Aquatic Reptiles & Amphibians:Aquatic Reptiles & Amphibians:Review of modern groupsReview of modern groupsSelect biology and physiologySelect biology and physiologyMajor topics related to environment & diseaseMajor topics related to environment & disease

PHC6937PHC6937Brian A Stacy, DVM, PhD, DACVPBrian A Stacy, DVM, PhD, DACVPAquatic Animal HealthAquatic Animal Health

Lecture outlineLecture outline

Herps as indicator speciesHerps as indicator species

Review of amphibians & reptilesReview of amphibians & reptiles Modern groupsModern groups Select biology and physiologySelect biology and physiology Ecological and economic importanceEcological and economic importance Key health topics of concern for each groupKey health topics of concern for each group

Reptiles & amphibians as indicator speciesReptiles & amphibians as indicator species

Presence indicates the presence of a set of other species and whosePresence indicates the presence of a set of other species and whoseabsence indicates the lack of that entire set of speciesabsence indicates the lack of that entire set of species

Keystone speciesKeystone species Presence indicates human-created abiotic conditions such as air or waterPresence indicates human-created abiotic conditions such as air or water

pollutionpollution A dominant species that provides much of the biomass or number ofA dominant species that provides much of the biomass or number of

individuals in an areaindividuals in an area Indicates particular environmental conditions such as certain soil or rockIndicates particular environmental conditions such as certain soil or rock

typestypes Sensitive to environmental changes, such as global warming or modifiedSensitive to environmental changes, such as global warming or modified

fire regimes (sometimes called a bioindicator species), and serves as anfire regimes (sometimes called a bioindicator species), and serves as anearly warning indicatorearly warning indicator

Reflect the effects of a disturbance regime or the efficacy of efforts toReflect the effects of a disturbance regime or the efficacy of efforts tomitigate disturbance effectsmitigate disturbance effects

From: Lindenmayer DB, et al., 2000. Indicators of biodiversity forecologically sustainable forest management. Conservation Biology 14:941-950

Extant amphibians Extant amphibians –– 3 lineages 3 lineages

Anura Anura –– Frogs & toads Frogs & toads Cosmopolitan, except where limited by cold &Cosmopolitan, except where limited by cold &

dry habitatdry habitat

Urodela Urodela –– Salamanders & newts Salamanders & newts Primarily North America and EurasiaPrimarily North America and Eurasia

Gymnophiona Gymnophiona –– Caecilians Caecilians PantropicalPantropical

Chinese pressD Canatella JD Wilson

Amphibians - common biological featuresAmphibians - common biological features

Two-phase life cycle / MetamorphosisTwo-phase life cycle / Metamorphosis Obligate or facultative neotenyObligate or facultative neoteny Second, limited metamorphosisSecond, limited metamorphosis

External fertilization / unshelled eggsExternal fertilization / unshelled eggs Internal fertilization in some salamandersInternal fertilization in some salamanders Viviparous, marsupial, mouth-brooding formsViviparous, marsupial, mouth-brooding forms

Permeable skinPermeable skin Cutaneous respiration Cutaneous respiration (also lungs & gills)(also lungs & gills)

Characteristic ear sensory anatomyCharacteristic ear sensory anatomy Pedicellate teethPedicellate teeth

S Dalton

S Haberling

Amphibians Amphibians –– Ecological importance Ecological importance Amphibians as indicator speciesAmphibians as indicator species

Species and community levelsSpecies and community levels Perceived sensitivity to Perceived sensitivity to ““environmental stressenvironmental stress”” due to due to

permeable skin and biphasic life cyclepermeable skin and biphasic life cycle Exposure during life stages to aquatic and atmosphericExposure during life stages to aquatic and atmospheric

principlesprinciples Repositories of bioindicator chemicalsRepositories of bioindicator chemicals Locally abundant, low-cost samplingLocally abundant, low-cost sampling

Critical predators & preyCritical predators & prey

Amphibians Amphibians –– Food, pets, and more Food, pets, and more……..

Food: Estimated 180 million to >1 billionfrogs harvested/year

Research: Xenopus species are widelyused in research

Pet trade: Many species, largelyunmonitored

Invasive species: Displacement of nativespecies

Live bait industry: Many species,largely unmonitored

Amphibian population declinesAmphibian population declines Estimated 32% of amphibian species currently are in declineEstimated 32% of amphibian species currently are in decline

Identified threats include:Identified threats include: Habitat lossHabitat loss Introduction of invasive species and pathogensIntroduction of invasive species and pathogens Increasing UVB exposureIncreasing UVB exposure Pollution (agricultural, acidification, etc.)Pollution (agricultural, acidification, etc.)

Initially debated as an over-reaction to natural or randomInitially debated as an over-reaction to natural or randomphenomenaphenomena Historical variation in amphibian population, lack of data based onHistorical variation in amphibian population, lack of data based on

long-term monitoringlong-term monitoring

Now well regarded as catastrophic phenomena with extinctionNow well regarded as catastrophic phenomena with extinctionrates far surpassing background ratesrates far surpassing background rates

Stuart SN, et al., 2004. Status and trends of amphibian declines and extinctionsworldwide. Science 306: 1783-1786

Key Health TopicsKey Health Topics

ChytridiomycosisChytridiomycosis

RanavirusRanavirus infections infections

MalformationsMalformations

UV radiationUV radiation

Habitat acidificationHabitat acidification

Climate changeClimate change

ChytridiomycosisChytridiomycosis Etiologic agent: Etiologic agent: BatrachochytridiumBatrachochytridium dendrobatidisdendrobatidis ((SporozooicSporozooic

fungus)fungus) Associated with multiple amphibian population declinesAssociated with multiple amphibian population declines First described in 1998 during mass mortality events in PanamaFirst described in 1998 during mass mortality events in Panama

and Australiaand Australia Oldest known record: 1938, Oldest known record: 1938, XenopusXenopus laevislaevis

Some hypotheses generated since discovery:Some hypotheses generated since discovery: Organism is endemic and declines only recently recognizedOrganism is endemic and declines only recently recognized Organism endemic and recently became more pathogenicOrganism endemic and recently became more pathogenic Organism is endemic and attains enhanced pathogenic potential whenOrganism is endemic and attains enhanced pathogenic potential when

combined with other factorscombined with other factors Climate-linked epidemic hypothesisClimate-linked epidemic hypothesis

Introduced invasive pathogenIntroduced invasive pathogen

Savethefrogs.com

J Parker

•• Outbreaks may be insidious, persistent, andOutbreaks may be insidious, persistent, andeasily overlookedeasily overlooked

••Prevalence varies by season, elevation, andPrevalence varies by season, elevation, andregion (higher in cooler, moist environmentsregion (higher in cooler, moist environments

•• Apparent variation in species susceptibility Apparent variation in species susceptibility

•• Widespread Widespread subclinical infectionsubclinical infection documented documentedin some areasin some areas

• Mortality in postmetanephricfrogs & toads

ChytridiomycosisChytridiomycosis

Point: Evidence for climate-linked epidemic hypothesisPoint: Evidence for climate-linked epidemic hypothesis Pounds JA et al., 2006. Widespread amphibian extinctions from epidemic disease drivenPounds JA et al., 2006. Widespread amphibian extinctions from epidemic disease driven

by global warming. Nature 39: 41-48by global warming. Nature 39: 41-48

Counterpoint: Data support introduction of invasive pathogenCounterpoint: Data support introduction of invasive pathogenhypothesishypothesis Lips KA et al., 2008. Riding the wave: reconciling the roles of disease and climate changeLips KA et al., 2008. Riding the wave: reconciling the roles of disease and climate change

in amphibian declines. in amphibian declines. PloSPloS Biology 6: 441-454 Biology 6: 441-454

Blame it all on Blame it all on XenopusXenopus?? Weldon C, et al., 2004. Origin of amphibian Weldon C, et al., 2004. Origin of amphibian chytridchytrid fungus. Emerging Infectious Diseases fungus. Emerging Infectious Diseases

10: 2100-210510: 2100-2105

Why widespread and subclinical in some areas (eastern NA) andWhy widespread and subclinical in some areas (eastern NA) andassociated with catastrophic die-offs in others?associated with catastrophic die-offs in others? RothermelRothermel BB, et al., 2008. Widespread occurrence of amphibian BB, et al., 2008. Widespread occurrence of amphibian chytridchytrid fungus fungus

BatrachochytridiumBatrachochytridium dendrobatidisdendrobatidis in the southeastern USA. Diseases of Aquatic in the southeastern USA. Diseases of AquaticOrganisms 82: 3-18Organisms 82: 3-18

Next logical step: Broad Next logical step: Broad phylogeneticphylogenetic study? study?

RanavirusRanavirus ( (IridovirusIridovirus) infections) infections First regarded as First regarded as ““orphanorphan”” viruses, then increasing recognition as viruses, then increasing recognition as

important pathogens starting ~20 years agoimportant pathogens starting ~20 years ago

May be actual disease agent in classic cases of May be actual disease agent in classic cases of ““red legred legsyndromesyndrome”” –– missed for years missed for years

Primarily larval salamanders, tadpoles, and recent Primarily larval salamanders, tadpoles, and recent metamorphsmetamorphs Asymptomatic adult carriers suspectedAsymptomatic adult carriers suspected

Multi-organ pathological lesionsMulti-organ pathological lesions

EpizootiologyEpizootiology Outbreaks with >90% mortalityOutbreaks with >90% mortality In North America:In North America:

Primarily have involved widespread, abundant speciesPrimarily have involved widespread, abundant species May be precipitated by dense crowdingMay be precipitated by dense crowding Summer monthsSummer months

Green DE, et al., Epizootiology of sixty-four amphibianmorbidity and mortality events in the USA, 1996-2001. Annalsof the New York Academy of Science 969: 323-339

• Commercial trade potential source forintroduction

•Picco AM & Collins JP, 2008. Amphibian commerceas a likely source of pathogen pollutionConservation Biology 22: 1582-1589

MalformationsMalformations Documented for since the 1700Documented for since the 1700’’ss

Populations with high prevalence source of concern in recentPopulations with high prevalence source of concern in recentyearsyears

Complex issue with variation in observations and trends at variousComplex issue with variation in observations and trends at varioussitessites

Four major causes identified Four major causes identified (USGS NWHC)(USGS NWHC):: TrematodeTrematode infections near limb buds infections near limb buds ContaminantsContaminants Injuries inflicted by predatorsInjuries inflicted by predators Nutritional deficienciesNutritional deficiencies

R Williams J Kieseker

Johnson PT, et al., Aquatic eutrophicationpromotes pathogenic infection in amphibians.PNAS 104: 15781-86

Ultraviolet radiationUltraviolet radiation Levels of UV radiation reaching earthLevels of UV radiation reaching earth’’s surface have increaseds surface have increased

since the 1970since the 1970’’ss

Amphibians thought to be susceptible to lethal and Amphibians thought to be susceptible to lethal and sublethalsublethaleffects due, especially due to shell-less eggseffects due, especially due to shell-less eggs Deformities, poor survival, endocrine disruptionDeformities, poor survival, endocrine disruption

Actual effect unknown, laboratory results mixedActual effect unknown, laboratory results mixed

Review: Croteau MC, et al., Global increases in ultraviolet B radiation: potential impacts onamphibian development and metamorphosis. Physiological and Biochemical Zoology 81: 743-761

Anthropogenic habitat acidificationAnthropogenic habitat acidification Cause by atmospheric deposition of sulfate and nitrogenCause by atmospheric deposition of sulfate and nitrogen

Concern as a contributor to amphibian population declinesConcern as a contributor to amphibian population declines

Acidic habitats (natural and anthropogenic) known to precludeAcidic habitats (natural and anthropogenic) known to precludesome speciessome species

Sub-lethal and lethal effects also knownSub-lethal and lethal effects also known

Clear association with amphibian declinesClear association with amphibian declinesnot demonstratednot demonstrated

Dunson WA, et al., 1992. A symposium on amphibiandeclines and habitat acidification. Journal ofHerpetology 26: 349-352

JD Wilson

Obvious concern with desiccation / loss of wetlandsObvious concern with desiccation / loss of wetlands

Confounding influence for other problemsConfounding influence for other problems PathogensPathogens Disease spread, manifestationDisease spread, manifestation

Global climate changeGlobal climate change

McMenamin SK, et al., 2008. Climate changeand wetland desiccation cause amphibiandecline in Yellowstone National Park. PNAS105: 16988-93

Extant reptiles Extant reptiles –– 2 lineages 2 lineages AnapsidsAnapsids

Turtles & tortoisesTurtles & tortoises

DiapsidsDiapsids Crocodilians, birds, tuataras, lizards, snakesCrocodilians, birds, tuataras, lizards, snakes

Tamar IbamaDivegallery.com R Stewart

SchmukyTheCat.images

Reptiles - some biological featuresReptiles - some biological features Many Many ““uniquely reptilianuniquely reptilian”” traits are less obvious features of traits are less obvious features of

anatomyanatomy

Shelled, amniotic eggsShelled, amniotic eggs Viviparous formsViviparous forms

Heavily keratinized skinHeavily keratinized skin

EctothermicEctothermic Various degrees of Various degrees of endothermyendothermy exhibited by marine turtles exhibited by marine turtles

Temperature dependent sex determinationTemperature dependent sex determination Crocodilians, chelonians,Crocodilians, chelonians,

some lizardssome lizards Multiple patternsMultiple patterns

Knowledge base on diseases ofreptiles is heavily biased towardscaptive animals

Reptilian phenomenaReptilian phenomena

Breeding aggregations of red-sided gartersnakes in Manitoba Canada

C Creighton D Perrine

Olive ridley turtle arribadas

Complex life histories, distant migrations ofmarine turtles

Maternal protection in prehensile-tail skinks

Reptiles Reptiles –– Ecological importance Ecological importance

Indicator speciesIndicator species Numerous regarded as indicator species for wetlands, tropicalNumerous regarded as indicator species for wetlands, tropical

marine, lake and river systemsmarine, lake and river systems Ecological requirements of many are precise and well-studiedEcological requirements of many are precise and well-studied Keystone speciesKeystone species Repositories of heavy metals and contaminantsRepositories of heavy metals and contaminants

Important predator & prey speciesImportant predator & prey species

T Brennan

Reptiles Reptiles –– Other important pointsOther important points

C East

Commerce: Turtle farming and wild turtletrade is a multi-million dollar industry andis at the core of a conservation crisis forsome species

Commerce: Crocodilian ranching /farming is a multi-million dollar industryand a conservation tool

Human conflicts: Snake bite and bigpredators

Invasive species: Many examplesP Morris / Guam rail SSP

Reptilian population declines - Reptilian population declines - big problem with less pressbig problem with less press

More reptilian species than amphibians listed under ESAMore reptilian species than amphibians listed under ESAand IUCNand IUCN

Often go unreported, unmonitoredOften go unreported, unmonitored Gibbons JW, et al., 2000. The global decline of reptiles, déjà vu amphibians. BioscienceGibbons JW, et al., 2000. The global decline of reptiles, déjà vu amphibians. Bioscience

50: 653-66650: 653-666

Habitat degradation the key concernHabitat degradation the key concern Gardner TA, et al., Paradox, presumption and pitfalls in conservation biology: TheGardner TA, et al., Paradox, presumption and pitfalls in conservation biology: The

importance of habitat change for amphibians and reptiles. Biological Conservation 138:importance of habitat change for amphibians and reptiles. Biological Conservation 138:166-179166-179

Greater home ranges, may be more susceptible to habitatGreater home ranges, may be more susceptible to habitatfragmentation and threats that cross geopolitical bordersfragmentation and threats that cross geopolitical borders

Winne CT, et al., 2007. Enigmatic decline of a protected population ofeastern kingsnakes, Lampropeltis getula, in South Carolina. Copiea3: 507-519

S Pinker

Select topics related to environmentalSelect topics related to environmentalstress/disturbance & reptilesstress/disturbance & reptiles

Degradation / loss of nesting habitatDegradation / loss of nesting habitat

Temperature-dependent sex determination and climateTemperature-dependent sex determination and climatechangechange Janzen FJ, 1994. Climate change and temperature-dependent sex determination inJanzen FJ, 1994. Climate change and temperature-dependent sex determination in

reptiles. Proceedings of the National Academy of Science 91: 7487-7490reptiles. Proceedings of the National Academy of Science 91: 7487-7490 WapstraWapstra E, et al., 2009. Climate effects of offspring ratio of a E, et al., 2009. Climate effects of offspring ratio of a vivaparousvivaparous lizard. Journal of lizard. Journal of

Animal Ecology 78: 84-90Animal Ecology 78: 84-90

Pollution / contaminationPollution / contamination MilnesMilnes MR, et al., 2008. Increased MR, et al., 2008. Increased posthatchingposthatching mortality and loss of sexually dimorphic mortality and loss of sexually dimorphic

gene expression in alligators (gene expression in alligators (Alligator Alligator mississippiensismississippiensis) from a contaminated) from a contaminatedenvironment. Biology of Reproduction 78: 932-938environment. Biology of Reproduction 78: 932-938

Harmful algal bloomsHarmful algal blooms

Enigmatic diseases /Enigmatic diseases /mortality eventsmortality events

M Nichols

FibropapillomatosisFibropapillomatosis of marine turtles of marine turtles

Best studied and most significant in green turtlesBest studied and most significant in green turtles

PanzooticPanzootic, prevalence has increased from the 1980, prevalence has increased from the 1980’’s throughs throughpresent daypresent day

Associated with Associated with herpesviralherpesviral infection, but cofactors strongly infection, but cofactors stronglysuspectedsuspected Foley AM, et al., 2005. Foley AM, et al., 2005. FibropapillomatosisFibropapillomatosis in stranded green turtles ( in stranded green turtles (CheloniaChelonia mydasmydas))

from the eastern United States (1980-98): Trends and associations with environmentalfrom the eastern United States (1980-98): Trends and associations with environmentalfactors. Journal of Wildlife Diseases 41: 29-41factors. Journal of Wildlife Diseases 41: 29-41

22% of stranded turtles in Florida, highest prevalence on Gulf22% of stranded turtles in Florida, highest prevalence on Gulfcoast (51.9%)coast (51.9%)

Reptiles and mass mortality eventsReptiles and mass mortality events Documented in turtles and crocodilians worldwideDocumented in turtles and crocodilians worldwide

American alligators, Lake Griffin 2000American alligators, Lake Griffin 2000 GharialGharial, Northern India 2008, Northern India 2008 Nile crocodiles, South Africa 2008-2009Nile crocodiles, South Africa 2008-2009 Loggerhead sea turtles, Florida 2000/01, 2006Loggerhead sea turtles, Florida 2000/01, 2006 Freshwater turtles, Florida 2007 (2 events), 2009?Freshwater turtles, Florida 2007 (2 events), 2009?

Important pointsImportant points

Reptiles and amphibians are diverse groups of animals with aReptiles and amphibians are diverse groups of animals with abroad range of unique features and adaptation to aquaticbroad range of unique features and adaptation to aquaticenvironmentsenvironments

Both include well-recognized indicator speciesBoth include well-recognized indicator species

Worldwide declines are of great concern and will result in furtherWorldwide declines are of great concern and will result in furtherextinctions and regional extirpations in coming yearsextinctions and regional extirpations in coming years

Critical areas of concern are habitat loss, introduction ofCritical areas of concern are habitat loss, introduction ofpathogens, invasive species, pollution, climate change, non-pathogens, invasive species, pollution, climate change, non-sustainable use, and other anthropogenic influencessustainable use, and other anthropogenic influences

QuestionsQuestions