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Natureza
&
Conservação
Brazilian
Journal
of
Nature
Conservation
SupportedbyBoticárioGroupFoundationforNatureProtection
Essays
and
Perspectives
Domestic
dogs
in
protected
areas:
a
threat
to
Brazilian
mammals?
Isadora
Lessa
a,∗,
Tainah
Corrêa
Seabra
Guimarães
b,
Helena
de
Godoy
Bergallo
c,
André
Cunha
a,
Emerson
M.
Vieira
daGraduatePrograminEcology,InstitutodeCiênciasBiológicas(IB),UniversidadedeBrasília(UnB),Brasília,DF,Brazil bInstitutoChicoMendesdeConservac¸ãodaBiodiversidade(ICMBio),Brasília,DF,Brazil
cLaboratoryofMammalEcology,InstitutodeBiologia,UniversidadedoEstadodoRiodeJaneiro(UERJ),RiodeJaneiro,RJ,Brazil dLaboratoryofVertebrateEcology,DepartamentofEcology,InstitutodeCiênciasBiológicas,UniversidadedeBrasília(UnB),Brasília,DF,
Brazil
a
r
t
i
c
l
e
i
n
f
o
Articlehistory:
Received13January2016 Accepted12May2016 Availableonline25May2016
Keywords:
Alienspecies
Canislupusfamiliaris
Protectedareamanagement Anthropogenicimpacts Invasionecology
a
b
s
t
r
a
c
t
Thepresenceofdomesticdogs(Canislupusfamiliaris)inBrazilianprotectedareasisfairly frequent.Theinteractionofsuchdogswithnativeanimalsleadstopopulationdeclines formanyspecies,particularlycarnivores.Inthispaperthemainthreatsdogsbringabout Brazilianbiodiversityareassessedwithafocusonprotectedareas.Wecollected informa-tionfrompapersontheinteractionofdogsandwildlifespeciesaswellasfrominterviews withNationalParkmanagers.StudiesinprotectedareasinBrazillisted37nativespecies affectedbythepresenceofdogsduetocompetition,predation,orpathogentransmission. Amongthe69threatenedspeciesoftheBrazilianfauna,55%havebeencitedinstudieson dogs.Dogoccurrencewasassessedfor31NationalParksinBrazil.Thepresenceofhuman residentsandhuntersinprotectedareaswerethefactorsmostoftenquotedasfacilitating dogoccurrence.Thesemaybeferal,streetordomesticallyowneddogsfoundinprotected areasinurban,ruralornaturalareas.Effectiveactionstocontrolthisinvasivealienspecies innaturalareasmustconsiderdogdependenceuponhumans,pathwaysofentry,andthe surroundinglandscapeandcontext.
©2016Associac¸ ˜aoBrasileiradeCi ˆenciaEcol ´ogicaeConservac¸ ˜ao.PublishedbyElsevier EditoraLtda.ThisisanopenaccessarticleundertheCCBY-NC-NDlicense(http://
creativecommons.org/licenses/by-nc-nd/4.0/).
Introduction
Theintroductionofalienspeciesisoneofthemost signifi-cantthreatsinflictedbyhumansonbiodiversity(Scholesand
Biggs,2005).Invasivealienspeciesmayalterenvironmental
∗ Correspondingauthor.
E-mailaddress:isadoracristinam@gmail.com(I.Lessa).
conditionsand causesevereimpactsinnaturalcommunity composition andstructure(Richardson,2011).The Conven-tiononBiologicalDiversitydefinesinvasivealienspeciesasa speciesoutsideitsnativerangewhichthreatenstheintegrity of ecosystems, habitats, and the permanence of indige-nous species. Interactions such as predation, competition,
http://dx.doi.org/10.1016/j.ncon.2016.05.001
1679-0073/©2016Associac¸ ˜aoBrasileiradeCi ˆenciaEcol ´ogicaeConservac¸ ˜ao.PublishedbyElsevierEditoraLtda.Thisisanopenaccess articleundertheCCBY-NC-NDlicense(http://creativecommons.org/licenses/by-nc-nd/4.0/).
pathogentransmissionand hybridizationinitiateecological processesthatleadtonativespeciespopulationdeclinesand changesinecosystemdynamics(Simberloffand VonHolle, 1999).Domesticcatsanddogsareconsideredinvasivealien specieswhenusingorlivinginnaturalareaswithouthuman assistance.Catsarelisted asoneofthe100worstinvasive alienspeciesontheplanet(Loweetal.,2000)andthemajority ofpaperspublishedinthepasttenyearsontheinteraction ofdogsandnativeanimalsstresstheirnegativeimpactson biodiversity(HughesandMacdonald,2013),eveninprotected areas.
Domesticdogs(Canislupusfamiliaris)maybeconsidereda potentialthreattotheintegrityofprotectedareasinBrazil, particularlyofthoseinthe highestlevelofprotection.The presenceof theseanimals inprotected areas or their sur-roundingsmayreduceeffectivenessinconservingbiodiversity (MMA,2013).TheNationalBiodiversityPolicydefinesthatit isvitaltoforesee,prevent,and takeactionagainstthe ori-ginofprocessesleadingtoconsiderablebiodiversitydecline orloss(Decreeno.4.339,August22nd,2002),suchasinvasive alienspecies.Inthisstudyweassessedinformationpublished ontheimpactofdomesticdogsinprotectedareas,described theseimpactsparticularlyforBrazilianprotectedareas,and provideddirectionsforprotectedareamanagementindealing withtheproblem.Aliteraturereviewonthetopicwascarried outandcomplementedbyinterviewswithNationalPark man-agersinBrazil.Theinformationgatheredwasclassifiedinfive topics,thefirsttwoonbasicinformationondognatural his-toryandinteractionswithnativespecies,thethirdonpapers publishedcoveringdogimpactsinprotectedareasaroundthe world,thefourthonproblemsinBraziliannationalparks,and thelastoneonguidanceforinvasivedogmanagementin pro-tectedareasinBrazil.Thisstudyisconsideredapreliminary approachtotheproblemandasourceofinformationforfuture actionandresearchforcontrollingdomesticdogsinBrazilian protectedareas.
Canis
lupus
familiaris
(Linnaeus,
1758)
natural
history
Theglobalpopulationofdomesticdogshasbeenestimatedat 700millionwidelydistributedaroundtheworld(Hughesand
Macdonald,2013).Brazilranksasthirdinhighestdognumbers
aftertheUnitedStatesandallEuropeancountriesconsidered asaunit,withabout27milliondogs(HughesandMacdonald, 2013).Thehighestdensityregisteredtothismomentis76dogs perkm2inaruralareainBrazilinPiracicaba,inSãoPaulostate
(Camposetal.,2007).Dogsaredistributedindifferent
land-scapes,mostly urbanand ruralunderhumanintervention, butalsoinprotectedareasunderthestrictprotectioncategory inBrazil.Dogshavebeenassociatedwithhumanpopulations formorethan33,000years(Ovodovetal.,2011).Inspiteof providingsomebenefitstosociety,domesticdogshave gener-atedmanynegativeimpactsonbiodiversity,particularlydue tointeractionswithnativeanimals.
Tobetterdefinetherelationshipofdogswithbiodiversity theyhavebeenclassifiedaccordingtotheirdependenceupon humans:owneddogs;streetorfreelivingdogs;andferaldogs
(Srbek-AraujoandChiarello,2008;Camposetal.,2007;Lacerda
etal.,2009;HughesandMacdonald,2013).Owneddogslivein
propertieswithresourcessuchasfood,shelter,and interac-tionsprovidedbyhumans.Streetdogsarenotunderhuman care,survivingopportunisticallyonfoodresourcesofferedby humans.Thisclassrepresents75%ofthe700milliondogsin the world(Hughesand Macdonald,2013).Feraldogslivein natural areas,legallyprotected or not,yet closetohuman dwellings. These dogs may occasionally feed on resources offeredbyhumans,butarenotdependentuponthem.They have a generalist diet(Macdonald and Carr, 1995;Campos etal.,2007),oftenfeedingonfoodresourcesmadeavailable byhumans,butalsoonanimalcarcassesandagreatvariety ofanimalandvegetalfooditems(Camposetal.,2007).
Domesticationeffortshavemadedogsreactwithspecific behaviorresponseswhenpromptedbyrewardsintheform offood,playing,pettingorsimplyattention(ScottandFuller, 1974).Dogsinnaturalareas,however(aloneoraccompanied byhumans),arestimulatedbytheenvironmentandreact sim-ilarlytotheirwildancestors(ScottandFuller,1974;Gompper, 2013).Thesedogsdevelopgreaterhuntingabilitiesandmake betterusethenaturalareas,changingtheirsocialbehaviorby formingpacks(RubinandBeck,1982).Thepresenceofdogsis thereforeathreattobiodiversityandneedstobetreatedwith effectivemanagementactionstargetedatspecificdogprofiles ineachprotectedarea(Beck,1973;Lavigne,2015;Gompper,
2013;Youngetal.,2011).
Main
threats
to
biodiversity
by
dogs
CompetitionforterritoryDogs are considered themost abundantcarnivores in sev-eralnaturalareas(Hughesand Macdonald,2013),including theBrazilianAtlanticForest(Paschoaletal.,2012).Theyoften occurinmuchhighernumbersthannativecarnivores, usu-allypresentinlowdensities.Thisindicatesthepotentialhigh impactofdogsonthecommunityasawhole,and particu-larlyonvertebrates(VanakandGompper,2009;Vanaketal., 2013).Highdogdensitiesinnaturalareasmay,atfirst,affect nativecarnivoresduetocompetition.Dogdensity,predatory behavior,andpathogentransmissionwilldeterminethe spa-tialrangeofcompetitionanditsresultingimpactonnative faunaasassessedthroughmodelingbasedonempiricaldata
(Vanak and Gompper,2009). Themerepresenceof dogsin
areas with native speciesintensifies competitionfor space andresources(Atickemetal.,2010).Thepresenceofdogsin naturalareasinIndianegativelyaffectsthespatial distribu-tion ofthe Indianfox, Vulpesbengalensis;the probabilityof site use by the foxis directly proportional tothe distance from sites used bydogs,regardless ofresource availability
forthe fox(Vanak andGompper, 2010). InBrazilian
Savan-nasthemanedwolf(Chrysocyonbrachyurus)avoidsareaswhere domesticdogsarepresent,possibleevidenceofcompetition forterritorybetweendogsandnativecarnivores(Lacerdaetal.,
2009).
Predation
Dogsoftendonottrulyprey,aspredationisdefinedasthe act ofcapturing (directlyor indirectly) and feeding on the
10 9 8 7 6 5 4 3 2 1 0 Predation Competition
Impacts of domestic dogs
Number of papers
Pathogens
Figure1–Numberofstudiescarriedoutinprotectedareas includingdomesticdogimpactstonativeanimalsby predation,competitionorpathogentransmission.
prey(Strauss,1991). Dogsusuallychase and captureother
species forfun. In these predator – prey games they may injureanimals,leadingtodeath,whilenotalwaysfeedingon
them(Gompper, 2013). Becausethis directinteraction with
wildspeciesisthemostfrequenttopicinthestudiesassessed wemaintainedtheuseofthetermpredationforthistypeof impact(Fig.1).
HughesandMacdonald(2013)indicatethatpredationisthe
highestimpactcausedbydogsonnativespecies,leadingto populationdeclineevenofrareorthreatenedspeciessuchas thedeerPudupudaintheAndes(Silva-Rodriguezetal.,2010) andmarineiguanasintheGalapagosIslands(KruukandSnell, 1981).Themostemblematiccaseregisteredistheannihilation ofakiwibird(Apteryxmantelli)populationbyonesingledog onanislandinNewZealand(Taborsky,1988).Dogshavebeen identifiedaspotentiallyefficientpredatorsinseveralpartsof theworldsuchasAustralia,Africa,andNewZealand(Butler etal.,2004).Publishedscientificinformationonnativespecies preyedbydogs inBrazilisscarce.Thesepublications most oftenrefertosmall and mediummammals killedbydogs, butalsotodeer,tapir,andprimates(GalettiandSazima,2006;
Camposetal.,2007;Oliveiraetal.,2008;Lacerdaetal.,2009).
Therearefewstudiesondogsasprey,butoneparticular examplefromAfricareportsleopardpopulationsdepending upondogfeedingforsurvivalinafarmingareawherenatural resourcesandanimalpopulationsaredepletedandfew leop-ardsremainduetohuntinganddisease(Bodendorferetal., 2006).Thejaguarisapotentialpredatorofdomesticanimals inBrazil,includingdogs(Leiteetal.,2002;Whitemanetal., 2007), butwould hardlybedependentupon dogsasafood source,giventheabundanceofotherspecies.Theinteraction ofdomesticdogswithjaguarscouldstillbenegativeforthe nativespecies,aspacks ofdogsmay ambushand transmit pathogenseventolargecats(Furtadoetal.,2008).
Pathogentransmission
Dogsfunctionasparasiteandpathogenreservoirsfornative animalsandhumanpopulations.Theyarepotentialvectors
of distemper, parvovirus, rabies, leishmaniosis and heart-worm,whichthreatennativevertebratepopulations.Canine distemper is a viral disease which has been a signifi-cant cause of the decline of wild carnivore populations
(Appel and Summers, 1995; Cleaveland et al., 2000). The
weaselMustelanigripeswasincludedinthelistofthreatened speciesintheUnitedStatesbecausethepopulationgreatly declined mainly due to distemper (Thorne and Williams, 1988).Thebeststudiedcarnivorepopulationdeclinecasesare inAfrica,whereanepidemic ofthe distempervirus trans-mittedbydogskilled30%ofalion(Pantheraleo)population in the Serengeti National Park in Tanzania (Roelke-Parker et al., 1996). Contamination by this same virus increased mortality of the African wolf (Lycaon pictus), which was already threatened with extinction (Alexander and Appel, 1994). The frequent contact of wild dogs (Cerdocyon thous)
with domestic dogs in an area in the Brazilian Amazon explainedthe high likelihood ofdistemperandheartworm transmission (Courtenay et al., 2001). Distemper has been detected in nine jaguars (Panthera onca) in the Ivinhema State Park(SaoPaulo) inthe BrazilianAtlantic Forest, rep-resenting 60% of its population. Pathogens were possibly transmitted by dogs in the park surroundings, as 100%of the dogs tested positive for canine distemper(Nava et al., 2009). A recentstudy showed that dogs are more exposed to canine distemper virus and parvovirus in small pro-tected areas than in larger ones, and that exposure was associated with the sex, age, and lack of health care of dogs (Curi et al., 2016). Such studies provide strong evi-dencetosupportmanagementactionsforthepreventionof virustransmission.Studiesprovidinginformationonfactors whichexplainhowdomesticdogsbecomeathreattoother speciesareimportanttosupportpreventativemanagement actions.
Rabiesisanother zoonosis causedbyavirusand trans-mittedbydomesticdogstonativeanimals,butcorroborating studiesarescant.Thepresenceofthisvirushasbeen dimin-ishing indomestic dogs whileincreasing in wild animals, especially in carnivores and bats (Rupprecht et al., 1995;
Iamamoto,2005).
Dogsarethemostfrequentreservoir(91%)of leishmanio-sisprotozoanstransmittedbyphlebotomicmosquitoes,but only 9%ofnative canids functionas reservoirs(Courtenay et al., 2002). The factors facilitating transmission require further studies. Approximately two million people in the worldarecontaminatedbyleishmaniosismosquitoes every year (WHO, 2013). Besides leishmaniosis, heartworm can be conveyed to dogs, native mammals, and humans by a nematode transmitted by mosquitoes (genera Culex, Aedes
and Anopheles). Half of the street dogs in the USA (50%) are infected with this parasite (Nayar and Knight, 1999), while in Spain 433 red foxes (Vulpes vulpes)were infected (Gortázar etal.,1994).Theprevalenceofthis pathogenwas verified in Brazil in 40% of street dogs in cities in the northeastern region, and 30% in the southeast (Ahid and
Lourenc¸o-de-Oliveira, 1999;Labartheetal., 1998).Advances
in research on potential disease transmission by domes-tic dogs as well as the severity of disease impacts on native vertebrates is essential for the conservation of the latter.
Dogs
in
protected
areas
Weassessed 23 papers on dog impacts inprotected areas around the world from which three types of interaction stood out (predation,competition, andpathogen transmis-sion;Fig.1,AnnexI).Predation,meaningattackingprey,was registeredinnineofthestudiesassessed.Researchwork car-riedoutinBrazilshowsthatpredationprobablytakesplace bothduringthedayandatnight(Srbek-AraujoandChiarello,
2008; Galetti and Sazima, 2006). Competition was inferred
whereverdogsco-occurredwithnativespecies.Moreover, spa-tialoverlapwasalsoconsideredasanindicatorofpossible pathogentransmissionand predation.Thepathogen trans-missionstudiesassessedindicatehighpotentialfornegative impactsonnativeanimals.Distempertestedpositivein27%of 101domesticdogssampledintheTucuruiEnvironmental Pro-tectionAreaintheAmazonregion(Whitemanetal.,2007).At SerradoCipóinMinasGerais19%ofthenativecanidssampled showedprevalencefortheleishmaniosisprotozoan,whichis verylikelytransmittedbydomesticdogsinruralareasaswell asferaldogs (Curietal.,2006, 2012).Despite therelevance ofthis issuenoneofthestudies,particularlyinBrazil,has assessedcontroland managementalternatives forinvasive dogsinprotectedareas.
The domestic dog survey in protected areas in Brazil-ianNational Parkswas implemented using questionnaires directedatparkmanagersbytelephoneorInthisinitialphase informationwassoughtbasedonthefollowingquestions:(i) Arethererecordsofdomesticdogs(feral ornot)insidethe park?;(ii) Are thererecords of dog interaction with native wildlife? (Please give details such as which native species havebeenregistered,typeandfrequencyofinteraction,range withinthepark.);(iii)Whichfactorsfacilitatedomesticdog entryinthepark:residents,visitors,hunters,others?(please specify);(iv)Arethereanydogmanagementorcontrolactions inplace(which)?;(v)Is thereanyresearchconcludedor in processaboutdogsinthepark?Thisapproachallowedusto collectbasicdatatodirectfutureresearchandmanagement strategiesforprotectedareas.
Allmanagersinthe71nationalparksinallBrazilianbiomes werecontacted(AnnexIII),includingmarinenationalparks which include terrestrial areas. Thirty-one park managers answeredthequestionnaire,28(90%)ofwhichcorroborated dogpresence, and26 (84%) confirmedexisting interactions betweendogs and wildlife. Nodifferences indog presence were observedin national parksbetweenBrazilian biomes (2=3.829,p=0.43,gl=4;seeTable1andAnnex1forreplies
fromallbiomes).Furthermoretherewasnodifferenceneither intheproportionofnationalparkswithdogsinforestareas, open vegetation,or marine parks (2=1.474, p=0.48,gl=2)
norbetweendensely populated biomesandthose oflower humanpopulationdensity (2=0.207, p=0.88,gl=2).
Hunt-ingwasreportedasadogpathwayofentryforoneinevery threenationalparks,andisoneofthemajorfactorsleading tobiodiversitydecline,particularlythreateningmammalsand compromisingtheeffectivenessofprotectedareas(Chiarello, 2000). Asmanyhuntersuse dogstocatchthe desiredprey this becomes an impact intensification factor. In other 11 nationalparks(40%)residentswithinandaroundtheparks
Table1–OccurrenceofdogsasdeclaredbyNational Parkmanagersineachbiome;“Marine”referstothe terrestrialareaswhichareincludedinmarinenational parks.Intotal31managersansweredthequestionnaire. Therelativepercentageofparkswithanswersonthe presenceorabsenceofdogsisgivenwithinthetotal numberofparksineachbiome.
Biome Nationalparkswithanswerstoquestionnaire Presenceofdogs Absenceofdogs AtlanticForest 10(24–41%) –
Amazon 7(18–38.8%) 1(18–5.5%)
Savanna 6(13–46.1%) 2(13–15.3%)
Caatinga 3(7–42.8%) –
Marine 2(9–22.2%) –
were responsibleforthepresenceofdogs.Thelackofland compensationtoprivateownersupon theestablishmentof protectedareasisarelevantfactorinfacilitatingdogpresence, aspeopleremainontheirlandawaitingpayment.Thereare aboutsixthousandresidentsinsidetheLenc¸óisMaranhenses NationalPark,acommonsituationinmanyothers.Although thenumberofdogspresentinprotectedareasinBrazilhasnot yetbeenestimated,theirhighfrequencyintheparksassessed inthisstudyindicatethatthisisarelevantimpactfactoron biodiversity.
Amongtheprotectedareaswithdogrecordswhose man-agersansweredourquestionnairearethefollowingnational parks:CavernasdoPeruac¸u,Amazonia,ChapadadasMesas, ChapadaDiamantina,ChapadadosGuimarães,Serrada Capi-vara, Serra do Divisor, Serra do Itajaí, Serra dos Órgaos, Emas,SempreVivas,BoaNova,Brasília,IlhaGrande,Pacaás Novos,Saint-Hillaire/Lange,SãoJoaquim,Catimbau,Jaú, Juru-ena, Monte Pascoal, Pico da Neblina, Superagui, Lenc¸óis Maranhenses,Itatiaia,FernandodeNoronha,Montanhasdo Tumucumaque, and Pau Brasil. National parkswhere dogs havenotbeenrecordedareChapadadosVeadeiros,Serrada Canastra,andSerradaCutia.
Potential
impact
of
dogs
on
biodiversity
InareviewbyHughesandMacdonald(2013)64wildanimal speciesinteractingwithdogswerelisted,showingexpressive impactsonnativebirdandmammalpopulations.Sixty-three ofthesespeciesarepartoftheIUCN(InternationalUnionfor ConservationofNature)RedListofThreatenedSpecies(IUCN, 2012),33%ofwhicharethreatenedatthegloballevel.Welisted thespecieswithrecordsofinteractionswithdogsinBrazilas wellasinteractiontypesaccordingtothepresentassessment. NativespeciesstatuswasassessedbasedontheIUCNRedList
(IUCN,2012)andontheNationalOfficiallistofBrazilianfauna
threatenedofextinction(PortariaMMAn◦ 444publishedon December17,2014).
Thirty-seven native vertebrate species were listed from the23studiesassessed(Table2).Onlythreeofthesespecies are not mammals, while 85% (27) are medium or large-sizemammals(heavierthan1kg).Eight(18%)speciesarein the IUCNRedList and 19(55%)are listed asthreatenedin Brazil. Considering that these species are already severely threatened of extinction by several other factors such as
Table2–ListofnativespeciesreportedtointeractwithdomesticdogscitedinstudiescarriedoutinBrazilianprotected areas.ThecategoriesusedintheIUCNRedListofThreatenedSpeciesandintheNationalOfficialBrazilRedList(Portaria MMAn◦444,December17,2014)areindicatedinthetableaswellasthetypeofdamagecausedbydogs(P,predation;C, competition;D,diseasetransmission)accordingtoeachreference.
Species Commonname(English/Portuguese) IUCN National
officiallist Threat
Amphibians
Leptodactyluslabyrinthicus Labyrinthfrog,Pepperfoamfrog,Pepperfrog/Rã-pimenta LC LC P
Reptiles
Salvatormerianae Blackandwhitetegu/Teiú LC LC P
Birds
Hydropsalisalbicollis Pauraque/Curiango LC LC P
Mammals
DIDELPHIMORPHIA
Didelphisaurita Braziliancommonopossum/Gambá-deorelhas-pretas LC LC P
Metachirusnudicaudatus Brownfour-eyedopossum/Cuíca-de-quatro-olhos LC LC P
Philanderfrenatus Southeasternfour-eyedopossum/Cuíca LC LC P
CINGULATA
Dasypusnovemcinctus Nine-bandedarmadillo,commonlong-nosedarmadillo/Tatu-galinha LC LC P
Dasypusseptemcinctus Brazilianlesserlong-nosedarmadillo,seven-bandedarmadillo/Tatu-mirim LC LC P
Euphractussexcintus Yellowarmadillo,six-bandedarmadillo/Tatu-peba LC LC P,C
Priodontesmaximus Giantarmadillo/Tatu-canastra VU VU C
PILOSA
Tamanduatetradactyla Southerntamandua,northerntamandua,collared anteater/Tamanduá-mirim
LC LC C
Myrmecophagatridactyla Giantanteater/ Tamanduá-bandeira
VU VU C
PRIMATES
Sapajusnigritus Black-hornedcapuchin,blackcapuchin/Macaco-prego NT NT P
Alouattaguaribaguariba Southernbrownhowlermonkey/Bugio LC CR P
CARNIVORA
Chrysocyonbrachyurus Manedwolf/Lobo-guará NT VU C,D
Cerdocyonthous Crabeatingfox,commonzorro/Cachorro-do-mato LC LC C,D
Lycalopexvetutlus Andeanfox,culpeo/Raposa-do-campo LC VU C,D
Leoparduspardalis Ocelot/Jaguatirica LC LC C,D
Leopardustigrinus Littlespottedcat/Gato-do-mato-pequeno VU EN C
Pantheraonca Jaguar/Onc¸a-pintada NT VU D
Pumaconcolor Puma,mountainlion,cougar/Onc¸a-parda LC VU D
Pumayagouaroundi Eyracat,jaguarondi/Jaguarundi LC VU C
Nasuanasua SouthAmericancoati/Quati LC LC C,D
Procyoncancrivorus Crab-eatingraccoon/Mão-pelada LC LC C
Eirabarbara Tayra,greyheadedtayra/Irara LC LC C
PERISSODACTYLA
Tapirusterrestris SouthAmericanTapir/Anta VU VU P,C
ARTIODACTYLA
Mazamagouazoubira Graybrocket,brownbrocket/Veado-catingueiro LC LC P,C
Ozotocerosbezoarticus Pampasdeer/Veado-mateiro NT VU
Pecaritajacu Collaredpeccary/Caititu LC LC C
Tayassupecari White-lippedpeccary/Queixada NT VU C
LAGOMORPHA
Sylvilagusbrasiliensis Forestrabbit,tapeti/Tapiti LC LC P
RODENTIA
Dasyproctaleporina Red-rumpedagouti,Brazilianagouti/Cutia LC LC P,C
Caviaaperea Brazilianguineapig/Preá LC LC P
Cuniculuspaca Spottedpaca/Paca LC LC P
Hydrochoerushydrochaeris Capybara/Capivara LC LC P,C
Sciurusaestuans Guianansquirrel/Caxinguelê LC LC P
Sphiggurusvillosus Orange-spinedhairydwarfporcupine/Ouric¸o-caxeiro LC LC C
NT,nearlythreatened;LC,leastconcern;CR,criticallyendangered;EN,endangered;VU,vulnerable.
habitatlossand hunting theresults ofthecurrent assess-ment bringup strong reasons forconcern.Protected areas establishedinthestrictprotectioncategoryarethelastrefuge for medium and large-size mammals, particularly in the AtlanticForestandSavannabiomesinBrazil.Astheresults
oftheresearchpapersassessedshowbyconsistentrecordsof predation,competitionandpathogentransmission,the pres-ence,invasion,andimpactsofdogsintheseareasaffectthe structureofvertebratecommunitiesandcontributetolocal extinctions.
AmongthepapersreviewedonlyPaschoaletal.(2012) esti-mateddogabundanceinaprotectedareafragmentinAtlantic Forest.Camera trapsgenerated 173records of32 domestic dogsincontrastwith13recordsoftheonlynativewildcanidin thearea(Cerdocyonthous)andtwoocelot(L.pardalis)records. Thehighestfrequencyofrecordsamongcarnivoresbelongs todomesticdogs.Theywerenotrestrictedtothebordersof this protected area but were found almost two kilometers inward.Besidesrepresenting themostabundantcarnivore, thedomesticdogwasalsothefourthmostfrequentspecies registered inaBiologicalReserve inAtlantic Forest(
Srbek-AraujoandChiarello,2008).
Recordsofdog interactions inBrazil were foundwith a criticallyendangeredspecies(CR),anendangeredone(EN), and ten vulnerable (VU) species according to the national official list (Table 2). Among these species is the maned wolf,the jaguar, and the pampasdeer,classified asnearly threatened (NT) at the global level (Table 2). In the revi-sionproducedbyHughesandMacdonald(2013)twocritically threatenedspeciesarewild canidswhosepopulationswere reduced by hybridization with domestic dogs. No stud-ies regarding hybridization have been identified so far for Brazil.
Dogspreyingon smalltolarge-sizeanimalssuchasthe giantanteaterare themajorcauseofmortalityofwild ani-malsintheBrasiliaNationalPark(Lacerdaetal.,2009).Dogs aresuspectedofhavingcontributedtothedeclineofbushdog (Speothosvenaticus,cachorro-do-mato-vinagre)populationsin thepark.Thepresenceofdogsindicatednegativeassociations withspeciessuchasthemanedwolf,whichwasfoundtobe 1.53timesmorefrequentinareaswithoutdogs,showingan inverseandsignificantrelation(p<0.05)(Lacerdaetal.,2009). Inthesamestudytheauthorsproveddogstobeinfectedwith rabiesand leishmaniosis.Inavisit totheBrasilia National ParkinApril,2013wenoteddogsretainingtheirwild behav-ior,includingformationofpacks.Onevisitorgaveuphiking forfearofattackbyapackoffivedogsfoundontheway.A fewdayslaterparkrangersreported savingatapir (Tapirus
terrestris)ambushedbydogs.TheBrasiliaNationalParkhas several entry points for dogs due to its urban surround-ingswithhumancommunities,privatecondominiums,and agarbage dump.Placedin anurbansetting, thispark has becomeanenclavesodoginvasionmaybeconsidereda bor-dereffect(Lacerdaetal.,2009)asisthecaseofotherprotected areasinasimilarcontext.
Thepresenceofdogsonislandsisalsoamatterofconcern. OnIlhaGrande,inRiodeJaneirostate,where80%oftheland areaisprotectedbytheIlhaGrandeStatePark,thereis evi-denceofimpactsbydogsaswellasbydomesticcats(Lessa
andBergallo,2012)onnativeanimals(Fig.2A).Theisland’s
medium-sizemammalpopulationsarelowerindensityonthe northernsideoftheislandwherehumanpopulationdensity ishigher(Lessa, 2012). Dogsinwild conditionswith lactat-ingbitcheshavebeenregisteredonthissideoftheislandby cameratrapsmorethan3kmawayfromurbanareas,which indicatestheyhavebecomeferal(Lessa,2012;Fig.2B).Dogs were alsothe mostfrequentcarnivores registeredby cam-eratrapsintheentireregion.Residentsoftheislandconfirm predationbydogsinforestareasaswellasfrequentcontact betweendogsandnativeanimals(Lessa,2012).
Figure2–(A)Domesticdogsniffingaprey(Dasypus
novemcinctus)intheIlhaGrandeStatePark.(B)Afemale dogwithterritorialmarkingbehaviorregisteredbya cameratrapinthesamePark;thedogwas3kmawayfrom thenearestvillage.
Photos:H.G.BergalloandI.C.M.Lessa.
HikerswhovisittheIlhaGrandeStateParkandother pro-tectedareasmayfacilitatetheentryofdogs(S.Muniz,Park manager,personalcommunication).Manystraydogsassume thefunctionofguidesforvisitorsusingtrailsontheisland. Many ofthe visitors are fond ofthis behavior astheyfeel welcomed bythe dogsand enjoytheir company.Dogsalso havefuninfindingnativeanimalsandplayinghuntinggames (Fig.2A).For thisreason,interactingwithvisitorsisagreat opportunityfordogswhosebehaviorcontributesto biodiver-sitydeclineintheselastrefugesfornativeanimals.
Guidelines
for
domestic
dog
management
in
protected
areas
DogmanagementplansforBrazilianprotectedareasshould followproceduresgenerallyadoptedtoreduceinvasivealien speciesimpacts.Theinvasionstageshouldbeidentifiedas abasetodecidewhethereradicationisfeasibleorpopulation controlandimpactmitigationactionsshouldbeimplemented
(Richardson,2011).AnactionplanwasdevelopedinAustralia
fordog controlin severalplaces, notonly targetingdingos,
(AllenandFleming,2011;Letnicetal.,2012).Basedon guide-linesdefinedinthisplanandoninformationobtainedinthe present study forBraziliannationalparkswe offergeneral guidelinestobeimplementedaccordingtothescopeofdog invasionproblemsineachprotectedarea.
Althoughmanagementactionsmaybeclassifiedas con-trol,containment,anderadication(Richardson,2011),anideal sequenceforprotectedareaswouldbeto(a)assesspathways ofspeciesentry; (b) establish anearly detection and rapid responsesystemtomaximizepotentialeradication opportu-nities;(c)applycontainmentmeasureswheneradicationis nolongerfeasiblebutinvasionisrestricted;(d)carryout per-manentcontrolworkifpreventionandearlydetectionareno longerviableeitherbecause theinvasivespeciesisalready widelydistributedorbecausenewspecimenskeepentering the area andcannot bedeterred(ex. dogsliving inhomes aroundparks).Inthecaseofdogsinprotectedareas,control measuresusingintegratedmanagementtechniquestendto beurgentinordertoavoiddamagingnativespecies popula-tions.Containmentreferstolimitinginvasivespeciesspread, requiringpopulationmonitoringandblockingprotectedarea borders to avoid newentries. Eradication refers to remov-ingor eliminatinginvasivespeciesfrom acertain areaand israrelyachievedincontinentalareas,being morefeasible onoceanicislands(DatabaseofIslandInvasiveSpecies Erad-ications,2015).Allthesemeasuresmustconsidersecondary effectsonbiologicaldiversityduetoinvasivespeciescontrol
(Richardson,2011).
Protectedareasareinsertedinparticularlandscape con-textswhichrequireparticularmanagementstrategies.From theinformationgatheredinthisstudy,sometrendsindog invasionsin protected areas became clear. Protected areas inurbansurroundingssuchastheBrasiliaNationalParkare moreexposedtodogentryaswellastomoreadvancedstages ofdegradationcausedbydogs,sotheirmanagersshouldbe moreconcerned withcontrollingdog density and isolating protectedareasfromadjacenturbanization.Protectedareas inruralareassuchasChapadadosVeadeirosNationalPark mustdirectcontrolactionstoruraldwellings,focuson rais-ing awarenessand use environmental education strategies topreventdoginvasionsanddiseasetransmissiontonative animals.Protectedareasmanagersinremoteregions,where humandensityislowinthesurroundingsanddogoccurrence isscarce,mustbeattentivetodogsenteringwithhunters.In anycaseitisessential toavertdogownershipbyresidents aroundprotectedareasandpreventdogsfromaccompanying visitorsalongtrailsinsideprotectedareas.Ifnoefficient bar-rierisbuilttoisolateprotectedareasfromsurroundinghouses andtheiranimalsthelikelihoodofinvasionisveryhigh, par-ticularlywhendenselypopulatedvillagesorcitiesareclose by.For managementpurposesitisidealtoregisteralldogs andhousesinthesurroundings(datasheetandphotographs) sothat,ifadogisfoundinaprotectedarea,theownercan beaccountable.Continuousneuteringandsterilization cam-paignsmustbepromotedtoreducedogpopulationsandavoid increasednumbersofstrayandferaldogs.
Containmentanderadicationactionsmustbedefinedand carriedoutinprotectedareas.Theremovalofdogshasproved efficient on an oceanic island, where preventing new dog arrivalsis morefeasible than incontinentalareas (Morley,
2006).Captureand removalmethodsusing trapsand tran-quilizersneedtobetestedandappliedwhilenewdogarrivals must bepreventedtoensurethatcontrolandcontainment actions are efficient. If newarrivals are not prevented the removal actionswill notgenerategood results. Eradication projectsincontinentalareasdonotworkwellunlessprevious removal and control actions are undertaken. The elimina-tion ofabout 700dogs intheBrasilia NationalParkin1995
(ICMBio,2013)wasnotefficientbecausenewdogskept
enter-ingtheparkafterwards,allowingthepopulationtogrowagain
(Horowitz,2003).Eventheremovalof900dogsfromthePark
bytheSanitaryandEnvironmentalAgencyinJuly,2001,did not yield the expected results. Dogpresence is persistent, andtheirabundance,high.Dogslivinginthesurroundings, andespeciallytheapproximately3000dogslivingfreelyina garbagedumpadjacenttothepark,entertheparkalongat least 40%ofits perimeter(ICMBio,2013), creatingconstant invasionevents.Evenowneddogsentertheparkfrom resi-dentialcondominiumsinthesurroundings(ICMBio,2013).
Thelackofpublicawarenessincontrollingand contain-ingpetreproductionaggravatestheproblemofdogimpacts onnativeanimals(LessaandBergallo,2012).Protectedarea effectivenessalsodependsheavilyonmanagementandonthe attentiongiventosocio-economicissuesaffectingeacharea
(Drummondetal.,2009).Itisnotnormallyfeasiblethatallthe
peopleinvolvedinactivitieswithprotectedareasareaware ofitsproblemsimpactingbiodiversityandmanagement effi-ciency.Still,dogmanagementisalsoneededtoensuresafety forhumanhealth,asithelpscontrolleishmaniosis,rabies, and distemper(Courtenayet al.,2002;Curietal.,2006).For thisreason,aswellasalltheconsequencesofdisease trans-mission and severe negative impacts on biodiversity, it is crucialthatenvironmentaleducationprogramsandpet ster-ilizationandvaccinationcampaignsareconceived,planned, andimplementedinhumansettlementsinthesurroundings ofprotectedareas(Jorgeetal.,2010;Curietal.,2014).
Thesuccessofdogcontrolplansinprotectedareaspartly depends on raising public awareness. Because dogs (Canis
lupusfamiliaris) are apetspecies highlyvaluedby humans thereismuchconflictofopinionwhichaffectsthesuccess ofcontrol and eradicationprograms. Promoting dialogand partnershipsbetweendifferentstakeholderssuchasresidents fromthesurroundings,parkmanagers,politicians,and repre-sentativesofanimalprotectionorganizationsisessentialfor societytounderstandtherelevanceofdogmanagementplans andgainmoresupportforprotectedareamanagers. Popula-tioncontrolbydogsterilizationandremovalisalsobeneficial fordogwell-beingasitreducestheirchancesofgettinghurt infightswithotheranimalsandtransmittingdiseases.
Conclusion
Dogsconstitute aclearanthropogenicallyderivedthreatto indigenousspecies.Thepresenceofdogsinareaswithwildlife increasestheriskofdiseasefordogs,humans andwildlife; moreover,thepresenceofdomesticdogsalsointerfereswith the spatial distribution of populations of wildlife species. Studiesundertakeninseveralpartsoftheworldidentify pre-dationasthemostfrequentresultofinteractionbetweendogs
andwildlife,followedbypathogentransmission.Thespecies identifiedasenduring theworstimpactsfrom dog interac-tionsinBrazilarethosealreadyseverelyimpactedbyhunting and habitat loss or fragmentation, especiallymedium and largemammals.Withinthisgroup,carnivoresaremore threat-enedbydogsduetocompetitionanddiseasetransmission, whichincreasetheriskoflocalextinctions.Thepresenceof dogsisacommonprobleminnearlyallnationalparks(>90%) andvery likelyinmany otherprotectedareas inall Brazil-ianbiomes,regardlessofthedensityofhumanpopulations. SimilarrecordswereobtainedforremoteareasintheAmazon regionandfordenselypopulatedareasinAtlanticForest.Dogs inflictnegativeimpactstoatleast63nativeanimalspecies, including12speciesthreatenedofextinction.
Thepresenceofdogsinprotectedareasisassociatedto otherimportantimpactfactorssuchashuntingandfailure atlandcompensationwhenprotectedareasareestablished. Solvingsuchproblemswillcontributetoreducingimpactsby dogs inthese areas.Evaluating dog abundanceand move-mentpatternsinprotectedareasisimportanttoassessdog impactsonbiodiversityatthelocalscale.Studiestoestimate dogabundanceandoccurrenceinprotectedareasareurgently neededandshouldberequestedbyprotectedareamanagers tohelpdefineimmediateprevention,eradication,andcontrol strategies.
Althoughscientificinformationontheimpactsbydogsin protectedareasisscarceandprecisediagnosticsaredifficult todevelop,itisimportanttodefineandimplementgeneral
control actions.These willbe moreeffective ifestablished consideringthetypesofdogspresentandtheleveland inten-sityoftheirinteractionswithnativeanimals.Containment, andparticularlyeradicationactionsincontinentalareas,must be carried out onlyafter dog removal. Once strategiesare defined according to the peculiarities ofeach area, imple-mentationshouldnotbedelayedtomaximize thechances ofreducingbiodiversityloss.
Conflicts
of
interest
Theauthorsdeclarenoconflictsofinterest.
Acknowledgements
Wethankallthenationalparkmanagerswhocontributedto thisassessment.ICMLthanksCAPES(forthedoctoral schol-arship financing this study aswell as the Biodiversity and ProtectedAreaLaboratoryoftheEcologyDepartmentatthe FederalUniversityofBrasiliaandtheMammalEcology Labora-toryattheRiodeJaneiroStateUniversity(UERJ).Wealsothank IUCNandICMBio(InstitutoChicoMendesdeConservac¸ãoda Biodiversidade)forthe onlineavailabilityofdataon threat-enedspecies.Thisstudy hasbeen renderedlegalstatusby SISBIOpermitn◦39768-1.
Annex
I.
Detail
of
selected
articles
Article(citation) Place Protectedarea Speciesortarget group
Impactcausedby domesticdog
AlexanderandAppel
(1994)
Africa–Kenya MasaiMaraNational Reserve
Lycaonpictus Pathogentransmission
Alexanderetal.
(2010)
Africa–Botswana ChobeNationalPark Lycaonpictus Pathogentransmission
Atickemetal.,2010 Africa–Ethiopia BaleMountains
NationalPark
Canissimensis Pathogentransmission
Bergeronand Demers(1981) NorthAmerica– Canada ForillanNational Park
Canislatran Competitionand predation
Britoetal.(2004) SouthAmerica–
Brazil
Poc¸odasAntas BiologicalReserve
Mammalcommunity Competitionand predation
ButlerandToit(2002) Africa–Zimbabwe SengwaWildlife
ResearchArea
Vertebrate community
Predation
Butleretal.,2004 Africa–Zimbabwe SengwaWildlife
ResearchArea Carnivore community Competitionand pathogentransmission Silva-Rodriguezetal. (2010) SouthAmerica– Chile AlerceCostero NationalPark
Vulpesvulpes Competition
Curietal.(2006) SouthAmerica–
Brazil SerradoCipó NationalPark Carnivore community Pathogentransmission
Fiorelloetal.(2004) SouthAmerica–
Bolivia Kaa-lyaNational Park Carnivore community Pathogentransmission
Godwinetal.(2013) North
America–Canada
PrinceEdwardPoint NationalWildlife Area
Odocoileusvirginianus Predation
Jhala(1993) Asia-India VelavadarNational
Park
Article(citation) Place Protectedarea Speciesortarget group
Impactcausedby domesticdog
Kamleretal.(2003) NorthAmerica–USA Fort-RileyMilitary
Reserve
Canislatran Competition
Lacerdaetal.(2009) SouthAmerica–
Brazil
BrasiliaNationalPark Mammalcommunity Competition
ManorandSaltz
(2004)
Asia–Israel HermonNational Park
Gazelle Predation
Meek(1999) Oceania–Australia YuraygirNational
Park
Vertebrate community
Competition
Oliveiraetal.(2008) SouthAmerica–
Brazil
SerradoBrigadeiro StatePark
Sapajusnigritus Predation
Paschoaletal.(2012) SouthAmerica–
Brazil FelicianoMiguel AbdalaReserve Vertebrate community Competition Srbek-Araujoand Chiarello(2008) SouthAmerica– Brazil SantaLúcia BiologicalReserve
Mammalcommunity Competition
Taborsky(1988) Oceania–New
Zealand
WaitangiStateForest Apteryxaustralis Predation
Whitemanetal. (2007) SouthAmerica– Brazil TucuruiLake ProtectedAreas Carnivore community Pathogentransmission
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