Burke and Gib-bons 1995)

August 2000 Vol 50 No 8 BioScience 655

Articles

Am eri c a ncro cod i l e Li ke manycro cod i l i a n s t h i ss pe cies hassu f f ered fro mco m m erci a loverexpl o i t a ti o nand habi t a td e s tru cti o n

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

Cu l tiva ted pine plantati ons in sout h e a s tern So ut hAfrica have been implicated in the endangerment of therare short-headed legless skink (Acontias breviceps) andthe disappearance of another lizard (Eastwoodrsquos long-tailed seps Tetradactylus eastwoodae Branch 1998) In theChiricahua mountains of southeastern Arizonathe elimi-nation of native bunchgrasses by cattle grazing was con-sidered to be the primary cause of a detectable decline inthe bu n ch grass lizard (S cel opo rus sc a l a ri s) wh i ch usebunchgrasses for cover from predators and for protectionfrom harsh winter conditions (Ballinger and Congdon1996) Habitat loss is the biggest problem in the decline ofsnakes in Australia (Shine 1991) The link between intacthabitat and species persistence and well-being is a basictenet of ecology and conservation biology (Meffe and Car-roll 1994 Mittermeier et al 1999) and needs no furtherdiscussion

The mere presence of humans may constitute an insid-ious form o f habitat degradation in some instances even

if the habitat itself remains intact Based on a 20-yearstudy a wood turtle (Clemmys insculpta) population ofmore than 130 animals in a forested watershed in NewHaven County Connecticut has been virtually eliminatedsince the area became open to the public (Garber andBurger 1995) The possible mechanisms of decline includ-ed removal road kill handling by recreationistsincreasednumber of predators attracted by food waste and distur-bance by dogs

In trodu ced inva s ive spe ci e sIntroduced species have been cited as a problem for manyamphibians (Stolzenburg 1999) For example the distrib-ution and abundance of several western US frog specieshave been severely reduced by non-native fishes and bull-frogs (Rana catesbeiana) which were and continue to beintroduced to wetland ldquoislandrdquohabitats of low- and high-elevation lakes (Fisher and Shaffer 1996) The collapse ofendemic reptile faunas on true islands after the introduc-tion of exotic species is similarly well documented andpervasivenon-native ratscatsand mongooses have extir-pated numerous lizard species on many islands (Case andBolger 1991) The tuatara (Sphenodon punctatus) a prim-itive reptilehistorically inhabited the two main islands ofNew Zealand and at least 40 of the offshore islands(Daugherty et al 1990) The tuatara became extinct on themain islands in the nineteenth century and on 10 offshoreislands within the last few decades and is experiencingpopulation declines on many of the other islands as aresult of introduced mammals primarily rats Feral pigs inthe Galapagos Islands first noted by Darwin in 1835 arejust one of the non-native species that have caused thenear extinction of the Galapagos tortoise (Geochelone ele -phantopus Thornton 1971) Introduced rats are suspectedto have destroyed both the eggs and young of the tortois-e s but the initial cause of decline was 18th-cen tu rymariners who stopped at the islands and stocked theirships with live tortoises as food f or the sailors (Pritchard1967)

Even the introduction of non-native reptiles can disruptindigenous reptile communities For example Losos et al(1993) showed that the invasion of Grand Cayman byexotic brown anoles (Anolis sagrei) caused behavioralchanges and shifts in habitat use by the native speciesAnolis conspersus Likewise the introduction of the browntree snake (Boiga irregularis) has been implicated in theex ti rp a ti on of the gecko (Na ctus pel a gi c u s) from theislands of Guam and Tinian the brown tree snake is alsoconsidered responsible for dramatic declines in otherspecies 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 native reptilesare not limited to islands In the continental United Statesi m ported fire ants (S ol en opsis invi ct a) i n trodu ced inMobile Alabama as early as 1918 (Wilson 1950) have

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Articles

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

been reported to prey on both eggs (Moulis 1997) andyoung (Allen et al1997) of reptilesFire ants are implicat-ed as a primary cause of extirpation of the Texas hornedlizard (Phrynosoma cornutum) from part of its geographicrange (Goin 1992)

Invasive species need not be other animals Both thedesert tortoise (Gopherus agassizii) and the gopher tortoiseare threatened by the introduction of non-native plantspecies (Stewart et al 1993 Lovich 1995) that alter habitatstructure native plant community composition and evenfire frequency The black legless lizard (Anniella pulchranigra) was considered for federal endangered status inpart because of the negative impact of non-native Hotten-tot fig plants on the lizardsrsquo prey base in disturbed sand-dune habitat (Rutherford and Rorabaugh 1995) nonethe-less an official decision was made not to list the speciesafter viable lizard populations were found in undisturbedhabitat with native vegetation (Morey 1998) In Idahoreptile sp ecies richness decreased an average o f 5 from1978 to 1998 at 24 sample sites in the Snake River Birds ofPrey Area (John Cossel Jr and Charles R Peterson IdahoState University Pocatello ID personal communication)According to Cossel and Peterson the changes in reptilepopulations may have been influenced by a decrease innative shrub habitat caused by the prevalence of exoticannual grasses and the effects of wildfires that have burnedover 50 of the area since the 1970s

Envi ro n m ental poll u ti o nNumerous environmental contaminantsmdashmetals pesti-cides and herbicidesand radioactive waste for examplemdashhave direct and indirect effects on both amphibians andreptiles (eg Hinton and Scott 1990 Hall and Henry1992) Amphibians have been the subject of numerousecotoxicological studiesincluding assessment of the directeffects of contaminants such as fertilizers (Marco et al1999) or the more subtle effects of steroid-mimicking con-taminants (Hayes 1997) Reptiles are studied far less thanamphibians with respect to the fate and effects of contam-inants (Hopkins et al 1999) but they have received suffi-cient toxicological study to provide convincing evidencethat some individual reptiles are adversely affected bymany contaminants (Hall 1980 Fontenot et al 1994) Forexampleslider turtles (Trachemys scripta) exposed to met-al and radioisotope contaminants incur genetic damage(Lamb et al 1995) The degree to which contaminantscause population-level effects remains largely unknownboth for amphibians and for reptiles

Contaminant effects in reptiles are known mainly fromturtles and crocodilians Many turtles and crocodiliansbecause they have environmental sex determination andlarge eggs that can incorporate high levels of environmen-tal pollutants are especially sensitive to endocrine-dis-rupting chemicals (Guillette and Crain 1996) At som econ 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 eggs (Bishop et al 1994 Cobb and Wood 1997) sexreversal and abnormal gonads have been found in turtlesexposed to PCBs (Bergeron et al 1994 Guillette et al1995) Male American alligators (Alligator mississippiensis)inhabiting Lake Apopka a chemically contaminated lakein Florida had significantly reduced plasma testosteronelevels and permanent gonadal alterations (Guillette et al1994)

Even nonlethal effects o f endocrine disrup ters on rep-tiles may result in demographic shifts whose consequencesfor populations are presumably detrimental Population-level effects might also occur through changes to patternsof individual energy allocation For example in coal-ashpolluted wetlands water snakes (Nerodia fasciata) withhigh body burdens of metal contaminants exhibit elevatedmetabolic rates which may result in less energy beingdevoted to reproduction growth and storage (Hopkins etal 1999)

Di sea se and pa ra s i ti s mParasites and disease have been documented or suspectedas causes for declines in some amphibian species (Daszaket al 1999) In some cases sublethal environmental stres-sors may suppress immune systems (Carey 1993) andallow disease agents to kill weakened animals (Alford andRichards 1999) Recently however a spreading ldquoextinctionwaverdquo of chytrid fungus is thought to be causing thedecline of anurans in Central America and Australia(Berger et al 1998 Lips 1999) moreover researchersbelieve that the fungus is killing otherwise healthy animals(Daszak et al 1999) An iridovirus may be the primarycause 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 ha m p h i bian and reptile popu l a ti o n s Co nversion ofwet 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 gterre s trial habitat to agri c u l tu ral (ill u s tra ted here) andot h er uses have re su l ted in wetland losses exceeding 80in many state s

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 nowbelieve that disease may rival habitat destruction as thelargest single cause o f the decline of amphibians

Among reptiles the widespread upper respiratory tractdisease a contagious respiratory ailment caused by thebacterium Mycoplasma agassizii is a potential cause ofpopulation declines in desert tortoises in the US South-west and gopher tortoises in the Southeast (Jacobson1993 Smith et al 1998)Shell diseases have been implicat-ed in the decline of turtles (eg shell lesions on slidersLovich et al 1996 cutaneous dyskeratosis affecting theshell and thickened forelimb scutes of desert tortoisesJacobson 1994 and emaciation and lesions of the plastronof federally listed flattened musk turtles Sternotherusdepressus Dodd 1988) Individuals in many green sea tur-tle populations are severely affected by viral fibropapillo-mas resulting in growths that can impair vision locomo-tionand feeding ability (Herbst 1994) As is often the casein amphibiansdiseases that are debilitating to wild popu-lations of reptiles are most likely secondary expressions inindividuals with impaired resistance caused by one ormore primary environmental stressors such as habitatdegradation invasive species or pollution

Un su s t a i n a ble useHuman use of animalsincluding reptiles and amphibiansis an integral part of many cultures Harvesting must bebi 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 andspecies are to persist (Pough et al 1998) Overcollectionfor food the pet trade and biological supply houses hasbeen suggested as having had an impact on some amphib-ian populations (Dodd 1997) In the United States note-worthy examples for amphibians occurred in the late1800s to early 1900s when commercial collectors harvest-ed for the frog legs market Hundreds of thousands of

red - l egged frogs (Rana auro ra drayto 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 frogsalthough itis 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 al1994) In Indiathe 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 illegallyeach 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 onsu 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 havebeen more perva s ive and severe than on amph i bians (eg s ee Wi lliams 1999) The severi ty of the tu rtle crisis on agl obal scale was em ph a s i zed by Rh odin (1999) wh oreported that of the approx i m a tely 293 taxa (mainlys 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 thelast few cen tu ri e s 3 (9 taxa) are alre ady ex ti n ct in thewi 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 foodsource Moreover the international trade in turtlesmdashwhich are eaten sold as pets or used in traditional Chi-nese medicinal remediesmdashis both extensive and unregu-lated (Sharma 1999) A recent report indicated that mostturtle sp ecies in Vietnam and southern China are endan-gered and that turtles can no longer be found in the wildin Vietnam (Kiester and Juvik 1997) China is the biggestconsumer of turtles in the food trade Because the trade inturtles is not regulated few records have been kept butexisting records indicate that the trade in live turtles toChina is thousands of tons per year (Mockenhaupt 1999)The commercial trade in freshwater turtles exceeds anypossible sustainable levels and extinction of some speciesin the wild can be expected within the next decade

Most species of sea turtles continue to decline in allwarm oceans of the world The leatherback sea turtle(Dermochelys coriacea) was recently reported to be ldquoon theroad to extinction and further population declines can beexpectedrdquounless appropriate measures are taken to reducemortality rates in adults hatchlings and eggs (Spotila eta l 1 9 9 6 ) The esti m a ted worl dwi de pop u l a ti on ofleatherbacks nesting on beaches in 1980 was 115000com p a red with just 34500 in 1995 Ex p l oi t a ti on ofleatherbacks in the Atlantic Ocean through illegal har-vesting of both adults and eggsis considered to be a majorcontributor to the decline of the species (Spotila et al1996) Likewise for Kemprsquos Ridley sea turtle (Lepidochelys

658 BioScience August 2000 Vol 50 No 8

Articles

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

kempii) harvests of nesting females and their eggs on thelargest known nesting site contributed to declines from42000 nesting females in 1947 to only a few hundred by1975 (Hildebrand 1982)

Among North American turtles the diamondback ter-rapin (Ma l a cl emys terra p i n) a small e s tu a rine tu rt l especies with a geographic range from Cape Cod to Texasdecl i n ed severely fo ll owing heavy ex p l oi t a ti on as agourmet food item from the late 1800s to the early 1900s(Carr 1952) With forced reductions in harvesting manypopulations were able to recover but the terrapin nowfaces significant new threats including highway mortality(Wood and Herlands 1997) and drowning in commercialand recreational crab traps (Bishop 1983 Roosenburg1991) Renewed commercial har vest of the diamondbackterrapin has also been documented (Garber 1988)

Commercial turtle trappers for the restaurant tradestepped up harvests of one of the largest freshwater turtlesin the world the alligator snapper (Macroclemys tem -minckii) from the 1960s through the 1980s (Roman et al1999) Consequently as evidence from survey efforts sug-gests the species has b een drastical ly reduced in numbersin some of the southeastern US rivers it once inhabited(Moler 1992 Jensen 1998)

The enormous and once common populations of thearrau (Podocnemis expansa) a communally nesting turtleof the Orinoco and Amazon Rivers in South America arenow greatly reduced in size because of human consump-tion of eggs and nesting females (Pritchard and Trebbau1984) an overexploitation problem identified almost twocenturies ago (Humboldt 1814 from Pritchard and Treb-bau 1984) Declines from similar causes have befallen theterecay (Podocnemis unifilis) in tropical lowlands of SouthAmerica (Thorbjarnarson et al 1993) and the river ter-rapin (Batagur baska) in India (Bhupathy 1997)

Overharvesting for food is a problem not just for turtlesbut also for lizardshaving contributed to declines in greeniguanas (Iguana iguana) and spiny - t a i l ed iguanas(Ctenosaura similis) in tropical America (Fitch et al1982)

The pet trade appears especially hazardous for someturtle sp ecies In 1994 population declines were reportedin box turtles (Terrapene carolina) in 16 states rangingfrom Massachusetts to Florida and Oklahoma to Wiscon-sin (Lieberman 1994) Doc u m en t a ti on of box tu rt l edecl i n e s mdash i n cluding records showing that s i n ce 199529896 box turtles had been collected for the pet trade andshipped from Louisianamdashresulted in unanimous passageof Act 81 by the Louisiana Senate and House of Represen-tatives in 1999the act prohibits the commercial harvest ofthe statersquos native box turtle populations Overcollection forexport is a serious factor in much of the box turtle declineand may exacerbate the effects of habitat loss (Lieberman1994) Habitat destruction and illegal collecting for the pettrade are the primary threats to bog turtles (Clemmysmuhlenbergii) Copeyon 1997) The number of northernpopulations has been reduced by 50 with most of the

decline occurring over the last 20 years Of the 191remaining bog turtle habitats known in 199633 were clas-sified as in good condition 67 as fair and 76 as poor thestatus of 15 was unknown

Overcollecting is also a problem for some snake speciesThe ocellated mountain viper (Vipera wagneri) in easternTurkey has been sought by the pet trade and removedfrom the wild in large numbers posing ldquoa serious threat tosurvival of the speciesrdquo (Nilson et al 1990) Populations ofseveral boa and python species have declined because ofharvesting of wild snakes for their skins (Pough et al1998) Rapid declines o f large-bodied snakes which tendto have a suite of life-history traits that make them moresusceptible to population declines than smaller species(eg Dodd 1993)have been documented throughout theworld in recent years (egShine and Fitzgerald 1996) Forexample females of the increasingly rare timber rat-tlesnake (Crotalus horridus) which may exceed a meter inlength and typically take 9 years to reach maturity pro-duce fewer than a dozen young every 3 years (Brown1993)Large-bodied species such as rattlesnakes (Crotalus)have long generation times a life-history t rait that whencom bi n ed with habitat loss human pers ec uti on a n di n ten s ive overco ll ecti on (eg ldquora t t l e s n a ke ro u n du p srdquo Brown 1993)has led to dramatic declines of some speciesand ma de approximately one-third of rattlesnake sp eciesvulnerable to extinction (Greene 1997) High harvest ratesof snakes with low reproductive frequencies such as thef 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 dalmost 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 ts tudies on reptiles have be en co n du cted on snapp i n gtu rtles and all i ga to rs in wh i ch sex reversal and abn o rm a lgonads have be en note d

These examples demonstrate that sustainable use ofsome long-lived reptile species is problematic Becauselongevity in reptiles is associated with delayed sexualm a tu ri ty h i gh adult su rvivors h i p and low fec u n d i ty(Pough et al1998) populations of long-lived species can-not remain stable (or grow) when adults and older juve-niles are harvested at high rates (Congdon et al 19931994) This is not to say however that all such long-livedspecies should be commercially 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 (Ross1998) and unsustainable harvest of adults for the leathertrade (Brazaitis 1989) After years of total protection sev-eral sp ecies have recovered a f ew are farmed or ranchedcommercially (King 1989) In some crocodile speciesadult females are protected and only small numbers ofeggs small juveniles and larger males are removed fromthe wild (King 1989) In contrast 7ndash8 of all alligatorsmore than 12 m in length are harvested annually in someFlorida populations (David et al1996) In additiona 50annual harvest rate of alligator eggs or hatchlings isallowed because removal at these life stages does notreduce recruitment into adult-size classes (Rice et al1999) Closely monitored alligator populations and pre-sumably populations of other long-lived species of rep-tiles can sustain the legal regulated harvest of some pro-porti on of eggs h a tch l i n gs or adults with negl i gi bl eeffects

G l obal cl i m a te ch a n geFew ecologists will dispute the link between increases ingreenhouse gases and gl obal tem pera tu re Howeverwhether the current rate of climate change reflects naturalvariation or has an anthropogenic cause is hotly debatedFor the purposes of this article we accept the argumentthat the earth is undergoing unprecedented rapid climaticchange (Schneider and Root 1998) that includes alter-ations in climate variables such as temperature and rain-fall patterns storm severity and storm frequency If oneaccepts that human-induced climate change is occurring(eg Vinnikov et al1999)then the consequences for her-petofaunal diversity can be addressed

The obvious effects of climate change on biodiversityare mediated through changes in habitat For exampleglobal warming may further diminish prairie wetlandhabitat in the United States (Poiani and Johnson 1991)Future wetland acreage in the United States may be great-ly reduced under a variety of climate circulation models(Halpin 1997) and aquatic and semiaquatic species willsuffer declines as habitat disappears Although many habi-tats are ex pected to under go dra m a tic ch a n ge (eg Guertin et al1997Still et al 1999) predictions of specieshabitat shifts in response to global warming cannot be

based solely on analyses of climatendashspace changes becausespecies distributions are also a function of dispersal abili-ty and biotic interactions (Davis et al 1998) Existingnature reserves will be inadequate to preserve current bio-diversity because an already fragmented landscape willi 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 theirlimited dispersal abilities reptiles and amphibians areespecially vulnerable to rapid habitat changes and maysuffer many more extinctions than birds as a result of arapid rate of climate change (Schneider and Root 1998)

In discussions of observed amphibian declines littlemention has been made of climate change (Dodd 1997)with two notable exceptions First the famed golden toad(Bufo periglenes) extinction in Costa Rica may have b eencausedat 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 changepatterns of cloud formation and thereby the availability ofwater (Still et al 1999) Second Blaustein et al (1994a)have suggested that ultraviolet B (UVB) radiation hasadverse effects on some amphibians including reducedhatching success and decreased survival to metamorpho-sis However an increase in the level of UVB caused bydepletion of the ozone layer probably does not pose ani m m ed i a te threat to reptile eggs wh i ch are sel domexposed to UVB radiation

As with the amphibian studies few researchers havedirectly assessed effects of climate change on r eptiles It isnonetheless reasonable to expect that climate changescould re sult in con d i ti ons that el i m i n a te or severelyrestrict sp ecies with limited dist ributions (Schneider andRoot 1998) as has been suggested for some Australianlizards (Brereton et al1995) and crotaline snakes of NorthAmerica and the neotropics (Greene and Campbell 1993)Additional effects of warming on some reptiles based onem p i rical evi den ce with fre s hw a ter tu rt l e s i n clu deenhanced juvenile growth rates earlier ages at maturityand shifts in functional sex ratios (Frazer et al 1993)Global warming may have the greatest impact on thosereptiles (crocodilians and some turtles) that have temper-ature-dependent sex determination (Janzen 1994) where-by the sex ratio of the hatchlings is determined by nesttemperatures during incubation Unless shifts occur in thepivotal temperatures at which sex is determined or femalenest-site choices (ie shade versus sun) evolve to keeppace with rising temperatures altered sex ratios couldaffect population demographics and persistence

En i gm a tic decl i n e sFinally in addition to the many cases of declines that haves ome re a s on a bly unders tood causes s ome amph i bi a npopulations have declined and even gone extinct withoutany discernible causes One well-known example is thegastric brooding frog (Rheobatrachus silus) of Australia

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Articles

S h ort ly after the discovery of its unu sual sys tem ofparental care in which the young develop in the safety ofthe motherrsquos stomach (Tyler and Carter 1981) the gastricbrooding frog ceased to be found in nature Disjunct pop-ulations of the g reen salamand er (Aneides aeneus ) in thes o ut h ern App a l achians have app a ren t ly decl i n ed butwithout similar declines in other portions of its range (JeffCorser USGS-BRD Twin Creeks Resource Center GSM-NP Gatlinburg TN personal communication)

Similar cases exist for reptiles For example no livingspecimen of the Round Island burrowing boa (Bolyeriamultocarinata) in the Indian Ocean has been seen since1975 (Bullock 1986) the species may have become extinctin recent decades (Greene 1997) Although all species ofreptiles native to North America in precolonial times per-sist in some regions the current ranges of many are but aremnant of the much larger areas formerly occupied Nat-ural populations of indigo snakes have not been found insome regions of their historic range in more than 40 years(Mount 1975 Conant and Collins 1998)and the species isldquodeclining in abundance and distribution throughout itsUS geographic rangerdquo (Hallam et al 1998) Likewises i gh ti n gs of the sout h ern hognose snake (Heterod o nsimus) 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 ) evenin 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 sRegrettably many amphibian populations and species thatare thought to be declining have not been monitored overlong 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 commoncharacteristic The subjects of these studies occur in highdensity either spatially (eg Jordanrsquos salamander Plethod -on jordanii Hairston 1987) or temporally (eg mole sala-manders Ambystoma talpoideum Pechmann et al 1991and natterjack toads Bufo calamita Banks et al 1994)

Many of the species that have become symbols for thedeclining amphibian phenomenon are seasonally activeanurans that arrive over restricted periods of time atbreeding sites where they congregate in greater densitiesthan at any other time of the year Researchers sit ready torecord their arrival and abundance and if the animals failto show up when expecteda problem is suspected if suchabsences are protracted then the change is presumablyreal (Blaustein et al 1994c) The phenology of theseamphibians permits detection of breeding activity there-fore determination of whether the absence of breedingadults is a short-term aberration or an indication of a realdecline becomes a matter of accumulating the data neces-sary to demonstrate a statistically significant trend (fordiscussion see Blaustein et al 1994c Pechmann andWilbur 1994 Reed and Blaustein 1995)

Among reptiles declines in sea turtles are perhaps the

best documented because like many amphibians theyengage in an annual reproductive event (in this caseoviposition) with a predictable site and time A few snakespecies in colder temperate regions are known to hiber-nate communally and numbers can be assessed upon

emergence (Parker and Brown 1973) But what of themajority of reptile species that do not congregate to breedor hibernate and do not occur in particularly high densi-ties F or example the r acer (Coluber const rictor) a com-mon North American snake is found in a wide variety ofterrestrial habitats Like most other ectotherms racers aremore active and therefore more commonly encounteredin the warmer months However aside from some regionswhere communal hibernation occurs (Parker and Brown1973) determining the abundance of racers is difficultbecause 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 howcould we take a census to know when and if racer popula-tions were declining at a substantial rate on a widespread

August 2000 Vol 50 No 8 BioScience 661

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

basis without mounting an intensive long-term samplingprogram The clandestine nature of many reptiles oftencombined with comparatively large home ranges lowpop u l a ti on den s i ti e s and ra reness of con grega ti on a lbehavior makes documenting population trends very dif-ficult As a result populations may wither with littlenoticeOnce an unmonitored species or population is rec-ognized as being unexpectedly depauperate or absent thecause of decline may be unknown and unknowable

Based on the accumulated evidence that many if notmost declines reported for amphibians are indeed realtheproper course for conservation initiatives is to assume theworst for all herpetofauna and therefore to implementabatement measures while gathering more data Althoughthe lack of long-term data often may preclude the id enti-fication of the cause of a decline or even in some cases thecorroboration o f a decline the absence of that data doesnot rule out the existence of a correctable problem

Co n clusion and re co m m en d a ti o n sThe declines of m a ny reptile pop u l a ti ons are similar tothose 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 ha m ph i bi a n s the causes are known with cert a i n ty ins ome instance s su s pected in many and unknown ino t h ers Some ex ti rp a ti ons are local wh ereas others arem ore wi de s pre ad The difficulty in doc u m en ting thes 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 causesof pop u l a ti on declines can be obvi a ted direct ly Th ei 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 ingeneral (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 ofinvasive non-native species that could be harmful to rep-tile populations must be proscribed Third restrictingtrade in sensitive reptile species for which sustainableremoval cannot be demonstrated will require the passageor strengthening and enforcement of legislation In thecase of Asian turtles legislative remedies could be too lit-tle too latemdasha stopgap remedy is necessary The only wayto prevent the imminent extinction of a large number ofthe more than 80 species of turtles native to southern Asiawill be to maintain populations in ex situ captive breedingand genetic reserve programs With changes in culturalattitudesstrengthening of international trade regulationsand increased habitat protection the reintroduction ofthese species into the wild may be possible

Much of todayrsquos commercial exploitation of reptiles inthe United States and elsewhere requires urgent govern-mental action to implement internationally accepted andenforced controls Despite the fact that conservation mea-sures can be implemented effectively through legislation(as happened with legislation for protection of Louisianabox turtles and American alligators) the political pres-sures against accomplishing such goals cannot be overstat-ed The lack of support by the World Trade Organizationfor recommendations to curtail sea turtle exploitation(WTO 1998) brings the problem into perspective on aninternational scale

Direct and indirect effects of environmental pol lutiondisease and parasitism and global climate change aremore difficult to quantify in many instances and will bemore difficult to change in the short term Nonetheless wemust endeavor to understand these potential factors toameliorate their impact on natural populations of reptilesand their habitats

Finally long-term monitoring o f reptile populations isessential and must be aided by the establishment of stan-dard methods and techniques It is equally important thatthe academic community land managers and conserva-tion organizations recognize that rigorous field programsfocusing on the distri buti on a bu n d a n ce s t a tu s a n dtrends of populations and species are critical and worth-while Herpetofaunal inventories should become a stan-dard part of environmental assessment programs and thepublication of field survey efforts that document potentialor suspected declines should be encouraged When long-term and widespread monitoring becomes the normdeclines are likely to become less equivocal (in terms ofprotracted declines versus natural fluctuations) and thecauses less mysterious

662 BioScience August 2000 Vol 50 No 8

Articles

Sand monitor (Va ra nus go u l d i ) Al t h ou gh sandm o n i to rs (genus Va ra nu s wh i ch includes the wo rl d rsquo sl a rgest lizards) appear to be thriving in many pa rts oft h eir natu ral habitats in Au s tra l i a ot h er spe cies of t h egenus in As i a Afri c a and the East Indies are threa ten e dby exten s ive habitat destru cti o n

The disappearance of reptiles from the natural world isgenuine and should be a matter of concern not simplybecause of reptilesrsquo perceived associations with amphib-ians but because reptile declineslike those of amphibiansare growing and serious in their own right Current evi-dence suggests that amphibian and reptile declines whichare exacerbated by burgeoning human populations con-stitute a worldwide crisis

Ack n owl e d gm en t sManuscript preparation was aided by Financial AssistanceAw a rd Nu m ber DE-FC09-96SR18546 from the USDep a rtm ent of E n er gy to the Un ivers i ty of G eor gi aResearch Foundation We thank Ab Abercrombie JustinCongdon William Hopkins Laura Janecek ChristopherRomanek and Joseph Pechmann for discussion and com-ments on the manuscript We also appreciate the help ofStephen H Bennett John Cossel Jr Charles R PetersonPaul Moler Woody Woodwardand Jeff Corser for provid-ing information on the status of particular species Thispaper supports the PARC (Partners in Amphibian andReptile Conservation) effort to promote education aboutreptiles and amphibians

Ref eren ces ci te dAl 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 ndash 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 ndash 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 119 8 3 ndash 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 ndash 6 9

Banks B Beebee TJC Coo ke KS 1 9 9 4 Con s erva ti on of the natter jack toadB u fo calamita in Britain over the peri od 1976ndash1990 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 ndash 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 eRe 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 eUn i ted States of Am erica 95 9 0 3 1 ndash 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 ndash 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 rba 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 ndash 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 ofE nvi ron m ental Con t a m i n a ti on Tox i co l ogy 27 8 2 ndash 8 7

Bi s h op JM1 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 ndash 4 3 0

Bl a u s tein A R Hoffman PD Hokit DG Ki e s ecker JM Wa lls SC Hays JB1 9 9 4 a UV repair and re s i s t a n ce to solar UV-B in amph i bian eggs Alink to pop u l a ti on declines Proceed i n gs of the Na ti onal Ac ademy ofS c i en ce of the Un i ted States of Am erica 91 1 7 9 1 ndash 1 7 9 5

Bl a u s tein A R Hokit DG Orsquo Ha ra RK Holt RA 1 9 9 4 b Pa t h ogenic funguscon tri butes to amph i bian losses in the Pacific Nort hwe s t Bi o l ogi c a lCon s erva ti on 67 2 5 1 ndash 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 gs 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 andgl obal ex ti n cti on s Con s erva ti on Bi o l ogy 8 6 0 ndash 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 196ndash201 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 tech 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 ndash 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 theS tu dy of Am ph i bians and Repti l e s Herpeto l ogy Ci rc u l a ti on 22 1 ndash 7 2

Buhlmann KA 1 9 9 5 Ha bitat use terre s trial movem ents and con s erva ti onof 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 ogy2 9 1 7 3 ndash 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 201ndash232 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 amp 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 dIsland and Gu n n er rsquos Quoi n Ma u ri tiu s Bi o l ogical Con s erva ti on 371 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 ndash 1 3 6 9

Ca rey C 1 9 9 3 Hypothesis con cerning the causes of the disappe a ra n ce ofboreal toads from the mountains of Co l orado Con s erva ti on Bi o l ogy 73 5 5 ndash 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 52 7 2 ndash 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 peRomain Na ti onal Wi l dl i fe Ref u ge Ch em o s ph ere 34 5 3 9 ndash 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 1ndash15 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 lm a tu ri ty and dem ogra phics of Bl a n d i n grsquos tu rtles (Emyd o i d e abl 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 ndash 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 ivedor ga n i s m s Am erican Zoo l ogist 34 3 9 7 ndash 4 0 8

[CITES] Conven ti on on In tern a ti onal Trade in Endangered Species ofWild Fauna and Flora 2 0 0 0 lt 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 tmlgt (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 lrule to list the nort h ern pop u l a ti on of the bog tu rtle as thre a ten ed andthe 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 ndash 5 9 6 2 3

August 2000 Vol 50 No 8 BioScience 663

Articles

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

Cu l tiva ted pine plantati ons in sout h e a s tern So ut hAfrica have been implicated in the endangerment of therare short-headed legless skink (Acontias breviceps) andthe disappearance of another lizard (Eastwoodrsquos long-tailed seps Tetradactylus eastwoodae Branch 1998) In theChiricahua mountains of southeastern Arizonathe elimi-nation of native bunchgrasses by cattle grazing was con-sidered to be the primary cause of a detectable decline inthe bu n ch grass lizard (S cel opo rus sc a l a ri s) wh i ch usebunchgrasses for cover from predators and for protectionfrom harsh winter conditions (Ballinger and Congdon1996) Habitat loss is the biggest problem in the decline ofsnakes in Australia (Shine 1991) The link between intacthabitat and species persistence and well-being is a basictenet of ecology and conservation biology (Meffe and Car-roll 1994 Mittermeier et al 1999) and needs no furtherdiscussion

The mere presence of humans may constitute an insid-ious form o f habitat degradation in some instances even

if the habitat itself remains intact Based on a 20-yearstudy a wood turtle (Clemmys insculpta) population ofmore than 130 animals in a forested watershed in NewHaven County Connecticut has been virtually eliminatedsince the area became open to the public (Garber andBurger 1995) The possible mechanisms of decline includ-ed removal road kill handling by recreationistsincreasednumber of predators attracted by food waste and distur-bance by dogs

In trodu ced inva s ive spe ci e sIntroduced species have been cited as a problem for manyamphibians (Stolzenburg 1999) For example the distrib-ution and abundance of several western US frog specieshave been severely reduced by non-native fishes and bull-frogs (Rana catesbeiana) which were and continue to beintroduced to wetland ldquoislandrdquohabitats of low- and high-elevation lakes (Fisher and Shaffer 1996) The collapse ofendemic reptile faunas on true islands after the introduc-tion of exotic species is similarly well documented andpervasivenon-native ratscatsand mongooses have extir-pated numerous lizard species on many islands (Case andBolger 1991) The tuatara (Sphenodon punctatus) a prim-itive reptilehistorically inhabited the two main islands ofNew Zealand and at least 40 of the offshore islands(Daugherty et al 1990) The tuatara became extinct on themain islands in the nineteenth century and on 10 offshoreislands within the last few decades and is experiencingpopulation declines on many of the other islands as aresult of introduced mammals primarily rats Feral pigs inthe Galapagos Islands first noted by Darwin in 1835 arejust one of the non-native species that have caused thenear extinction of the Galapagos tortoise (Geochelone ele -phantopus Thornton 1971) Introduced rats are suspectedto have destroyed both the eggs and young of the tortois-e s but the initial cause of decline was 18th-cen tu rymariners who stopped at the islands and stocked theirships with live tortoises as food f or the sailors (Pritchard1967)

Even the introduction of non-native reptiles can disruptindigenous reptile communities For example Losos et al(1993) showed that the invasion of Grand Cayman byexotic brown anoles (Anolis sagrei) caused behavioralchanges and shifts in habitat use by the native speciesAnolis conspersus Likewise the introduction of the browntree snake (Boiga irregularis) has been implicated in theex ti rp a ti on of the gecko (Na ctus pel a gi c u s) from theislands of Guam and Tinian the brown tree snake is alsoconsidered responsible for dramatic declines in otherspecies 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 native reptilesare not limited to islands In the continental United Statesi m ported fire ants (S ol en opsis invi ct a) i n trodu ced inMobile Alabama as early as 1918 (Wilson 1950) have

656 BioScience August 2000 Vol 50 No 8

Articles

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

been reported to prey on both eggs (Moulis 1997) andyoung (Allen et al1997) of reptilesFire ants are implicat-ed as a primary cause of extirpation of the Texas hornedlizard (Phrynosoma cornutum) from part of its geographicrange (Goin 1992)

Invasive species need not be other animals Both thedesert tortoise (Gopherus agassizii) and the gopher tortoiseare threatened by the introduction of non-native plantspecies (Stewart et al 1993 Lovich 1995) that alter habitatstructure native plant community composition and evenfire frequency The black legless lizard (Anniella pulchranigra) was considered for federal endangered status inpart because of the negative impact of non-native Hotten-tot fig plants on the lizardsrsquo prey base in disturbed sand-dune habitat (Rutherford and Rorabaugh 1995) nonethe-less an official decision was made not to list the speciesafter viable lizard populations were found in undisturbedhabitat with native vegetation (Morey 1998) In Idahoreptile sp ecies richness decreased an average o f 5 from1978 to 1998 at 24 sample sites in the Snake River Birds ofPrey Area (John Cossel Jr and Charles R Peterson IdahoState University Pocatello ID personal communication)According to Cossel and Peterson the changes in reptilepopulations may have been influenced by a decrease innative shrub habitat caused by the prevalence of exoticannual grasses and the effects of wildfires that have burnedover 50 of the area since the 1970s

Envi ro n m ental poll u ti o nNumerous environmental contaminantsmdashmetals pesti-cides and herbicidesand radioactive waste for examplemdashhave direct and indirect effects on both amphibians andreptiles (eg Hinton and Scott 1990 Hall and Henry1992) Amphibians have been the subject of numerousecotoxicological studiesincluding assessment of the directeffects of contaminants such as fertilizers (Marco et al1999) or the more subtle effects of steroid-mimicking con-taminants (Hayes 1997) Reptiles are studied far less thanamphibians with respect to the fate and effects of contam-inants (Hopkins et al 1999) but they have received suffi-cient toxicological study to provide convincing evidencethat some individual reptiles are adversely affected bymany contaminants (Hall 1980 Fontenot et al 1994) Forexampleslider turtles (Trachemys scripta) exposed to met-al and radioisotope contaminants incur genetic damage(Lamb et al 1995) The degree to which contaminantscause population-level effects remains largely unknownboth for amphibians and for reptiles

Contaminant effects in reptiles are known mainly fromturtles and crocodilians Many turtles and crocodiliansbecause they have environmental sex determination andlarge eggs that can incorporate high levels of environmen-tal pollutants are especially sensitive to endocrine-dis-rupting chemicals (Guillette and Crain 1996) At som econ 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 eggs (Bishop et al 1994 Cobb and Wood 1997) sexreversal and abnormal gonads have been found in turtlesexposed to PCBs (Bergeron et al 1994 Guillette et al1995) Male American alligators (Alligator mississippiensis)inhabiting Lake Apopka a chemically contaminated lakein Florida had significantly reduced plasma testosteronelevels and permanent gonadal alterations (Guillette et al1994)

Even nonlethal effects o f endocrine disrup ters on rep-tiles may result in demographic shifts whose consequencesfor populations are presumably detrimental Population-level effects might also occur through changes to patternsof individual energy allocation For example in coal-ashpolluted wetlands water snakes (Nerodia fasciata) withhigh body burdens of metal contaminants exhibit elevatedmetabolic rates which may result in less energy beingdevoted to reproduction growth and storage (Hopkins etal 1999)

Di sea se and pa ra s i ti s mParasites and disease have been documented or suspectedas causes for declines in some amphibian species (Daszaket al 1999) In some cases sublethal environmental stres-sors may suppress immune systems (Carey 1993) andallow disease agents to kill weakened animals (Alford andRichards 1999) Recently however a spreading ldquoextinctionwaverdquo of chytrid fungus is thought to be causing thedecline of anurans in Central America and Australia(Berger et al 1998 Lips 1999) moreover researchersbelieve that the fungus is killing otherwise healthy animals(Daszak et al 1999) An iridovirus may be the primarycause of the periodic population crashes in the Sonora

August 2000 Vol 50 No 8 BioScience 657

Articles

Ha bitat loss and degra d a tion are pri m a ry threats to bot ha m p h i bian and reptile popu l a ti o n s Co nversion ofwet 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 gterre s trial habitat to agri c u l tu ral (ill u s tra ted here) andot h er uses have re su l ted in wetland losses exceeding 80in many state s

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 nowbelieve that disease may rival habitat destruction as thelargest single cause o f the decline of amphibians

Among reptiles the widespread upper respiratory tractdisease a contagious respiratory ailment caused by thebacterium Mycoplasma agassizii is a potential cause ofpopulation declines in desert tortoises in the US South-west and gopher tortoises in the Southeast (Jacobson1993 Smith et al 1998)Shell diseases have been implicat-ed in the decline of turtles (eg shell lesions on slidersLovich et al 1996 cutaneous dyskeratosis affecting theshell and thickened forelimb scutes of desert tortoisesJacobson 1994 and emaciation and lesions of the plastronof federally listed flattened musk turtles Sternotherusdepressus Dodd 1988) Individuals in many green sea tur-tle populations are severely affected by viral fibropapillo-mas resulting in growths that can impair vision locomo-tionand feeding ability (Herbst 1994) As is often the casein amphibiansdiseases that are debilitating to wild popu-lations of reptiles are most likely secondary expressions inindividuals with impaired resistance caused by one ormore primary environmental stressors such as habitatdegradation invasive species or pollution

Un su s t a i n a ble useHuman use of animalsincluding reptiles and amphibiansis an integral part of many cultures Harvesting must bebi 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 andspecies are to persist (Pough et al 1998) Overcollectionfor food the pet trade and biological supply houses hasbeen suggested as having had an impact on some amphib-ian populations (Dodd 1997) In the United States note-worthy examples for amphibians occurred in the late1800s to early 1900s when commercial collectors harvest-ed for the frog legs market Hundreds of thousands of

red - l egged frogs (Rana auro ra drayto 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 frogsalthough itis 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 al1994) In Indiathe 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 illegallyeach 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 onsu 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 havebeen more perva s ive and severe than on amph i bians (eg s ee Wi lliams 1999) The severi ty of the tu rtle crisis on agl obal scale was em ph a s i zed by Rh odin (1999) wh oreported that of the approx i m a tely 293 taxa (mainlys 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 thelast few cen tu ri e s 3 (9 taxa) are alre ady ex ti n ct in thewi 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 foodsource Moreover the international trade in turtlesmdashwhich are eaten sold as pets or used in traditional Chi-nese medicinal remediesmdashis both extensive and unregu-lated (Sharma 1999) A recent report indicated that mostturtle sp ecies in Vietnam and southern China are endan-gered and that turtles can no longer be found in the wildin Vietnam (Kiester and Juvik 1997) China is the biggestconsumer of turtles in the food trade Because the trade inturtles is not regulated few records have been kept butexisting records indicate that the trade in live turtles toChina is thousands of tons per year (Mockenhaupt 1999)The commercial trade in freshwater turtles exceeds anypossible sustainable levels and extinction of some speciesin the wild can be expected within the next decade

Most species of sea turtles continue to decline in allwarm oceans of the world The leatherback sea turtle(Dermochelys coriacea) was recently reported to be ldquoon theroad to extinction and further population declines can beexpectedrdquounless appropriate measures are taken to reducemortality rates in adults hatchlings and eggs (Spotila eta l 1 9 9 6 ) The esti m a ted worl dwi de pop u l a ti on ofleatherbacks nesting on beaches in 1980 was 115000com p a red with just 34500 in 1995 Ex p l oi t a ti on ofleatherbacks in the Atlantic Ocean through illegal har-vesting of both adults and eggsis considered to be a majorcontributor to the decline of the species (Spotila et al1996) Likewise for Kemprsquos Ridley sea turtle (Lepidochelys

658 BioScience August 2000 Vol 50 No 8

Articles

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

kempii) harvests of nesting females and their eggs on thelargest known nesting site contributed to declines from42000 nesting females in 1947 to only a few hundred by1975 (Hildebrand 1982)

Among North American turtles the diamondback ter-rapin (Ma l a cl emys terra p i n) a small e s tu a rine tu rt l especies with a geographic range from Cape Cod to Texasdecl i n ed severely fo ll owing heavy ex p l oi t a ti on as agourmet food item from the late 1800s to the early 1900s(Carr 1952) With forced reductions in harvesting manypopulations were able to recover but the terrapin nowfaces significant new threats including highway mortality(Wood and Herlands 1997) and drowning in commercialand recreational crab traps (Bishop 1983 Roosenburg1991) Renewed commercial har vest of the diamondbackterrapin has also been documented (Garber 1988)

Commercial turtle trappers for the restaurant tradestepped up harvests of one of the largest freshwater turtlesin the world the alligator snapper (Macroclemys tem -minckii) from the 1960s through the 1980s (Roman et al1999) Consequently as evidence from survey efforts sug-gests the species has b een drastical ly reduced in numbersin some of the southeastern US rivers it once inhabited(Moler 1992 Jensen 1998)

The enormous and once common populations of thearrau (Podocnemis expansa) a communally nesting turtleof the Orinoco and Amazon Rivers in South America arenow greatly reduced in size because of human consump-tion of eggs and nesting females (Pritchard and Trebbau1984) an overexploitation problem identified almost twocenturies ago (Humboldt 1814 from Pritchard and Treb-bau 1984) Declines from similar causes have befallen theterecay (Podocnemis unifilis) in tropical lowlands of SouthAmerica (Thorbjarnarson et al 1993) and the river ter-rapin (Batagur baska) in India (Bhupathy 1997)

Overharvesting for food is a problem not just for turtlesbut also for lizardshaving contributed to declines in greeniguanas (Iguana iguana) and spiny - t a i l ed iguanas(Ctenosaura similis) in tropical America (Fitch et al1982)

The pet trade appears especially hazardous for someturtle sp ecies In 1994 population declines were reportedin box turtles (Terrapene carolina) in 16 states rangingfrom Massachusetts to Florida and Oklahoma to Wiscon-sin (Lieberman 1994) Doc u m en t a ti on of box tu rt l edecl i n e s mdash i n cluding records showing that s i n ce 199529896 box turtles had been collected for the pet trade andshipped from Louisianamdashresulted in unanimous passageof Act 81 by the Louisiana Senate and House of Represen-tatives in 1999the act prohibits the commercial harvest ofthe statersquos native box turtle populations Overcollection forexport is a serious factor in much of the box turtle declineand may exacerbate the effects of habitat loss (Lieberman1994) Habitat destruction and illegal collecting for the pettrade are the primary threats to bog turtles (Clemmysmuhlenbergii) Copeyon 1997) The number of northernpopulations has been reduced by 50 with most of the

decline occurring over the last 20 years Of the 191remaining bog turtle habitats known in 199633 were clas-sified as in good condition 67 as fair and 76 as poor thestatus of 15 was unknown

Overcollecting is also a problem for some snake speciesThe ocellated mountain viper (Vipera wagneri) in easternTurkey has been sought by the pet trade and removedfrom the wild in large numbers posing ldquoa serious threat tosurvival of the speciesrdquo (Nilson et al 1990) Populations ofseveral boa and python species have declined because ofharvesting of wild snakes for their skins (Pough et al1998) Rapid declines o f large-bodied snakes which tendto have a suite of life-history traits that make them moresusceptible to population declines than smaller species(eg Dodd 1993)have been documented throughout theworld in recent years (egShine and Fitzgerald 1996) Forexample females of the increasingly rare timber rat-tlesnake (Crotalus horridus) which may exceed a meter inlength and typically take 9 years to reach maturity pro-duce fewer than a dozen young every 3 years (Brown1993)Large-bodied species such as rattlesnakes (Crotalus)have long generation times a life-history t rait that whencom bi n ed with habitat loss human pers ec uti on a n di n ten s ive overco ll ecti on (eg ldquora t t l e s n a ke ro u n du p srdquo Brown 1993)has led to dramatic declines of some speciesand ma de approximately one-third of rattlesnake sp eciesvulnerable to extinction (Greene 1997) High harvest ratesof snakes with low reproductive frequencies such as thef 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 dalmost certainly be unsustainable (Shine et al 1995)

August 2000 Vol 50 No 8 BioScience 659

Articles

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

These examples demonstrate that sustainable use ofsome long-lived reptile species is problematic Becauselongevity in reptiles is associated with delayed sexualm a tu ri ty h i gh adult su rvivors h i p and low fec u n d i ty(Pough et al1998) populations of long-lived species can-not remain stable (or grow) when adults and older juve-niles are harvested at high rates (Congdon et al 19931994) This is not to say however that all such long-livedspecies should be commercially 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 (Ross1998) and unsustainable harvest of adults for the leathertrade (Brazaitis 1989) After years of total protection sev-eral sp ecies have recovered a f ew are farmed or ranchedcommercially (King 1989) In some crocodile speciesadult females are protected and only small numbers ofeggs small juveniles and larger males are removed fromthe wild (King 1989) In contrast 7ndash8 of all alligatorsmore than 12 m in length are harvested annually in someFlorida populations (David et al1996) In additiona 50annual harvest rate of alligator eggs or hatchlings isallowed because removal at these life stages does notreduce recruitment into adult-size classes (Rice et al1999) Closely monitored alligator populations and pre-sumably populations of other long-lived species of rep-tiles can sustain the legal regulated harvest of some pro-porti on of eggs h a tch l i n gs or adults with negl i gi bl eeffects

G l obal cl i m a te ch a n geFew ecologists will dispute the link between increases ingreenhouse gases and gl obal tem pera tu re Howeverwhether the current rate of climate change reflects naturalvariation or has an anthropogenic cause is hotly debatedFor the purposes of this article we accept the argumentthat the earth is undergoing unprecedented rapid climaticchange (Schneider and Root 1998) that includes alter-ations in climate variables such as temperature and rain-fall patterns storm severity and storm frequency If oneaccepts that human-induced climate change is occurring(eg Vinnikov et al1999)then the consequences for her-petofaunal diversity can be addressed

The obvious effects of climate change on biodiversityare mediated through changes in habitat For exampleglobal warming may further diminish prairie wetlandhabitat in the United States (Poiani and Johnson 1991)Future wetland acreage in the United States may be great-ly reduced under a variety of climate circulation models(Halpin 1997) and aquatic and semiaquatic species willsuffer declines as habitat disappears Although many habi-tats are ex pected to under go dra m a tic ch a n ge (eg Guertin et al1997Still et al 1999) predictions of specieshabitat shifts in response to global warming cannot be

based solely on analyses of climatendashspace changes becausespecies distributions are also a function of dispersal abili-ty and biotic interactions (Davis et al 1998) Existingnature reserves will be inadequate to preserve current bio-diversity because an already fragmented landscape willi 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 theirlimited dispersal abilities reptiles and amphibians areespecially vulnerable to rapid habitat changes and maysuffer many more extinctions than birds as a result of arapid rate of climate change (Schneider and Root 1998)

In discussions of observed amphibian declines littlemention has been made of climate change (Dodd 1997)with two notable exceptions First the famed golden toad(Bufo periglenes) extinction in Costa Rica may have b eencausedat 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 changepatterns of cloud formation and thereby the availability ofwater (Still et al 1999) Second Blaustein et al (1994a)have suggested that ultraviolet B (UVB) radiation hasadverse effects on some amphibians including reducedhatching success and decreased survival to metamorpho-sis However an increase in the level of UVB caused bydepletion of the ozone layer probably does not pose ani m m ed i a te threat to reptile eggs wh i ch are sel domexposed to UVB radiation

As with the amphibian studies few researchers havedirectly assessed effects of climate change on r eptiles It isnonetheless reasonable to expect that climate changescould re sult in con d i ti ons that el i m i n a te or severelyrestrict sp ecies with limited dist ributions (Schneider andRoot 1998) as has been suggested for some Australianlizards (Brereton et al1995) and crotaline snakes of NorthAmerica and the neotropics (Greene and Campbell 1993)Additional effects of warming on some reptiles based onem p i rical evi den ce with fre s hw a ter tu rt l e s i n clu deenhanced juvenile growth rates earlier ages at maturityand shifts in functional sex ratios (Frazer et al 1993)Global warming may have the greatest impact on thosereptiles (crocodilians and some turtles) that have temper-ature-dependent sex determination (Janzen 1994) where-by the sex ratio of the hatchlings is determined by nesttemperatures during incubation Unless shifts occur in thepivotal temperatures at which sex is determined or femalenest-site choices (ie shade versus sun) evolve to keeppace with rising temperatures altered sex ratios couldaffect population demographics and persistence

En i gm a tic decl i n e sFinally in addition to the many cases of declines that haves ome re a s on a bly unders tood causes s ome amph i bi a npopulations have declined and even gone extinct withoutany discernible causes One well-known example is thegastric 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 ofparental care in which the young develop in the safety ofthe motherrsquos stomach (Tyler and Carter 1981) the gastricbrooding frog ceased to be found in nature Disjunct pop-ulations of the g reen salamand er (Aneides aeneus ) in thes o ut h ern App a l achians have app a ren t ly decl i n ed butwithout similar declines in other portions of its range (JeffCorser USGS-BRD Twin Creeks Resource Center GSM-NP Gatlinburg TN personal communication)

Similar cases exist for reptiles For example no livingspecimen of the Round Island burrowing boa (Bolyeriamultocarinata) in the Indian Ocean has been seen since1975 (Bullock 1986) the species may have become extinctin recent decades (Greene 1997) Although all species ofreptiles native to North America in precolonial times per-sist in some regions the current ranges of many are but aremnant of the much larger areas formerly occupied Nat-ural populations of indigo snakes have not been found insome regions of their historic range in more than 40 years(Mount 1975 Conant and Collins 1998)and the species isldquodeclining in abundance and distribution throughout itsUS geographic rangerdquo (Hallam et al 1998) Likewises i gh ti n gs of the sout h ern hognose snake (Heterod o nsimus) 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 ) evenin 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 sRegrettably many amphibian populations and species thatare thought to be declining have not been monitored overlong 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 commoncharacteristic The subjects of these studies occur in highdensity either spatially (eg Jordanrsquos salamander Plethod -on jordanii Hairston 1987) or temporally (eg mole sala-manders Ambystoma talpoideum Pechmann et al 1991and natterjack toads Bufo calamita Banks et al 1994)

Many of the species that have become symbols for thedeclining amphibian phenomenon are seasonally activeanurans that arrive over restricted periods of time atbreeding sites where they congregate in greater densitiesthan at any other time of the year Researchers sit ready torecord their arrival and abundance and if the animals failto show up when expecteda problem is suspected if suchabsences are protracted then the change is presumablyreal (Blaustein et al 1994c) The phenology of theseamphibians permits detection of breeding activity there-fore determination of whether the absence of breedingadults is a short-term aberration or an indication of a realdecline becomes a matter of accumulating the data neces-sary to demonstrate a statistically significant trend (fordiscussion see Blaustein et al 1994c Pechmann andWilbur 1994 Reed and Blaustein 1995)

Among reptiles declines in sea turtles are perhaps the

best documented because like many amphibians theyengage in an annual reproductive event (in this caseoviposition) with a predictable site and time A few snakespecies in colder temperate regions are known to hiber-nate communally and numbers can be assessed upon

emergence (Parker and Brown 1973) But what of themajority of reptile species that do not congregate to breedor hibernate and do not occur in particularly high densi-ties F or example the r acer (Coluber const rictor) a com-mon North American snake is found in a wide variety ofterrestrial habitats Like most other ectotherms racers aremore active and therefore more commonly encounteredin the warmer months However aside from some regionswhere communal hibernation occurs (Parker and Brown1973) determining the abundance of racers is difficultbecause 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 howcould we take a census to know when and if racer popula-tions were declining at a substantial rate on a widespread

August 2000 Vol 50 No 8 BioScience 661

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

basis without mounting an intensive long-term samplingprogram The clandestine nature of many reptiles oftencombined with comparatively large home ranges lowpop u l a ti on den s i ti e s and ra reness of con grega ti on a lbehavior makes documenting population trends very dif-ficult As a result populations may wither with littlenoticeOnce an unmonitored species or population is rec-ognized as being unexpectedly depauperate or absent thecause of decline may be unknown and unknowable

Based on the accumulated evidence that many if notmost declines reported for amphibians are indeed realtheproper course for conservation initiatives is to assume theworst for all herpetofauna and therefore to implementabatement measures while gathering more data Althoughthe lack of long-term data often may preclude the id enti-fication of the cause of a decline or even in some cases thecorroboration o f a decline the absence of that data doesnot rule out the existence of a correctable problem

Co n clusion and re co m m en d a ti o n sThe declines of m a ny reptile pop u l a ti ons are similar tothose 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 ha m ph i bi a n s the causes are known with cert a i n ty ins ome instance s su s pected in many and unknown ino t h ers Some ex ti rp a ti ons are local wh ereas others arem ore wi de s pre ad The difficulty in doc u m en ting thes 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 causesof pop u l a ti on declines can be obvi a ted direct ly Th ei 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 ingeneral (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 ofinvasive non-native species that could be harmful to rep-tile populations must be proscribed Third restrictingtrade in sensitive reptile species for which sustainableremoval cannot be demonstrated will require the passageor strengthening and enforcement of legislation In thecase of Asian turtles legislative remedies could be too lit-tle too latemdasha stopgap remedy is necessary The only wayto prevent the imminent extinction of a large number ofthe more than 80 species of turtles native to southern Asiawill be to maintain populations in ex situ captive breedingand genetic reserve programs With changes in culturalattitudesstrengthening of international trade regulationsand increased habitat protection the reintroduction ofthese species into the wild may be possible

Much of todayrsquos commercial exploitation of reptiles inthe United States and elsewhere requires urgent govern-mental action to implement internationally accepted andenforced controls Despite the fact that conservation mea-sures can be implemented effectively through legislation(as happened with legislation for protection of Louisianabox turtles and American alligators) the political pres-sures against accomplishing such goals cannot be overstat-ed The lack of support by the World Trade Organizationfor recommendations to curtail sea turtle exploitation(WTO 1998) brings the problem into perspective on aninternational scale

Direct and indirect effects of environmental pol lutiondisease and parasitism and global climate change aremore difficult to quantify in many instances and will bemore difficult to change in the short term Nonetheless wemust endeavor to understand these potential factors toameliorate their impact on natural populations of reptilesand their habitats

Finally long-term monitoring o f reptile populations isessential and must be aided by the establishment of stan-dard methods and techniques It is equally important thatthe academic community land managers and conserva-tion organizations recognize that rigorous field programsfocusing on the distri buti on a bu n d a n ce s t a tu s a n dtrends of populations and species are critical and worth-while Herpetofaunal inventories should become a stan-dard part of environmental assessment programs and thepublication of field survey efforts that document potentialor suspected declines should be encouraged When long-term and widespread monitoring becomes the normdeclines are likely to become less equivocal (in terms ofprotracted declines versus natural fluctuations) and thecauses less mysterious

662 BioScience August 2000 Vol 50 No 8

Articles

Sand monitor (Va ra nus go u l d i ) Al t h ou gh sandm o n i to rs (genus Va ra nu s wh i ch includes the wo rl d rsquo sl a rgest lizards) appear to be thriving in many pa rts oft h eir natu ral habitats in Au s tra l i a ot h er spe cies of t h egenus in As i a Afri c a and the East Indies are threa ten e dby exten s ive habitat destru cti o n

The disappearance of reptiles from the natural world isgenuine and should be a matter of concern not simplybecause of reptilesrsquo perceived associations with amphib-ians but because reptile declineslike those of amphibiansare growing and serious in their own right Current evi-dence suggests that amphibian and reptile declines whichare exacerbated by burgeoning human populations con-stitute a worldwide crisis

Ack n owl e d gm en t sManuscript preparation was aided by Financial AssistanceAw a rd Nu m ber DE-FC09-96SR18546 from the USDep a rtm ent of E n er gy to the Un ivers i ty of G eor gi aResearch Foundation We thank Ab Abercrombie JustinCongdon William Hopkins Laura Janecek ChristopherRomanek and Joseph Pechmann for discussion and com-ments on the manuscript We also appreciate the help ofStephen H Bennett John Cossel Jr Charles R PetersonPaul Moler Woody Woodwardand Jeff Corser for provid-ing information on the status of particular species Thispaper supports the PARC (Partners in Amphibian andReptile Conservation) effort to promote education aboutreptiles and amphibians

Ref eren ces ci te dAl 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 ndash 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 ndash 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 119 8 3 ndash 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 ndash 6 9

Banks B Beebee TJC Coo ke KS 1 9 9 4 Con s erva ti on of the natter jack toadB u fo calamita in Britain over the peri od 1976ndash1990 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 ndash 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 eRe 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 eUn i ted States of Am erica 95 9 0 3 1 ndash 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 ndash 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 rba 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 ndash 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 ofE nvi ron m ental Con t a m i n a ti on Tox i co l ogy 27 8 2 ndash 8 7

Bi s h op JM1 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 ndash 4 3 0

Bl a u s tein A R Hoffman PD Hokit DG Ki e s ecker JM Wa lls SC Hays JB1 9 9 4 a UV repair and re s i s t a n ce to solar UV-B in amph i bian eggs Alink to pop u l a ti on declines Proceed i n gs of the Na ti onal Ac ademy ofS c i en ce of the Un i ted States of Am erica 91 1 7 9 1 ndash 1 7 9 5

Bl a u s tein A R Hokit DG Orsquo Ha ra RK Holt RA 1 9 9 4 b Pa t h ogenic funguscon tri butes to amph i bian losses in the Pacific Nort hwe s t Bi o l ogi c a lCon s erva ti on 67 2 5 1 ndash 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 gs 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 andgl obal ex ti n cti on s Con s erva ti on Bi o l ogy 8 6 0 ndash 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 196ndash201 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 tech 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 ndash 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 theS tu dy of Am ph i bians and Repti l e s Herpeto l ogy Ci rc u l a ti on 22 1 ndash 7 2

Buhlmann KA 1 9 9 5 Ha bitat use terre s trial movem ents and con s erva ti onof 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 ogy2 9 1 7 3 ndash 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 201ndash232 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 amp 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 dIsland and Gu n n er rsquos Quoi n Ma u ri tiu s Bi o l ogical Con s erva ti on 371 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 ndash 1 3 6 9

Ca rey C 1 9 9 3 Hypothesis con cerning the causes of the disappe a ra n ce ofboreal toads from the mountains of Co l orado Con s erva ti on Bi o l ogy 73 5 5 ndash 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 52 7 2 ndash 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 peRomain Na ti onal Wi l dl i fe Ref u ge Ch em o s ph ere 34 5 3 9 ndash 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 1ndash15 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 lm a tu ri ty and dem ogra phics of Bl a n d i n grsquos tu rtles (Emyd o i d e abl 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 ndash 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 ivedor ga n i s m s Am erican Zoo l ogist 34 3 9 7 ndash 4 0 8

[CITES] Conven ti on on In tern a ti onal Trade in Endangered Species ofWild Fauna and Flora 2 0 0 0 lt 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 tmlgt (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 lrule to list the nort h ern pop u l a ti on of the bog tu rtle as thre a ten ed andthe 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 ndash 5 9 6 2 3

August 2000 Vol 50 No 8 BioScience 663

Articles

been reported to prey on both eggs (Moulis 1997) andyoung (Allen et al1997) of reptilesFire ants are implicat-ed as a primary cause of extirpation of the Texas hornedlizard (Phrynosoma cornutum) from part of its geographicrange (Goin 1992)

Invasive species need not be other animals Both thedesert tortoise (Gopherus agassizii) and the gopher tortoiseare threatened by the introduction of non-native plantspecies (Stewart et al 1993 Lovich 1995) that alter habitatstructure native plant community composition and evenfire frequency The black legless lizard (Anniella pulchranigra) was considered for federal endangered status inpart because of the negative impact of non-native Hotten-tot fig plants on the lizardsrsquo prey base in disturbed sand-dune habitat (Rutherford and Rorabaugh 1995) nonethe-less an official decision was made not to list the speciesafter viable lizard populations were found in undisturbedhabitat with native vegetation (Morey 1998) In Idahoreptile sp ecies richness decreased an average o f 5 from1978 to 1998 at 24 sample sites in the Snake River Birds ofPrey Area (John Cossel Jr and Charles R Peterson IdahoState University Pocatello ID personal communication)According to Cossel and Peterson the changes in reptilepopulations may have been influenced by a decrease innative shrub habitat caused by the prevalence of exoticannual grasses and the effects of wildfires that have burnedover 50 of the area since the 1970s

Envi ro n m ental poll u ti o nNumerous environmental contaminantsmdashmetals pesti-cides and herbicidesand radioactive waste for examplemdashhave direct and indirect effects on both amphibians andreptiles (eg Hinton and Scott 1990 Hall and Henry1992) Amphibians have been the subject of numerousecotoxicological studiesincluding assessment of the directeffects of contaminants such as fertilizers (Marco et al1999) or the more subtle effects of steroid-mimicking con-taminants (Hayes 1997) Reptiles are studied far less thanamphibians with respect to the fate and effects of contam-inants (Hopkins et al 1999) but they have received suffi-cient toxicological study to provide convincing evidencethat some individual reptiles are adversely affected bymany contaminants (Hall 1980 Fontenot et al 1994) Forexampleslider turtles (Trachemys scripta) exposed to met-al and radioisotope contaminants incur genetic damage(Lamb et al 1995) The degree to which contaminantscause population-level effects remains largely unknownboth for amphibians and for reptiles

Contaminant effects in reptiles are known mainly fromturtles and crocodilians Many turtles and crocodiliansbecause they have environmental sex determination andlarge eggs that can incorporate high levels of environmen-tal pollutants are especially sensitive to endocrine-dis-rupting chemicals (Guillette and Crain 1996) At som econ 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 eggs (Bishop et al 1994 Cobb and Wood 1997) sexreversal and abnormal gonads have been found in turtlesexposed to PCBs (Bergeron et al 1994 Guillette et al1995) Male American alligators (Alligator mississippiensis)inhabiting Lake Apopka a chemically contaminated lakein Florida had significantly reduced plasma testosteronelevels and permanent gonadal alterations (Guillette et al1994)

Even nonlethal effects o f endocrine disrup ters on rep-tiles may result in demographic shifts whose consequencesfor populations are presumably detrimental Population-level effects might also occur through changes to patternsof individual energy allocation For example in coal-ashpolluted wetlands water snakes (Nerodia fasciata) withhigh body burdens of metal contaminants exhibit elevatedmetabolic rates which may result in less energy beingdevoted to reproduction growth and storage (Hopkins etal 1999)

Di sea se and pa ra s i ti s mParasites and disease have been documented or suspectedas causes for declines in some amphibian species (Daszaket al 1999) In some cases sublethal environmental stres-sors may suppress immune systems (Carey 1993) andallow disease agents to kill weakened animals (Alford andRichards 1999) Recently however a spreading ldquoextinctionwaverdquo of chytrid fungus is thought to be causing thedecline of anurans in Central America and Australia(Berger et al 1998 Lips 1999) moreover researchersbelieve that the fungus is killing otherwise healthy animals(Daszak et al 1999) An iridovirus may be the primarycause of the periodic population crashes in the Sonora

August 2000 Vol 50 No 8 BioScience 657

Articles

Ha bitat loss and degra d a tion are pri m a ry threats to bot ha m p h i bian and reptile popu l a ti o n s Co nversion ofwet 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 gterre s trial habitat to agri c u l tu ral (ill u s tra ted here) andot h er uses have re su l ted in wetland losses exceeding 80in many state s

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 nowbelieve that disease may rival habitat destruction as thelargest single cause o f the decline of amphibians

Among reptiles the widespread upper respiratory tractdisease a contagious respiratory ailment caused by thebacterium Mycoplasma agassizii is a potential cause ofpopulation declines in desert tortoises in the US South-west and gopher tortoises in the Southeast (Jacobson1993 Smith et al 1998)Shell diseases have been implicat-ed in the decline of turtles (eg shell lesions on slidersLovich et al 1996 cutaneous dyskeratosis affecting theshell and thickened forelimb scutes of desert tortoisesJacobson 1994 and emaciation and lesions of the plastronof federally listed flattened musk turtles Sternotherusdepressus Dodd 1988) Individuals in many green sea tur-tle populations are severely affected by viral fibropapillo-mas resulting in growths that can impair vision locomo-tionand feeding ability (Herbst 1994) As is often the casein amphibiansdiseases that are debilitating to wild popu-lations of reptiles are most likely secondary expressions inindividuals with impaired resistance caused by one ormore primary environmental stressors such as habitatdegradation invasive species or pollution

Un su s t a i n a ble useHuman use of animalsincluding reptiles and amphibiansis an integral part of many cultures Harvesting must bebi 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 andspecies are to persist (Pough et al 1998) Overcollectionfor food the pet trade and biological supply houses hasbeen suggested as having had an impact on some amphib-ian populations (Dodd 1997) In the United States note-worthy examples for amphibians occurred in the late1800s to early 1900s when commercial collectors harvest-ed for the frog legs market Hundreds of thousands of

red - l egged frogs (Rana auro ra drayto 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 frogsalthough itis 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 al1994) In Indiathe 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 illegallyeach 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 onsu 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 havebeen more perva s ive and severe than on amph i bians (eg s ee Wi lliams 1999) The severi ty of the tu rtle crisis on agl obal scale was em ph a s i zed by Rh odin (1999) wh oreported that of the approx i m a tely 293 taxa (mainlys 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 thelast few cen tu ri e s 3 (9 taxa) are alre ady ex ti n ct in thewi 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 foodsource Moreover the international trade in turtlesmdashwhich are eaten sold as pets or used in traditional Chi-nese medicinal remediesmdashis both extensive and unregu-lated (Sharma 1999) A recent report indicated that mostturtle sp ecies in Vietnam and southern China are endan-gered and that turtles can no longer be found in the wildin Vietnam (Kiester and Juvik 1997) China is the biggestconsumer of turtles in the food trade Because the trade inturtles is not regulated few records have been kept butexisting records indicate that the trade in live turtles toChina is thousands of tons per year (Mockenhaupt 1999)The commercial trade in freshwater turtles exceeds anypossible sustainable levels and extinction of some speciesin the wild can be expected within the next decade

Most species of sea turtles continue to decline in allwarm oceans of the world The leatherback sea turtle(Dermochelys coriacea) was recently reported to be ldquoon theroad to extinction and further population declines can beexpectedrdquounless appropriate measures are taken to reducemortality rates in adults hatchlings and eggs (Spotila eta l 1 9 9 6 ) The esti m a ted worl dwi de pop u l a ti on ofleatherbacks nesting on beaches in 1980 was 115000com p a red with just 34500 in 1995 Ex p l oi t a ti on ofleatherbacks in the Atlantic Ocean through illegal har-vesting of both adults and eggsis considered to be a majorcontributor to the decline of the species (Spotila et al1996) Likewise for Kemprsquos Ridley sea turtle (Lepidochelys

658 BioScience August 2000 Vol 50 No 8

Articles

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

kempii) harvests of nesting females and their eggs on thelargest known nesting site contributed to declines from42000 nesting females in 1947 to only a few hundred by1975 (Hildebrand 1982)

Among North American turtles the diamondback ter-rapin (Ma l a cl emys terra p i n) a small e s tu a rine tu rt l especies with a geographic range from Cape Cod to Texasdecl i n ed severely fo ll owing heavy ex p l oi t a ti on as agourmet food item from the late 1800s to the early 1900s(Carr 1952) With forced reductions in harvesting manypopulations were able to recover but the terrapin nowfaces significant new threats including highway mortality(Wood and Herlands 1997) and drowning in commercialand recreational crab traps (Bishop 1983 Roosenburg1991) Renewed commercial har vest of the diamondbackterrapin has also been documented (Garber 1988)

Commercial turtle trappers for the restaurant tradestepped up harvests of one of the largest freshwater turtlesin the world the alligator snapper (Macroclemys tem -minckii) from the 1960s through the 1980s (Roman et al1999) Consequently as evidence from survey efforts sug-gests the species has b een drastical ly reduced in numbersin some of the southeastern US rivers it once inhabited(Moler 1992 Jensen 1998)

The enormous and once common populations of thearrau (Podocnemis expansa) a communally nesting turtleof the Orinoco and Amazon Rivers in South America arenow greatly reduced in size because of human consump-tion of eggs and nesting females (Pritchard and Trebbau1984) an overexploitation problem identified almost twocenturies ago (Humboldt 1814 from Pritchard and Treb-bau 1984) Declines from similar causes have befallen theterecay (Podocnemis unifilis) in tropical lowlands of SouthAmerica (Thorbjarnarson et al 1993) and the river ter-rapin (Batagur baska) in India (Bhupathy 1997)

Overharvesting for food is a problem not just for turtlesbut also for lizardshaving contributed to declines in greeniguanas (Iguana iguana) and spiny - t a i l ed iguanas(Ctenosaura similis) in tropical America (Fitch et al1982)

The pet trade appears especially hazardous for someturtle sp ecies In 1994 population declines were reportedin box turtles (Terrapene carolina) in 16 states rangingfrom Massachusetts to Florida and Oklahoma to Wiscon-sin (Lieberman 1994) Doc u m en t a ti on of box tu rt l edecl i n e s mdash i n cluding records showing that s i n ce 199529896 box turtles had been collected for the pet trade andshipped from Louisianamdashresulted in unanimous passageof Act 81 by the Louisiana Senate and House of Represen-tatives in 1999the act prohibits the commercial harvest ofthe statersquos native box turtle populations Overcollection forexport is a serious factor in much of the box turtle declineand may exacerbate the effects of habitat loss (Lieberman1994) Habitat destruction and illegal collecting for the pettrade are the primary threats to bog turtles (Clemmysmuhlenbergii) Copeyon 1997) The number of northernpopulations has been reduced by 50 with most of the

decline occurring over the last 20 years Of the 191remaining bog turtle habitats known in 199633 were clas-sified as in good condition 67 as fair and 76 as poor thestatus of 15 was unknown

Overcollecting is also a problem for some snake speciesThe ocellated mountain viper (Vipera wagneri) in easternTurkey has been sought by the pet trade and removedfrom the wild in large numbers posing ldquoa serious threat tosurvival of the speciesrdquo (Nilson et al 1990) Populations ofseveral boa and python species have declined because ofharvesting of wild snakes for their skins (Pough et al1998) Rapid declines o f large-bodied snakes which tendto have a suite of life-history traits that make them moresusceptible to population declines than smaller species(eg Dodd 1993)have been documented throughout theworld in recent years (egShine and Fitzgerald 1996) Forexample females of the increasingly rare timber rat-tlesnake (Crotalus horridus) which may exceed a meter inlength and typically take 9 years to reach maturity pro-duce fewer than a dozen young every 3 years (Brown1993)Large-bodied species such as rattlesnakes (Crotalus)have long generation times a life-history t rait that whencom bi n ed with habitat loss human pers ec uti on a n di n ten s ive overco ll ecti on (eg ldquora t t l e s n a ke ro u n du p srdquo Brown 1993)has led to dramatic declines of some speciesand ma de approximately one-third of rattlesnake sp eciesvulnerable to extinction (Greene 1997) High harvest ratesof snakes with low reproductive frequencies such as thef 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 dalmost certainly be unsustainable (Shine et al 1995)

August 2000 Vol 50 No 8 BioScience 659

Articles

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

These examples demonstrate that sustainable use ofsome long-lived reptile species is problematic Becauselongevity in reptiles is associated with delayed sexualm a tu ri ty h i gh adult su rvivors h i p and low fec u n d i ty(Pough et al1998) populations of long-lived species can-not remain stable (or grow) when adults and older juve-niles are harvested at high rates (Congdon et al 19931994) This is not to say however that all such long-livedspecies should be commercially 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 (Ross1998) and unsustainable harvest of adults for the leathertrade (Brazaitis 1989) After years of total protection sev-eral sp ecies have recovered a f ew are farmed or ranchedcommercially (King 1989) In some crocodile speciesadult females are protected and only small numbers ofeggs small juveniles and larger males are removed fromthe wild (King 1989) In contrast 7ndash8 of all alligatorsmore than 12 m in length are harvested annually in someFlorida populations (David et al1996) In additiona 50annual harvest rate of alligator eggs or hatchlings isallowed because removal at these life stages does notreduce recruitment into adult-size classes (Rice et al1999) Closely monitored alligator populations and pre-sumably populations of other long-lived species of rep-tiles can sustain the legal regulated harvest of some pro-porti on of eggs h a tch l i n gs or adults with negl i gi bl eeffects

G l obal cl i m a te ch a n geFew ecologists will dispute the link between increases ingreenhouse gases and gl obal tem pera tu re Howeverwhether the current rate of climate change reflects naturalvariation or has an anthropogenic cause is hotly debatedFor the purposes of this article we accept the argumentthat the earth is undergoing unprecedented rapid climaticchange (Schneider and Root 1998) that includes alter-ations in climate variables such as temperature and rain-fall patterns storm severity and storm frequency If oneaccepts that human-induced climate change is occurring(eg Vinnikov et al1999)then the consequences for her-petofaunal diversity can be addressed

The obvious effects of climate change on biodiversityare mediated through changes in habitat For exampleglobal warming may further diminish prairie wetlandhabitat in the United States (Poiani and Johnson 1991)Future wetland acreage in the United States may be great-ly reduced under a variety of climate circulation models(Halpin 1997) and aquatic and semiaquatic species willsuffer declines as habitat disappears Although many habi-tats are ex pected to under go dra m a tic ch a n ge (eg Guertin et al1997Still et al 1999) predictions of specieshabitat shifts in response to global warming cannot be

based solely on analyses of climatendashspace changes becausespecies distributions are also a function of dispersal abili-ty and biotic interactions (Davis et al 1998) Existingnature reserves will be inadequate to preserve current bio-diversity because an already fragmented landscape willi 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 theirlimited dispersal abilities reptiles and amphibians areespecially vulnerable to rapid habitat changes and maysuffer many more extinctions than birds as a result of arapid rate of climate change (Schneider and Root 1998)

In discussions of observed amphibian declines littlemention has been made of climate change (Dodd 1997)with two notable exceptions First the famed golden toad(Bufo periglenes) extinction in Costa Rica may have b eencausedat 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 changepatterns of cloud formation and thereby the availability ofwater (Still et al 1999) Second Blaustein et al (1994a)have suggested that ultraviolet B (UVB) radiation hasadverse effects on some amphibians including reducedhatching success and decreased survival to metamorpho-sis However an increase in the level of UVB caused bydepletion of the ozone layer probably does not pose ani m m ed i a te threat to reptile eggs wh i ch are sel domexposed to UVB radiation

As with the amphibian studies few researchers havedirectly assessed effects of climate change on r eptiles It isnonetheless reasonable to expect that climate changescould re sult in con d i ti ons that el i m i n a te or severelyrestrict sp ecies with limited dist ributions (Schneider andRoot 1998) as has been suggested for some Australianlizards (Brereton et al1995) and crotaline snakes of NorthAmerica and the neotropics (Greene and Campbell 1993)Additional effects of warming on some reptiles based onem p i rical evi den ce with fre s hw a ter tu rt l e s i n clu deenhanced juvenile growth rates earlier ages at maturityand shifts in functional sex ratios (Frazer et al 1993)Global warming may have the greatest impact on thosereptiles (crocodilians and some turtles) that have temper-ature-dependent sex determination (Janzen 1994) where-by the sex ratio of the hatchlings is determined by nesttemperatures during incubation Unless shifts occur in thepivotal temperatures at which sex is determined or femalenest-site choices (ie shade versus sun) evolve to keeppace with rising temperatures altered sex ratios couldaffect population demographics and persistence

En i gm a tic decl i n e sFinally in addition to the many cases of declines that haves ome re a s on a bly unders tood causes s ome amph i bi a npopulations have declined and even gone extinct withoutany discernible causes One well-known example is thegastric 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 ofparental care in which the young develop in the safety ofthe motherrsquos stomach (Tyler and Carter 1981) the gastricbrooding frog ceased to be found in nature Disjunct pop-ulations of the g reen salamand er (Aneides aeneus ) in thes o ut h ern App a l achians have app a ren t ly decl i n ed butwithout similar declines in other portions of its range (JeffCorser USGS-BRD Twin Creeks Resource Center GSM-NP Gatlinburg TN personal communication)

Similar cases exist for reptiles For example no livingspecimen of the Round Island burrowing boa (Bolyeriamultocarinata) in the Indian Ocean has been seen since1975 (Bullock 1986) the species may have become extinctin recent decades (Greene 1997) Although all species ofreptiles native to North America in precolonial times per-sist in some regions the current ranges of many are but aremnant of the much larger areas formerly occupied Nat-ural populations of indigo snakes have not been found insome regions of their historic range in more than 40 years(Mount 1975 Conant and Collins 1998)and the species isldquodeclining in abundance and distribution throughout itsUS geographic rangerdquo (Hallam et al 1998) Likewises i gh ti n gs of the sout h ern hognose snake (Heterod o nsimus) 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 ) evenin 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 sRegrettably many amphibian populations and species thatare thought to be declining have not been monitored overlong 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 commoncharacteristic The subjects of these studies occur in highdensity either spatially (eg Jordanrsquos salamander Plethod -on jordanii Hairston 1987) or temporally (eg mole sala-manders Ambystoma talpoideum Pechmann et al 1991and natterjack toads Bufo calamita Banks et al 1994)

Many of the species that have become symbols for thedeclining amphibian phenomenon are seasonally activeanurans that arrive over restricted periods of time atbreeding sites where they congregate in greater densitiesthan at any other time of the year Researchers sit ready torecord their arrival and abundance and if the animals failto show up when expecteda problem is suspected if suchabsences are protracted then the change is presumablyreal (Blaustein et al 1994c) The phenology of theseamphibians permits detection of breeding activity there-fore determination of whether the absence of breedingadults is a short-term aberration or an indication of a realdecline becomes a matter of accumulating the data neces-sary to demonstrate a statistically significant trend (fordiscussion see Blaustein et al 1994c Pechmann andWilbur 1994 Reed and Blaustein 1995)

Among reptiles declines in sea turtles are perhaps the

best documented because like many amphibians theyengage in an annual reproductive event (in this caseoviposition) with a predictable site and time A few snakespecies in colder temperate regions are known to hiber-nate communally and numbers can be assessed upon

emergence (Parker and Brown 1973) But what of themajority of reptile species that do not congregate to breedor hibernate and do not occur in particularly high densi-ties F or example the r acer (Coluber const rictor) a com-mon North American snake is found in a wide variety ofterrestrial habitats Like most other ectotherms racers aremore active and therefore more commonly encounteredin the warmer months However aside from some regionswhere communal hibernation occurs (Parker and Brown1973) determining the abundance of racers is difficultbecause 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 howcould we take a census to know when and if racer popula-tions were declining at a substantial rate on a widespread

August 2000 Vol 50 No 8 BioScience 661

Articles

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

basis without mounting an intensive long-term samplingprogram The clandestine nature of many reptiles oftencombined with comparatively large home ranges lowpop u l a ti on den s i ti e s and ra reness of con grega ti on a lbehavior makes documenting population trends very dif-ficult As a result populations may wither with littlenoticeOnce an unmonitored species or population is rec-ognized as being unexpectedly depauperate or absent thecause of decline may be unknown and unknowable

Based on the accumulated evidence that many if notmost declines reported for amphibians are indeed realtheproper course for conservation initiatives is to assume theworst for all herpetofauna and therefore to implementabatement measures while gathering more data Althoughthe lack of long-term data often may preclude the id enti-fication of the cause of a decline or even in some cases thecorroboration o f a decline the absence of that data doesnot rule out the existence of a correctable problem

Co n clusion and re co m m en d a ti o n sThe declines of m a ny reptile pop u l a ti ons are similar tothose 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 ha m ph i bi a n s the causes are known with cert a i n ty ins ome instance s su s pected in many and unknown ino t h ers Some ex ti rp a ti ons are local wh ereas others arem ore wi de s pre ad The difficulty in doc u m en ting thes 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 causesof pop u l a ti on declines can be obvi a ted direct ly Th ei 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 ingeneral (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 ofinvasive non-native species that could be harmful to rep-tile populations must be proscribed Third restrictingtrade in sensitive reptile species for which sustainableremoval cannot be demonstrated will require the passageor strengthening and enforcement of legislation In thecase of Asian turtles legislative remedies could be too lit-tle too latemdasha stopgap remedy is necessary The only wayto prevent the imminent extinction of a large number ofthe more than 80 species of turtles native to southern Asiawill be to maintain populations in ex situ captive breedingand genetic reserve programs With changes in culturalattitudesstrengthening of international trade regulationsand increased habitat protection the reintroduction ofthese species into the wild may be possible

Much of todayrsquos commercial exploitation of reptiles inthe United States and elsewhere requires urgent govern-mental action to implement internationally accepted andenforced controls Despite the fact that conservation mea-sures can be implemented effectively through legislation(as happened with legislation for protection of Louisianabox turtles and American alligators) the political pres-sures against accomplishing such goals cannot be overstat-ed The lack of support by the World Trade Organizationfor recommendations to curtail sea turtle exploitation(WTO 1998) brings the problem into perspective on aninternational scale

Direct and indirect effects of environmental pol lutiondisease and parasitism and global climate change aremore difficult to quantify in many instances and will bemore difficult to change in the short term Nonetheless wemust endeavor to understand these potential factors toameliorate their impact on natural populations of reptilesand their habitats

Finally long-term monitoring o f reptile populations isessential and must be aided by the establishment of stan-dard methods and techniques It is equally important thatthe academic community land managers and conserva-tion organizations recognize that rigorous field programsfocusing on the distri buti on a bu n d a n ce s t a tu s a n dtrends of populations and species are critical and worth-while Herpetofaunal inventories should become a stan-dard part of environmental assessment programs and thepublication of field survey efforts that document potentialor suspected declines should be encouraged When long-term and widespread monitoring becomes the normdeclines are likely to become less equivocal (in terms ofprotracted declines versus natural fluctuations) and thecauses less mysterious

662 BioScience August 2000 Vol 50 No 8

Articles

Sand monitor (Va ra nus go u l d i ) Al t h ou gh sandm o n i to rs (genus Va ra nu s wh i ch includes the wo rl d rsquo sl a rgest lizards) appear to be thriving in many pa rts oft h eir natu ral habitats in Au s tra l i a ot h er spe cies of t h egenus in As i a Afri c a and the East Indies are threa ten e dby exten s ive habitat destru cti o n

The disappearance of reptiles from the natural world isgenuine and should be a matter of concern not simplybecause of reptilesrsquo perceived associations with amphib-ians but because reptile declineslike those of amphibiansare growing and serious in their own right Current evi-dence suggests that amphibian and reptile declines whichare exacerbated by burgeoning human populations con-stitute a worldwide crisis

Ack n owl e d gm en t sManuscript preparation was aided by Financial AssistanceAw a rd Nu m ber DE-FC09-96SR18546 from the USDep a rtm ent of E n er gy to the Un ivers i ty of G eor gi aResearch Foundation We thank Ab Abercrombie JustinCongdon William Hopkins Laura Janecek ChristopherRomanek and Joseph Pechmann for discussion and com-ments on the manuscript We also appreciate the help ofStephen H Bennett John Cossel Jr Charles R PetersonPaul Moler Woody Woodwardand Jeff Corser for provid-ing information on the status of particular species Thispaper supports the PARC (Partners in Amphibian andReptile Conservation) effort to promote education aboutreptiles and amphibians

Ref eren ces ci te dAl 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 ndash 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 ndash 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 119 8 3 ndash 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 ndash 6 9

Banks B Beebee TJC Coo ke KS 1 9 9 4 Con s erva ti on of the natter jack toadB u fo calamita in Britain over the peri od 1976ndash1990 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 ndash 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 eRe 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 eUn i ted States of Am erica 95 9 0 3 1 ndash 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 ndash 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 rba 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 ndash 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 ofE nvi ron m ental Con t a m i n a ti on Tox i co l ogy 27 8 2 ndash 8 7

Bi s h op JM1 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 ndash 4 3 0

Bl a u s tein A R Hoffman PD Hokit DG Ki e s ecker JM Wa lls SC Hays JB1 9 9 4 a UV repair and re s i s t a n ce to solar UV-B in amph i bian eggs Alink to pop u l a ti on declines Proceed i n gs of the Na ti onal Ac ademy ofS c i en ce of the Un i ted States of Am erica 91 1 7 9 1 ndash 1 7 9 5

Bl a u s tein A R Hokit DG Orsquo Ha ra RK Holt RA 1 9 9 4 b Pa t h ogenic funguscon tri butes to amph i bian losses in the Pacific Nort hwe s t Bi o l ogi c a lCon s erva ti on 67 2 5 1 ndash 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 gs 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 andgl obal ex ti n cti on s Con s erva ti on Bi o l ogy 8 6 0 ndash 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 196ndash201 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 tech 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 ndash 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 theS tu dy of Am ph i bians and Repti l e s Herpeto l ogy Ci rc u l a ti on 22 1 ndash 7 2

Buhlmann KA 1 9 9 5 Ha bitat use terre s trial movem ents and con s erva ti onof 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 ogy2 9 1 7 3 ndash 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 201ndash232 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 amp 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 dIsland and Gu n n er rsquos Quoi n Ma u ri tiu s Bi o l ogical Con s erva ti on 371 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 ndash 1 3 6 9

Ca rey C 1 9 9 3 Hypothesis con cerning the causes of the disappe a ra n ce ofboreal toads from the mountains of Co l orado Con s erva ti on Bi o l ogy 73 5 5 ndash 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 52 7 2 ndash 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 peRomain Na ti onal Wi l dl i fe Ref u ge Ch em o s ph ere 34 5 3 9 ndash 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 1ndash15 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 lm a tu ri ty and dem ogra phics of Bl a n d i n grsquos tu rtles (Emyd o i d e abl 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 ndash 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 ivedor ga n i s m s Am erican Zoo l ogist 34 3 9 7 ndash 4 0 8

[CITES] Conven ti on on In tern a ti onal Trade in Endangered Species ofWild Fauna and Flora 2 0 0 0 lt 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 tmlgt (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 lrule to list the nort h ern pop u l a ti on of the bog tu rtle as thre a ten ed andthe 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 ndash 5 9 6 2 3

August 2000 Vol 50 No 8 BioScience 663

Articles

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 nowbelieve that disease may rival habitat destruction as thelargest single cause o f the decline of amphibians

Among reptiles the widespread upper respiratory tractdisease a contagious respiratory ailment caused by thebacterium Mycoplasma agassizii is a potential cause ofpopulation declines in desert tortoises in the US South-west and gopher tortoises in the Southeast (Jacobson1993 Smith et al 1998)Shell diseases have been implicat-ed in the decline of turtles (eg shell lesions on slidersLovich et al 1996 cutaneous dyskeratosis affecting theshell and thickened forelimb scutes of desert tortoisesJacobson 1994 and emaciation and lesions of the plastronof federally listed flattened musk turtles Sternotherusdepressus Dodd 1988) Individuals in many green sea tur-tle populations are severely affected by viral fibropapillo-mas resulting in growths that can impair vision locomo-tionand feeding ability (Herbst 1994) As is often the casein amphibiansdiseases that are debilitating to wild popu-lations of reptiles are most likely secondary expressions inindividuals with impaired resistance caused by one ormore primary environmental stressors such as habitatdegradation invasive species or pollution

Un su s t a i n a ble useHuman use of animalsincluding reptiles and amphibiansis an integral part of many cultures Harvesting must bebi 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 andspecies are to persist (Pough et al 1998) Overcollectionfor food the pet trade and biological supply houses hasbeen suggested as having had an impact on some amphib-ian populations (Dodd 1997) In the United States note-worthy examples for amphibians occurred in the late1800s to early 1900s when commercial collectors harvest-ed for the frog legs market Hundreds of thousands of

red - l egged frogs (Rana auro ra drayto 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 frogsalthough itis 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 al1994) In Indiathe 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 illegallyeach 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 onsu 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 havebeen more perva s ive and severe than on amph i bians (eg s ee Wi lliams 1999) The severi ty of the tu rtle crisis on agl obal scale was em ph a s i zed by Rh odin (1999) wh oreported that of the approx i m a tely 293 taxa (mainlys 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 thelast few cen tu ri e s 3 (9 taxa) are alre ady ex ti n ct in thewi 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 foodsource Moreover the international trade in turtlesmdashwhich are eaten sold as pets or used in traditional Chi-nese medicinal remediesmdashis both extensive and unregu-lated (Sharma 1999) A recent report indicated that mostturtle sp ecies in Vietnam and southern China are endan-gered and that turtles can no longer be found in the wildin Vietnam (Kiester and Juvik 1997) China is the biggestconsumer of turtles in the food trade Because the trade inturtles is not regulated few records have been kept butexisting records indicate that the trade in live turtles toChina is thousands of tons per year (Mockenhaupt 1999)The commercial trade in freshwater turtles exceeds anypossible sustainable levels and extinction of some speciesin the wild can be expected within the next decade

Most species of sea turtles continue to decline in allwarm oceans of the world The leatherback sea turtle(Dermochelys coriacea) was recently reported to be ldquoon theroad to extinction and further population declines can beexpectedrdquounless appropriate measures are taken to reducemortality rates in adults hatchlings and eggs (Spotila eta l 1 9 9 6 ) The esti m a ted worl dwi de pop u l a ti on ofleatherbacks nesting on beaches in 1980 was 115000com p a red with just 34500 in 1995 Ex p l oi t a ti on ofleatherbacks in the Atlantic Ocean through illegal har-vesting of both adults and eggsis considered to be a majorcontributor to the decline of the species (Spotila et al1996) Likewise for Kemprsquos Ridley sea turtle (Lepidochelys

658 BioScience August 2000 Vol 50 No 8

Articles

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

kempii) harvests of nesting females and their eggs on thelargest known nesting site contributed to declines from42000 nesting females in 1947 to only a few hundred by1975 (Hildebrand 1982)

Among North American turtles the diamondback ter-rapin (Ma l a cl emys terra p i n) a small e s tu a rine tu rt l especies with a geographic range from Cape Cod to Texasdecl i n ed severely fo ll owing heavy ex p l oi t a ti on as agourmet food item from the late 1800s to the early 1900s(Carr 1952) With forced reductions in harvesting manypopulations were able to recover but the terrapin nowfaces significant new threats including highway mortality(Wood and Herlands 1997) and drowning in commercialand recreational crab traps (Bishop 1983 Roosenburg1991) Renewed commercial har vest of the diamondbackterrapin has also been documented (Garber 1988)

Commercial turtle trappers for the restaurant tradestepped up harvests of one of the largest freshwater turtlesin the world the alligator snapper (Macroclemys tem -minckii) from the 1960s through the 1980s (Roman et al1999) Consequently as evidence from survey efforts sug-gests the species has b een drastical ly reduced in numbersin some of the southeastern US rivers it once inhabited(Moler 1992 Jensen 1998)

The enormous and once common populations of thearrau (Podocnemis expansa) a communally nesting turtleof the Orinoco and Amazon Rivers in South America arenow greatly reduced in size because of human consump-tion of eggs and nesting females (Pritchard and Trebbau1984) an overexploitation problem identified almost twocenturies ago (Humboldt 1814 from Pritchard and Treb-bau 1984) Declines from similar causes have befallen theterecay (Podocnemis unifilis) in tropical lowlands of SouthAmerica (Thorbjarnarson et al 1993) and the river ter-rapin (Batagur baska) in India (Bhupathy 1997)

Overharvesting for food is a problem not just for turtlesbut also for lizardshaving contributed to declines in greeniguanas (Iguana iguana) and spiny - t a i l ed iguanas(Ctenosaura similis) in tropical America (Fitch et al1982)

The pet trade appears especially hazardous for someturtle sp ecies In 1994 population declines were reportedin box turtles (Terrapene carolina) in 16 states rangingfrom Massachusetts to Florida and Oklahoma to Wiscon-sin (Lieberman 1994) Doc u m en t a ti on of box tu rt l edecl i n e s mdash i n cluding records showing that s i n ce 199529896 box turtles had been collected for the pet trade andshipped from Louisianamdashresulted in unanimous passageof Act 81 by the Louisiana Senate and House of Represen-tatives in 1999the act prohibits the commercial harvest ofthe statersquos native box turtle populations Overcollection forexport is a serious factor in much of the box turtle declineand may exacerbate the effects of habitat loss (Lieberman1994) Habitat destruction and illegal collecting for the pettrade are the primary threats to bog turtles (Clemmysmuhlenbergii) Copeyon 1997) The number of northernpopulations has been reduced by 50 with most of the

decline occurring over the last 20 years Of the 191remaining bog turtle habitats known in 199633 were clas-sified as in good condition 67 as fair and 76 as poor thestatus of 15 was unknown

Overcollecting is also a problem for some snake speciesThe ocellated mountain viper (Vipera wagneri) in easternTurkey has been sought by the pet trade and removedfrom the wild in large numbers posing ldquoa serious threat tosurvival of the speciesrdquo (Nilson et al 1990) Populations ofseveral boa and python species have declined because ofharvesting of wild snakes for their skins (Pough et al1998) Rapid declines o f large-bodied snakes which tendto have a suite of life-history traits that make them moresusceptible to population declines than smaller species(eg Dodd 1993)have been documented throughout theworld in recent years (egShine and Fitzgerald 1996) Forexample females of the increasingly rare timber rat-tlesnake (Crotalus horridus) which may exceed a meter inlength and typically take 9 years to reach maturity pro-duce fewer than a dozen young every 3 years (Brown1993)Large-bodied species such as rattlesnakes (Crotalus)have long generation times a life-history t rait that whencom bi n ed with habitat loss human pers ec uti on a n di n ten s ive overco ll ecti on (eg ldquora t t l e s n a ke ro u n du p srdquo Brown 1993)has led to dramatic declines of some speciesand ma de approximately one-third of rattlesnake sp eciesvulnerable to extinction (Greene 1997) High harvest ratesof snakes with low reproductive frequencies such as thef 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 dalmost certainly be unsustainable (Shine et al 1995)

August 2000 Vol 50 No 8 BioScience 659

Articles

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

These examples demonstrate that sustainable use ofsome long-lived reptile species is problematic Becauselongevity in reptiles is associated with delayed sexualm a tu ri ty h i gh adult su rvivors h i p and low fec u n d i ty(Pough et al1998) populations of long-lived species can-not remain stable (or grow) when adults and older juve-niles are harvested at high rates (Congdon et al 19931994) This is not to say however that all such long-livedspecies should be commercially 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 (Ross1998) and unsustainable harvest of adults for the leathertrade (Brazaitis 1989) After years of total protection sev-eral sp ecies have recovered a f ew are farmed or ranchedcommercially (King 1989) In some crocodile speciesadult females are protected and only small numbers ofeggs small juveniles and larger males are removed fromthe wild (King 1989) In contrast 7ndash8 of all alligatorsmore than 12 m in length are harvested annually in someFlorida populations (David et al1996) In additiona 50annual harvest rate of alligator eggs or hatchlings isallowed because removal at these life stages does notreduce recruitment into adult-size classes (Rice et al1999) Closely monitored alligator populations and pre-sumably populations of other long-lived species of rep-tiles can sustain the legal regulated harvest of some pro-porti on of eggs h a tch l i n gs or adults with negl i gi bl eeffects

G l obal cl i m a te ch a n geFew ecologists will dispute the link between increases ingreenhouse gases and gl obal tem pera tu re Howeverwhether the current rate of climate change reflects naturalvariation or has an anthropogenic cause is hotly debatedFor the purposes of this article we accept the argumentthat the earth is undergoing unprecedented rapid climaticchange (Schneider and Root 1998) that includes alter-ations in climate variables such as temperature and rain-fall patterns storm severity and storm frequency If oneaccepts that human-induced climate change is occurring(eg Vinnikov et al1999)then the consequences for her-petofaunal diversity can be addressed

The obvious effects of climate change on biodiversityare mediated through changes in habitat For exampleglobal warming may further diminish prairie wetlandhabitat in the United States (Poiani and Johnson 1991)Future wetland acreage in the United States may be great-ly reduced under a variety of climate circulation models(Halpin 1997) and aquatic and semiaquatic species willsuffer declines as habitat disappears Although many habi-tats are ex pected to under go dra m a tic ch a n ge (eg Guertin et al1997Still et al 1999) predictions of specieshabitat shifts in response to global warming cannot be

based solely on analyses of climatendashspace changes becausespecies distributions are also a function of dispersal abili-ty and biotic interactions (Davis et al 1998) Existingnature reserves will be inadequate to preserve current bio-diversity because an already fragmented landscape willi 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 theirlimited dispersal abilities reptiles and amphibians areespecially vulnerable to rapid habitat changes and maysuffer many more extinctions than birds as a result of arapid rate of climate change (Schneider and Root 1998)

In discussions of observed amphibian declines littlemention has been made of climate change (Dodd 1997)with two notable exceptions First the famed golden toad(Bufo periglenes) extinction in Costa Rica may have b eencausedat 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 changepatterns of cloud formation and thereby the availability ofwater (Still et al 1999) Second Blaustein et al (1994a)have suggested that ultraviolet B (UVB) radiation hasadverse effects on some amphibians including reducedhatching success and decreased survival to metamorpho-sis However an increase in the level of UVB caused bydepletion of the ozone layer probably does not pose ani m m ed i a te threat to reptile eggs wh i ch are sel domexposed to UVB radiation

As with the amphibian studies few researchers havedirectly assessed effects of climate change on r eptiles It isnonetheless reasonable to expect that climate changescould re sult in con d i ti ons that el i m i n a te or severelyrestrict sp ecies with limited dist ributions (Schneider andRoot 1998) as has been suggested for some Australianlizards (Brereton et al1995) and crotaline snakes of NorthAmerica and the neotropics (Greene and Campbell 1993)Additional effects of warming on some reptiles based onem p i rical evi den ce with fre s hw a ter tu rt l e s i n clu deenhanced juvenile growth rates earlier ages at maturityand shifts in functional sex ratios (Frazer et al 1993)Global warming may have the greatest impact on thosereptiles (crocodilians and some turtles) that have temper-ature-dependent sex determination (Janzen 1994) where-by the sex ratio of the hatchlings is determined by nesttemperatures during incubation Unless shifts occur in thepivotal temperatures at which sex is determined or femalenest-site choices (ie shade versus sun) evolve to keeppace with rising temperatures altered sex ratios couldaffect population demographics and persistence

En i gm a tic decl i n e sFinally in addition to the many cases of declines that haves ome re a s on a bly unders tood causes s ome amph i bi a npopulations have declined and even gone extinct withoutany discernible causes One well-known example is thegastric 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 ofparental care in which the young develop in the safety ofthe motherrsquos stomach (Tyler and Carter 1981) the gastricbrooding frog ceased to be found in nature Disjunct pop-ulations of the g reen salamand er (Aneides aeneus ) in thes o ut h ern App a l achians have app a ren t ly decl i n ed butwithout similar declines in other portions of its range (JeffCorser USGS-BRD Twin Creeks Resource Center GSM-NP Gatlinburg TN personal communication)

Similar cases exist for reptiles For example no livingspecimen of the Round Island burrowing boa (Bolyeriamultocarinata) in the Indian Ocean has been seen since1975 (Bullock 1986) the species may have become extinctin recent decades (Greene 1997) Although all species ofreptiles native to North America in precolonial times per-sist in some regions the current ranges of many are but aremnant of the much larger areas formerly occupied Nat-ural populations of indigo snakes have not been found insome regions of their historic range in more than 40 years(Mount 1975 Conant and Collins 1998)and the species isldquodeclining in abundance and distribution throughout itsUS geographic rangerdquo (Hallam et al 1998) Likewises i gh ti n gs of the sout h ern hognose snake (Heterod o nsimus) 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 ) evenin 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 sRegrettably many amphibian populations and species thatare thought to be declining have not been monitored overlong 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 commoncharacteristic The subjects of these studies occur in highdensity either spatially (eg Jordanrsquos salamander Plethod -on jordanii Hairston 1987) or temporally (eg mole sala-manders Ambystoma talpoideum Pechmann et al 1991and natterjack toads Bufo calamita Banks et al 1994)

Many of the species that have become symbols for thedeclining amphibian phenomenon are seasonally activeanurans that arrive over restricted periods of time atbreeding sites where they congregate in greater densitiesthan at any other time of the year Researchers sit ready torecord their arrival and abundance and if the animals failto show up when expecteda problem is suspected if suchabsences are protracted then the change is presumablyreal (Blaustein et al 1994c) The phenology of theseamphibians permits detection of breeding activity there-fore determination of whether the absence of breedingadults is a short-term aberration or an indication of a realdecline becomes a matter of accumulating the data neces-sary to demonstrate a statistically significant trend (fordiscussion see Blaustein et al 1994c Pechmann andWilbur 1994 Reed and Blaustein 1995)

Among reptiles declines in sea turtles are perhaps the

best documented because like many amphibians theyengage in an annual reproductive event (in this caseoviposition) with a predictable site and time A few snakespecies in colder temperate regions are known to hiber-nate communally and numbers can be assessed upon

emergence (Parker and Brown 1973) But what of themajority of reptile species that do not congregate to breedor hibernate and do not occur in particularly high densi-ties F or example the r acer (Coluber const rictor) a com-mon North American snake is found in a wide variety ofterrestrial habitats Like most other ectotherms racers aremore active and therefore more commonly encounteredin the warmer months However aside from some regionswhere communal hibernation occurs (Parker and Brown1973) determining the abundance of racers is difficultbecause 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 howcould we take a census to know when and if racer popula-tions were declining at a substantial rate on a widespread

August 2000 Vol 50 No 8 BioScience 661

Articles

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

basis without mounting an intensive long-term samplingprogram The clandestine nature of many reptiles oftencombined with comparatively large home ranges lowpop u l a ti on den s i ti e s and ra reness of con grega ti on a lbehavior makes documenting population trends very dif-ficult As a result populations may wither with littlenoticeOnce an unmonitored species or population is rec-ognized as being unexpectedly depauperate or absent thecause of decline may be unknown and unknowable

Based on the accumulated evidence that many if notmost declines reported for amphibians are indeed realtheproper course for conservation initiatives is to assume theworst for all herpetofauna and therefore to implementabatement measures while gathering more data Althoughthe lack of long-term data often may preclude the id enti-fication of the cause of a decline or even in some cases thecorroboration o f a decline the absence of that data doesnot rule out the existence of a correctable problem

Co n clusion and re co m m en d a ti o n sThe declines of m a ny reptile pop u l a ti ons are similar tothose 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 ha m ph i bi a n s the causes are known with cert a i n ty ins ome instance s su s pected in many and unknown ino t h ers Some ex ti rp a ti ons are local wh ereas others arem ore wi de s pre ad The difficulty in doc u m en ting thes 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 causesof pop u l a ti on declines can be obvi a ted direct ly Th ei 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 ingeneral (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 ofinvasive non-native species that could be harmful to rep-tile populations must be proscribed Third restrictingtrade in sensitive reptile species for which sustainableremoval cannot be demonstrated will require the passageor strengthening and enforcement of legislation In thecase of Asian turtles legislative remedies could be too lit-tle too latemdasha stopgap remedy is necessary The only wayto prevent the imminent extinction of a large number ofthe more than 80 species of turtles native to southern Asiawill be to maintain populations in ex situ captive breedingand genetic reserve programs With changes in culturalattitudesstrengthening of international trade regulationsand increased habitat protection the reintroduction ofthese species into the wild may be possible

Much of todayrsquos commercial exploitation of reptiles inthe United States and elsewhere requires urgent govern-mental action to implement internationally accepted andenforced controls Despite the fact that conservation mea-sures can be implemented effectively through legislation(as happened with legislation for protection of Louisianabox turtles and American alligators) the political pres-sures against accomplishing such goals cannot be overstat-ed The lack of support by the World Trade Organizationfor recommendations to curtail sea turtle exploitation(WTO 1998) brings the problem into perspective on aninternational scale

Direct and indirect effects of environmental pol lutiondisease and parasitism and global climate change aremore difficult to quantify in many instances and will bemore difficult to change in the short term Nonetheless wemust endeavor to understand these potential factors toameliorate their impact on natural populations of reptilesand their habitats

Finally long-term monitoring o f reptile populations isessential and must be aided by the establishment of stan-dard methods and techniques It is equally important thatthe academic community land managers and conserva-tion organizations recognize that rigorous field programsfocusing on the distri buti on a bu n d a n ce s t a tu s a n dtrends of populations and species are critical and worth-while Herpetofaunal inventories should become a stan-dard part of environmental assessment programs and thepublication of field survey efforts that document potentialor suspected declines should be encouraged When long-term and widespread monitoring becomes the normdeclines are likely to become less equivocal (in terms ofprotracted declines versus natural fluctuations) and thecauses less mysterious

662 BioScience August 2000 Vol 50 No 8

Articles

Sand monitor (Va ra nus go u l d i ) Al t h ou gh sandm o n i to rs (genus Va ra nu s wh i ch includes the wo rl d rsquo sl a rgest lizards) appear to be thriving in many pa rts oft h eir natu ral habitats in Au s tra l i a ot h er spe cies of t h egenus in As i a Afri c a and the East Indies are threa ten e dby exten s ive habitat destru cti o n

The disappearance of reptiles from the natural world isgenuine and should be a matter of concern not simplybecause of reptilesrsquo perceived associations with amphib-ians but because reptile declineslike those of amphibiansare growing and serious in their own right Current evi-dence suggests that amphibian and reptile declines whichare exacerbated by burgeoning human populations con-stitute a worldwide crisis

Ack n owl e d gm en t sManuscript preparation was aided by Financial AssistanceAw a rd Nu m ber DE-FC09-96SR18546 from the USDep a rtm ent of E n er gy to the Un ivers i ty of G eor gi aResearch Foundation We thank Ab Abercrombie JustinCongdon William Hopkins Laura Janecek ChristopherRomanek and Joseph Pechmann for discussion and com-ments on the manuscript We also appreciate the help ofStephen H Bennett John Cossel Jr Charles R PetersonPaul Moler Woody Woodwardand Jeff Corser for provid-ing information on the status of particular species Thispaper supports the PARC (Partners in Amphibian andReptile Conservation) effort to promote education aboutreptiles and amphibians

Ref eren ces ci te dAl 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 ndash 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 ndash 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 119 8 3 ndash 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 ndash 6 9

Banks B Beebee TJC Coo ke KS 1 9 9 4 Con s erva ti on of the natter jack toadB u fo calamita in Britain over the peri od 1976ndash1990 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 ndash 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 eRe 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 eUn i ted States of Am erica 95 9 0 3 1 ndash 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 ndash 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 rba 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 ndash 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 ofE nvi ron m ental Con t a m i n a ti on Tox i co l ogy 27 8 2 ndash 8 7

Bi s h op JM1 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 ndash 4 3 0

Bl a u s tein A R Hoffman PD Hokit DG Ki e s ecker JM Wa lls SC Hays JB1 9 9 4 a UV repair and re s i s t a n ce to solar UV-B in amph i bian eggs Alink to pop u l a ti on declines Proceed i n gs of the Na ti onal Ac ademy ofS c i en ce of the Un i ted States of Am erica 91 1 7 9 1 ndash 1 7 9 5

Bl a u s tein A R Hokit DG Orsquo Ha ra RK Holt RA 1 9 9 4 b Pa t h ogenic funguscon tri butes to amph i bian losses in the Pacific Nort hwe s t Bi o l ogi c a lCon s erva ti on 67 2 5 1 ndash 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 gs 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 andgl obal ex ti n cti on s Con s erva ti on Bi o l ogy 8 6 0 ndash 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 196ndash201 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 tech 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 ndash 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 theS tu dy of Am ph i bians and Repti l e s Herpeto l ogy Ci rc u l a ti on 22 1 ndash 7 2

Buhlmann KA 1 9 9 5 Ha bitat use terre s trial movem ents and con s erva ti onof 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 ogy2 9 1 7 3 ndash 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 201ndash232 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 amp 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 dIsland and Gu n n er rsquos Quoi n Ma u ri tiu s Bi o l ogical Con s erva ti on 371 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 ndash 1 3 6 9

Ca rey C 1 9 9 3 Hypothesis con cerning the causes of the disappe a ra n ce ofboreal toads from the mountains of Co l orado Con s erva ti on Bi o l ogy 73 5 5 ndash 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 52 7 2 ndash 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 peRomain Na ti onal Wi l dl i fe Ref u ge Ch em o s ph ere 34 5 3 9 ndash 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 1ndash15 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 lm a tu ri ty and dem ogra phics of Bl a n d i n grsquos tu rtles (Emyd o i d e abl 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 ndash 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 ivedor ga n i s m s Am erican Zoo l ogist 34 3 9 7 ndash 4 0 8

[CITES] Conven ti on on In tern a ti onal Trade in Endangered Species ofWild Fauna and Flora 2 0 0 0 lt 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 tmlgt (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 lrule to list the nort h ern pop u l a ti on of the bog tu rtle as thre a ten ed andthe 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 ndash 5 9 6 2 3

August 2000 Vol 50 No 8 BioScience 663

Articles

kempii) harvests of nesting females and their eggs on thelargest known nesting site contributed to declines from42000 nesting females in 1947 to only a few hundred by1975 (Hildebrand 1982)

Among North American turtles the diamondback ter-rapin (Ma l a cl emys terra p i n) a small e s tu a rine tu rt l especies with a geographic range from Cape Cod to Texasdecl i n ed severely fo ll owing heavy ex p l oi t a ti on as agourmet food item from the late 1800s to the early 1900s(Carr 1952) With forced reductions in harvesting manypopulations were able to recover but the terrapin nowfaces significant new threats including highway mortality(Wood and Herlands 1997) and drowning in commercialand recreational crab traps (Bishop 1983 Roosenburg1991) Renewed commercial har vest of the diamondbackterrapin has also been documented (Garber 1988)

Commercial turtle trappers for the restaurant tradestepped up harvests of one of the largest freshwater turtlesin the world the alligator snapper (Macroclemys tem -minckii) from the 1960s through the 1980s (Roman et al1999) Consequently as evidence from survey efforts sug-gests the species has b een drastical ly reduced in numbersin some of the southeastern US rivers it once inhabited(Moler 1992 Jensen 1998)

The enormous and once common populations of thearrau (Podocnemis expansa) a communally nesting turtleof the Orinoco and Amazon Rivers in South America arenow greatly reduced in size because of human consump-tion of eggs and nesting females (Pritchard and Trebbau1984) an overexploitation problem identified almost twocenturies ago (Humboldt 1814 from Pritchard and Treb-bau 1984) Declines from similar causes have befallen theterecay (Podocnemis unifilis) in tropical lowlands of SouthAmerica (Thorbjarnarson et al 1993) and the river ter-rapin (Batagur baska) in India (Bhupathy 1997)

Overharvesting for food is a problem not just for turtlesbut also for lizardshaving contributed to declines in greeniguanas (Iguana iguana) and spiny - t a i l ed iguanas(Ctenosaura similis) in tropical America (Fitch et al1982)

The pet trade appears especially hazardous for someturtle sp ecies In 1994 population declines were reportedin box turtles (Terrapene carolina) in 16 states rangingfrom Massachusetts to Florida and Oklahoma to Wiscon-sin (Lieberman 1994) Doc u m en t a ti on of box tu rt l edecl i n e s mdash i n cluding records showing that s i n ce 199529896 box turtles had been collected for the pet trade andshipped from Louisianamdashresulted in unanimous passageof Act 81 by the Louisiana Senate and House of Represen-tatives in 1999the act prohibits the commercial harvest ofthe statersquos native box turtle populations Overcollection forexport is a serious factor in much of the box turtle declineand may exacerbate the effects of habitat loss (Lieberman1994) Habitat destruction and illegal collecting for the pettrade are the primary threats to bog turtles (Clemmysmuhlenbergii) Copeyon 1997) The number of northernpopulations has been reduced by 50 with most of the

decline occurring over the last 20 years Of the 191remaining bog turtle habitats known in 199633 were clas-sified as in good condition 67 as fair and 76 as poor thestatus of 15 was unknown

Overcollecting is also a problem for some snake speciesThe ocellated mountain viper (Vipera wagneri) in easternTurkey has been sought by the pet trade and removedfrom the wild in large numbers posing ldquoa serious threat tosurvival of the speciesrdquo (Nilson et al 1990) Populations ofseveral boa and python species have declined because ofharvesting of wild snakes for their skins (Pough et al1998) Rapid declines o f large-bodied snakes which tendto have a suite of life-history traits that make them moresusceptible to population declines than smaller species(eg Dodd 1993)have been documented throughout theworld in recent years (egShine and Fitzgerald 1996) Forexample females of the increasingly rare timber rat-tlesnake (Crotalus horridus) which may exceed a meter inlength and typically take 9 years to reach maturity pro-duce fewer than a dozen young every 3 years (Brown1993)Large-bodied species such as rattlesnakes (Crotalus)have long generation times a life-history t rait that whencom bi n ed with habitat loss human pers ec uti on a n di n ten s ive overco ll ecti on (eg ldquora t t l e s n a ke ro u n du p srdquo Brown 1993)has led to dramatic declines of some speciesand ma de approximately one-third of rattlesnake sp eciesvulnerable to extinction (Greene 1997) High harvest ratesof snakes with low reproductive frequencies such as thef 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 dalmost certainly be unsustainable (Shine et al 1995)

August 2000 Vol 50 No 8 BioScience 659

Articles

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

These examples demonstrate that sustainable use ofsome long-lived reptile species is problematic Becauselongevity in reptiles is associated with delayed sexualm a tu ri ty h i gh adult su rvivors h i p and low fec u n d i ty(Pough et al1998) populations of long-lived species can-not remain stable (or grow) when adults and older juve-niles are harvested at high rates (Congdon et al 19931994) This is not to say however that all such long-livedspecies should be commercially 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 (Ross1998) and unsustainable harvest of adults for the leathertrade (Brazaitis 1989) After years of total protection sev-eral sp ecies have recovered a f ew are farmed or ranchedcommercially (King 1989) In some crocodile speciesadult females are protected and only small numbers ofeggs small juveniles and larger males are removed fromthe wild (King 1989) In contrast 7ndash8 of all alligatorsmore than 12 m in length are harvested annually in someFlorida populations (David et al1996) In additiona 50annual harvest rate of alligator eggs or hatchlings isallowed because removal at these life stages does notreduce recruitment into adult-size classes (Rice et al1999) Closely monitored alligator populations and pre-sumably populations of other long-lived species of rep-tiles can sustain the legal regulated harvest of some pro-porti on of eggs h a tch l i n gs or adults with negl i gi bl eeffects

G l obal cl i m a te ch a n geFew ecologists will dispute the link between increases ingreenhouse gases and gl obal tem pera tu re Howeverwhether the current rate of climate change reflects naturalvariation or has an anthropogenic cause is hotly debatedFor the purposes of this article we accept the argumentthat the earth is undergoing unprecedented rapid climaticchange (Schneider and Root 1998) that includes alter-ations in climate variables such as temperature and rain-fall patterns storm severity and storm frequency If oneaccepts that human-induced climate change is occurring(eg Vinnikov et al1999)then the consequences for her-petofaunal diversity can be addressed

The obvious effects of climate change on biodiversityare mediated through changes in habitat For exampleglobal warming may further diminish prairie wetlandhabitat in the United States (Poiani and Johnson 1991)Future wetland acreage in the United States may be great-ly reduced under a variety of climate circulation models(Halpin 1997) and aquatic and semiaquatic species willsuffer declines as habitat disappears Although many habi-tats are ex pected to under go dra m a tic ch a n ge (eg Guertin et al1997Still et al 1999) predictions of specieshabitat shifts in response to global warming cannot be

based solely on analyses of climatendashspace changes becausespecies distributions are also a function of dispersal abili-ty and biotic interactions (Davis et al 1998) Existingnature reserves will be inadequate to preserve current bio-diversity because an already fragmented landscape willi 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 theirlimited dispersal abilities reptiles and amphibians areespecially vulnerable to rapid habitat changes and maysuffer many more extinctions than birds as a result of arapid rate of climate change (Schneider and Root 1998)

In discussions of observed amphibian declines littlemention has been made of climate change (Dodd 1997)with two notable exceptions First the famed golden toad(Bufo periglenes) extinction in Costa Rica may have b eencausedat 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 changepatterns of cloud formation and thereby the availability ofwater (Still et al 1999) Second Blaustein et al (1994a)have suggested that ultraviolet B (UVB) radiation hasadverse effects on some amphibians including reducedhatching success and decreased survival to metamorpho-sis However an increase in the level of UVB caused bydepletion of the ozone layer probably does not pose ani m m ed i a te threat to reptile eggs wh i ch are sel domexposed to UVB radiation

As with the amphibian studies few researchers havedirectly assessed effects of climate change on r eptiles It isnonetheless reasonable to expect that climate changescould re sult in con d i ti ons that el i m i n a te or severelyrestrict sp ecies with limited dist ributions (Schneider andRoot 1998) as has been suggested for some Australianlizards (Brereton et al1995) and crotaline snakes of NorthAmerica and the neotropics (Greene and Campbell 1993)Additional effects of warming on some reptiles based onem p i rical evi den ce with fre s hw a ter tu rt l e s i n clu deenhanced juvenile growth rates earlier ages at maturityand shifts in functional sex ratios (Frazer et al 1993)Global warming may have the greatest impact on thosereptiles (crocodilians and some turtles) that have temper-ature-dependent sex determination (Janzen 1994) where-by the sex ratio of the hatchlings is determined by nesttemperatures during incubation Unless shifts occur in thepivotal temperatures at which sex is determined or femalenest-site choices (ie shade versus sun) evolve to keeppace with rising temperatures altered sex ratios couldaffect population demographics and persistence

En i gm a tic decl i n e sFinally in addition to the many cases of declines that haves ome re a s on a bly unders tood causes s ome amph i bi a npopulations have declined and even gone extinct withoutany discernible causes One well-known example is thegastric 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 ofparental care in which the young develop in the safety ofthe motherrsquos stomach (Tyler and Carter 1981) the gastricbrooding frog ceased to be found in nature Disjunct pop-ulations of the g reen salamand er (Aneides aeneus ) in thes o ut h ern App a l achians have app a ren t ly decl i n ed butwithout similar declines in other portions of its range (JeffCorser USGS-BRD Twin Creeks Resource Center GSM-NP Gatlinburg TN personal communication)

Similar cases exist for reptiles For example no livingspecimen of the Round Island burrowing boa (Bolyeriamultocarinata) in the Indian Ocean has been seen since1975 (Bullock 1986) the species may have become extinctin recent decades (Greene 1997) Although all species ofreptiles native to North America in precolonial times per-sist in some regions the current ranges of many are but aremnant of the much larger areas formerly occupied Nat-ural populations of indigo snakes have not been found insome regions of their historic range in more than 40 years(Mount 1975 Conant and Collins 1998)and the species isldquodeclining in abundance and distribution throughout itsUS geographic rangerdquo (Hallam et al 1998) Likewises i gh ti n gs of the sout h ern hognose snake (Heterod o nsimus) 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 ) evenin 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 sRegrettably many amphibian populations and species thatare thought to be declining have not been monitored overlong 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 commoncharacteristic The subjects of these studies occur in highdensity either spatially (eg Jordanrsquos salamander Plethod -on jordanii Hairston 1987) or temporally (eg mole sala-manders Ambystoma talpoideum Pechmann et al 1991and natterjack toads Bufo calamita Banks et al 1994)

Many of the species that have become symbols for thedeclining amphibian phenomenon are seasonally activeanurans that arrive over restricted periods of time atbreeding sites where they congregate in greater densitiesthan at any other time of the year Researchers sit ready torecord their arrival and abundance and if the animals failto show up when expecteda problem is suspected if suchabsences are protracted then the change is presumablyreal (Blaustein et al 1994c) The phenology of theseamphibians permits detection of breeding activity there-fore determination of whether the absence of breedingadults is a short-term aberration or an indication of a realdecline becomes a matter of accumulating the data neces-sary to demonstrate a statistically significant trend (fordiscussion see Blaustein et al 1994c Pechmann andWilbur 1994 Reed and Blaustein 1995)

Among reptiles declines in sea turtles are perhaps the

best documented because like many amphibians theyengage in an annual reproductive event (in this caseoviposition) with a predictable site and time A few snakespecies in colder temperate regions are known to hiber-nate communally and numbers can be assessed upon

emergence (Parker and Brown 1973) But what of themajority of reptile species that do not congregate to breedor hibernate and do not occur in particularly high densi-ties F or example the r acer (Coluber const rictor) a com-mon North American snake is found in a wide variety ofterrestrial habitats Like most other ectotherms racers aremore active and therefore more commonly encounteredin the warmer months However aside from some regionswhere communal hibernation occurs (Parker and Brown1973) determining the abundance of racers is difficultbecause 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 howcould we take a census to know when and if racer popula-tions were declining at a substantial rate on a widespread

August 2000 Vol 50 No 8 BioScience 661

Articles

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

basis without mounting an intensive long-term samplingprogram The clandestine nature of many reptiles oftencombined with comparatively large home ranges lowpop u l a ti on den s i ti e s and ra reness of con grega ti on a lbehavior makes documenting population trends very dif-ficult As a result populations may wither with littlenoticeOnce an unmonitored species or population is rec-ognized as being unexpectedly depauperate or absent thecause of decline may be unknown and unknowable

Based on the accumulated evidence that many if notmost declines reported for amphibians are indeed realtheproper course for conservation initiatives is to assume theworst for all herpetofauna and therefore to implementabatement measures while gathering more data Althoughthe lack of long-term data often may preclude the id enti-fication of the cause of a decline or even in some cases thecorroboration o f a decline the absence of that data doesnot rule out the existence of a correctable problem

Co n clusion and re co m m en d a ti o n sThe declines of m a ny reptile pop u l a ti ons are similar tothose 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 ha m ph i bi a n s the causes are known with cert a i n ty ins ome instance s su s pected in many and unknown ino t h ers Some ex ti rp a ti ons are local wh ereas others arem ore wi de s pre ad The difficulty in doc u m en ting thes 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 causesof pop u l a ti on declines can be obvi a ted direct ly Th ei 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 ingeneral (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 ofinvasive non-native species that could be harmful to rep-tile populations must be proscribed Third restrictingtrade in sensitive reptile species for which sustainableremoval cannot be demonstrated will require the passageor strengthening and enforcement of legislation In thecase of Asian turtles legislative remedies could be too lit-tle too latemdasha stopgap remedy is necessary The only wayto prevent the imminent extinction of a large number ofthe more than 80 species of turtles native to southern Asiawill be to maintain populations in ex situ captive breedingand genetic reserve programs With changes in culturalattitudesstrengthening of international trade regulationsand increased habitat protection the reintroduction ofthese species into the wild may be possible

Much of todayrsquos commercial exploitation of reptiles inthe United States and elsewhere requires urgent govern-mental action to implement internationally accepted andenforced controls Despite the fact that conservation mea-sures can be implemented effectively through legislation(as happened with legislation for protection of Louisianabox turtles and American alligators) the political pres-sures against accomplishing such goals cannot be overstat-ed The lack of support by the World Trade Organizationfor recommendations to curtail sea turtle exploitation(WTO 1998) brings the problem into perspective on aninternational scale

Direct and indirect effects of environmental pol lutiondisease and parasitism and global climate change aremore difficult to quantify in many instances and will bemore difficult to change in the short term Nonetheless wemust endeavor to understand these potential factors toameliorate their impact on natural populations of reptilesand their habitats

Finally long-term monitoring o f reptile populations isessential and must be aided by the establishment of stan-dard methods and techniques It is equally important thatthe academic community land managers and conserva-tion organizations recognize that rigorous field programsfocusing on the distri buti on a bu n d a n ce s t a tu s a n dtrends of populations and species are critical and worth-while Herpetofaunal inventories should become a stan-dard part of environmental assessment programs and thepublication of field survey efforts that document potentialor suspected declines should be encouraged When long-term and widespread monitoring becomes the normdeclines are likely to become less equivocal (in terms ofprotracted declines versus natural fluctuations) and thecauses less mysterious

662 BioScience August 2000 Vol 50 No 8

Articles

Sand monitor (Va ra nus go u l d i ) Al t h ou gh sandm o n i to rs (genus Va ra nu s wh i ch includes the wo rl d rsquo sl a rgest lizards) appear to be thriving in many pa rts oft h eir natu ral habitats in Au s tra l i a ot h er spe cies of t h egenus in As i a Afri c a and the East Indies are threa ten e dby exten s ive habitat destru cti o n

The disappearance of reptiles from the natural world isgenuine and should be a matter of concern not simplybecause of reptilesrsquo perceived associations with amphib-ians but because reptile declineslike those of amphibiansare growing and serious in their own right Current evi-dence suggests that amphibian and reptile declines whichare exacerbated by burgeoning human populations con-stitute a worldwide crisis

Ack n owl e d gm en t sManuscript preparation was aided by Financial AssistanceAw a rd Nu m ber DE-FC09-96SR18546 from the USDep a rtm ent of E n er gy to the Un ivers i ty of G eor gi aResearch Foundation We thank Ab Abercrombie JustinCongdon William Hopkins Laura Janecek ChristopherRomanek and Joseph Pechmann for discussion and com-ments on the manuscript We also appreciate the help ofStephen H Bennett John Cossel Jr Charles R PetersonPaul Moler Woody Woodwardand Jeff Corser for provid-ing information on the status of particular species Thispaper supports the PARC (Partners in Amphibian andReptile Conservation) effort to promote education aboutreptiles and amphibians

Ref eren ces ci te dAl 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 ndash 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 ndash 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 119 8 3 ndash 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 ndash 6 9

Banks B Beebee TJC Coo ke KS 1 9 9 4 Con s erva ti on of the natter jack toadB u fo calamita in Britain over the peri od 1976ndash1990 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 ndash 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 eRe 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 eUn i ted States of Am erica 95 9 0 3 1 ndash 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 ndash 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 rba 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 ndash 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 ofE nvi ron m ental Con t a m i n a ti on Tox i co l ogy 27 8 2 ndash 8 7

Bi s h op JM1 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 ndash 4 3 0

Bl a u s tein A R Hoffman PD Hokit DG Ki e s ecker JM Wa lls SC Hays JB1 9 9 4 a UV repair and re s i s t a n ce to solar UV-B in amph i bian eggs Alink to pop u l a ti on declines Proceed i n gs of the Na ti onal Ac ademy ofS c i en ce of the Un i ted States of Am erica 91 1 7 9 1 ndash 1 7 9 5

Bl a u s tein A R Hokit DG Orsquo Ha ra RK Holt RA 1 9 9 4 b Pa t h ogenic funguscon tri butes to amph i bian losses in the Pacific Nort hwe s t Bi o l ogi c a lCon s erva ti on 67 2 5 1 ndash 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 gs 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 andgl obal ex ti n cti on s Con s erva ti on Bi o l ogy 8 6 0 ndash 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 196ndash201 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 tech 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 ndash 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 theS tu dy of Am ph i bians and Repti l e s Herpeto l ogy Ci rc u l a ti on 22 1 ndash 7 2

Buhlmann KA 1 9 9 5 Ha bitat use terre s trial movem ents and con s erva ti onof 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 ogy2 9 1 7 3 ndash 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 201ndash232 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 amp 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 dIsland and Gu n n er rsquos Quoi n Ma u ri tiu s Bi o l ogical Con s erva ti on 371 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 ndash 1 3 6 9

Ca rey C 1 9 9 3 Hypothesis con cerning the causes of the disappe a ra n ce ofboreal toads from the mountains of Co l orado Con s erva ti on Bi o l ogy 73 5 5 ndash 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 52 7 2 ndash 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 peRomain Na ti onal Wi l dl i fe Ref u ge Ch em o s ph ere 34 5 3 9 ndash 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 1ndash15 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 lm a tu ri ty and dem ogra phics of Bl a n d i n grsquos tu rtles (Emyd o i d e abl 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 ndash 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 ivedor ga n i s m s Am erican Zoo l ogist 34 3 9 7 ndash 4 0 8

[CITES] Conven ti on on In tern a ti onal Trade in Endangered Species ofWild Fauna and Flora 2 0 0 0 lt 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 tmlgt (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 lrule to list the nort h ern pop u l a ti on of the bog tu rtle as thre a ten ed andthe 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 ndash 5 9 6 2 3

August 2000 Vol 50 No 8 BioScience 663

Articles

These examples demonstrate that sustainable use ofsome long-lived reptile species is problematic Becauselongevity in reptiles is associated with delayed sexualm a tu ri ty h i gh adult su rvivors h i p and low fec u n d i ty(Pough et al1998) populations of long-lived species can-not remain stable (or grow) when adults and older juve-niles are harvested at high rates (Congdon et al 19931994) This is not to say however that all such long-livedspecies should be commercially 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 (Ross1998) and unsustainable harvest of adults for the leathertrade (Brazaitis 1989) After years of total protection sev-eral sp ecies have recovered a f ew are farmed or ranchedcommercially (King 1989) In some crocodile speciesadult females are protected and only small numbers ofeggs small juveniles and larger males are removed fromthe wild (King 1989) In contrast 7ndash8 of all alligatorsmore than 12 m in length are harvested annually in someFlorida populations (David et al1996) In additiona 50annual harvest rate of alligator eggs or hatchlings isallowed because removal at these life stages does notreduce recruitment into adult-size classes (Rice et al1999) Closely monitored alligator populations and pre-sumably populations of other long-lived species of rep-tiles can sustain the legal regulated harvest of some pro-porti on of eggs h a tch l i n gs or adults with negl i gi bl eeffects

G l obal cl i m a te ch a n geFew ecologists will dispute the link between increases ingreenhouse gases and gl obal tem pera tu re Howeverwhether the current rate of climate change reflects naturalvariation or has an anthropogenic cause is hotly debatedFor the purposes of this article we accept the argumentthat the earth is undergoing unprecedented rapid climaticchange (Schneider and Root 1998) that includes alter-ations in climate variables such as temperature and rain-fall patterns storm severity and storm frequency If oneaccepts that human-induced climate change is occurring(eg Vinnikov et al1999)then the consequences for her-petofaunal diversity can be addressed

The obvious effects of climate change on biodiversityare mediated through changes in habitat For exampleglobal warming may further diminish prairie wetlandhabitat in the United States (Poiani and Johnson 1991)Future wetland acreage in the United States may be great-ly reduced under a variety of climate circulation models(Halpin 1997) and aquatic and semiaquatic species willsuffer declines as habitat disappears Although many habi-tats are ex pected to under go dra m a tic ch a n ge (eg Guertin et al1997Still et al 1999) predictions of specieshabitat shifts in response to global warming cannot be

based solely on analyses of climatendashspace changes becausespecies distributions are also a function of dispersal abili-ty and biotic interactions (Davis et al 1998) Existingnature reserves will be inadequate to preserve current bio-diversity because an already fragmented landscape willi 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 theirlimited dispersal abilities reptiles and amphibians areespecially vulnerable to rapid habitat changes and maysuffer many more extinctions than birds as a result of arapid rate of climate change (Schneider and Root 1998)

In discussions of observed amphibian declines littlemention has been made of climate change (Dodd 1997)with two notable exceptions First the famed golden toad(Bufo periglenes) extinction in Costa Rica may have b eencausedat 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 changepatterns of cloud formation and thereby the availability ofwater (Still et al 1999) Second Blaustein et al (1994a)have suggested that ultraviolet B (UVB) radiation hasadverse effects on some amphibians including reducedhatching success and decreased survival to metamorpho-sis However an increase in the level of UVB caused bydepletion of the ozone layer probably does not pose ani m m ed i a te threat to reptile eggs wh i ch are sel domexposed to UVB radiation

As with the amphibian studies few researchers havedirectly assessed effects of climate change on r eptiles It isnonetheless reasonable to expect that climate changescould re sult in con d i ti ons that el i m i n a te or severelyrestrict sp ecies with limited dist ributions (Schneider andRoot 1998) as has been suggested for some Australianlizards (Brereton et al1995) and crotaline snakes of NorthAmerica and the neotropics (Greene and Campbell 1993)Additional effects of warming on some reptiles based onem p i rical evi den ce with fre s hw a ter tu rt l e s i n clu deenhanced juvenile growth rates earlier ages at maturityand shifts in functional sex ratios (Frazer et al 1993)Global warming may have the greatest impact on thosereptiles (crocodilians and some turtles) that have temper-ature-dependent sex determination (Janzen 1994) where-by the sex ratio of the hatchlings is determined by nesttemperatures during incubation Unless shifts occur in thepivotal temperatures at which sex is determined or femalenest-site choices (ie shade versus sun) evolve to keeppace with rising temperatures altered sex ratios couldaffect population demographics and persistence

En i gm a tic decl i n e sFinally in addition to the many cases of declines that haves ome re a s on a bly unders tood causes s ome amph i bi a npopulations have declined and even gone extinct withoutany discernible causes One well-known example is thegastric 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 ofparental care in which the young develop in the safety ofthe motherrsquos stomach (Tyler and Carter 1981) the gastricbrooding frog ceased to be found in nature Disjunct pop-ulations of the g reen salamand er (Aneides aeneus ) in thes o ut h ern App a l achians have app a ren t ly decl i n ed butwithout similar declines in other portions of its range (JeffCorser USGS-BRD Twin Creeks Resource Center GSM-NP Gatlinburg TN personal communication)

Similar cases exist for reptiles For example no livingspecimen of the Round Island burrowing boa (Bolyeriamultocarinata) in the Indian Ocean has been seen since1975 (Bullock 1986) the species may have become extinctin recent decades (Greene 1997) Although all species ofreptiles native to North America in precolonial times per-sist in some regions the current ranges of many are but aremnant of the much larger areas formerly occupied Nat-ural populations of indigo snakes have not been found insome regions of their historic range in more than 40 years(Mount 1975 Conant and Collins 1998)and the species isldquodeclining in abundance and distribution throughout itsUS geographic rangerdquo (Hallam et al 1998) Likewises i gh ti n gs of the sout h ern hognose snake (Heterod o nsimus) 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 ) evenin 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 sRegrettably many amphibian populations and species thatare thought to be declining have not been monitored overlong 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 commoncharacteristic The subjects of these studies occur in highdensity either spatially (eg Jordanrsquos salamander Plethod -on jordanii Hairston 1987) or temporally (eg mole sala-manders Ambystoma talpoideum Pechmann et al 1991and natterjack toads Bufo calamita Banks et al 1994)

Many of the species that have become symbols for thedeclining amphibian phenomenon are seasonally activeanurans that arrive over restricted periods of time atbreeding sites where they congregate in greater densitiesthan at any other time of the year Researchers sit ready torecord their arrival and abundance and if the animals failto show up when expecteda problem is suspected if suchabsences are protracted then the change is presumablyreal (Blaustein et al 1994c) The phenology of theseamphibians permits detection of breeding activity there-fore determination of whether the absence of breedingadults is a short-term aberration or an indication of a realdecline becomes a matter of accumulating the data neces-sary to demonstrate a statistically significant trend (fordiscussion see Blaustein et al 1994c Pechmann andWilbur 1994 Reed and Blaustein 1995)

Among reptiles declines in sea turtles are perhaps the

best documented because like many amphibians theyengage in an annual reproductive event (in this caseoviposition) with a predictable site and time A few snakespecies in colder temperate regions are known to hiber-nate communally and numbers can be assessed upon

emergence (Parker and Brown 1973) But what of themajority of reptile species that do not congregate to breedor hibernate and do not occur in particularly high densi-ties F or example the r acer (Coluber const rictor) a com-mon North American snake is found in a wide variety ofterrestrial habitats Like most other ectotherms racers aremore active and therefore more commonly encounteredin the warmer months However aside from some regionswhere communal hibernation occurs (Parker and Brown1973) determining the abundance of racers is difficultbecause 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 howcould we take a census to know when and if racer popula-tions were declining at a substantial rate on a widespread

August 2000 Vol 50 No 8 BioScience 661

Articles

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

basis without mounting an intensive long-term samplingprogram The clandestine nature of many reptiles oftencombined with comparatively large home ranges lowpop u l a ti on den s i ti e s and ra reness of con grega ti on a lbehavior makes documenting population trends very dif-ficult As a result populations may wither with littlenoticeOnce an unmonitored species or population is rec-ognized as being unexpectedly depauperate or absent thecause of decline may be unknown and unknowable

Based on the accumulated evidence that many if notmost declines reported for amphibians are indeed realtheproper course for conservation initiatives is to assume theworst for all herpetofauna and therefore to implementabatement measures while gathering more data Althoughthe lack of long-term data often may preclude the id enti-fication of the cause of a decline or even in some cases thecorroboration o f a decline the absence of that data doesnot rule out the existence of a correctable problem

Co n clusion and re co m m en d a ti o n sThe declines of m a ny reptile pop u l a ti ons are similar tothose 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 ha m ph i bi a n s the causes are known with cert a i n ty ins ome instance s su s pected in many and unknown ino t h ers Some ex ti rp a ti ons are local wh ereas others arem ore wi de s pre ad The difficulty in doc u m en ting thes 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 causesof pop u l a ti on declines can be obvi a ted direct ly Th ei 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 ingeneral (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 ofinvasive non-native species that could be harmful to rep-tile populations must be proscribed Third restrictingtrade in sensitive reptile species for which sustainableremoval cannot be demonstrated will require the passageor strengthening and enforcement of legislation In thecase of Asian turtles legislative remedies could be too lit-tle too latemdasha stopgap remedy is necessary The only wayto prevent the imminent extinction of a large number ofthe more than 80 species of turtles native to southern Asiawill be to maintain populations in ex situ captive breedingand genetic reserve programs With changes in culturalattitudesstrengthening of international trade regulationsand increased habitat protection the reintroduction ofthese species into the wild may be possible

Much of todayrsquos commercial exploitation of reptiles inthe United States and elsewhere requires urgent govern-mental action to implement internationally accepted andenforced controls Despite the fact that conservation mea-sures can be implemented effectively through legislation(as happened with legislation for protection of Louisianabox turtles and American alligators) the political pres-sures against accomplishing such goals cannot be overstat-ed The lack of support by the World Trade Organizationfor recommendations to curtail sea turtle exploitation(WTO 1998) brings the problem into perspective on aninternational scale

Direct and indirect effects of environmental pol lutiondisease and parasitism and global climate change aremore difficult to quantify in many instances and will bemore difficult to change in the short term Nonetheless wemust endeavor to understand these potential factors toameliorate their impact on natural populations of reptilesand their habitats

Finally long-term monitoring o f reptile populations isessential and must be aided by the establishment of stan-dard methods and techniques It is equally important thatthe academic community land managers and conserva-tion organizations recognize that rigorous field programsfocusing on the distri buti on a bu n d a n ce s t a tu s a n dtrends of populations and species are critical and worth-while Herpetofaunal inventories should become a stan-dard part of environmental assessment programs and thepublication of field survey efforts that document potentialor suspected declines should be encouraged When long-term and widespread monitoring becomes the normdeclines are likely to become less equivocal (in terms ofprotracted declines versus natural fluctuations) and thecauses less mysterious

662 BioScience August 2000 Vol 50 No 8

Articles

Sand monitor (Va ra nus go u l d i ) Al t h ou gh sandm o n i to rs (genus Va ra nu s wh i ch includes the wo rl d rsquo sl a rgest lizards) appear to be thriving in many pa rts oft h eir natu ral habitats in Au s tra l i a ot h er spe cies of t h egenus in As i a Afri c a and the East Indies are threa ten e dby exten s ive habitat destru cti o n

The disappearance of reptiles from the natural world isgenuine and should be a matter of concern not simplybecause of reptilesrsquo perceived associations with amphib-ians but because reptile declineslike those of amphibiansare growing and serious in their own right Current evi-dence suggests that amphibian and reptile declines whichare exacerbated by burgeoning human populations con-stitute a worldwide crisis

Ack n owl e d gm en t sManuscript preparation was aided by Financial AssistanceAw a rd Nu m ber DE-FC09-96SR18546 from the USDep a rtm ent of E n er gy to the Un ivers i ty of G eor gi aResearch Foundation We thank Ab Abercrombie JustinCongdon William Hopkins Laura Janecek ChristopherRomanek and Joseph Pechmann for discussion and com-ments on the manuscript We also appreciate the help ofStephen H Bennett John Cossel Jr Charles R PetersonPaul Moler Woody Woodwardand Jeff Corser for provid-ing information on the status of particular species Thispaper supports the PARC (Partners in Amphibian andReptile Conservation) effort to promote education aboutreptiles and amphibians

Ref eren ces ci te dAl 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 ndash 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 ndash 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 119 8 3 ndash 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 ndash 6 9

Banks B Beebee TJC Coo ke KS 1 9 9 4 Con s erva ti on of the natter jack toadB u fo calamita in Britain over the peri od 1976ndash1990 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 ndash 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 eRe 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 eUn i ted States of Am erica 95 9 0 3 1 ndash 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 ndash 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 rba 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 ndash 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 ofE nvi ron m ental Con t a m i n a ti on Tox i co l ogy 27 8 2 ndash 8 7

Bi s h op JM1 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 ndash 4 3 0

Bl a u s tein A R Hoffman PD Hokit DG Ki e s ecker JM Wa lls SC Hays JB1 9 9 4 a UV repair and re s i s t a n ce to solar UV-B in amph i bian eggs Alink to pop u l a ti on declines Proceed i n gs of the Na ti onal Ac ademy ofS c i en ce of the Un i ted States of Am erica 91 1 7 9 1 ndash 1 7 9 5

Bl a u s tein A R Hokit DG Orsquo Ha ra RK Holt RA 1 9 9 4 b Pa t h ogenic funguscon tri butes to amph i bian losses in the Pacific Nort hwe s t Bi o l ogi c a lCon s erva ti on 67 2 5 1 ndash 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 gs 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 andgl obal ex ti n cti on s Con s erva ti on Bi o l ogy 8 6 0 ndash 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 196ndash201 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 tech 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 ndash 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 theS tu dy of Am ph i bians and Repti l e s Herpeto l ogy Ci rc u l a ti on 22 1 ndash 7 2

Buhlmann KA 1 9 9 5 Ha bitat use terre s trial movem ents and con s erva ti onof 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 ogy2 9 1 7 3 ndash 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 201ndash232 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 amp 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 dIsland and Gu n n er rsquos Quoi n Ma u ri tiu s Bi o l ogical Con s erva ti on 371 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 ndash 1 3 6 9

Ca rey C 1 9 9 3 Hypothesis con cerning the causes of the disappe a ra n ce ofboreal toads from the mountains of Co l orado Con s erva ti on Bi o l ogy 73 5 5 ndash 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 52 7 2 ndash 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 peRomain Na ti onal Wi l dl i fe Ref u ge Ch em o s ph ere 34 5 3 9 ndash 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 1ndash15 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 lm a tu ri ty and dem ogra phics of Bl a n d i n grsquos tu rtles (Emyd o i d e abl 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 ndash 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 ivedor ga n i s m s Am erican Zoo l ogist 34 3 9 7 ndash 4 0 8

[CITES] Conven ti on on In tern a ti onal Trade in Endangered Species ofWild Fauna and Flora 2 0 0 0 lt 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 tmlgt (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 lrule to list the nort h ern pop u l a ti on of the bog tu rtle as thre a ten ed andthe 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 ndash 5 9 6 2 3

August 2000 Vol 50 No 8 BioScience 663

Articles

S h ort ly after the discovery of its unu sual sys tem ofparental care in which the young develop in the safety ofthe motherrsquos stomach (Tyler and Carter 1981) the gastricbrooding frog ceased to be found in nature Disjunct pop-ulations of the g reen salamand er (Aneides aeneus ) in thes o ut h ern App a l achians have app a ren t ly decl i n ed butwithout similar declines in other portions of its range (JeffCorser USGS-BRD Twin Creeks Resource Center GSM-NP Gatlinburg TN personal communication)

Similar cases exist for reptiles For example no livingspecimen of the Round Island burrowing boa (Bolyeriamultocarinata) in the Indian Ocean has been seen since1975 (Bullock 1986) the species may have become extinctin recent decades (Greene 1997) Although all species ofreptiles native to North America in precolonial times per-sist in some regions the current ranges of many are but aremnant of the much larger areas formerly occupied Nat-ural populations of indigo snakes have not been found insome regions of their historic range in more than 40 years(Mount 1975 Conant and Collins 1998)and the species isldquodeclining in abundance and distribution throughout itsUS geographic rangerdquo (Hallam et al 1998) Likewises i gh ti n gs of the sout h ern hognose snake (Heterod o nsimus) 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 ) evenin 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 sRegrettably many amphibian populations and species thatare thought to be declining have not been monitored overlong 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 commoncharacteristic The subjects of these studies occur in highdensity either spatially (eg Jordanrsquos salamander Plethod -on jordanii Hairston 1987) or temporally (eg mole sala-manders Ambystoma talpoideum Pechmann et al 1991and natterjack toads Bufo calamita Banks et al 1994)

Many of the species that have become symbols for thedeclining amphibian phenomenon are seasonally activeanurans that arrive over restricted periods of time atbreeding sites where they congregate in greater densitiesthan at any other time of the year Researchers sit ready torecord their arrival and abundance and if the animals failto show up when expecteda problem is suspected if suchabsences are protracted then the change is presumablyreal (Blaustein et al 1994c) The phenology of theseamphibians permits detection of breeding activity there-fore determination of whether the absence of breedingadults is a short-term aberration or an indication of a realdecline becomes a matter of accumulating the data neces-sary to demonstrate a statistically significant trend (fordiscussion see Blaustein et al 1994c Pechmann andWilbur 1994 Reed and Blaustein 1995)

Among reptiles declines in sea turtles are perhaps the

best documented because like many amphibians theyengage in an annual reproductive event (in this caseoviposition) with a predictable site and time A few snakespecies in colder temperate regions are known to hiber-nate communally and numbers can be assessed upon

emergence (Parker and Brown 1973) But what of themajority of reptile species that do not congregate to breedor hibernate and do not occur in particularly high densi-ties F or example the r acer (Coluber const rictor) a com-mon North American snake is found in a wide variety ofterrestrial habitats Like most other ectotherms racers aremore active and therefore more commonly encounteredin the warmer months However aside from some regionswhere communal hibernation occurs (Parker and Brown1973) determining the abundance of racers is difficultbecause 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 howcould we take a census to know when and if racer popula-tions were declining at a substantial rate on a widespread

August 2000 Vol 50 No 8 BioScience 661

Articles

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

basis without mounting an intensive long-term samplingprogram The clandestine nature of many reptiles oftencombined with comparatively large home ranges lowpop u l a ti on den s i ti e s and ra reness of con grega ti on a lbehavior makes documenting population trends very dif-ficult As a result populations may wither with littlenoticeOnce an unmonitored species or population is rec-ognized as being unexpectedly depauperate or absent thecause of decline may be unknown and unknowable

Based on the accumulated evidence that many if notmost declines reported for amphibians are indeed realtheproper course for conservation initiatives is to assume theworst for all herpetofauna and therefore to implementabatement measures while gathering more data Althoughthe lack of long-term data often may preclude the id enti-fication of the cause of a decline or even in some cases thecorroboration o f a decline the absence of that data doesnot rule out the existence of a correctable problem

Co n clusion and re co m m en d a ti o n sThe declines of m a ny reptile pop u l a ti ons are similar tothose 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 ha m ph i bi a n s the causes are known with cert a i n ty ins ome instance s su s pected in many and unknown ino t h ers Some ex ti rp a ti ons are local wh ereas others arem ore wi de s pre ad The difficulty in doc u m en ting thes 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 causesof pop u l a ti on declines can be obvi a ted direct ly Th ei 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 ingeneral (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 ofinvasive non-native species that could be harmful to rep-tile populations must be proscribed Third restrictingtrade in sensitive reptile species for which sustainableremoval cannot be demonstrated will require the passageor strengthening and enforcement of legislation In thecase of Asian turtles legislative remedies could be too lit-tle too latemdasha stopgap remedy is necessary The only wayto prevent the imminent extinction of a large number ofthe more than 80 species of turtles native to southern Asiawill be to maintain populations in ex situ captive breedingand genetic reserve programs With changes in culturalattitudesstrengthening of international trade regulationsand increased habitat protection the reintroduction ofthese species into the wild may be possible

Much of todayrsquos commercial exploitation of reptiles inthe United States and elsewhere requires urgent govern-mental action to implement internationally accepted andenforced controls Despite the fact that conservation mea-sures can be implemented effectively through legislation(as happened with legislation for protection of Louisianabox turtles and American alligators) the political pres-sures against accomplishing such goals cannot be overstat-ed The lack of support by the World Trade Organizationfor recommendations to curtail sea turtle exploitation(WTO 1998) brings the problem into perspective on aninternational scale

Direct and indirect effects of environmental pol lutiondisease and parasitism and global climate change aremore difficult to quantify in many instances and will bemore difficult to change in the short term Nonetheless wemust endeavor to understand these potential factors toameliorate their impact on natural populations of reptilesand their habitats

Finally long-term monitoring o f reptile populations isessential and must be aided by the establishment of stan-dard methods and techniques It is equally important thatthe academic community land managers and conserva-tion organizations recognize that rigorous field programsfocusing on the distri buti on a bu n d a n ce s t a tu s a n dtrends of populations and species are critical and worth-while Herpetofaunal inventories should become a stan-dard part of environmental assessment programs and thepublication of field survey efforts that document potentialor suspected declines should be encouraged When long-term and widespread monitoring becomes the normdeclines are likely to become less equivocal (in terms ofprotracted declines versus natural fluctuations) and thecauses less mysterious

662 BioScience August 2000 Vol 50 No 8

Articles

Sand monitor (Va ra nus go u l d i ) Al t h ou gh sandm o n i to rs (genus Va ra nu s wh i ch includes the wo rl d rsquo sl a rgest lizards) appear to be thriving in many pa rts oft h eir natu ral habitats in Au s tra l i a ot h er spe cies of t h egenus in As i a Afri c a and the East Indies are threa ten e dby exten s ive habitat destru cti o n

The disappearance of reptiles from the natural world isgenuine and should be a matter of concern not simplybecause of reptilesrsquo perceived associations with amphib-ians but because reptile declineslike those of amphibiansare growing and serious in their own right Current evi-dence suggests that amphibian and reptile declines whichare exacerbated by burgeoning human populations con-stitute a worldwide crisis

Ack n owl e d gm en t sManuscript preparation was aided by Financial AssistanceAw a rd Nu m ber DE-FC09-96SR18546 from the USDep a rtm ent of E n er gy to the Un ivers i ty of G eor gi aResearch Foundation We thank Ab Abercrombie JustinCongdon William Hopkins Laura Janecek ChristopherRomanek and Joseph Pechmann for discussion and com-ments on the manuscript We also appreciate the help ofStephen H Bennett John Cossel Jr Charles R PetersonPaul Moler Woody Woodwardand Jeff Corser for provid-ing information on the status of particular species Thispaper supports the PARC (Partners in Amphibian andReptile Conservation) effort to promote education aboutreptiles and amphibians

Ref eren ces ci te dAl 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 ndash 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 ndash 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 119 8 3 ndash 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 ndash 6 9

Banks B Beebee TJC Coo ke KS 1 9 9 4 Con s erva ti on of the natter jack toadB u fo calamita in Britain over the peri od 1976ndash1990 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 ndash 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 eRe 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 eUn i ted States of Am erica 95 9 0 3 1 ndash 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 ndash 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 rba 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 ndash 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 ofE nvi ron m ental Con t a m i n a ti on Tox i co l ogy 27 8 2 ndash 8 7

Bi s h op JM1 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 ndash 4 3 0

Bl a u s tein A R Hoffman PD Hokit DG Ki e s ecker JM Wa lls SC Hays JB1 9 9 4 a UV repair and re s i s t a n ce to solar UV-B in amph i bian eggs Alink to pop u l a ti on declines Proceed i n gs of the Na ti onal Ac ademy ofS c i en ce of the Un i ted States of Am erica 91 1 7 9 1 ndash 1 7 9 5

Bl a u s tein A R Hokit DG Orsquo Ha ra RK Holt RA 1 9 9 4 b Pa t h ogenic funguscon tri butes to amph i bian losses in the Pacific Nort hwe s t Bi o l ogi c a lCon s erva ti on 67 2 5 1 ndash 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 gs 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 andgl obal ex ti n cti on s Con s erva ti on Bi o l ogy 8 6 0 ndash 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 196ndash201 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 tech 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 ndash 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 theS tu dy of Am ph i bians and Repti l e s Herpeto l ogy Ci rc u l a ti on 22 1 ndash 7 2

Buhlmann KA 1 9 9 5 Ha bitat use terre s trial movem ents and con s erva ti onof 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 ogy2 9 1 7 3 ndash 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 201ndash232 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 amp 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 dIsland and Gu n n er rsquos Quoi n Ma u ri tiu s Bi o l ogical Con s erva ti on 371 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 ndash 1 3 6 9

Ca rey C 1 9 9 3 Hypothesis con cerning the causes of the disappe a ra n ce ofboreal toads from the mountains of Co l orado Con s erva ti on Bi o l ogy 73 5 5 ndash 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 52 7 2 ndash 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 peRomain Na ti onal Wi l dl i fe Ref u ge Ch em o s ph ere 34 5 3 9 ndash 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 1ndash15 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 lm a tu ri ty and dem ogra phics of Bl a n d i n grsquos tu rtles (Emyd o i d e abl 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 ndash 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 ivedor ga n i s m s Am erican Zoo l ogist 34 3 9 7 ndash 4 0 8

[CITES] Conven ti on on In tern a ti onal Trade in Endangered Species ofWild Fauna and Flora 2 0 0 0 lt 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 tmlgt (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 lrule to list the nort h ern pop u l a ti on of the bog tu rtle as thre a ten ed andthe 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 ndash 5 9 6 2 3

August 2000 Vol 50 No 8 BioScience 663

Articles

basis without mounting an intensive long-term samplingprogram The clandestine nature of many reptiles oftencombined with comparatively large home ranges lowpop u l a ti on den s i ti e s and ra reness of con grega ti on a lbehavior makes documenting population trends very dif-ficult As a result populations may wither with littlenoticeOnce an unmonitored species or population is rec-ognized as being unexpectedly depauperate or absent thecause of decline may be unknown and unknowable

Based on the accumulated evidence that many if notmost declines reported for amphibians are indeed realtheproper course for conservation initiatives is to assume theworst for all herpetofauna and therefore to implementabatement measures while gathering more data Althoughthe lack of long-term data often may preclude the id enti-fication of the cause of a decline or even in some cases thecorroboration o f a decline the absence of that data doesnot rule out the existence of a correctable problem

Co n clusion and re co m m en d a ti o n sThe declines of m a ny reptile pop u l a ti ons are similar tothose 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 ha m ph i bi a n s the causes are known with cert a i n ty ins ome instance s su s pected in many and unknown ino t h ers Some ex ti rp a ti ons are local wh ereas others arem ore wi de s pre ad The difficulty in doc u m en ting thes 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 causesof pop u l a ti on declines can be obvi a ted direct ly Th ei 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 ingeneral (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 ofinvasive non-native species that could be harmful to rep-tile populations must be proscribed Third restrictingtrade in sensitive reptile species for which sustainableremoval cannot be demonstrated will require the passageor strengthening and enforcement of legislation In thecase of Asian turtles legislative remedies could be too lit-tle too latemdasha stopgap remedy is necessary The only wayto prevent the imminent extinction of a large number ofthe more than 80 species of turtles native to southern Asiawill be to maintain populations in ex situ captive breedingand genetic reserve programs With changes in culturalattitudesstrengthening of international trade regulationsand increased habitat protection the reintroduction ofthese species into the wild may be possible

Much of todayrsquos commercial exploitation of reptiles inthe United States and elsewhere requires urgent govern-mental action to implement internationally accepted andenforced controls Despite the fact that conservation mea-sures can be implemented effectively through legislation(as happened with legislation for protection of Louisianabox turtles and American alligators) the political pres-sures against accomplishing such goals cannot be overstat-ed The lack of support by the World Trade Organizationfor recommendations to curtail sea turtle exploitation(WTO 1998) brings the problem into perspective on aninternational scale

Direct and indirect effects of environmental pol lutiondisease and parasitism and global climate change aremore difficult to quantify in many instances and will bemore difficult to change in the short term Nonetheless wemust endeavor to understand these potential factors toameliorate their impact on natural populations of reptilesand their habitats

Finally long-term monitoring o f reptile populations isessential and must be aided by the establishment of stan-dard methods and techniques It is equally important thatthe academic community land managers and conserva-tion organizations recognize that rigorous field programsfocusing on the distri buti on a bu n d a n ce s t a tu s a n dtrends of populations and species are critical and worth-while Herpetofaunal inventories should become a stan-dard part of environmental assessment programs and thepublication of field survey efforts that document potentialor suspected declines should be encouraged When long-term and widespread monitoring becomes the normdeclines are likely to become less equivocal (in terms ofprotracted declines versus natural fluctuations) and thecauses less mysterious

662 BioScience August 2000 Vol 50 No 8

Articles

Sand monitor (Va ra nus go u l d i ) Al t h ou gh sandm o n i to rs (genus Va ra nu s wh i ch includes the wo rl d rsquo sl a rgest lizards) appear to be thriving in many pa rts oft h eir natu ral habitats in Au s tra l i a ot h er spe cies of t h egenus in As i a Afri c a and the East Indies are threa ten e dby exten s ive habitat destru cti o n

The disappearance of reptiles from the natural world isgenuine and should be a matter of concern not simplybecause of reptilesrsquo perceived associations with amphib-ians but because reptile declineslike those of amphibiansare growing and serious in their own right Current evi-dence suggests that amphibian and reptile declines whichare exacerbated by burgeoning human populations con-stitute a worldwide crisis

Ack n owl e d gm en t sManuscript preparation was aided by Financial AssistanceAw a rd Nu m ber DE-FC09-96SR18546 from the USDep a rtm ent of E n er gy to the Un ivers i ty of G eor gi aResearch Foundation We thank Ab Abercrombie JustinCongdon William Hopkins Laura Janecek ChristopherRomanek and Joseph Pechmann for discussion and com-ments on the manuscript We also appreciate the help ofStephen H Bennett John Cossel Jr Charles R PetersonPaul Moler Woody Woodwardand Jeff Corser for provid-ing information on the status of particular species Thispaper supports the PARC (Partners in Amphibian andReptile Conservation) effort to promote education aboutreptiles and amphibians

Ref eren ces ci te dAl 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 ndash 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 ndash 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 119 8 3 ndash 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 ndash 6 9

Banks B Beebee TJC Coo ke KS 1 9 9 4 Con s erva ti on of the natter jack toadB u fo calamita in Britain over the peri od 1976ndash1990 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 ndash 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 eRe 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 eUn i ted States of Am erica 95 9 0 3 1 ndash 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 ndash 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 rba 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 ndash 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 ofE nvi ron m ental Con t a m i n a ti on Tox i co l ogy 27 8 2 ndash 8 7

Bi s h op JM1 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 ndash 4 3 0

Bl a u s tein A R Hoffman PD Hokit DG Ki e s ecker JM Wa lls SC Hays JB1 9 9 4 a UV repair and re s i s t a n ce to solar UV-B in amph i bian eggs Alink to pop u l a ti on declines Proceed i n gs of the Na ti onal Ac ademy ofS c i en ce of the Un i ted States of Am erica 91 1 7 9 1 ndash 1 7 9 5

Bl a u s tein A R Hokit DG Orsquo Ha ra RK Holt RA 1 9 9 4 b Pa t h ogenic funguscon tri butes to amph i bian losses in the Pacific Nort hwe s t Bi o l ogi c a lCon s erva ti on 67 2 5 1 ndash 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 gs 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 andgl obal ex ti n cti on s Con s erva ti on Bi o l ogy 8 6 0 ndash 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 196ndash201 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 tech 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 ndash 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 theS tu dy of Am ph i bians and Repti l e s Herpeto l ogy Ci rc u l a ti on 22 1 ndash 7 2

Buhlmann KA 1 9 9 5 Ha bitat use terre s trial movem ents and con s erva ti onof 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 ogy2 9 1 7 3 ndash 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 201ndash232 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 amp 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 dIsland and Gu n n er rsquos Quoi n Ma u ri tiu s Bi o l ogical Con s erva ti on 371 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 ndash 1 3 6 9

Ca rey C 1 9 9 3 Hypothesis con cerning the causes of the disappe a ra n ce ofboreal toads from the mountains of Co l orado Con s erva ti on Bi o l ogy 73 5 5 ndash 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 52 7 2 ndash 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 peRomain Na ti onal Wi l dl i fe Ref u ge Ch em o s ph ere 34 5 3 9 ndash 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 1ndash15 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 lm a tu ri ty and dem ogra phics of Bl a n d i n grsquos tu rtles (Emyd o i d e abl 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 ndash 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 ivedor ga n i s m s Am erican Zoo l ogist 34 3 9 7 ndash 4 0 8

[CITES] Conven ti on on In tern a ti onal Trade in Endangered Species ofWild Fauna and Flora 2 0 0 0 lt 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 tmlgt (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 lrule to list the nort h ern pop u l a ti on of the bog tu rtle as thre a ten ed andthe 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 ndash 5 9 6 2 3

August 2000 Vol 50 No 8 BioScience 663

Articles

The disappearance of reptiles from the natural world isgenuine and should be a matter of concern not simplybecause of reptilesrsquo perceived associations with amphib-ians but because reptile declineslike those of amphibiansare growing and serious in their own right Current evi-dence suggests that amphibian and reptile declines whichare exacerbated by burgeoning human populations con-stitute a worldwide crisis

Ack n owl e d gm en t sManuscript preparation was aided by Financial AssistanceAw a rd Nu m ber DE-FC09-96SR18546 from the USDep a rtm ent of E n er gy to the Un ivers i ty of G eor gi aResearch Foundation We thank Ab Abercrombie JustinCongdon William Hopkins Laura Janecek ChristopherRomanek and Joseph Pechmann for discussion and com-ments on the manuscript We also appreciate the help ofStephen H Bennett John Cossel Jr Charles R PetersonPaul Moler Woody Woodwardand Jeff Corser for provid-ing information on the status of particular species Thispaper supports the PARC (Partners in Amphibian andReptile Conservation) effort to promote education aboutreptiles and amphibians

Ref eren ces ci te dAl 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 ndash 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 ndash 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 119 8 3 ndash 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 ndash 6 9

Banks B Beebee TJC Coo ke KS 1 9 9 4 Con s erva ti on of the natter jack toadB u fo calamita in Britain over the peri od 1976ndash1990 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 ndash 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 eRe 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 eUn i ted States of Am erica 95 9 0 3 1 ndash 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 ndash 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 rba 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 ndash 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 ofE nvi ron m ental Con t a m i n a ti on Tox i co l ogy 27 8 2 ndash 8 7

Bi s h op JM1 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 ndash 4 3 0

Bl a u s tein A R Hoffman PD Hokit DG Ki e s ecker JM Wa lls SC Hays JB1 9 9 4 a UV repair and re s i s t a n ce to solar UV-B in amph i bian eggs Alink to pop u l a ti on declines Proceed i n gs of the Na ti onal Ac ademy ofS c i en ce of the Un i ted States of Am erica 91 1 7 9 1 ndash 1 7 9 5

Bl a u s tein A R Hokit DG Orsquo Ha ra RK Holt RA 1 9 9 4 b Pa t h ogenic funguscon tri butes to amph i bian losses in the Pacific Nort hwe s t Bi o l ogi c a lCon s erva ti on 67 2 5 1 ndash 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 gs 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 andgl obal ex ti n cti on s Con s erva ti on Bi o l ogy 8 6 0 ndash 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 196ndash201 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 tech 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 ndash 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 theS tu dy of Am ph i bians and Repti l e s Herpeto l ogy Ci rc u l a ti on 22 1 ndash 7 2

Buhlmann KA 1 9 9 5 Ha bitat use terre s trial movem ents and con s erva ti onof 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 ogy2 9 1 7 3 ndash 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 201ndash232 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 amp 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 dIsland and Gu n n er rsquos Quoi n Ma u ri tiu s Bi o l ogical Con s erva ti on 371 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 ndash 1 3 6 9

Ca rey C 1 9 9 3 Hypothesis con cerning the causes of the disappe a ra n ce ofboreal toads from the mountains of Co l orado Con s erva ti on Bi o l ogy 73 5 5 ndash 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 52 7 2 ndash 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 peRomain Na ti onal Wi l dl i fe Ref u ge Ch em o s ph ere 34 5 3 9 ndash 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 1ndash15 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 lm a tu ri ty and dem ogra phics of Bl a n d i n grsquos tu rtles (Emyd o i d e abl 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 ndash 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 ivedor ga n i s m s Am erican Zoo l ogist 34 3 9 7 ndash 4 0 8

[CITES] Conven ti on on In tern a ti onal Trade in Endangered Species ofWild Fauna and Flora 2 0 0 0 lt 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 tmlgt (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 lrule to list the nort h ern pop u l a ti on of the bog tu rtle as thre a ten ed andthe 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 ndash 5 9 6 2 3

August 2000 Vol 50 No 8 BioScience 663

Articles

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 lt 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 tmgt (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 3471 7 7 ndash 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 arsquos all i ga tor managem ent progra m an update1 9 8 7 ndash 1 9 9 5 Pa ges 410ndash428 in Crocod i l e s Proceed i n gs of the 13thWorking Meeting of the Crocodile Specialist Gro u p I U C N ndash The Worl dCon s erva ti on Un i on 11ndash17 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 gm i s t a kes wh en pred i cting shifts in species ra n ge in re s ponse to gl ob a lw a rm i n g Na tu re 391 7 8 3 ndash 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 tm a n a gem ent and amph i bian eco l ogy A revi ew of the North Am eri c a nl i tera tu re E nvi ron m ental Revi ews 3 2 3 0 ndash 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 ktu rt l e Stern ot h erus depre s su s Am erican Mi dlands Na tu ralist 1193 9 4 ndash 4 0 1

_ _ _ _ _ _ 1 9 9 3 S tra tegies for snake con s erva ti on Pa ges 363ndash394 in Sei gelRA 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 s165ndash200 in Benz GW Co llins DE ed s Aqu a tic Fauna in Peri l t h eSo 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 ackswamp snake Pa ges 6791ndash6795 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 sand 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 andCa 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 arsquosGreat Cen tral Va ll ey Con s erva ti on Bi o l ogy 10 1 3 8 7 ndash 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 397ndash417 in Bu r gh a rdt GM Rand A S ed s Ig u a n a sof 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 sand repti l e s Herpeto l ogical Revi ew 25 1 5 0 ndash 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 hra te and age at matu ri ty of male painted tu rt l e s C h rysemys pict aAm erican Mi dlands Na tu ralist 130 3 1 4 ndash 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 171 8 ndash 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 pbet ween tu rtle decline and human rec re a ti on E co l ogical App l i c a ti on s5 1 1 5 1 ndash 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 171ndash182 in Gibbons JW ed L i fe Hi s tory and Eco l ogy ofthe 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 tBad 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 sin the New Mi ll en iu m Proceed i n gs of the Pa rtn ers in Am ph i bian andReptile Con s erva ti on (PA RC) Con feren ce 2ndash4 June 1999 At l a n t a( G A ) Ai ken (SC) Savannah River Eco l ogy Labora tory Herp Outre achPu 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 ndash 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 421ndash427 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 trsquos 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 sin the Great Plains Bi o S c i en ce 47 2 8 7 ndash 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 andreprodu ctive abn orm a l i ties in repti l e s Com m ents in Tox i co l ogy 53 8 1 ndash 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 rdA R 1 9 9 4 Devel opm ental abn orm a l i ties of the gon ad and abn orm a ls ex horm one con cen tra ti ons in juvenile all i ga tors from con t a m i n a tedand con trol lakes in Flori d a E nvi ron m ental Health Pers pectives 1026 8 0 ndash 6 8 8

Gu i ll et te LJ Jr Crain DA Roon ey A A P i ck ford DB1 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 ndash 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 139ndash158 in Hermann SM ed The Lon gl e a f P i n eE 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 eTa 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 NewYork 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 ewUS Fish and Wi l dl i fe Servi ce Special Scien ce Report on Wi l dl i fe 2281 ndash 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 andrepti l e s Herpeto l ogy Jo u rnal 2 6 5 ndash 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 goSn 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 theSo ut h e a s tern Un i ted State s Wa s h i n g ton (DC ) US Army Corps ofE n gi n eers Technical Report SERDP- 9 8 - 2 Ava i l a ble from the US ArmyCorps 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 78 2 8 ndash 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 rpo ten tial role in amph i bian decl i n e s Pa ges 145ndash149 in Bohme WBi 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 e8th Ord i n a ry Gen eral Meeting of the Soc i etas Eu rop aea Herpeto l ogi-c a 23ndash27 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 ofFish Disease 4 3 8 9 ndash 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 447ndash453 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 ogywith an em phasis on fre s hw a ter tu rt l e s Pa ges 267ndash287 in Gibbons JWed 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 ndash 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 en1 7 9 9 ndash 1 8 0 4 Pt 1 Pa ri s S ch oell

I U C N ndash World Con s erva ti on Un i on 2 0 0 0 lt 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 tmgt (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 ndash 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 ndash 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 lex ti n cti on of Vi pera aspis in the nort h ern Swiss Ju ra mountainsAm ph i bi a - Reptilia 20 2 5 ndash 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 ati gri num stebbi n s i Diseases of Aqu a tic Organisms 31161ndash167

664 BioScience August 2000 Vol 50 No 8

Articles

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 ofthe Un i ted States of Am erica 91 7 4 8 7 ndash 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 ndash 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 78thAn nual Meeting of the Am erican Soc i ety of Ich t hyo l ogists and Her-peto l ogi s t s 16ndash22 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 2848 0 2 ndash 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 inVi etnam and Ch i n a Pa per pre s en ted at the Joint Meeting of Am eri c a nSoc i ety of Ich t hyo l ogists and Herpeto l ogi s t s Herpeto l ogi s t srsquo Le a g u e and Soc i ety for the Stu dy of Am ph i bians and Repti l e s 26 Junendash2 Ju ly1 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 216ndash229 in CARo 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 anenvi ron m ental sen ti n el Mu l tiple ti s sue assays using flow cytom etri ca n a lys i s E co tox i co l ogy 4 5 ndash 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 na 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 rsquos su rvey Am erican Mi dlands Na tu ralist 131 3 1 1 ndash 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 ncon s erva ti on initi a tive s Pa ges 345ndash353 in Lannoo MJ ed S t a tus andCon s erva ti on of Mi dwe s tern Am ph i bi a n s Iowa Ci ty (IA) Un ivers i tyof Iowa Pre s s

L i eberman S 1 9 9 4 Can CITES Save the Box Tu rtle Endangered Spec i e sTechnical Bu ll eti n US Dep a rtm ent of the In teri or Fish and Wi l dl i feServi ce Federal Regi s ter 19 (5) 1 5 ndash 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 anupland site in we s tern Pa n a m a Con s erva ti on Bi o l ogy 13 1 1 7 ndash 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 dCaym a n with a revi ew of the outcomes of anole introdu cti on s O eco l ogia 95 5 2 5 ndash 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 terof the Ca l i fornia Exo tic Pest Plant Council 3 4 ndash 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 sf rom Lake Bl ack s h e a r G eor gi a Jo u rnal of Wi l dl i fe Diseases 322 5 9 ndash 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 andn 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 ndash 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 aF l orida pop u l a ti on of f l a t woods salamander Con s erva ti on Bi o l ogy 104 2 6 ndash 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 hrsquosBi 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 canrsquot hide from hu n gry hu m a n s Ca m bodian Daily 1 ndash 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 lRegi s ter 63 4 3 1 2 9 ndash 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 1rsquoet h o l ogie et1 rsquo evo luti on drsquoune pop u l a ti on de Vi pera aspis (L) au nord du Ju raSu i s s e Am ph i bi a - Reptilia 5 3 7 3 ndash 3 9 3

Moulis RA 1997 Pred a ti on of the imported fire ant (S ol en opsis invi ct a) onl oggerh e ad sea tu rtle (C a retta caret t a) nests on Wa s s aw Na ti on a lWi l dl i fe Ref u ge G eor gi a Ch el onian Con s erva ti on and Bi o l ogy 24 3 3 ndash 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 perf 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 ndash 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 ndash 3 7 5

Oza GM 1 9 9 0 E co l ogical ef fects of the frogrsquos leg trade E nvi ron m en t a l i s t1 0 3 9 ndash 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 sin 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 ndash 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 ndash 8 4

Pechmann JHK S cott DE Sem l i t s ch RD Ca l dwell JP Vitt LJ G i bbons JW1 9 9 1 Declining amph i bian pop u l a ti on s The probl em of s ep a ra ti n ghuman impact from natu ral flu ctu a ti on s S c i en ce 253 8 9 2 ndash 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 ndash 6 1 8

Po u gh FH An d rews RM Cadle JE Crump ML Savi t z ky A H Wells KD1 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 ndash 6 1 5

Pri tch a rd PCH 1 9 6 7 L iving Tu rtles of the Worl d Neptune (NJ) T F HPu 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 theS 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 ldquon on decl i n i n grdquo a m ph i bi a npop u l a ti ons using power analys i s Con s erva ti on Bi o l ogy 9 1 2 9 9 ndash 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 perpre s en ted at Powderm i ll 1999 4th Occ a s i onal Fre s hw a ter Tu rtle Con-feren ce 13ndash16 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 andh a tchling harvest on Am erican all i ga tors in Flori d a Jo u rnal of Wi l dl i feMa n a gem ent 63 1 1 9 3 ndash 1 2 0 0

Rodda GH 1 9 9 2 Loss of n a tive reptiles assoc i a ted with introdu cti ons ofexo tics in the Ma riana Is l a n d s Pacific Scien ce 46 3 9 9 ndash 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 reand 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 ndash 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 s227ndash234 in Mi hu rs ky JA Ch a n ey A ed s New Pers pectives in theCh 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 Plan2nd ed lt 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 tmgt (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 andp 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 ter6 0 3 9 3 2 6 ndash 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 89ndash116 in Mac MJOp l er PA Haecker CEP Doran PD ed s S t a tus and Trends of t h eNa ti onrsquos Bi o l ogical Re s o u rce s Vo l 1 Re s ton (VA ) US Dep a rtm ent ofIn teri or US Geo l ogical Su rvey

August 2000 Vol 50 No 8 BioScience 665

Articles

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 forpon d - breeding salamanders Con s erva ti on Bi o l ogy 121113ndash1119

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 221ndash227 inKn obil E Nei ll JD ed s The Encycl opedia of Reprodu cti on Vo l 3 NewYork 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 frommu l ti l egged frogs Are reti n oids to blame Scien ce 284 8 0 0 ndash 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 inPen 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 ellUn 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 eeco l ogy of c a rpet pyt h ons Mo relia spilot a ( Serpen te s Pyt h on i d ae) inCoastal Eastern Au s tra l i a Bi o l ogical Con s erva ti on 76 1 1 3 ndash 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 ndash 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 toryTract 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 ndash 4 3 0

S po tila JR Dunham A E Leslie A J S teyerm a rk AC Plotkin PT Pa l adino FV1 9 9 6 Worl dwi de pop u l a ti on decline of Derm o ch elys co ri a ce a Arel 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 ndash 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 567 0 ndash 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 tech a n ge on tropical montane cloud fore s t s Na tu re 398 6 0 8 ndash 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 ndash 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 273 4 4 ndash 3 4 7

Th orn ton I 1 9 7 1 D a rwi nrsquos 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 lof Elisha Mi tch ell Scien tific Soc i ety 116(1) 1 9 ndash 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 gf rog Rh e oba tra chus silus Animal Beh avi or 29 2 8 0 ndash 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 lt en d a n gered f ws gov box s core h tmlgt (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 DJMi tch ell JFB G a rrett D Za k h a rov V F 1 9 9 9 G l obal warming andn ort h ern hem i s ph ere sea ice ex ten t S c i en ce 286 1 9 3 4 ndash 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 eform er lon gl e a f pine fore s t Pa ges 447ndash493 in Ma rtin W H Boyce SGE 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 amp Son s

Wi lliams T 1 9 9 9 The terri ble tu rtle trade Au du bon Ma gazine 101 4 4 ndash 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 rsquos thesisUn ivers i ty of Al a b a m a Tu s c a l oo s a A L

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