snake fungal disease in canada rapid threat assessment · canada has 26 species1 of snakes. eight...

CREATING A WORLDTHAT IS SAFE AND SUSTAINABLE

FOR WILDLIFE AND SOCIETY

Snake Fungal Disease in CanadaRapid Threat Assessment

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Snake Fungal Disease in Canada Rapid Threat Assessment

ContentsExecutive summary 1Purpose of the assessment 3 Rationale for the threat assessment 3Format of the report 4Part 1- Overview of snake fungal disease (SFD) 5Part 2 – Answering questions from the decision framework 7 AretheresusceptiblespeciesinCanada? 7 SFDinCanada 7 WasSFDexpected? 10 CanSFDcauseseriousharm? 12 Aretherehighlevelsand/orpersistentexposuretothethreat? 14 Arethereknown,effectivemeanstoprevent,mitigateoreliminatetheharmsfromthethreat? 16 CanSFDbegeographicallyisolated? 18 CanvulnerabilitybereducedtoSFD? 19 MonitoringandSurveillance 21Conclusions and recommendations 23Appendix 1: Decision tree framework for the threat assessment of SFD 29 Usingthedecisiontree 30Appendix 2: Diagnosing SFD 34Appendix 3: Summary of key cases in SFD history 37Appendix 4: Citations 39

Prepared for Environment and Climate Change Canada

Prepared by the Canadian Wildlife Health CooperativeCraigStephen,LennyShirose,HeindrichSnyman

January, 2017





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Executive summary

Snakefungaldisease(SFD)isanemerginganddebilitatingdiseaseaffectingavarietyoffreerangingandcaptivesnakespeciesacrossNorthAmerica.ItwasfirstdocumentedinCanadain2015insouthernOntariointheendangeredeasternfoxsnake.SFDhassincebeendetectedintheendangeredqueensnakeinOntarioanditspathogenhasbeendetected,withoutdiseaseinOntariointheeasternfoxsnake,queensnake,easternmassassauga(allthreatened-endangered),and5subspeciesofgartersnakes(statusnotdetermined).

The purpose of this assessment is: tohelptheWildlifeIssuesUnit,WildlifeManagementandRegulatoryAffairs,CanadianWildlifeServicedetermineactionstobetakenonSFDtosupporttheunit’smandateofpreservingwildlifehealthinCanadianspeciesandoverallactivitiesofpolicydevelopmentandimplementationtothatend.

Snake fungal disease is an example of managing uncertainty. Therecentappearanceofthedisease,scantinvestmentortimeforresearchandinvestigation,lackofongoingsurveillanceofsnakehealthandgenerallackofecologicalandmonitoringinformationonCanadiansnakepopulationsprecludesaquantitativeriskassessmentoraconfidentforecastofthefutureimpactsandbehaviourofSFD.

TheCanadianWildlifeHealthCooperativecreatedadecisiontreetohelptransparentlyassessthecredibilityandseriousnessofSFDasathreattoCanadianbiodiversityandtoinformtheneedornatureofriskmanagementactions.Fromthisweconcluded:

1. SFD is a credible threat to Canadian biodiversity but the magnitude of the harms caused by SFD cannot be estimated with confidence. WhilethereremainmanyuncertaintiesabouttheextentofpopulationeffectsofSFDandtheconditionsunderwhichtheseeffectsresultinseriousandirreversibleharms,aprecautionaryapproachwouldsuggestitcanbeasignificantadditivestressorandshouldbeconsideredseriousforspeciesatriskand/orforpopulationsstrugglingwithothercumulativestressors.Thereareanalogoussituationswhereemergingfungaldiseaseshavehadprofoundconservationeffectsonwildanimalsandplants.WhileitisnotsurprisingthatSFDisinCanada,wehavelittleinformationwithwhichtopredictwhereSFDwillspreadinspace,timeorspeciesandwhichpopulationsaremostvulnerable.Wecannotbeassureditisnotinotherlocationsorspeciesduetothelowlevelofsubmissionstodiagnosticlaboratoriesandcomparativelylowlevelofpopulationmonitoringandhealthassessment.

2. It is not currently possible to forecast the epidemiological or ecological fate of SFD in Canada. SFDisanewlydescribedcondition,involvinganunderstudiedpathogenoccurringinspecieshistoricallysubjecttolittlediseasesurveillancewithalmostnodataontheassociationofSFDandpopulationabundanceanddistribution.EstimatesofSFDasaconservationriskandidentificationofhighriskscenariosare,todate,largelyopinionbased,relyingheavilyoncasestudiesandanalogy.ImpactsofSFDonindividualanimals,differentpopulationsanddifferentspeciesisvariableorpoorlydocumentedundernaturalconditions.ThecasualmechanismsofSFD,especiallytheroleofenvironmentriskfactorsremainunresolved,precludingrankingofSFDriskfactors.

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3. There are reasonable grounds to implement a management response to SFD. RespondingtoSFDwouldbeconsistentwiththemissionoftheWildlifeIssuesUnitandwouldcontributetoprotectingspeciesatriskandpreparingthemforfurtherimpactsfromclimatechange.Canadahas26species1ofsnakes.Eightareendangered,5arethreatened,4areofspecialconcern.SeveralthreatenedandendangeredspeciesinCanadaaresusceptibletothediseaseandsomearealreadyknowntobeinfectedoraffected.CanadacannotbeassuredthatSFDisnewtothecountryandisrestrictedonlytothetwospeciesdiscoveredwithSFDtodatebecauseofchallengesinmonitoringsnakehealthandsubjectingthemtodiagnosticassessments.

4. There are limited options to directly manage SFD. DeficienciesinknowledgeaboutthetransmissionsystemforSFDplusthepracticallimitationstoconstrainingthemovementsoffree-ranginganimalsmakeisolationorquarantineimpracticalforwildsnakes.Becauseofprevailinguncertainties,aprecautionaryapproachwouldbetolimitfurtherreleaseofthefungusassociatedwithSFDintotheenvironmentthrougheducationcampaignstothepettradeandherpetologiststoadvocateandsupportbiosecurityandtopreventunintentionalmovementofthefungusfromaknownSFD-positiveareatoareasofunknownorassumednegativestatus.Therearenoprovenmethodstoprevent,mitigateoreliminateharmstopopulationsfromSFDthroughstandardveterinaryinterventions.Therehasbeensomesuccessintreatingindividualanimals,anactionthatmaybeimportantincriticallyendangeredspecieswhereeachindividualanimalisrequiredtomaintainthegeneticdiversityofthepopulation.

5. A reasonable argument can be made to invest in a harm reduction approach focussed on increasing capacity to cope with SFD. ReducingpopulationvulnerabilitythroughaharmreductionapproachwouldsynergizewithspeciesrecoveryplansandattackplausibleSFDriskfactors.Vulnerabilityresultsfromacombinationofexposure,susceptibility,capacitytocopeandcumulativeeffectsofotherstressors.AstherearenocurrentoptionstoreduceexposureorSFD-specificsusceptibilityinfreerangingpopulations,vulnerabilityreductionmustfocusonimprovingindividualandpopulationresilienceandmanagingplausibleenvironmentalriskfactorsorcausalco-factors.Thesuggestedco-factorsinfluencingthespreadandeffectsofSFDoverlapwiththemajorchallengesfacingsnakesinCanada(ex.climate,habitatloss,habitatdegradation).Snakehealthmanagement,withspecificattentiontoSFDandotherunknowndiseases,shouldbeintegratedintospeciesmanagementplansduetosynergiesincurrentrecoveryplansandbestevidencetodealwithSFD.EffortsshouldbedirectedtoidentifyingvulnerablepopulationsbyoverlayinginformationonputativeSFDriskfactorsandpopulationstatus.SurveillancespecifictoSFDshouldtargetvulnerablepopulationsandthecurrentleadingedgesofthedisease’sknowndistributioninCanada.OutreachshouldencourageincreasedsubmissionsofsnakecasestotheCanadianWildlifeHealthCooperativeandlinkingthosediagnosticresultstosnakepopulationdatatobetterestimatetherolefordiseases,includingSFD,withpopulationoutcomes.

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1Canadahas26speciesbutsomearesplitintosubspeciesforstatusreports,givingatotalof33






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Purpose of the assessment

TheWildlifeIssuesUnit,WildlifeManagementandRegulatoryAffairs,CanadianWildlifeService,EnvironmentandClimateChangeCanada,requestedathreatassessmentonsnakefungaldiseasetodetermineactiontobetakenonthediseasetosupporttheunit’smandateofpreservingwildlifehealthinCanadianspeciesandoverallactivitiesofpolicydevelopmentandimplementationtothatend.

The objective of this threat assessmentistodeterminetheoptionstoprotectCanadiansusceptiblespeciesfromsnakefungaldisease(SFD)anditsetiologiccause,Ophidiomyces ophiodiicola.ItwillfocusonreviewingwhichspeciesinCanadaarevulnerabletothedisease,whatcircumstancesaffectspeciesvulnerabilityandCanada’scapacitytoidentify,assess,andmanagebiodiversityandecosystemrisksfromthisdisease.Unlikeariskassessment,thepurposeisnottoassesstheprobabilityormagnitudeofeffects,butrathertoidentifygapsandweaknessesinCanada’sthreatmanagementcapacityandthustoinformtheneedornatureofresponsetothisemergingdisease.

The purpose of the report istoassessthecredibilityandseriousnessofsnakefungaldiseaseasathreattoCanadianbiodiversityorothervaluesandtoinformtheneedornatureofriskmanagementactions

Rationale for the threat assessmentKey Points

• ManyCanadiansnakespeciesareconfrontingmultiplestressors.Theadditionofanewdiseasewouldfurthercomplicaterecoveryplans

• SFDhasbeendetectedinCanadaanditsrangeisexpandingintheeasternUnitedStates• Emergingfungihaveseverelyimpactedotherwildlifespecies,elevatingemergingfungaldiseaseslike

SFDtobeconservationconcerns.• Therearemultipleuncertaintiespreventinganevidence-baseddiseaseresponseorassessmentof

theecologicalorpopulationimplicationsofSFD

DetailsGlobally,nearlyoneinfivereptilespeciesarethreatenedwithextinction,withanotheroneinfivespecieslackingsufficientinformationtoassesstheirpopulationstatus(Böhmetal,2013).Thebreadthofspecies,geographicscope,andseverityofdeclinesinreptilepopulationsislikethosebeingexperiencedbyamphibians.Canadahas26speciesofsnakeswith33distinctsubspecies.COSEWIClists4asspecialconcern,5threatenedand9endangeredinatleastpartoftheirrange.Thestatusof12hasnotbeenestablished.Thecauseofreptilepopulationdeclinesisknownwithcertaintyinsomeinstances,suspectedinmany,andunknowninothers(Gibbonsetal,2000).HabitatdestructionandroadmortalityareproblemsforalmosteverysnakespeciesinCanadaandtheyarefactorsthatleadtosmall,isolated,geneticallydepauperatepopulationsthataremorepronetostochasticevents,suchasdiseaseoutbreaks.

Inmid-March2015,anadultfemaleeasternfoxsnake(Pantherophis vulpinus)withsignsofdermatitiswasaccidentallydisturbedwhilehibernatingnearLakeErieinOntario.ThiswasthefirstdocumentedcaseofSFDinCanada.Thediseasehassincebeendiagnosedinthequeensnake(Regina septemvittata)inOntarioand

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thefungusOphidiomyces ophiodiicola (believedtobetheproximatecauseofSFD)hasbeendetectedin3otherCanadianspecies(Seetable1).BoththeeasternfoxsnakeandqueensnakearelistedasendangeredbyCOSEWIC.

SFDhasbeenshowingupwithincreasingfrequencyinsnakesaroundtheeasternandmidwesternUnitedStatessince2006.Emergingfungalinfectionscausingwidespreadpopulationdeclineshaveincreasinglybeendocumentedacrossdiversetaxafrombats,andfrogs,tocoralsandbees(Fisheretal,2012).Emergingfungalpathogensandthere-emergenceofpreviouslyuncommonfungaldiseasesinpeoplehasbeenassociatedwithanincreasingnumberofsusceptiblepeopleduetoconcurrentimmunosuppressivefactorssuchasHIV,cancertherapyandothercauses.

Thebiologyoffungalpathogensprovidesthemtheabilitytobeaprimarydriverofpopulationextinctions.Theindependenceofmanyfungalpathogensfromtheirhostsmaypromotetheirsurvivalandvirulenceinnewecosystemsandnovelhostspecies,precludingtheirattenuationtolessvirulentforms,asisoftenseeninbacterialandviralpathogens(IOM,2011).

Giventhesevereconservationimpactsofotheremergingfungaldiseasessuchaswhitenosesyndromeinbats,salamanderchytriddiseaseandfrogchytriddisease,conservationistsfearSFDcouldposeasimilarthreattosnakes.

Format of the report

Adecisionframeworkwascreatedtoguidethisassessment(appendix1).Thereaderisencouragedtoreviewthisappendixpriortoreadingthereport.

Part1ofthereportprovidesabriefhistoryandoverviewofSFD.

Part2goesthroughthestepsinthedecisionframework.At each step, key points summarize the answers to the questions in the decision framework. More detailed information follows them. AdditionalinformationonSFDisprovidedintheappendices.

Theguidingframeworkconsistentofsixquestions:1. AretherespeciessusceptibletothisdiseaseinCanada?2. Wasthediseaseexpected?3. Canthediseasecauseseriousharm?4. Aretheiropportunitiesforhighlevelsand/orwidespreadexposuretothecausativeagentand/orrisk

factors?5. Arethereproveneffectivemethodstorespondtoandeliminateormitigatethethreat?6. Arethereprovenwaystocontainorisolatethethreat?

Underconditionsofuncertaintywehavetakenaprecautionaryapproachandassumedtheanswerinthedecisiontreequestionstobeyeswhen(i)analogoussituationspresentareasonableprobabilitythecorrectanswerisyes;(ii)thespeciesatriskarehighlyvalued;(iii)therearemultiplespecies(includingpeople)thatmaybeatriskand/or(iii)therearemultiplepossibleharms.

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Part 1- Overview of snake fungal disease

Key Points• SFDisanewlydescribeddisease,butitsfungaletiologyislikelyanendemicenvironmentalorganism

thatactsasanopportunisticpathogenunderconduciveconditions.• SFDispresentinOntarioaswellasin20easternstatesintheUSA.• TheeffectsofSFDvarybyspecies,populationandindividualbuttherearereportsofthisbeinga

fataldiseaselinkedtopopulationdeclines.• Environmentalco-factorsappeartoplayanimportantroleintheemergenceandimpactsofSFD

Details

Brief history of the diseaseSFDisanemerginganddebilitatingskindiseasesyndromeaffectingavarietyoffreerangingandcaptivesnakespeciesacrossNorthAmerica.Diseasereportsinfreerangingwildpopulationshavegenerallybeengeographicallyrestricted,withmostcasesbeinglimitedtotheeasternUnitedStates.SomeofthefirstSFDreportsoriginatedinNewHampshire,in2006wherethediseasewasassociatedwitha50%populationdeclineinapopulationoftimberrattlesnakes(Crotalus horridus)(Clarketal.2011).SFDhasnowbeenidentifiedin20U.S.states(Ohio,NewJersey,Massachusetts,NewYork,Florida,Alabama,Minnesota,NewHampshire,SouthCarolina,Wisconsin,Connecticut,Vermont,Virginia,Kentucky,Louisiana,Illinois,Pennsylvania,Georgia,Michigan,Tennessee)andOntario.(Cheatwoodetal.2003;Rajeevetal.2009;Clarketal.2011;Allenderetal.2011;Allenearetal2013;Fentonetal.2015;McBrideetal.2015;Tetzlaffetal.2015;Allenderetal.2016;Gloriosoetal.2016;Guthrieetal.2016;Lorcheta.l2016;Okhuraetal.2016;Ravesietal.2016).

Figure1presentsSFD’sgeographicdistribution.

What causes SFD?ThenameSFDhasbeenproposedtoexclusivelyrefertoskindiseaseassociatedwithinfectiononlywiththefungusOphidiomyces ophiodiicola(Lorchetal.2015).O. ophiodiicolawasoriginallyisolatedandcharacterizedfromanabscessinacaptiveblackratsnake(Elaphe obsoleta obsolete)(Rajeevetal.2009).O. ophiodiicolahasbeendemonstratedtoresultinthelesionsofSFDinexperimentalinfections(Lorchetal.2015)andisbelievedtobetheprimarypathogenassociatedwithSFD(Allenderetal.2015).However,thereiscurrentlynoconclusiveevidencedemonstratingthatitisthesoleagentresponsibleforSFD(Tetzlaffetal.2015).Co-infectionwithvariousotherfungalagentsiscommon.OpportunisticinfectionbyavarietyofotherfungalpathogenscanalsoresultinsimilarskindiseaseandshouldberuledoutinanySFDcase(Lorchetal.2016).ThegenusOphidiomycesiscomposedofasinglespecies,O. ophiodiicola,andtodatesnakeshaveproventobetheonlyhostofthisfungus(Sigleretal.2013).

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Figure 1: Geographic distribution of snake fungal disease in Ontario. The map insert shows US states where SFD has been detected. The map was created in December, 2016.

O. ophiodiicolaisoccasionallyfoundontheskinofsnakeswithoutanyclinicalsignsofSFDoraccompanyinghistologicallesions(Bohuski2015).GiventhatthefungusismorewidespreadthanthediseaseandnotallspeciesofsnakesinanSFDpositiveareaarefoundwithdisease,itislikelythatO. ophiodiicola isnecessaryforSFDbutinsufficienttocausesdiseaseonitown.Itispossiblethatthisfungusmightrepresentaskincommensaloratleastanunapparentsubclinicalinfectionundercertainconditions(Lorchetal2016).Thefungusappearstohavetemperaturedependentgrowthandthismightallowitaspecificnicheingrowingonexternalskinsurfacesofhibernatingsnakes.

Environmentalco-factorsappeartoberequiredforSFDtoemerge.Climatechange,particularlywarmerhibernationtemperaturesandwetweatherafterhibernationhavebeenlinkedtotheoutbreakofSFDintimerrattlesnakesinNewHampshire(Allenderetal2015,Clarketal2011).However,temperatureandmoistureseemtonoteffectspeciesequallyasotherspeciesofsnakesinthetimberrattlesnakeecosystemwerenotseentobeaffectedbySFDatthetimeoftheoutbreak(Clarketal.2011).DocumentedoutbreaksofsevereSFDhavetypicallybeeninrelativelysmallorisolatedsnakepopulations(althoughsuchpopulationsmaybeundergreaterscrutinythanlarger,lessthreatenedpopulations).Habitatfragmentation

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anddestructionaswellasinbreedingdepressionhavebeensuggestedtobeimportantco-factors(Lorchetal2016).Despitethesesuppositions,thereisnodefinitiveinformationtoidentify,quantifyandrankco-factorstodirectmanagementactions.

What does SFD do to individual snakes?O. ophiodiicola invadesthesuperficiallayerofskinwhereitsubsequentlycausesthickening,crustinganddeathoftheepidermis.Whenthecrustsfalloff,ulceratedanderodedskinisrevealed.CasesofsnakeswithnoapparentdiseasehavetestedpositiveforO.phiodiicolabyPCRintheabsenceofmortalityornotedpopulationeffects.Therearethreecoursesoftheinfection;recovery,deathfromsecondarydiseaseprocesses;ordeathafterthefungusinvadesmusclesanddeepertissues.Seethesectionbelowaddressingthequestion,“DoesSFDcausesseriousharms?”forfurtherdetails.

What does SFD do to snake populations?TherehasbeeninadequateintegrationofdiseaseinvestigationinformationwithecologicalmonitoringdatatodeterminethepopulationimpactsofSFD.Lesionsrunthegamutfrommildtosevere/lethalandpopulation-leveleffectshavebeensevereinsomecasesbutarenotinevitable.Multiplefactors(presenceofanopportunisticpathogen,enhancedsusceptibilityduetogeneticisolationandstochasticweatherevents)withinteractiveorsynergisticfeedbacksmaycombinedtoproduceseverepopulationleveleffects.Whileseverepopulationeffectsappeartobeexceptionalatthistime,thecircumstancesthatarethoughttoproducethemarebecomingincreasinglycommon.Seethesectionbelowaddressingthequestion,“DoesSFDcausesseriousharms?”forfurtherdetails.

Part 2 – Answering questions from the decision framework

Are there susceptible species in Canada?

Key points• TherearespeciesinCanadathataresusceptibletoSFDandarevulnerabletoadditiveeffectsofthe

diseaseduetoconcurrentstressorsandbecausetheyareinsmall,isolatedpopulations.• SFDwasfirstfoundintheendangeredeasternfoxsnakeinOntario.Thediseasehassincebeen

detectedintheendangeredqueensnakeinOntarioandthepathogenhasbeendetected,withoutdiseaseinOntariointheeasternfoxsnake,queensnake,easternmassassauga(allthreatened-endangered),andthecommongartersnake(statusnotdetermined).

• ThenumberanddistributionofsusceptiblespeciesinCanadalikelyexceedsthislist.• Todate,onlysnakeshavebeenshowntobesusceptibletoSFD,butithasaffectedmultiplespecies.

Details

SFD in CanadaThefirstcaseexaminedbytheCWHCasSFD-suspectwasaskinsamplefromaneasterngartersnakecollectedinearlyJune2014fromRondeauProvincialParkontheshoreofLakeErieinOntario;however,cultureofthatspecimenfailedtodemonstratethepresenceofO. ophiodiicola.Inmid-March2015,anadult

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femaleeasternfoxsnakewithdermatitiswasaccidentallydisturbedwhilehibernatingatalocationclosetoLakeErieinOntario.ThisbecamethefirstdocumentedcaseofSFDinCanada.SFDhassincebeenconfirmedbyhistologyin3easternfoxsnakesandonequeensnake(Table1).

Table 1: Snake fungal disease status for Canadian snakes as of December, 2016

(1) IncludesValley,Maritime,Red-sided,PugetSoundandEasterngartersnakes

TheCWHCaugmentedpassivesurveillancewithaparallelprogramusingreal-timePCR(qPCR)toscreenapparentlyunaffectedsnakesforpresenceofthefungusin2016,andbeganscreeningarchivedsamplesfromcasesgoingbackto2012.AsoftheendofNovember,2016,theCWHChadexamined126specimenscomprising9species(Table2).Diagnosticmaterialincludedcasessubmittedforgeneralscanningsurveillance,casessubmittedspecificallyforSFDtesting,andopportunisticsamplescomprisingroadmortality,shedskins,andswabsfromapparentlyasymptomaticsnakes.

Table 2: Results of enhanced surveillance for snake fungal disease and O. ophiodiicola in Ontario 2015-16

Species (Common name) No. TestedPCR Positive for O. ophiodiicola

SFD positive diagnosis Known Mortality

Massasauga 17 3 0 0Easternfoxsnake 62 13 3 0Easternmilksnake 2 0 0 0Easterngartersnake 13 1 0 0Northernwatersnake 2 2 0 0Queensnake 4 4 1 0Butler’sgartersnake 3 0 0 0Dekay’sbrownsnake 14 0 0 0Grayratsnake 1 0 0 0TOTAL 126 23 4 0

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Table 1: Snake fungal disease status for Canadian snakes as of December, 2016 Species COSEWIC Status Disease Diagnosed Exposure

determined by PCR

Free ranging in Canada

Free ranging in USA

Free ranging in Canada

Eastern foxsnake

Endangered X X X

Northern watersnake

Not at risk - X X

Queensnake Endangered X X X Common gartersnake sspp1

Not determined - X X

Eastern massasauga

Threated and endangered

- X X

(1) Includes Valley, Maritime, Red-sided, Puget Sound and Eastern gartersnakes





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Sevenofthe25snakecarcassessubmittedfrom2012-2016forgeneralscanningsurveillancewerepositiveforO. ophiodiicolabyqPCR,indicatingexposuretopathogenbutnotnecessarilypresenceofdisease.TheearliestpositivesamplewasamassasaugasubmittedfromtheParrySoundareainOntarioin2012.Therewerenosignsofdermatitisnotedatnecropsyandhistologyrevealednoindicationoffungalinfection.

Twelvesamplesweresubmittedfromlive,apparentlyaffectedsnakesspecificallyforSFDtesting.Seven(58.3%)ofthosesampleswerepositiveforO. ophiodiicolabyqPCR.Histologywasavailablefor8ofthose12cases,andSFDwasconfirmedwithhistologyin4ofthose8cases.Todate,allconfirmedcasesofSFDinfree-rangingsnakesinCanadahavebeendiagnosedinlivingsnakes.ManyoftheseindividualsaremonitoredcloselyandtherehavebeennoknowndeathsasofNovember2016.

Of89opportunisticsamplesfromapparentlyunaffectedindividuals,9(10.1%)werepositiveforO. ophiodiicolabyqPCR.Diseasecouldnotbeconfirmedbecausehistologicalsampleswerenotavailable;however,preliminaryresultssuggestthefungusmayalreadybewidespreadinsouthernOntarioalthoughincidencesofseriousdiseaseappearstobeinfrequentatthistime.

ItisreasonabletobelievethatthelistofsusceptiblespeciesextendsbeyondwhathasbeendocumentedsofarinCanadabecause:(i)Therehasbeenarelativelylowlevelandshorttimeframeforsurveillanceand/orsurveysforthedisease;(ii)“O. ophiodiicolaiswidelydistributedineasternNorthAmerica,hasabroadhostrange,isthepredominantcauseoffungalskininfectionsinwildsnakesandoftencausesmildinfectionsinsnakesemergingfromhibernation”(Lorchetal,2016),and(iii)SFDhasbeenfoundin30snakespeciesintheUnitedStates,manyofwhichalsoresideinCanada.

TodateO. ophiodiicolahasbeenisolatedfromsixfamiliesofsnakes(Lorchetal.2016).Affectedfree-rangingsnakesintheViperidaefamilyincludethepygmyrattlesnake,massasauga,timberrattlesnakeandcopperhead,(Cheatwoodetal.2003,Allenderetal.2011,Clarketal.2011,Smithetal.2013,Tetzlaffetal.2015,McBrideetal.2015,Lorchetal.2016,).CaptivecasesinViperidaeincludecottonmouth(Lorchetal.2016)andcasesineasterndiamond-backedrattlesnakenotclassifiedascaptiveorwild(Sigleretal.2013)

Non-crotalidspeciesinwhichSFDhasbeenobservedincludethenorthernwatersnake,gartersnake,northernribbonsnake,easternfoxsnake,queensnake,plainsgartersnake,saltmarshsnake,racer,easternmilksnake,ratsnake,mudsnake,broad-bandedwatersnake,rainbowsnake,easternblackkingsnake,bullsnake,Louisianapinesnakeandthebrownwatersnake(Cheatwoodetal.2003,Rajeevetal.2009,Sigleretal.2013,Sleeman2013,Dolinskietal.2014,Fentonetal.2015,Priceeta;2015,Gloriosoetal.2016,Guthrieetal.2016,Lorchetal.2016,Ohkuraetal.2016,Ravesietal.2016)

Speciesthatexhibitlatematurityandslowreproductionareespeciallysensitivetomortalityinadultsingeneral,andespeciallytomortalityinadultfemales.Thereissomeevidencetosuggestthisgroupishardesthitbydisease.AstudyinVirginiafoundthatfemalesnakesweretwiceaslikelytohaveskinlesionsthanmales(Guthrieetal.2016).Theauthorssuggestedthatlateseasonlesionsfoundingravidfemalesmaybeevidencethatthestressofpregnancymaypredisposefemalestoanincreasedriskofexposureortheinabilitytocleartheinfection.AsmorepopulationsofsnakesarestudiedacrossNorthAmerica,thespecific

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genetic,physiological,behaviouralandecologicalfactorsunderlyinganyspeciesdifferencesinsusceptibilitywillperhapsbecomeclearer(Lorchetal.2016).

Was SFD expected?

Key Points• ItwasnotsurprisingtofindcasesinCanadagiven;(i)theNorthAmericandistribution,species

affectedandpatternofspreadofSFD,(ii)previousevidenceofasimilardiseaseinarchivedsamplesintheUSAandCanadaand(iii)theincreasedfrequencyofemergingfungaldiseases.

• CanadacannotbeassuredthatthisdiseaseisnewtothecountryandisrestrictedtotwospeciesduetochallengesinmonitoringsnakehealthincludingthelowlevelofsubmissionstolabsandcomparativelylowlevelofpopulationmonitoringandhealthassessmentandduetoevidenceofinfectionwithoutdiseaseinotherspeciesinCanada.

• Giventhemanystressessnakesfaceandtheincreasingroleoffungiasemergingpathogens,itwasnotsurprisingthatSFDcouldoccurbuttherewasnoforewarningthatthisspecificdiseasewouldemergeorwhereinCanadaitwouldfirstappearorwillsubsequentlybefound.

Detailed answerThepasttwodecadeshasseenanunprecedentednumberoffungalandfungal-likediseaseslinkedwiththemostseveredie-offsandextinctionseverwitnessedinwildanimalsandplants(Fisheretal,2012).Chytridiomycosisisbelievedtohavecontributedtotheextinctionofmorethan100frogspecies(Skerratetal,2007).MicrosporidianfungiinthegenusSteinhausiahavebeenlinkedtotheeradicatedoftheirsnailhosts(Gurretal,2011).White-nosesyndromeofbatshaskilledmillionsofbatssincefirstdetectedinNorthAmericain2007,leadingseveralspeciesontotheendangeredspecieslist.Emergingfungalinfectionscausingwidespreadpopulationdeclineshaveincreasinglybeendocumentedacrossdiversetaxaincludingbats,frogs,softcoralsandbees(Fisheretal,2012).

ThepatternofSFDspreadisnotconsistentwithapointsourceintroductionandLorchetal(2016)concludedthatO. ophiodiicolahasbeenpresentinNorthAmericaforalongtimebutrecentenvironmentalchangesaredrivingSFDemergence.Skinlesionsdescribedashibernation‘blisters’or‘sores’havebeendescribedfordecadesinsnakesemergingfromhibernation,buttheircauseswererarelyexplored.Fungalinfectionshavebeendescribedinsnakesformanydecades,andhavebeenassociatedwithsomepopulationeffectsforacoupleofdecades.HistoricalreportsoffreerangingsnakeswithsimilarskinlesionsanddiseasealsoexistandmolecularevidencesuggestthepresenceofO. ophiodiicolaincaptivesnakesintheeasternUSAsinceatleast1986(Sigler2013).MoleculartestingconductedbytheCWHC(unpublished)ofarchivedsamplesfrommassasaugarattlesnakessuggeststhatO. ophiodiicolawaspresentinCanadain2012.

ThelackofdetectionsofSFDorO. ophiodiicolainwesternNorthAmericamaybeduetosurveybiasand/orlowerdiseaseprevalenceorseverity(Lorchetal,2016).ThesamecanbesaidforCanada.Snakesaredifficulttofindandmonitorwhenhibernating,whichmaybeavulnerabletimeforSFD.ThedocumentedgeographicaldistributionofO. ophiodiicolaisbroaderamongcaptivesnakesthanwildsnakes(Lorchetal,2016).Anexactoriginatingtimelineremainsunclearandamoredetailedmappingofthegeographicaldistributionofthisfungusisneededtofurtherunderstandthisemergingdisease(Lorch2016).

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Therehasrecentlybeenanincreaseinthenumberoffree-rangingsnakeswithfungaldermatitissubmittedtosomeUSwildlifediagnosticlaboratories2.TheCWHCreceivesveryfewsnakesfordiagnosticexamination(tables3and4).

Table 3 – Summary of free-ranging snake diagnostic examination conducted by the Canadian Wildlife Health Cooperative 2005-November 2016 Province Year(s) Animals examinedAlberta 2012 1BritishColumbia 2015 2Saskatchewan 2005-16 14Manitoba 2011 100Ontario 2006-16 129NewBrunswick 2010 5NovaScotia 2008-09 3PrinceEdwardIsland 2006-16 6Total 258

Table 4 – Variety of snake species examined at the Canadian Wildlife Health Cooperative 2005-2016 NovemberSnake species/group Count Snake species/group CountBoidae(BoasAndPythons) 2 Butler’sGarterSnake 5Colubridae 1 CommonGartersnake 106CommonWatersnake 3 EasternGartersnake 19EasternFoxsnake 65 WesternGartersnake 1Massasauga 21 WanderingGartersnake 1PacificRattlesnake 1 PlainsGartersnake 6EasternHog-nosedSnake 1 EasternRibbonsnake 1Milksnake 2 NorthAmericanRacer 1NorthernBrownsnake 13 Queensnake 5RedCornsnake 1 Red-BelliedSnake 5

TherearefewCanadianresearchersworkingwithsnakesorsnakeinfections.Theyhavegenerallynotre-portedtheirdiseasefindingstotheCWHC.Canadacannotsay,withanyconfidence,thattherehasbeensufficientsurveillanceofsnakestoconcludethatSFDisnewtoCanada,butthebalanceofevidenceinNorthAmericawouldsuggestitisanemergingdiseaseoratleastthere-emergenceofanendemicfungusduetochangingenvironmentalco-factors.

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2https://www.nwhc.usgs.gov/disease_information/other_diseases/snake_fungal_disease.jsp





https://www.nwhc.usgs.gov/disease_information/other_diseases/snake_fungal_disease.jsp

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Can SFD cause serious harm?

Key Points• TheeffectsofSFDvarywithinandbetweenspeciesandindividuals• Theinfrequencyoflinkingpopulationmonitoringdatawithdiseasesurveillanceinformation

preventsgeneralizedconclusionsofthepopulationeffectsofSFDalthoughtherearecasesthathaveimplicatedSFDasacausesofseverepopulationdeclines.

• ThereisnoevidencethatSFDisarisktopublichealthorariskfordomesticanimalsapartfrompetsnakes.

• ThereareexpertswhoconsiderSFDtobeaconservationemergencybecauseofsomecasesofapparentpopulationimpactsandtheseverepopulationeffectsofotheremergingfungaldiseasesofwildlife.

• WhilethereremainmanyuncertaintiesabouttheextentofpopulationeffectsofSFDandtheconditionsunderwhichtheseeffectsresultinseriousandirreversibleharms,aprecautionaryapproachwouldsuggestitcanbeasignificantadditivestressorandshouldbeconsideredseriousforspeciesatriskand/orforpopulationsstrugglingwithothercumulativestressors.

Details

Evidence specific to SFDTheexactexpressionofclinicalsignsanddiseaseseveritydiffersbetweenindividualanimalsandspecies.Thisvariationmaybedueinparttotheexactstageofinfectionatwhichanaffectedsnakeiscaptured.Mostdiseasereportsrepresentasingleobservationwithinthetimelineoflesiondevelopmentandlackfollow-upwithaffectedanimalsoveritslifecourse.Giventhesecretivenatureofsnakes,thisdiseaseisextremelydifficulttostudyundernaturalconditionsandinformationonfreerangingsnakesis,therefore,extremelylimited.SFDoutbreaksareprobablyonlyidentifiedoncesnakescontainwelldevelopedand/orextensiveskinlesionswithmanycasespresentinginastateofadvanceillnessordeath.Assuchithasbeendifficulttoreconstructtheexactpathogenesisforthisdiseaseinwildfreerangingsnakesandidentifyanypertinentcausalorcontributoryhistory,specificbehaviouraladaptationsorcopingmechanisms,thatputanimalsatriskandultimatelycontributetoanindividualsnakessurvivalordeath(Lorch2015).

Mortalityinsevereinfectionsmightbedirectlyrelatedtothefungalinfectionitself(especiallyinthecaseofdisseminatedinfectiontovitalorgans);however,thechronicandslowlyprogressivenatureofthisdiseasesuggeststhatthemajorityofnegativeeffectsareprobablyrelatedtosecondarycomplicationssuchas(i)skinulcerationandsecondaryinfections;(ii)obstructionofnaresinterferingwithvomero-nasalorgan,affectingolfaction,andhunting;(iii)associateddiscomfortandpainresultinginanorexiaandinappetence,(iv)orallesionsobstructingorinterferingwithnormalfeedingandorhunting(jawmisalignment,oralobstruction);(v)behavioursthatincreasetherisksofpredationsuchasincreasedfrequencyofbaskingand(vi)excessivemetabolicdemandduetofrequentskinmoulting.Infectioncanresultinbehaviouralalterationsleadingtosnakesbeingobservedinexposedsites.

Insomepopulations,SFDhasbeenassociatedwithsignificantpopulationdeclinesbutpopulation

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andindividualresponsestoSFDhasbeeninconsistentacrossspeciesandlocations,rangingfrominconsequentialtocatastrophic.Allenderetal.(2011)reported100%mortalityinIllinoismassasaugarattlesnakesthathadSFD.Clarketal.(2011)documentedovera50%declineinapopulationoftimberrattlesnakesfollowingtheappearanceofclinicalsignsconsistentwithSFD.

Ofthefewstudiesinwhichpopulationsweremonitoredandpopulation-leveleffectscanbeevaluated,thereisonecaseinwhichdeclinewasnoted(Clarketal.2011),andthreeinwhichnodeclinewasnoted

(Cheatwoodetal.2003,Allenderetal2011,Smithetal.2013).InOntario,snakeswithnoapparentdiseasehavetestingpositiveforO. ophiodiicolabyPCRusedattheCWHC(thesemaybesubclinicalcasesorjustexposedanimalscarryingsporesontheirskin).TheCWHChasnotyetseencasesofseverediseaseordeathduetoSFD.

Aswithcrotalidsnakes,lesionsinnon-crotalidspeciesvaryinseverity,butseverediseaseandmortalityhavebeenreportedlessfrequentlyinnon-crotalidspecies.In2014afree-rangingplainsgartersnake(Thamnophis radix)inIllinoiswasfoundtohaveseveredisseminatedophidiomycosis.SystemicinfectionsareveryrareintheliteraturebutthiscasewaslikeacaseofsystemicophidiomycosisreportedinacaptivegartersnakeinEurope(Vissiennonetal.1999,Sigleretal.2013)suggestingthepossibilitythatgartersnakesmaybeunusuallysusceptibletosystemicinfection(Dolinskietal.2014).

Althoughrattlesnakes(Crotalus spp.and Sistrurusspp.)areoftenimplicatedinclinicaldiseasereportsandhaveoftenbeenconsideredtosufferfromespeciallysevere

disease(Clark2011;Allender2011;McBride2015)similarlyseverediseaseoutbreakshavebeenreportedinotherspecies(e.g.LakeEriewatersnake,easternfoxsnake,andgartersnakes(Vissiennon1999;Dolinski2014,Lorch2016)).Themorefrequentreportsinrattlesnakesmayreflectuniquesusceptibilityormaybebiasedduetomoreactivemonitoringprogramstakingplaceinthesehigh-profilespecies.ThedeterminantsofthisvariabilityinobservedpopulationimpactsarecurrentlyunprovenandthereislittledirectevidencetoforecastwhichpopulationsaremostvulnerabletoharmfromSFD.Therehasbeeninsufficient time to determine if/how severe impacts are reversible in affected populations and little work linking disease investigations with population data. Appendix3providessomedetailsonwellreportedcasesofSFD.

Opinion specific to SFDSome experts viewing SFD as a conservation emergencybasedon;(i)experiencewithfrogchytriddiseaseandwhite-nosesyndrome;(ii)thegrowthinnumberofemergingfungaldiseasesingeneral;(iii)the

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Case Study - Self resolving SFD

Eighttimberrattlesnakesfrom2populationsinMassachusettswereobservedwithmild-to-severeSFDaffectingprimarilythehead,eye,pitorgans,andmouth(McBrideetal.2015).Nonediedasadirectresultofinfection,althoughonediedunderanesthetictodebridethelesionsandobtainsamples.Fiveshowedimprovementorresolutionoftheirlesionswithouttreatment.Self-limitingSFDwithspontaneousrecoveryintimberrattlesnakeshasbeenreported(Clarketal.2011,Smithetal.2013),indicatingthatnotallmildormoderateinfectionswillprogresstoseverediseaseanddeathintheviperidae.





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detectionofsomecaseswhereSFDhashadsignificantnegativeeffectsand;(iv)theapparentincreaseindistributionandabundanceofSFDcases.Supportingtheseconcernsaresimilaritiesbetween O. ophiodiicola andthefungusassociatedwithwhite-nosedsyndromewhichhaskilledmillionsofbats.Bothoccursinthesoil,seemtogrowonawidevarietyofsubstances,andpossessesmanyofthesameenzymes.Thevirulence,long-livedenvironmentalstagesandopportunisticandgeneralistnatureoffungalpathogenscancreateuniquechallengesfortheircontrol.

Landdevelopment,especiallytransportationnetworks,isincreasinglyfragmentingandisolatingsnakepopulationsandthisposesanincreasingriskofinbreedingdepressionandincreasedsusceptibilitytodisease.Iftheinteractiveandsynergisticeffectsofstochasticenvironmentalevents,lowgeneticdiversityandpresenceofapathogencanresultinan“extinctionvortex”(GilpinandSoule1986,Clarketal.2011)then,forisolatedpopulationslackinggeneticdiversityandfacingincreasinglyextreme,variableandunpredictableweatherpatternsduetoclimatechange,thepresenceofanopportunisticpathogenlikeO. ophiodiicolacouldhavesignificantimpactsonlongtermviability.

Evidence from analogyThepasttwodecadeshasseenan unprecedented number of fungal diseases in both animals and plants, many of which have caused some of the most severe die-offs and extinctions ever witnessed in wild species(Fisheretal,2012).Fungaldiseasesofwildlifeareofmanagementconcernfor3reasons:

1. Theycancauseseverepopulationdeclinesandextinctions.a. Bestknownarefrogchytriddisease,salamanderchytriddiseaseandwhite-nosesyndromeof

bats.Bees,seaturtles,crayfishandottershavealsobeenchallengedbyfungaldiseaseashaveawidevarietyofplants.Fungicancausepopulationlimitingeffectsbecauseoftheirlifehistorycharacteristicsincluding;long-livedinfectiousstages,survivalnotdependentonhostsduetofreelivingstages;beinggeneralistsandthusabletoinfectedtoleranthoststhatcanmaintainandshedthepathogen;rapidreproductionratesandhighvirulence.Thus,muchofpastdogmaontheinabilityofpathogenstodrivepopulationstoextinctbecauseofhostdensityregulatingeffectsdonotnecessarilyholdforfungi.

2. Theyaresymptomsofstressedenvironments.a. Fungiareoftenopportunisticpathogensthatusuallyinfectcompromisedhosts.Theexpansion

innumbersofimmunocompromisedpeopleisanexplanationforemergingofhumanfungaldiseases.Ithasbeenpostulatedthatclimatechange,pollutants,habitatdegradationandcompetitionwithinvasivespeciesmaybestressingwildlife,makingthemmoresusceptibletoendemic,opportunisticfungi.

Are there high levels and/or persistent exposure to the threat?

Key Points• O. ophiodiicolaisanenvironmentalopportunisticpathogenthatcanpersistoffitshostinawide

varietyofecologicalconditions.Multiplesnakespeciescanharbourthefungus.Thehazardis,therefore,presentinmultipleexposuresettings.

• ThedistributionofthefungusisgreaterthanthedistributionofSFDbutsitstruerangeandecologicnicheisunknown.

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• ThereareanecdotalreportsofSFDincaptivesnakesinCanadaincludingoutsideofOntario. • ThedistributionofSFDhasbeenexpandinginNorthAmericabutthemechanismsoftransmission

andspreadareunresolved.• Exposuretoplausibleco-factorsispervasive,especiallyforspeciesatriskandconsideringclimate

change

DetailsO. ophiodiicolacanaffectmultiplesnakespeciesandcanpersistsintheenvironment.TheglobaldistributionofO. ophiodiicolaisunknown(Allenderetal,2015).Itsgeographicaldistributionisbroaderamongcaptivesnakesthanwildsnakes,includingAustralia,GermanyandtheUnitedKingdom(Lorchetal,2016).ThedistributionofSFDandvarietyofspeciesaffectedbythediseaseindicatethatO. ophiodiicolaiswidespreadineasternNorthAmerica.Severalfactorssupport O. ophiodiicola occurringasanenvironmentalsaprobe(Allenderetal,2016).LaboratoryworksuggestsO. ophiodiicolahascharacteristicsthatallowthispathogentosurviveinnumerousecosystems,andthusprovideawidespreadopportunityforsnakeexposure(Allenderetal,2016).

“Themodeoftransmissionandtheinfluenceofenvironmentaltriggersonprevalenceofthisdiseasearenotunderstood”(Allenderetal,2015).O. ophiodiicola isoccasionallyfoundontheskinofsnakeswithoutanyclinicalsignsofSFDoraccompanyinghistologicallesions(Bohuski2015)suggestingthatthisfungusmightactsasaskincommensaloratleastanunapparentsubclinicalinfection(Lorch2016).CWHCobservationstodateinCanadiancasessupportthispossibility.

TheCWHCisawareofsomeSFDsuspectcasesincaptivesnakesinBritishColumbia.Onewasaclusterofcasesinagroupofballpythons(Python regius)andcommonboas/redtailboas(Boa constrictor imperator)inalargereptilerescuefacility.TheanimalshadclinicalandpathologicalsignsoffungalinfectionsbutwithconflictingO. ophiodiicolaPCRresults;aCanadianlabdetectedthefungusbyPCRbutaUSlabreportednegativePCRresults.Re-extractionandretestingoftheoriginalextractinCanadaagaintestedpositivesuggestingthatthefungusmighthavebeenpresentasatransientcarrierorskincommensalinsomesectionsoftheskin.Thesecondcasewasinanemeraldtreeboa(Corallus caninus)fromanAmericanAssociationofZoosandAquariaaccreditedfacility.Thesnakehadclinicalandpathologicalsignsoffungalinfections.FungalculturesyieldedColonostachyssp.andTrichosporonsp.andPCRtestingwaspositiveforO. ophiodiicola.SamplescouldnotbeforwardedtoaUSlabforspecializedfungalcultureorfurtherPCRconfirmationasnoCITESpermitwasavailableatthetimeforexporttotheUSA.

ConfirmingthepresenceofO. ophiodiicolainskinlesionsorintheenvironmenthasbeenhamperedbydifficultyinisolatingthefungusincultureandproblemsinidentifyingofO. ophiodiicolabasedonmorphologicalcharacteristics.Recentadvancesinmoleculardiagnosticswillbeanimportantadjuncttoresearchaimedatestablishingtheprevalence,distributionandtransmissionofthisfungus(Bohuskietal,2015).

TheeasternfoxsnakeandqueensnakearebothdesignatedbyCOSEWICasendangered.Sharedcausesoftheirdeclineincludehabitatloss,impactsofhousingandcottagedevelopment,andintentionalanddirect

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harmfrompeople.Thefoxsnakesarefurtherchallengedbywetlanddrainageforagriculture,androadmortalitywhileintroducedspeciesandaspecializeddietcreateuniquechallengesforthequeensnake.OtherCanadianspeciesknownsusceptibletoSFDsharesimilarchallenges.SmallpopulationsizesandslowreproductionreducesmanyspeciescapacitytocopewithorrecoveryfromadditivemortalityduetoSFD.Forisolatedpopulationslackinggeneticdiversityandfacingclimatechange,thepresenceofanopportunisticpathogenlikeO. ophiodiicolacouldhaveamajorimpactonlongtermviability.VulnerabilityassessmentfordiseaseingeneralandSFDspecificallyhavenotbeenundertakenforCanadiansnakepopulations,sotheextentoftheseenvironmentalstressorshasnotbeendocumentedorconsideredfromasnakehealthperspective.Theprovincialrecoveryplanforeasternfoxsnakesnotesthelackofacomprehensivehealthanddiseasescreeningstudyasanimportantknowledgegap.

McBrideetal.(2015)pointedoutthatincreasedcloudcoverandhumidityassociatedwithhighprecipitationcanbeespeciallydetrimentalinSFDinfectedtimberrattlesnakesbecausetheseconditionsarecorrelatedwithreproductivefailureinfemales(Martin1993,2002,Clarketal.2011)andtheymayhavefacilitateinfectionwithO. ophiodiicolasincefungaldiseaseincaptivereptilesisoftenassociatedwithinappropriatetemperatures,highhumidity,andstress-relatedimmunosuppression(Paréetal.2007,MitchellandWalden2013).InbreedingdepressioncausedbyIsolationofpopulationscanleadtoincreasedpopulationsusceptibilitytodisease(Frankhametal.2002,Ilmonenetal.2008,Townsendetal.2009).

Are there known, effective means to prevent, mitigate or eliminate the harms from the threat?

Key Points• Therearenoprovenmethodstoprevent,mitigateoreliminateharmstopopulationsfromSFD.• Therehasbeensomesuccessintreatingindividualanimals,anactionthatmaybeimportantin

criticallyendangeredspecieswhereeachindividualanimalisrequiredtomaintainthegeneticdiversityofthepopulation.

Detailed answerTherelativenoveltyofSFDresultsinascantbodyofliteratureorresearchdoneonresponseoptions.Wearelefttoworkfromfirstprinciplesofdiseasecontroltoexploremanagementoptions.Thereare6generalwaystoattackanydisease;(1)treataffectedindividualsorpopulationstospeedrecoveryandlimitimpacts;(2)promotesufficientimmunologicalresponse(innateoracquired)toreducediseasesusceptibility;(3)avoidexposurethroughpathogenexclusion,hostisolationordepopulation;(4)excludeallsusceptiblehostfromtheexposureareathroughquarantineorculling;(5)modifyenvironmentalandsocialriskfactors,and(6)reducepopulationvulnerability

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Option 1 – Treatment (Not viable for populations but a potential option for individuals)

ReportsoftheeffectivenessoftreatmentsforSFDhavebeenvariable.Noclinicaltrialsortreatmentcaseserieshavebeenpublishedtodate.Thefeasibilityofdeliveringtreatmentseitherthroughdrugsorenvironmentalmodificationsarelimitedtomanagingclinicaldiseaseinindividualcaptiveanimalsduetopracticalconstraintstodeliveringdrugsorchemicalstofree-ranging,butcrypticanimals.Thisoptionshouldbeexploredtomanagediseaseinendangeredspecieswhereindividualanimalsarehighlyvaluedandimportantforspeciespersistenceanddiversity,butisnotaviablepopulationmanagementresponse.

Option 2 – Promoting immunity (Potential utility by promoting general, innate immunity)

Aleadinghypothesisforincreasedfungaldiseaseinwildlifeisincreasedhostpopulationsusceptibilityresultingfromenvironmentalstressors(Fisheretal,2012).Vaccinesareusedtoreducediseasesusceptibility.However,vaccinesofanyform,includingforSFD,arenotavailableforsnakes.Thereremainsignificantchallengestomakingvaccinesforfungalinfectionsincluding;lackofcapitalforresearch;thebeliefthatpatientswithsignificantfungaldiseasesmaybeimmunologicallycompromisedandalackofbasicknowledgeofthemarkerstotargetforfungalvaccines.Antibodyproductionistemperaturedependentinsnakes,therefore,vaccinationdeliverywouldneedtobelinkedtotheoptimaltemperatureforanimmuneresponse.Coupledwiththechallengesindeliveringsufficientvaccinetoenoughofapopulationtopreventdiseaseinwildlife,vaccination is unlikely to be a viable optionintheneartomediumterm.

Age,nutrition,generalhealth,ambienttemperatureandseasonaffecttheinnateimmunesystemofsnakes.Intemperatespecies,organsimportantforimmunefunctionregressseasonally.Seeoption6forfurtherdiscussiononimprovingresiliencetoincreaseinnateresistancetoinfection.

Option 3: Avoid exposure through pathogen exclusion, host isolation or depopulation (Potential to minimize anthropogenic spread, otherwise not viable)

Whilecullinghasbeenusedwidelyindomesticanimalstoremovesusceptiblehostsinthefaceofanoutbreak,thisisunlikelytoworkinsnakesbecause;(1)anumberofspecieshavelegalprotectionduetotheirconservationstatus;(2)theprevalenceandroleofasymptomatichoststhatmaybereservoirsforinfectionisunclear;(3)therearenosurveysandmethodstodifferentiatepreclinicalinfectionsfromnegativeanimalsand(4)thereareethicalissuesandpublicperceptionsthatspeakagainstcullingasanoption.

SeethenextsectiononthepossibilityofgeographicallyisolatingSFD

Option 4: Remove all susceptible species from environments with the pathogen (Not viable)

ThemechanismsoftransmissionofO. ophiodiicolahasyettobedefinedandtheenvironmentaldistributionofthispathogenisunknown.Thispreventsidentificationofgeographiclocationsfromwhichtoexcludeorremovesusceptiblespecies.

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Option 5: Modify social and environmental risk factors (Uncertain)

WhilehypothesesexistregardingtheroleofriskfactorsinthegenesisofSFD,welldesignedepidemiologicalstudiesarelacking,thuspreventingassignmentofprioritytoputativeriskfactorstotargetinmanagementplans.Atthistime,definitiveevidencethatO. ophiodiicolaisthesolecauseofSFDisinconclusiveasadditionalfungiareisolatedfromaffectedsnakes.Thereareopinionsandhypothesesthatenvironmentalchangesmaybeariskfactor,particularlyastheyrelatetohabitatqualityandquantity,andweather(temperatureandhumidity).Someofthesechangescanbelinkedtoanthropogenicinfluencesonhabitatandtoclimatechange.Specificriskmanagementadvicemustawaitfurtherresearch.

Option 6: Reduce population vulnerability (Uncertain but synergistic with other management goals)

Seetheanswertothequestionbelowonreducingvulnerability.

Can SFD be geographically isolated?

Key Points• DeficienciesinknowledgeaboutthetransmissionsystemforSFDplusthepracticallimitationsto

constrainingthemovementsoffree-rangingmakesisolationorquarantineimpracticalforwildsnakes.

• ThereareopinionsandevidencethatO. ophiodiicolaisanenvironmentalfungusalreadyfurthergeographicallydistributedthancurrentreportsofSFDinNorthAmerica.

• Becauseofprevailinguncertainties,aprecautionaryapproachwouldbetolimitfurtherreleaseofO. ophiodiicolaintotheenvironmentthrougheducationcampaignstothepettradeandherpetologiststoadvocateforandsupportbiosecuritytopreventunintentionalmovementofthefungusfromaknownSFD-positiveareatoareasofunknownorassumednegativestatus.

DetailsAsecondhypothesesfortheincreaseinfungaldiseasesofwildlifeisincreasedanthropogenictransferoffungibetweenlocations(Fisheretal,2012).

WhileitisunknownifO. ophiodiicolawasintroducedfromoutsideofNorthAmerica,theprevailingopinionisthatthisisanenvironmentalfungusthatexistsinmanylocationsinNorthAmerica.SFDhasbeenfoundinmultiplebutunconnectedlocationsoverthesamerelativelyshorttimeframe,leadingtothesuppositionthatSFDisnotanexampleofanintroducedpathogen,butratherthatsomethinghaschangedinsnakepopulations,makingthemmoresusceptibletothisenvironmentalfungal.Thisconclusioncanbechallengedbythelackoffindingsnakessufferingfromotheropportunisticorenvironmentalpathogens.ThismayreflectauniqueaspectofO. ophiodiicolaordifficultiesindetectingsickanddeadsnakes.

Borderprotectionandmanagementofthepettrademaypreventtheintroductionofnewpathogensandsusceptiblehosts,butisunlikelytoaffecttheprogressofSFDnowthatithasemerged.GiventhatO. ophiodiicolaisanenvironmentalopportunist,thatitsdistributionhasyettobelinkedtospecificlandscape

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features,thatthemechanismofspreadandtransmissionof O. ophiodiicolaisunknown,andthechallengeofconstrainingthemovementoffree-rangingwildlife, itisnotlikelythatsusceptiblesnakescouldbeisolatedfromthepathogen.Fisheretal(2012)opinedthatbiosecurityeffortsforwildlifepaleincomparisontoprotectionofagricultureassetsbecausewildlifearenotcorrectlyvaluedeconomically.

Theroleofmechanicaltransferonfomitessuchasbootsandfieldequipmenthasnotbeendetermined.However,areasonableprecautionaryapproachtominimizefurthertheprobabilityofanthropogenicdistributionofSFDcouldbeachievedbyadvocatingfororrequiring;(1)permissionsandpermitstotranslocatesnakesforresearchorconservationthatcreateapotentialtomovepathogensbetweenhabitats;(2)peoplehandlingsnakesadheretobiosecurityanddisinfectionprotocolssuitableforfungalpathogensand(3)peopleworkinginareasknowntobepositiveforSFDfollowdisinfectionandbiosecurityprotocolsbeforemovingtoareasofunknownSFDstatus.Disinfectionandbiosecurityprotocolswillneedtobebasedonbasicprinciplesandexpertopinionuntilresearchisconductedtodeterminetheoptimalprotocols.

Can vulnerability be reduced to SFD?

Key Points• SFDhascharacteristicsofanendemicdiseasethathasoccurredduetoan increasedinhostrangeor

pathogenicityduetochangesinthepathogen,hostand/orenvironment• Strategiestocombatendemicpathogensemphasizeinvestigatingandmanagingco-factors,

synergies,andcontextdependencies• Thereisevidencethatenvironmentalco-factors,especiallyclimatechange,andhabitatlossand

alterationmaybeimportantco-factorsdeterminingriskandimpactsofSFD• Giventhatvulnerabilityisthecombinedoutcomeofexposure,susceptibility,capacitytocopeand

cumulativeeffectsofotherstressorsandgiventhattherearenocurrentoptionstoreduceexposureorsusceptibility,vulnerabilityreductionmustfocusonimprovingindividualandpopulationresilienceandmanagingco-stressors

• Thesuggestedco-factorsinfluencingthespreadandeffectsofSFDoverlapwiththemajorchallengesfacingsnakesinCanada,therefore,SFDmanagementshouldbeintegratedintospeciesmanagementplansduetosynergiesincurrentrecoveryplansandbestevidencetodealwithSFD.

DetailsVulnerabilityisthestateofsusceptibilitytoharmfromexposuretostressesassociatedwithenvironmentalandsocialchangeandfromtheabsenceofcapacitytorespondto,andrecoverfromstressfulevents(Adger,2006).AnswerstotheprecedingquestionsofthedecisionframeworkindicatethattherearenooptionstopromoteacquiredimmunitytoSFDandthatnon-specificpromotionofinnateimmunitymaymostlikelybeachievedbysecuringappropriatehabitatforthermoregulation,adequatepreyofsuitablequalityandsufficientgeneticdiversity.TheprecedinganswersalsoindicatethattherearenoknownviableoptionstopreventwildsnakeexposuretoO. ophiodiicola apartfromgenericrecommendationsonbiosecurityandimportcontrols.VulnerabilitymanagementforSFDseemsdependentonpromotingtheabilityofsnakesandsnakepopulationstorespondtoandrecoveryfromthedisease.

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Thefirsteversuccessfuleradicationofafungaldiseaseofwildlifethroughinterventionsonthechytrid-infectedislandofMallorcaprovidedenthusiasmforbiomedicalinterventionsagainstemergingfungaldiseasesorwildlife(Fisheretal,2016)andseveralresearchersareseekingsimilarapproachestodiseasessuchaswhitenosesyndromeandsalamanderchytridinfections.Butchallengesindeliveringmedications,vaccinesorenvironmentaldisinfectantsplusthepersistenceofO. ophiodiicola,andthepresenceofmultipleandcumulativestressorsaffectingmanysnakepopulationsarguesforapragmaticapproachfocusedonhelpingspeciescopewithSFDtofosterlong-termhost–pathogencoexistence.

Harmreduction(Figure2)aimstoreducethetotalamountofharmbyreducingpopulationvulnerabilitytotheharmsaswellasreducingthetotalimpactoftheharmsbypromotingthepopulationscapacitytocope withthespecificharmandreducingtheimpactsofcumulativeeffectsofotherstressors.Harmreductionalsotriestoreducetheadverseconsequencesofahealththreatwithoutnecessarilyreducingthatthreat.Interventionsmaybetargetedattheindividual,thepopulation,communityorecosystem.Itsgoalistooptimizepopulationhealthwithinthecurrentrealisticcircumstances.

Figure 2 – Generic harm reduction model

Foranyemergingdisease,eitherthediseasehasrecentlyspreadintonewgeographicareasorithasbeenpresentintheenvironmentbutrecentlyemerged.SFDhascharacteristicsofthelatter.Strategiesforanintroduceddiseaseoftenfocusonidentifyingandcontrollingagentsofspread,whereasstrategiesforlatterfocusonminimizingco-factorsaffectingvulnerabilityorenhancedvirulence(Rachowicz.2005).Proposedco-factorstoSFDarealsocriticalthreatstosnakeconservationinCanada.Vulnerabilityassessmentandmanagementarealsofundamentalcomponentsofclimatechangeadaptationandpreparedness.Therefore,co-benefitsacrossprogramscouldbeachievedthroughavulnerabilityfocusonSFDmanagement.

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Figure 2 – Generic harm reduction model

Total Harm

Total Amount

Exposure

Suspectibility

Total Impact

Coping capacity

Cumualtive stressors





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Options to consider for vulnerability management1. Reducetheamountofharm

a. Reduceexposurei. Notviable(Seeprecedingdiscussiononoption3above)

b. Reducesusceptibilityi. Promotingspecificimmunityisnotviable(Seeoption2above)ii. Reptileimmunityinvolvesinnate,cell-mediatedandhumoralcompartmentsbut,there

iscomparativelylittleknownaboutimmunefunctioninreptiles.Resistancetopathogensisassociatedwithfitness(UivariandMadsen2006)andstressfulsituationhavebeenassociatedwithlowereddiseaseresistanceinreptiles(Oppligeretal1998).Forreptilesincaptivity,excessivelyhighhumidity,lowenvironmentaltemperature,alreadyhavinganotherdisease,malnutrition,andstressfrompoorhusbandrycanaffectthedevelopmentoffungaldiseases3,suggestinglandscapeattributes,includinghabitatqualityandquantity,climate,andpreyavailabilitymayaffectSFDsusceptibility.

2. Reducethecumulativeeffectoftheharma. Increasecopingcapacity.

i. Copingstrategiesarecloselyrelatedtoresourcesandassets.ForsnakepopulationstocopewiththreatslikeSFD,itcanbehypothesizedthattheremustbeeither;(i)reproductionratesexceedingorequivalenttoadditionalmortalityfromSFD;(ii)adequategeneticvariabilitytoallowpopulationstoadapttothediseaseif/whenitevolvestoamorebenignmanifestation;(iii)suitablehabitatconnectivitytoallowanimalstorelocatetoareaswithlowratesofexposuretothethreatand/or(v)suitablehabitattomeetsnakesneedsfordailyliving(food,shelter,security,appropriateweather)tosupportinnateimmunefunctions.

b. ReduceotherstressorscausingadversecumulativeeffectsthatreducethediversityandnumbersofanimalsneededtohelppopulationswithstandandrecoverfromSFDi. Habitatlossanddegradation,additionalmortalityorlossduetoanthropogeniceffects

(ex.roads,intentionalkilling,collectionforthepettrade)andclimatechangearecommonchallengestoatrisksnakesinCanada.Manyspeciesareexceptionalsensitivetoadditionalcausesofmortalityduetotheirlowreproductiverateandprolongeddevelopmentaltimes.Reducingtheseandotherstressorsmayhaveco-benefitsofaddressingputativeSFDco-factors,addressingprioritiesinrecoveryplansandpromotespeciesresiliencetobothclimatechangeanddisease.

Monitoring and Surveillance

Key Points• Evidence-basedselectionofpriorityareasandspeciestoimplementSFDmanagementiscomplicated

bythelackonroutinesnakediseasesurveillanceandduetothelackofmonitoringSFDplausibleco-factors

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• IfSFDmanagementstepsaretaken,monitoring,asaminimum,shouldbeadvocatedtoassistinadaptivemanagementofSFD

• TheCWHChasdiagnosticcapacityandexpertiseforsnakediseasesurveillancebutrequiresassistancefromresourceandwildlifeagenciestoencouragemoresubmissionsofsnakes

• EfficienciescanbegainedbyintegratingdiseasesurveillanceandSFDco-factormonitoringwithongoingpopulationandhabitatassessmentsbeingusedtosupportspeciesrecoveryplans.

DetailsThedecisionframeworkinappendix1identifiestwosituationswheresurveillanceormonitoringistheprin-cipleresponse.

1. Insituationswheretherearesusceptiblespeciesbutnoevidencethatanexpecteddiseaseresultsinseriousorirreversibleharms,anappropriateactionwouldbetomonitorco-factorsthatcouldinfluencethepopulationsvulnerabilityoralterimportantcausalvariablesthataffectthemagnitudeorlikelihoodofharm.Thiswouldberecommendedinsituationswhere;(i)thepopulationsinvolvedarehighlyvaluedorhighlyvulnerabletodeclinesfromotherorcumulativeeffects;or(ii)whentherearefewoptionstoavoidtheharmsfromthediseaseiftheepidemiologicalconditionschangetofavourdiseaseoutbreaksorchangingvirulenceorimpacts.

2. Insituationswhereanunexpecteddiseaseaffectssusceptiblespecieswithoutevidenceofharm,itisreasonabletoundertakediseasesurveillancebecauseofuncertaintiesabouthowanunexpecteddiseasewillaffectpopulationsofconcern.Monitoring,ratherthansurveillancemightbeadvocatedforinsituationswheretheaffectedpopulationsarenotatconservation-riskorthereareviableoptionsforrapidandeffectiveinterventionstomitigateoravoidharm.ThesecretivenatureofsnakesmakesmonitoringtheeffectsofSFDdifficult.FurthercomplicatingelucidationofSFDimpacts

aretheclearvariationsindiseaseseveritybetweendifferentgeographicregionswhichmaybelinkedtostraindifferencesinthepathogen,geneticcompositionofagivensnakepopulation,orenvironmentaland/orbehaviouralfactorsthatinfluencediseaseecology.

Athirdsurveillancescenariooccurswhenadiseaseknowntocauseharmexistsandaninterventionisimplemented.Surveillanceallowsmanagerstoevaluatetheimpactsofinterventionsandprovidesongoingfeedbackregardingtheneedtomodifyinterventionsbasedonchangesintheeffectsanddistributionofthedisease.

Afourthscenarioinvolvestheneedtoimplementtargetedsurveystoanswerspecificresearchquestionsincludingestablishingthedescriptiveepidemiology

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SURVELLANCE VS MONITORING

Monitoring-intermittentperformanceandanalysisofroutinemeasurementsandobservationstodetectchangesintheenvironmentorhealthstatusofapopulation,butwithoutelicitingaresponse.

Surveillance-Systematicandcontinuouscollection,analysis,andinterpretationofdata,closelyintegratedwiththetimelyandcoherentdisseminationoftheresultsandassessmenttothosewhoneedtoknowsothatactioncanbetaken.





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ofthedisease(whoisaffected,where,whenandwhatharmsitcauses)ortohelpprovidefoundationalinformationtosupportcausalresearch.

Selectionofwhichform(s)ofsurveillanceormonitoringisrequired/desiredispredicatedonmanagementobjectives,thecost:benefitofsurveillanceandtheimplicationsofbeingwrongifimportantchangestothediseasebehaviourareundetected.SFDispartiallyexpected,mayundercertainconditionscauseseriousharmsbutlacksspecificinterventionstoattackthedisease.It,therefore,fallsacrossanumberofthemonitoringandsurveillancescenarios.Theprevailinguncertaintiesaboutthediseasesuggestthatscenario#4maybeadvisableandthathypothesisdrivensurveillanceatstrategicsitesismostappropriate.

Table3revealsthattheCWHChasaverylimitedinsightintotrendsinsnakediseasesduetotheverylownumbersofanimalssubmittedtothelaboratory.TheCWHC-Ontario/NunavutandPacificregionalcentreshavedevelopedthenecessarydiagnosticcapacitytodetectSFD.CWHC-Ontario/Nunavuthaslaunchedsmallscale,local,cooperativescanningsurveillance.FurthersurveillanceinitiativesinOntariowillrequireconsultationwithprovincialpartners.

Conclusions and recommendationsWildlifediseaseisnowrecognizedasanincreasinglyfrequentcontributortospeciesdeclineandextinctionandisbecomingamoreregularmanagementconcern(Dasaketal,2000)Itcanbeanticipatedthatwithclimatechange,therewillbegrowingneedstoevaluatetheemergenceofnewpathogensandparasitesinwildlife(StephenandDuncan,inpress)andthatineachofthosesituations,therewillbehighdegreesofuncertainty.Notallemergingthreatsareofequalsignificancebutthereisnoagreeduponmeanstorankrelativeimportanceofemergingdiseasethreatsinwildlifeandtodevelopanexplicitrationaleforactionsorinactions.Inthisreport,wehaveusedadecisionframeworktosystematicallyconsolidatetheexistinginformationonSFDandoverlapitwithbasicdiseasecontrolprinciplestoassessSFDasabiodiversitythreatandidentifyareasonablecourseofaction.

Wehaveconcludedthefollowing.

A management response to SFD is justifiable

• TheSpeciesatRiskActnotes–“theGovernmentofCanadaiscommittedtoconservingbiologicaldiversityandtotheprinciplethat,iftherearethreatsofseriousorirreversibledamagetoawildlifespecies,cost-effectivemeasurestopreventthereductionorlossofthespeciesshouldnotbepostponedforalackoffullscientificcertainty.”TheActdirectsmanagerstoconsiderCanada’scommitmentstotheconservationofbiodiversityandtotheprecautionaryprinciplewhenpreparingrecoverystrategies.

o SFDhasthepotentialforseriousharminspeciesalreadyatrisk.Despitesignificantscientificuncertainty,aprecautionaryapproachcanbejustifiedastheharmreductionstepsforSFDwouldcomplementactionsrecommendedunderspeciesrecoveryplansand/orclimatechangeadaptationplanning.

o Thepotentialforharmisderivedinthisassessmentinpartfromsomereportsofadverse

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populationimpactsbutmoresofromthefindingthatmanyspeciesatriskinCanadaaresusceptibletoSFDandarealreadyoverburdenedwithmultipleotherstressors.

• Inthedocument,“PlanningforaSustainableFuture:AFederalSustainableDevelopmentStrategyforCanada2013–2016,”Target4.7includesanimplementationstrategyofprovidinginformationtoreducetheriskof,andadviceinresponseto,theoccurrenceofeventssuchaswildlifediseaseevents4.

o ThereviewhasrevealedweaknessesindiseasesurveillanceforreptilesingeneralandSFDspecificallyaswellastheneedtocoordinateinformationamongststakeholdersthroughinformationsharing.

• TheWildlifeHealth/IssuesSection(WildlifeManagementandRegulatoryAffairsDivision‎.ECCC)hasresponsibilitytomanageCanadianWildlifeServiceenvironmentalemergencypreparednesspoliciesandcontingencyplansfornationalconsistencyandeffectiveness

o SFDshouldbeconsideredabioticemergencyuntilevidencecanbefoundtoshowitisnotcapableofseverepopulationlimitingeffects.Aninitialresponseplanshoulddefinethethresholdto‘de-classify”SFDasanemergency.

Despite uncertainties, a response based on harm reduction principles is justifiable and can act in synergy with recommendations in some species recovery plans

• Figure3summarizesapopulationhealthapproach,adaptedinbrieftoSFD.ASFDmanagementprogram,ratherthanasinglebiomedicalorbiologicalinterventionisrecommended.

• SomemonitoringandsurveillanceshouldbesupportedtostarttofillsomegapsonspreadanddistributionofSFDandtohelpidentifymostvulnerablepopulationsuponwhichtostrategicallyfocusdiseaseandriskmonitoring.

o Itwouldreasonabletoadvocateforincreasedscanningsurveillance(achievedthrougheffortstoencouragemoresnakesubmissionstotheCWHCacrossCanada)andzonalsurveillancetargetingtheedgesofknownSFDoccurrenceinCanada.

Figure4summarizestheanswerstothequestionsoutlinedinthedecisiontree,supportingarecommenda-tiontofocusonreducingvulnerabilityastheprinciplestrategyforSFDinCanadaatthepresenttime.

Reducevulnerability

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Figure 3 – Application of population health principles for SFD harm reduction

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Figure 3 – Application of population health principles for SFD harm reduction

Reduce exposure

Reduce susceptibility

Promote coping capacity

Surveillance

•Disinfection of personnel and field equipment •Disease control provisions for species introductions

and transfer permits

•Promote innate immunity by reducing other environmental stressors and ensuring adequate food and habitat quality and quantity

•Use SFD disease as an incentive to invest in removing critical barriers to species recovery•Protect suitable habitat quantity, quality and connectivity

•Incorporate SFD into climate change planning for species at risk

•Strategic surveillance for most vulnerable species and at at edges of current distribution

•Monitoring of risk factors to re-assess changing vulnerability





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Figure 4 – Application of the decision tree to snake fungal disease in Canada

Reduce exposureDevelopanddistributestandardizedrecommendationsfordisinfectionandhandlingofsnakes,especiallyinorattheedgesofknowngeographicdistributionsofSFD.

• Disinfection o SFDspecificdisinfectionprotocolsarenotyetavailablebutshouldbepursued.ECCCshould

spearheadthedevelopmentofgenericprotocolsthatareadaptabletovariousspeciesandpathogensforuseinallwildlifehandlingscenarios.Disinfectionprotocolsrecommendedforthecontrolofchytridfungiinamphibiansmayactasinterimrecommendations.

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Figure 4 – Application of the decision tree to snake fungal disease in Canada

Suspectible species?

No

No action

Yes

Expected?

No

Serious harm?

No

Track the disease

Yes

Hi or ongoing exposure?

Yes

Known response?

Yes

Respond

No

No

Can it be isolated?

No Yes

Isolate

Yes

Serious harm?

Yes No

Track risk factors

Decision node

Action node

Reduce vulnerability





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o Handling ▪ Experimentalevidencesuggeststhatbreaksinthesuperficialkeratinlayermightplay

asignificantroleinearlyinfectionandthepathophysiologyofthedisease(Lorchetal,2015).ThiscouldinformrecommendationsontheapplicationofexternalmarkingsorimplantationoftransmittersorotherabrasivemethodsofidentificationthatmightputsomesnakesatanincreasedriskfordevelopingSFD.AlternativemethodsofidentificationandmonitoringshouldbeconsideredinpopulationswhereSFDhasalreadybeenidentified.

o Translocations ▪ Wildsnakesshouldnotbemovedandreleasedintonewlocationswithoutassessmentof

SFDrisks ▪ Captivereptilesshouldneverbereleasedintothewild. ▪ ECCCshouldkeepup-to-dateonemergingevidencethatlinksSFDwiththepettrade,but

todate,thereisnoevidencetoimplicatepetimportationfortheintroductionorspreadofSFD.

Reduce susceptibility• SFDhascharacteristicsofanendemicopportunisticpathogenthathasbeenpresentinthe

environmentbuthasincreasedinpathogenicitybecauseofenvironmentalchangesorpossibly,simplyescapedprevioushumannotice.

o Strategiesforthesetypesofdiseasesfocusonmanagingco-factorsthatmayeitherincreaseexposureorincreasesusceptibilitytoinfectionorworsentheeffectsofinfection(Rachowiczetal,2005).

o ImmunosuppressiveenvironmentalstressorsthatmaypredisposesnakestoO. ophiodiicola infectioncanbehypothesizedtobelikepopulationstressorsconsideredinspeciesrecoveryplansassociatedwithhabitatabundanceandquality,preyavailability,andhabitatconnectivitytoallowformovementandsharingofgenericdiversity. ▪ SpeciesrecoveryshouldaccountforSFDriskfactorstoaddressindividualandpopulation

susceptibility

Promote Coping Capacity• Resiliencecanbedefinedasthecapacitytorespondtoadisturbancebyresistingdamageand

recoveringquicklyorasthecapacitytoabsorbchangewhileexhibitingasimilarsetofstructuresandprocesses.Byadaptingsomeconceptsofmanagingforresiliencefrompublichealthandconservation,wecanconcludethatafocusoncopingcapacitywouldneedtoincludethefollowing:

o AdaptivemanagementbasedonongoingmonitoringoffactorsthatcouldaffectfunctionsorimpactsofSFDintheforeseeablefuture

o InvestmentinpreparednessthatidentifiesvulnerablepopulationsinadvanceofharmandactstoreduceotherimpedimentstorecoveryandabilitytomaintainfunctioninthefaceofSFDemergence

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o Ensurepopulationshavethebasic‘buildingblocks”ofcopingandrecoverycapacitybyprotectingabioticdeterminantsofhealthincludinghabitat,genericdiversity,populationconnectivityandspeciesabundanceanddistribution.

Surveillance and Monitoring• SFDsurveillance,andsnakediseasesurveillancemoregenerally,shouldnotbeviewedasastand-

aloneactivity,butinsteadasacomponentofsnakeconservationmanagement.MonitoringtoestablishthedescriptiveepidemiologyofSFDaswellastobetterassociateenvironmentalriskfactorswithimpactsandsusceptibilitytoSFDwillhelpimprovethebiologicalunderstandingofSFDandbetterdirectfuturemanagement.

• TherestrictionsassociatedwithshippingofmedicalsamplesfordiagnostictestingofCITESclassifiedanimalswillrequirethatsufficientandreliabletestingmodalitiesbeavailablewithinCanada.TheCWHChastworegionalcentreswithO. ophiodiicolaPCRcapacityandexperienceddiagnosticpathologiststhroughallcentres.ECCCshouldexploremeanstoovercometheseCITESassociatedconstraintsonwildlifediagnostictesting.

• Thereareuniquechallengestoundertakingsurveillanceinsnakesduetotheircrypticnature,thelackofinvestmentinpopulationmonitoringandsmallthecohortofpeoplewithactiveinterestsintrackingsnakepopulations

o ActiveoutreachtotheherpatologicalcommunitytoadvocateforincreasedsubmissionsofsnakesamplestoCWHCdiagnosticlabsisashortterm,no-to-lowcostmethodstoincreaseourunderstandingofsnakediseasesinCanada.

• Cooperationwithprovincialpartnerscouldfosterlow-costepidemiologicalstudiesifmoreeffectiveintegrationofdiseasesurveillanceinformationwithpopulationdatawasencouraged.

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Appendix 1: Decision tree framework for the threat assessment of SFD

Reducevulnerability

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Appendix 1: Decision tree framework for the threat assessment of SFD.

Disease threat event

Suspectible species?

No

No action

Yes

Expected?

No

Serious harm?

No

Track the disease

Yes

Hi or ongoing exposure?

Yes

Known response?

Yes

Respond

No

No

Can it be isolated?

No Yes

Isolate

Yes

Serious harm?

Yes No

Track risk factors

Decision node

Action node

Reduce vulnerability





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Using the decision tree

Answer questions posed at decision nodes

Decision Node D1- Are there species susceptible to the threat?

Susceptibilityconsiderstheextenttowhichindividuals,populationsorcommunitiesarenegativelyaffected,influenced,orharmedwhenexposedtoathreat.Aspeciesisconsideredsusceptibleifendogenousfactorsaresufficienttoallowthethreattomanifestasadiseaseprocessinindividualsand/orifexogenousfactorsmakeapopulations/communitiesorecosystemsmorelikelytoexperienceharmsfromthethreat.

Athreatissubjectivelyscoredhigherinthisdecisionnodewhen:• Morethanonespeciesissusceptible• Speciesinmultiplegenera(includingpeople)aresusceptible• Thespecies/populationofinterestisexperiencingmultiplestressorsthatmightmagnifyormake

morelikelytheadditiveharmfromthethreat.

Decision node D2 – was the threat expected?

Unexpectedthreatsareknowntoinfluencetheresponsetoahealththreataswellasperceptionsofrisk.Decisionmakersatallscalesareconcernedaboutreducingthelikelihoodofsurprisesbecausesurprisesreduceourtrustintheknowledgeandpeopleuponwhomwerelytoprotectus.Thistypicallyrequiresamoreprecautionaryapproachtobetakenwhenmanagingunexpectedeventsuntilthelevelofuncertaintyisreduced.

Athreatissubjectivelyscoredhigherinthisdecisionnodewhen:• thereisanalogytoindicatethethreatislikelytocauseharm• thenumberofeffectedspecies/populationsandgeographicdistributionrapidlyincreases.• thereisadiversityofspeciesaffected

Decision node D3 – can the threat cause serious harm?

Finaljudgementofthethresholdfortoestablishifathreatisseriouscanbesubjectiveandbasedonriskperceptions.Athreatwillbeconsideredabletocauseseriousharmif:

Individuals:(i)Animals-itcausesmorbidityormortalitythatimpedestheanimal’sabilitytofulfillitexpectedecologicaloreconomicfunction.(ii)People–itcausesmorbidityormortalityorcausesnotableeconomicorculturalimpacts

Populations:thethreatconstrainstheabundanceand/ordistributionofapopulationbeyondcapacityforthepopulationtocompensateand/oritreducesavailabilityorsafetyofanecologicalserviceprovidedbythepopulation.

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Community:Multiplepopulationsareaffectedbythethreat. Athreatissubjectivelyscorehigherinthisdecisionnodewhen:

• Theharmsareirreversible• Thepopulationisunabletocopewithorcompensatefortheharms• Morethanoneharmoccurs

Decision node 4 – is there high levels and/or persistent exposure to the threat?

Riskcannotexistifthereisnoexposuretothehazardcausingtherisk.Exposureisgenerallynothomogenousoverspaceandtimeorwithinpopulationsandcommunities.Sub-populationswithhigherexposureareathigherrisk,assumingequivalentsusceptibility.

Athreatissubjectivelyscoredhigherinthisdecisionnodewhen:• Thehazardcanpersistentintheenvironment• Thehazardispresentinmultipleexposurepathways• Thereisalargeamountofthehazardorhighconcentrationsintheenvironment

Decision node 5: Are there know, effective means to prevent, mitigate or eliminate the harms from the threat?

Riskscanbeeliminated,reducedormanagedtotolerablelevelsiftherearerapid,cost-effectivemeanstoreducetheexposureorharmsfromahazard.Thisactionsshouldcauseaslittledamageaspossibleandnotresultinadditionalharms. Athreatissubjectivelyscoredhigherinthisdecisionnodewhen:

• Thereislittleornoevidencewithwhichtoprescribethemosteffectiveandefficientactions• Thecostoftheactionsexceedsthebenefitand/ortheactionsarenotpracticallyorsociallyfeasible

oracceptable• Collateralseriousharmstotheaffectedorconnectedspecies/populationsmayoccurduetotherisk

mitigationactions

Decision node 6: Can the threat or harm be isolated or contained to minimize its geographic dis-tribution to tolerable levels?

Theharmsassociatedwithathreataremorelikelytoirreversibleorunacceptablewhentheycanbecomedispersedoveralargergeographicarea,thusexposingmoresusceptibleindividualsand/orincreasingtheextentanddurationofexposureopportunities.Spreadofadiseaseincreasesthelikelihoodthatvulnerablepopulationsmaybecomeexposed.

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Athreatissubjectivelyscorehigherinthisdecisionnodewhen:• Therearenoproven,feasibleorsociallyacceptablemeanstoisolateorcontainathreator

vulnerablepopulationstopreventgeographicspread• Actionstoisolatethethreatcauseunacceptablecollateraldamagetospeciesorpopulationsof

concern• Themechanismsofspreadofthethreatareunknown

Dealing with uncertainty at a decision node

Underconditionsofuncertaintyweassumeananswerisyesif;(i)analogoussituationspresentareasonableprobabilitytheanswercouldbeyes;(ii)thespeciesatriskarehighlyvalued;(iii)therearemultiplespecies(includingpeople)thatmaybeatriskand/or;(iv)therearemultiplepossibleharms

Details and justifications of the action nodes

Notes on interpreting the action nodes: Thenodesarenotmutuallyexclusive.Mosteffectivediseasecontrolprogramsrequiremultiplestrategiestobesuccessful.Theactionsnodesreflectthemajoremphasisorgoaltowhichcontroleffortsshouldaspirebuttheydonotprescribethespecificmeans,orcombinationofmeans,toachievethosegoals.

Action Node 1 – No action taken Scenario-thereishighconfidencethatnosusceptiblespeciesorpopulationsexistinplausibleexposurepathways,indicatingnoriskexists.Thegoalinthisstepistoprovideassuranceofnoharmthroughriskcommunication.Ifthereisahighperceptionofriskaboutthediseaseevent,researchcanbeundertakentoconfirmlackofsusceptiblepopulationsand/ortodetermineandmonitorthefactorsthatcouldalterspeciesorpopulationsusceptibility.

Action node 2: Track the disease through surveillance or monitoring programsScenario-susceptiblespecies/populationsexistforanunexpecteddisease,butthereisnoevidenceitcancauseharmunderthecurrentconditions.Thegoalatthisstepistoprovideassurancethatthediseaseepidemiologyiseithernotbeinginappropriatelycharacterizedaslowriskandtocontributetopreparednessplansinanticipationofchangingdiseaseepidemiology.Becausethediseaseisnew,emergingorre-emerging,therewillbesomeuncertaintyregardinghowitmaybehave,especiallyunderchangingenvironmentalconditions.Ifthesusceptiblepopulationsarehighlyvalued,effortsshouldbeplacedtotrackthedisease,tomonitoritsspreadintimeandplace,andevaluateifthatspreadisrelatedtounanticipatedseriousharms.Whetherthistakestheformofsystematicsurveillance,periodicsurveysand/orresearchdependsonthevalueplacedontheaffectedpopulations.

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Action node 3 – Monitor risk factors Scenario-anendemicofexpecteddiseaseeventoccursinvolvingsusceptiblespecies,butthediseaseisnotknowntocauseseriousharm.Becausediseaseecologyandepidemiologyisnotafixedcharacteristicofadisease,theimpactsofadiseasecanchangewithsocialandecologicalchange.Thegoalofthisstepistomaintainasituationalawarenessofanendemicrisktoinformpreparednessplansinresponsetochangingriskfactors.Ifthesusceptiblespeciesareofhighvalueorprovidehighlyvaluedservices,programsshouldbeinplacetoreviewand/ormonitorriskfactorsthatmayinfluencetheepidemiologyandimpactsofthedisease.

Action node 4 – Implement disease response planScenario-asusceptiblespeciesisaffectedbyanexpectedorunexpecteddiseasethatcancauseharmandtherearewidespreadorhighlevelsofexposure.Actionsshouldbetakentoreducethedistributionandimpactsofthedisease.Thegoalofthisstepistomitigatetheharmsfromthedisease.Thisactionistakenwhenthereisevidenceofeffective,cost-efficientmeanstomitigatetheharmsfromthedisease,preventotherpopulationsfrombeingeffectedand/orreducethegeographicspreadofthedisease.

Action node 5 – Contain or isolate the disease and hazard to a restricted geographic areaScenario-asusceptiblespeciesisaffectedbyanexpectedorunexpecteddiseasethatcancauseharmbutthereisreasonableevidencethatthegeographicdistributionisrestrictedtoafocallocation.Thegoalinthisstepistorestricttheharmstoaspecificgeographiclocation.Optionstorestrictthemovementsofinfectedpopulationsorthehazardshouldincludehumandimensionsofspeciesandhazardstransmissionandwillrequireagoodunderstandingoftransmissiondynamicsandenvironmentalpersistenceofthehazards.

Action node 6 – Reduce the vulnerability of the populations at risk to the harms of concernScenario-asusceptiblespeciesisaffectedbyanexpectedorunexpecteddiseasethatcancauseharmbuttherearenoevidence-based,cost-effectivemeanstomitigatetheharmorisolateittoaspecificlocation.Thegoalatthisstepistohelpthespeciescopewithandrecoveryfromtheimpactsofthethreat.Optionstoreducevulnerabilityinclude;reducingexposuretothethreat,reducingsusceptibility,reducingothercumulativestressorsandprovidingtheintrinsicandextrinsiccapacitytotolerate,copeandrecoverfromharms.

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Appendix 2: Diagnosing snake fungal disease

SUSPECT case definition–thatcouldbeusedasatentativecasedefinitionbasedonclinicalsignsforuseinthefield.

Grossly visible lesions of SFD

• Signaretypifiedbypatchyareasofthicklightbrowntoyellowscabs,crustyscales,patchesofirregularskinthickeningandpallor(hyperkeratosis),orsuperficialfluidfilledblistersorpustules.Chroniccasesoftenincludefirm,encapsulated,subcutaneousnoduleswhichareindicativeofdeepdermalinvasion,granulomatousinflammation,andfibrousencapsulationwhichoftenmayresultinswellinganddistortionofthefaceandhead.Lesionsareespeciallyprominentwithinareasoftheskinthataretypicallyexposedtonaturalabrasiveforcessuchastheventro-lateralaspectsofthemouth,jaws,head,face,andnosetip,andtheventralscutesextendingtheentirelengthofthesnake.Althoughtheselocationsarethemosttypicallyaffectedareas,lesionsmayextendintoadjacentsurfacesorcanbescatteredanywherealongtheskinsurfaceofthesnake.Affectedsnakesoftenalsoundergofrequentboutsofskinshedding/molting(prematureseparationofthesuperficialepidermisnotwithinanormalmoltperiod).Lesionsoftenappearlessapparentfollowingshedding;however,affectedfocioftenretainsmallpatchesofadheredskinshed(dysecdysis).Affectedfocicanoftenalsobeidentifiedintheskinsheditselfasirregularmottled,orangetobrown,foci.Extensionofthefungalorganismintothespecializedkeratinlayeroverlyingtheeye(spectacle)oftenalsoresultsinedemaandthickeningwhichgrosslyappearsasopaquecloudinessoftheeye.Associatedinflammationoftenresultsinsubcuticularedema(anasarca)orfluidaccumulation(fluidfilledvesicles)betweenanimpendingskinshedandthenewlyformedepidermis.Immediatelyafterinfectedsnakesshedtheirskin,lesionsmaybelessnoticeable(atleasttemporarily).

CONFIRMED case definitionifaccompaniedbycharacteristicclinicalandhistologicallesions

Histopathological lesions

• Histologicallythereiscoagulativenecrosisofthesuperficialkeratinlayersoftheepidermiswithepidermalthickeningandhyperkeratosisand/orfullthicknessulcerationintotheunderlyingdermis.Lesionsoftencontainfewtolargenumbersoffungalhyphaethatarepredominantlydistributedalongtheskinsurfaceandsuperficialkeratinlayerswithextensionoffungialongareasofnecrosisandulcerationintotheunderlyingdermis,subcutisandoccasionallyskeletalmusclelayersand/orbone.Inchroniccases,subcutaneousnodulesarecomposedofcentralcoresofeosinophilicnecroticdebriswithadmixedfungalhyphaethatarewalledoffbyvariablenumbersofheterophils,macrophages,multinucleatedgiantcells,andperipherallayersoffibrousencapsulation(typicalheterophilicgranulomas).Hyphaearehyalineandclear,measurebetween2.0to7.0µmwide,containparalleltoslightlyirregularsides,areoccasionallyseptate,andexhibitraredichotomousbranching,andoccasionalcharacteristicrectangulararthroconidiaareformedbysurfacehyphae(Rajeev2009;Allender2011;Latney2013;McBride2015).Hyphaecanbeaccentuatedwithspecial

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histochemicalstains(e.g.PeriodicAcid-Schiff;Grocott’sMethenamineSilver)whichareespeciallyhelpfulinchronicheterophilicgranulomaswherehyphaeareoftenfewinnumbersand/orblendedwithnecroticdebris.Althoughthehisto-morphologicalfeaturesareoftenhighlysuggestiveofO. ophiodiicola,itcanbedifficulttodifferentiateitfromothercommonopportunisticfungalinfectionsinsnakes(e.g.Trichophyton spp., Fusarium spp.etc.)ortoidentifyspecificcharacteristichyphalfeaturesinmixedfungalinfections.Therefore,specificpathologicalcriteriaforthediseasehaveyettobeestablishedandadditionalancillarydiagnostictestingsuchasmolecularPCRtestsand/orfungalcultureandidentificationisoftennecessarytoultimatelyconfirmthediagnosis(Rajeev2009;Allender2015a;Bohuski2015).

Molecular diagnostics/PCR testing

• Thisisthemostsensitivetestsavailable.ItshouldbeconsideredthatapositivetestresultsdoesnotconfirmadiagnosisofSFDbutratherconfirmsthedetectionofthepresenceofO. ophiodiicola.

o Testsavailable ▪ Allenderetal.2015a–currentlyavailableatAnimalHealthLaboratory,Universityof

Guelph,Box3612,Guelph,Ontario,Canada.Real-timePCR(qPCR)assaythattargetstheinternaltranscribedspacer1regionbetweenthe18Sand5.8SribosomalRNAgene.Crossreactionwithcloselyrelatedfungalspeciesnotspecificallyinvestigated;however,sequenceanalysisofthetargetedregionshouldbespecificforO. ophiodiicola.

▪ Bohuskietal.2015PCRisavailableatUnitedStatesGeologicalSurvey(USGS)NationalWildlifeHealthCenterwhichhasthemandatetotestfreerangingnativesnakesbutwilldocaptiveorexotictradesnakesaspartofresearchprojectstoestablishtheglobaldistributionofthefungus.Consistsoftworeal-timePCR(qPCR)assays,onethattargetstheinternaltranscribedspacerregion(ITS)ofthefungalgenome,whiletheothertargetsthemorevariableintergenicspacerregion(IGS).TheNWHChasinvestigatedthepotentialforcrossreactionwith28closelyrelatedfungalspeciesandfoundnone.

▪ White1990–conventionalPCRassaytargetingfungus-directed18srRNAgeneandusedforgeneralidentificationofvariousfungalspeciesbasedonthegeneratedDNAsequence.AlthoughthisisafunctionalassayformostfungalinfectionsithasperformedpoorlywithcasesofO. ophiodiicola(personalcommunicationDr.JeffLorchUSGSandpersonalexperiencewithsuspectSFDcasesatAnimalHealthCentreBritishColumbia).MixedinfectionsalsoposeasignificanthurdleandthemixedDNAsequenceisofteneitherimpossibletodecipherorthesequencefromthemostnumerousorfastestgrowingfungusmightdominateandoverwhelmthesequencesobtainedfromotherfungi.

Fungal culture and morphological identification

• TheoriginaldescriptionandcharacterizationofthisfungusoutlinesavarietyofdiagnosticmorphologicfeaturesandbiochemicaltestresultsforO. ophiodiicola(Rajeev2009).Themostdistinctmorphologicalfeaturesofthisfungusoncultureincludetheformationofabundantnarrow,cylindrical-to-slightlyclavateconidia.Culturesareaccompaniedbyastrongpungentodor

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characteristicofonygenales(orderofkeratinlysing)fungi.Althoughhighlyeffectiveiffungalgrowthisobtained,themostsignificantdrawbackoffungalcultureistheextendedtimeframeneededtoreachadefinitivediagnosis.O. ophiodiicolaisalsoreportedlyafastidiousandslowgrowerthatisoftenoutcompetedbyotherfungalorganisms(eitherasco-infectionsorenvironmentalcontaminants)andspecializedmediaisrequired(personalcommunicationDr.JeffLorchUSGS).

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Appendix 3: Summary of key cases in SFD history

Free-ranging snakes -- USA

The first documented report of fungal disease in free-ranging snakes in North AmericaSeverenecrotizingfungaldermatitis,stomatitisandopthalmitiswasdiagnosedin1997-98inpygmyrattlesnakesfromtheLakeWoodruffNationalWildlifeRefugeinFlorida(Cheatwoodetal.2003).In1997-1998,inapopulationofroughly600snakes(Mayetal.1996),16pigmyrattlesnakeswithsevereeye,head,mouth,andmultifocalskinlesionswerefoundduringregularsurveysofthestudysite,nineofwhichwereeitherfounddeadinthefieldorweremoribund(Cheatwoodetal.2003).Atthepeakofthisoutbreak,onegartersnake(Thamnophis sirtalis)andoneribbonsnake(Thamnophis sauritis)alsowerefoundwithlesionsconsistentwithSFD.Aretrospectiveanalysisofcapturerecordsbetween1992and1997revealedafurther59pygmyrattlesnakeswithsignsconsistentwithfungaldiseaseinthispopulation,buttheselesionsallwerecharacterizedasfocaltomultifocalmildintegumentarylesionswithoutapparentmortality.ItisnotclearifthisincidentwasaSFDoutbreak.FungalcultureofsamplesfromaffectedanimalsfailedtogrowO. ophiodiicola.Theunusualmortalityandsix-foldincreaseinincidenceofdiseasein1997-1998relativetothebalanceofthe1992-1999intervalsupportthecharacterizationofthisincidentasanepizootic.

The first case of population decline associated with SFDIn2006,signsoffungaldermatitiswereassociatedwiththedeclineofanisolatedpopulationofthetimberrattlesnake(Crotalus horridus)inNewHampshire(Clarketal.2011).Otherpopulationsofthisspeciesmonitoredatthesametimewereapparentlyunaffectedanddiseasewasnominatedasanimportantconstituentofasuiteoffactorsdrivingtheobserveddecline(Clarketal.2011).Theeffectedtimberrattlesnakepopulationwasexceptionalinthatitwasasmall,isolated,lastknownpopulationoftimberrattlesnakesinNewHampshire.Thepopulationhadbeenconstantataround40individualsfrom1995-2005(TaylorandMarchand2006),anddisplayedsignsofdepauperategeneticdiversityatbothphenotypic(highproportionofdarkandpiebaldmorphsthatareveryrareordonotoccuratallinotherpopulations)andgenotypiclevels(significantlylowerallelicrichness,and,forremainingalleles,anexcessofheterozygosityatneutrallocithatisindicativeofarecentpopulationbottleneck)(Clarketal.2011).Thedeclinealsocoincidedwithaperiodofunusuallywetweatherin2005and2006.AveragemonthlyprecipitationtotaledforthestateofNewHampshirefortheMay–Octoberactiveseasonfor2006was101.3cm,thehighestonrecordfromtheUnitedStatesNationalClimaticDataCenteratnearlydoubletheaverage57.1cm(McBrideetal.2015).Theaveragefor2005was91.4cm,thesecond-highestonrecordfollowing2006.Theauthorspointoutthatincreasedcloudinessandhumidityassociatedwithhighprecipitationcanbedetrimentaltotimberrattlesnakes,astheseconditionsarecorrelatedwithreproductivefailureinfemales(Martin1993,2002,Clarketal.2011).Inadditiontoapossibledirectimpact,theunusualandextremeweathermayhavefacilitatedinfectionwithO. ophiodiicolasincefungaldiseaseincaptivereptilesisoftenassociatedwithinappropriatetemperatures,highhumidity,andstress-relatedimmunosuppression(Paréetal.2007,MitchellandWalden2013).Becauseoftheseconcurrentenvironmentalandpopulationattributes,theextentofdeclinesfromSFDmaynotbegeneralizedtoallaffectedsnakepopulations.Whilethislevelofmortalityappearstobeexceptionalatthistime,thecircumstancesthatproduceditarebecomingincreasinglycommon.

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Inthe2006outbreak,manytimberrattlesnakesdisplayedskinlesionsaroundthehead,chin,andbody.Oneindividualwithseveremycoticstomatitiswasfounddead.AlthoughtimberrattlesnakesinthisareatypicallyenterhibernationduringthefirstweekofOctober(Clarketal.2011),eightindividualsremainedvisibleoutsideofthehibenaculumareainOctober,andatleastthreeoftheselingeredoutofthedenintothefirstweekofNovember.Onlyoneofthoseeightsnakeswasseenaliveinspringof2007,andithadaseverelyswolleneye,andhasnotbeenobservedsubsequently.Twooftheremainingsevensnakeswerefounddeadinearlyspringof2007;theothershavenotbeenseensince2006.TheroleofSFDinlateentrancetothehibernaculumisnotclearlydemonstratedhere,butinappropriatebaskingassociatedwithSFDwasobservedininfectedtimberrattlesnakesinMassachusettswherefourinfectedsnakeswereobservedbaskinginthesunduringthewintermonths(December-March)(McBrideetal.2015).Populationsurveysfrom2007-2010observedonly19individuals,indicatingthatthepopulationdeclinedbyapproximately50%in2006-2007atthetimethediseasewasobserved. Outbreak in Carlyle Lake population of eastern massasaugasO. ophiodiicolawasconfirmedasthecauseoftheseverefungaldermatitisthatcausedmortalityintheCarlyleLakepopulationofeasternmassasaugas(Sistrurus catenatus)beginningin2008(Allenderetal.2011).In2008threesnakes(representingapproximately4%ofthepopulation)withseverefacialswellinganddisfigurationdiedwithin3weeksafterdiscovery(Allenderetal.2011).In2010afourthsnakewithsimilarsignsapparentlysurvivedwithtreatment.Noattemptwasmadetoassesspopulation-leveleffects.In2011thesamepopulationwassurveyedand0of34apparentlynormalsnakeswerepositiveforO. ophiodiicolabyPCR(Allenderetal2013),althoughthreeindividualswereobservedwithsubtletomildlesionsconsistentwithSFD.Therewerenoobservationsofsevereinfectionormortalityduringthe2011survey.Morerecently,O. OphiodiicolahasbeenconfirmedasthecauseofmortalityintwoeasternmassasaugasseveralhundredkilometresnorthofCarlyleLakeMichiganin2013(Tetzlaffetal.2015).

Gartersnakes in USAIn2012afree-rangingplainsgartersnake(Thamnophisradix)inIllinoiswasfoundtohaveseveredisseminatedophidiomycosis(Dolinskietal.2014).SystemicinfectionsareveryrareintheliteraturebutthiscasewassimilartoacaseofsystemicophidiomycosisreportedinacaptivegartersnakeinEurope(Vissiennonetal.1999,Sigleretal.2013)andagartersnakeinPennsylvaniainwhichnecropsyrevealedmycoticlesionsinlungandpancreas(Ohkuraetal.2016)suggestingthepossibilitythatgartersnakesmaybeunusuallysusceptibletosystemicinfection(Dolinskietal.2014).

Weather and SFD in Massachusetts rattlesnakesTheroleofSFDinlateentrancetothehibernaculumisnotclearlydemonstrated,butinappropriatebaskingassociatedwithophidiomycosiswasobservedininfectedtimberrattlesnakesinMassachusettswherefourinfectedsnakeswereobservedbaskinginthesunduringthewintermonths(December-March)(McBrideetal.2015).

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