-1 Exotic vertebrate fauna in the remote and pristine sub-Antarctic Cape Horn Archipelago, Chile CHRISTOPHER B. ANDERSON1,2,*, RICARDO ROZZI2,3,4, JUAN C. TORRES-MURA2,5, STEVEN M. MCGEHEE2, MARGARET F. SHERRIFFS2,6, ELKE SCHU¨ TTLER2,7,8 and AMY D. ROSEMOND1 1InstituteofEcology,UniversityofGeorgia,Athens,GA30602,USA;2ParqueEtnobota´nicoOmora, Puerto Williams, Magallanes, Chile; 3Universidad de Magallanes, Casilla 113-D, Punta Arenas, Magallanes,Chile;4DepartmentofPhilosophyandReligionStudies,UniversityofNorthTexas,P.O. Box310980,Denton,TX76203,USA;5MuseoNacionaldeHistoriaNatural,Seccio´ndeZoologı´a, QuintaNormal,SantiagodeChile;6CenterforPopulationBiology,SectionofEvolutionandEcology, University of California, One Shields Avenue, Davis, CA 95616, USA; 7UFZ-Center for Environ- mental Research UFZ, Permoserstrasse 15, 04318 Leipzig, Germany; 8Department of Ecology, TechnicalUniversityMunique-Weihenstephan,AmHochanger6,85350Freising,Germany;*Author for correspondence (e-mail: [email protected]; phone: +1-706-542-4366; fax: +1-706- 542-4819) Key words: Cape Horn, Chile, Exotic species, Global change, Invasive, Sub-Antarctic Forests, TierradelFuego,Wilderness Abstract. Pristine wilderness is a scarce global resource, but exotic species are so common that theyconstituteaprincipalcomponentofworldwideecologicalchange.Therelationshipbetween thesetwotopics,invasionandremoteness,wastheimpetusbehindfiveyearsoffieldworkaimed at identifying the assemblage and range of exotic vertebrates in Cape Horn, Chile, identified as one of the world’s most pristine wilderness areas. While the archipelago has extremely low human population density and vast tracts of undisturbed land, we discovered that several ter- restrial vertebrate groups were dominated by exotic species. Native birds were diverse (approx. 154 spp), and only 1.3% (or two spp.) were introduced. In contrast, exotic terrestrial mammals (12 spp.) and freshwater fish (three spp.) outnumbered their native counterparts, constituting 55%and75%oftheassemblages.UsingGIS,wefoundthatnotallareaswereimpactedequally, largely due to intensity of human occupation. Human settled islands (Navarino and Tierra del Fuego) hosted the greatest number of exotics, but humans alone did not explain observed pat- terns. Remoteislandsalso hadintroduced species.NorthAmericanbeavers(Castorcanadensis), Americanminks (Mustela vison) and feral domesticdogs and cats were particularlywidespread, and their range in isolated parts of the study arearaised important ecological and management questions. In conclusion, the Cape Horn Archipelago retained areas free of exotic vertebrates, particularly parts of the Cape Horn and Alberto D’Agostini National Parks, but at many sites introduced species were overwhelming native biota and altering these previously remote natural ecosystems. Abbreviations: TDF–TierradelFuego Introduction Theimpactanddistributionofexoticspeciesistodayamajorareaofscientific interest and conservation concern (Courchamp et al. 2003). Together with habitat fragmentation and global warming, species introductions constitute a principalcauseofcurrentglobalecologicalchange(Vitouseket al.1996).Asa country, Chile hosts proportionally few exotic vertebrates. Introduced species represent only 3.9% of the Chilean vertebrate assemblage (Jaksic 1998). However,withinthePatagonianecoregionofsouthernSouthAmerica,exotics constitute a higher proportion of vertebrate fauna. For example, in the Argentine portion of Tierra del Fuego 67% of mammal species were found to be exotic (Lizarralde and Escobar 2000), and a study of freshwater fish in the ChileanportionofTierradelFuegoIslanddescribedtwoexoticsandonlyone native species (Vila et al. 1999). The political unit of Cape Horn County is the world’s southernmost for- ested ecosystem and encompasses all of the islands south of the Beagle Channel, in addition to the Chilean portion of Tierra del Fuego Island located south of the highest peaks in the Darwin Mountain Range (Figure 1). The area belongs biogeographically to the Magellanic Biome (Pisano 1981), Figure1. Map of southern South America with inset of the area that includes the Southern Patagonian and Sub-Antarctic Ecoregions. South of the dashed line lies the biogeographic and administrativeterritoryofCapeHornCounty,Chile. and more specifically to the Magellanic Sub-Antarctic Forest Ecoregion (Rozzi 2002). It recently has been classified as one of the world’s most pristine remaining wilderness areas due to its extensive size, the intact nature of its native vegetation and its low human population density (Mittermeier et al. 2002). Mittermeier et al. (2002) also point out that the Magellanic Sub-Antarctic Forests have a very high percentage of protected area (75% in Cape Horn County and 51% for the whole region), compared to the world’s other remaining wilderness areas, and consequently merit special recognition. Based on these criteria, this region is apparently remote from direct human influence,butinfacttheYahgansfirstsettledtheecosystemsofsouthernChile 7500 yearsago(OcampoandRivas2000).Europeanexplorationsbeganinthe 1500s,andcolonizationcommencedinearnestinthelate1800s,provokingthe first major landscape changes and introductions of exotic vertebrate fauna, principally associated with livestock grazing (Martinic 1973). The first record of a deliberate introduction of vertebrates to the islands south of the Beagle Channel was in 1867, when goats were brought to Lewaia Bay on Navarino Island by Anglican missionaries (Martinic 1973). During the 20th century the number of introductions increased and expanded from domestic animals, including invasive species that expanded throughout the archipelago and others that did not become established at all. The realization that non-native biota can reach even the most remote areas left on the planet poses a conser- vation challenge for southern Chile, particularly given that a large portion is also classified by the Chilean environmental commission (CONAMA) as a priority area for national biodiversity conservation (Rozzi and Massardo 2002). Despite the area’s importance, detailed and precise information about exotic species in this area is currently lacking. Effective management of the extant national parks (Cape Horn and Alberto D’Agostini) and the newly designated UNESCO Cape Horn Biosphere Reserve requires up-to-date knowledge of the assemblage and distribution of exotics, as well as their associated impacts. In order to achieve this goal, this paper (1) synthesizes existing information of native and non-native vertebrate fauna in the Cape Horn Archipelago, (2) uses 5 years of monitoring and survey information to describe in greater detail the exotic vertebrate assemblage and distribution patterns and (3) analyzes three taxa identified as particularly harmful or widespread: the North American beaver (Castor canadensis), the American mink (Mustela vison) and feral domestic predators (dogs and cats). These species further are used to highlight the implications of invasion, demon- strating the effect of ecological barriers, the potential rapidity of establish- ment and the possibility for changing positive ecosystem feedback loops to negative. While providing relevant information for local managers, our information also serves to better comprehend the global context of species invasion dynamics. Materials and methods Study area Cape Horn County is located within the administrative district known as the Chilean Antarctic Province, which in turn is itself part of the Magallanes and ChileanAntarcticRegion(Figure 1).Thestudyareaconsistsofanarchipelago with hundreds of islands that cover approximately 15,488 km2. The political boundaries also correspond largely to biogeographic barriers created by the icecap found towards the north in the Darwin Mountain Range on Tierra del Fuego Island and the sea barriers on all other sides. The area is part of the Magellanic Sub-Antarctic Forest Biome (for a detailed site description see Rozzi et al. 2004a). Data collection and analysis Thedatapresentedherewerecollectedbytheauthorsover5 yearsoffieldwork associated with the Omora Ethnobotanical Park’s long-term ecological re- search efforts in the sub-Antarctic ecoregion. A total of 40 sites on 19 islands were surveyed over the course of 5 years (Appendix 1). Sampling included systematic and opportunistic mistnetting, point-count transects and checklists forbirds,whichwereconductedinalpine,shrub,pastureandforestedhabitats betweenJanuary2000andJanuary2005.Aviansamplinghasbeencarriedout systematically six days per month on Navarino Island since 2000. In addition during January and April 2002; April 2003; January and May 2004; January and May 2005 bird surveys were conducted during boating expeditions throughout the archipelago. Data concerning fish presence and absence were based on at least one day of rod-and-reel fishing per surveyed water body on Navarino, Hoste and Tierra del Fuego Islands, as well as opportunistic observational evidence and interviews with fishermen. Sherman traps for small mammals were deployed on Navarino Island in quarter hectare grids in shrub, rush wetlands, cushion bog, pasture and ever- green, deciduous and mixed forest habitats. In addition, traps were placed around human settlements. Traps were baited with oats and checked twice daily. In January and May 2004 and January and May 2005 expeditions were conducted by boat through the archipelago in order to access remote and difficult portions of the county, and qualitative Sherman trap sampling for small rodents was conducted from one to two nights per site on Hoste, Her- schel and Horn Islands. Live traps (20·20·70 cm) were used in April and May 2005 at Pia Sound, Olla Cove and Yendegaia Bay (Tierra del Fuego Island) and on Navarino Islandtosampleformink.Atotaleffortof420trapnightswascarriedouton Navarino Island and twenty-five trap nights for TDF. Visual surveys were conducted at each site for a distance of 0.5–2 km of stream or coastline and dividedinto200 msectionsthatwereclassifiedaspositiveornegativedetection ofminkevidence.Detectionsurveysweremadeoftheplaceswheretrackswere likelytobefound,suchassandyormuddyground,andscatsweresearchedfor on exposed marking places, such as rocks and fallen trees for territorial scent marking (Dunstone 1993). Ateachstopduringexpeditions,visualtransectsandsurveyswerealsoused to detect evidence (spoor, rooting, disturbance and tracks) of larger exotic species, such as beavers, muskrats and feral domestic animals, throughout the archipelago during stays of 1–3 days. Locations where observationaltransects were conducted during expeditions included: London Island; Romanche Bay (Gordon Island); Ventisquero Sound, Pı´a Sound, Olla Cove and Yendegaia Bay (TDF); Islotes Holger; Parque Omora, Inu´til Bay, Wulaia Bay and Douglas Bay (Navarino); Jemmy Button Island; Orange Bay and Ponsonby Sound (Hoste Island); Mascart Island; Kendall Cove (Wollaston Island); Puerto Dillon (Grevy Island); Victoria and Washington Channels (Bayly Is- land);PuertoMaxwellandSaintMartinCove(HermiteIsland);MartialCove (Herschel Island); and Cape Horn Island (for details see Appendix 1). All survey and observational information was geo-referenced in order to utilize GIS to produce distribution maps. Maps were then used to identify areasfreeofexoticsandalsorecognizethespeciesthatwereparticularlywide- spreadandindependentofhuman-association.Inaddition,collectedfielddata were supplemented with a bibliographic review and questionnaires of local residents, sailors, fishermen and scientists. Non-native species under domestic oranimalhusbandrypractices,suchassheeporchickens,werenotconsidered in the analysis because they are kept exclusively in enclosures. On the other hand,pigs,cows,dogs,catsandhorseswereexaminedbecausemanyalsohave become feral or are free ranging. Results Human inhabited islands–Navarino and Tierra del Fuego We identified atotal of17exoticvertebrate species,including mammals,birds andfreshwaterfish,inhabitingCape HornCounty,Chile(Table 1).Nonative orintroducedamphibiansorreptileswerediscoveredinthestudyarea.The12 recorded exotic mammal species represented a majority (55%) of the total mammalian assemblage (22 total spp.) (Table 2). Rodents and carnivores contributed the most introduced species with four non-native species each. Two typically associated human rodents, Rattus norvegicus and Mus mus- culus, were found only in Puerto Williams on Navarino Island. Likewise, the only wild exotic birds detected in the whole stud area were the rock dove (Columba livia) and the house sparrow (Passer domesticus), which were con- fined to Puerto Williams. The pigeon (C. livia) was introduced deliberately by residents of Puerto Williams during the past decade, while P. domesticus Table1. Summary of introduced vertebratefauna recordedfor CapeHorn County, Chile with theirmodeofarrivalandsourceofinformation. IntroducedVertebrateSpeciesofCapeHornCounty,Chile Order Scientificname Commonname Source(s) MAMMALS Artiodactyla Susscrofa Feralpig 1 Bostarus Feralcow 1 Carnivora Canislupusfamiliaris Feraldog 1,2 Felisdomesticus Feralcat 1 Mustelavison Americanmink 1,3 Pseudalopexgriseus Patagoniangreyfox 1 Lagomorpha Oryctolaguscuniculus Europeanrabbit 1 Perissodactyla Equuscaballus Feralhorse 1 Rodentia Castorcanadensis NorthAmericanbeaver 1,4,5 Ondatrazibethica Muskrat 1,5 Musmusculus Housemouse 1 Rattusnorvegicus Norwayrat 1 FRESHWATERFISH Salmoniformes Salmotrutta Browntrout 1 Oncorhynchusmykiss Rainbowtrout 1 Salvelinusfontinalis Brooktrout 1* BIRDS Paseriformes Passerdomesticus Housesparrow 1 Columbiformes Columbalivia Rockpigeon 1 1.Omoradatabase,2.Canclini(1999),3.RozziandSherriffs(2003),4.SielfeldandVenegas(1980), 5.Sielfeld(1977).*indicatesreliablefishermanreport. probablycrossedfromtheArgentineportionofTierradelFuego(TDF).These two exotic avifauna made up only 1.3% of the approximately 154 native bird speciesthatinhabitterrestrialandcoastalareasofthearchipelago(Couveand Vidal 2000). The introduced grey fox (Pseudalopex griseus), which is native to the continental mainland of South America, was only found in the study area at Yendegaia Bay on TDF. Among freshwater fishes, we identified three exotic species, which repre- sented 75% of the archipelago’s total assemblage. Only one native species (Galaxias maculatus) was confirmed within the county, while three more were describedfortheadjacentareaofArgentinabyCussacet al.(2004).Theexotic freshwater fish fauna in the study area were all Northern Hemisphere trout (Salmoniformes), including brown (Salmo trutta), rainbow (Oncorhynchus mykiss) and reliable fishermen accounts of brook (Salvelinus fontinalis) (Table 3). No exotic fish were found in the western portion of the county on Hoste or Tierra del Fuego Islands.The only water bodies found to have trout were on Navarino Island and included: (1) Windhond watershed (brown and rainbow), (2) Robalo River below the dam (rainbow), (3) Navarino Lake (brook),(4)MejillonesRiver(rainbow),(5)Farao´nesRiver(rainbow),(6)Lum River(rainbow),(7)PilushejanRiver(rainbow)and(8)DouglasRiver(brown). a v Site Navarino,Hoste1&GordonTDF&NavarinoTDF,Navarino,1Hoste&Horn Navarino&1Horn Navarino,Hoste1&ArgentineTDF1Yendegaia,TDFYendegaia,TDF1&Navarino1TDF&Navarino TDF,Navarino,Hoste,Picton,Nue1&Lennox e Commonname Feralpig FeralcowFeraldog Feralcat AmericanminkGreyfoxEuropeanrabbitFeralhors NorthAmericanbeaver aris usulus Exoticspecies Scientificname Susscrofa BostarusCanislupusfamili Felisdomesticus Mustelavison PseudalopexgriseOryctolaguscunic Equuscaballus Castorcanadensis e. Site 1TDF&Navarino TDF,Grevy,Picton,Lennox,Wollaston,5Hermite,Grevy&10GordonTDF,Hoste,Grevy,1Picton,Wollaston,Bayly,5Hermite,Herschel,10Grevy&Gordon5TDF&Hoste 5,7TDF,Navarino&5Wollston5,7TDF,Navarino&5GrevyTDF,Navarino1&3,9Hoste hil C y, nt u ofCapeHornCo Commonname Guanaco Largeriverotter Seaotter Fuegianredfox Earedbat ´Chiloebat Yellow-nosedmouse als eus s m a u andexoticmam Nativespecies Scientificname Lamaguanicoe Lontraprovocax Lontrafelina Pseudalopexculplycoides Histiotusmontan Myotischiloensis Abrothrixxanthorhinus 2.Native malsorder dactyla vora morpha odactylaptera ntia Table Mam Artio Carni Lago PerissChiro Rode 1rino 1rino 4.Milne984),11. Site TDF,Navarino,Hoste,Picton,1Nueva&LennoxPuertoWilliams,Nava PuertoWilliams,Nava 905),3.Cabrera(1961),eld(1977),10.Sielfeld(1 (1elf nSi me e Alle9. Commonna Muskrat Housemous Norwayrat database,2.enegas(1987), aV Exoticspecies Scientificname Ondatrazibethica Musmusculus Rattusnorvegicus 12 hipelago.1.Omor972),8.Reiseand c1 Site Herschel,Hermite&1,6HornTDF,Wollaston,Hermite&1Hoste8TDF,1Wollaston,3,11Hermite&4Hoste andsinthear´aandBarrıa( oislPen˜ Commonname CapeHornmouse Fuegianchinchillamouse Long-tailedmouse othernamesrefertsonetal.(1984),7. r ee thatt e dP d. Nativespecies Scientificnam Akodonhershkovitzi Euneomyschinchilloides Oligoryzomyslongicaudatus 10 radelFuegoanOlrog(1950),6. Table2.Continue Mammalsorder Total TDFindicatesTierEdwards(1881),5.Thomas(1916). Site(s) Pilushejan,Mejillones,Windhondand1DouglasRiversLum,Guanaco,Mejillones,and1´RobaloRiversNavarinoLake nlycitedforareasNavarinoIsland. on Commonname Browntrout Rainbowtrout Brooktrout *indicatesspeciessitesarelocatedo ExoticSpecies Scientificname Salmotrutta Oncorhynchusmykiss Salvelinusfontinalis3 3=Vilaetal.(1999),ennototherwisenoted, HornCountyChile. Site(s) 1NavarinoI.,Hardy23Peninsula(HosteI.)&TDF´Roca,Escondido,Fagnano,Yehuın&MargaritaLakes(ArgentineTDF)ArgentinecoastofBeagleChannelonTDFAreanearFagnanoLake(ArgentineTDF) =Omoradatabase,2=Jenyns(1842),erradelFuego(Cussacetal.2004).Wh Cape ame alaxia ea:1nofTi xoticfreshwaterfishfaunafoundin NativeSpecies ScientificnameCommonn GalaxiasmaculatusCommong Galaxiasplatei* Aplochitontaeniatus* Aplochitonzebra* 1(3*) nativefishconfirmedforthestudyarCounty,ChileintheArgentineportio ande Order eonlyHorn Table3.Native FreshwaterFish Osmeriformes Salmoniformes Total G.maculatusisthadjacenttoCape In addition, several bog lakes along the north coast of the island, which are unconnected to adjacent water courses, contained brown and rainbow trout. Feral animals WhileferaldomesticanimalsweremostabundantonNavarinoandTierradel Fuego, they were not strictly confined to those human-inhabited islands. We discovered, for example, scat and rooting disturbance from Sus scrofa at Ro- manche Bay on uninhabited Gordon Island in the western portion of the county and on Hoste Island. Pet dogs and cats likewise are being kept at isolated military outposts and ranches throughout the archipelago, such as Hoste, Horn, Lennox, Picton and Wollaston Islands. A similar native terres- trialpredator(theFuegianredfox,Pseudalopexculpaeus)onlyinhabitedHoste and Tierra del Fuego Islands. On Navarino Island, dogs were found in all types of habitats, ranging from sea-level to above tree line. Cats, likewise, were observed even in remote for- ests.OnseveraloccasionstheywereseenpreyinguponsongbirdsintheOmora Ethnobotanical Park, Puerto Inu´til and the small Holger Islands off the northwest coast of Navarino Island. Sus scrofa, the feral hog, was detected mostly around the northern and western coastlines of Navarino Island, espe- cially in coastal, shrub and mixed forest habitats. Human-inhabited Navarino andTierradelFuegoIslandswerealsotheonlylocationswheretheEuropean rabbit (Oryctolagus cuniculus) was seen. At Yendegaia Bay, they were com- monlyfoundalongriverandcoastalshorelines.Rabbitswereoncecommonon Navarino Island, as well, but they were virtually eliminated with the viral control program conducted in the 1950s. In 2004, however, we observed rab- bitsonseveraloccasionsonthenorthwesterntipoftheisland,andtheymaybe a new introduction from an adjacent ranch. Mink, beaver and muskrat Based on surveys and mapping, we determined that three of the most wide- spreadorpotentiallyharmfulexoticvertebratespeciesfoundinthearchipelago were the North American beaver (Castor canadensis), the American mink (Mustela vison) and the muskrat (Ondatra zibethica). All three were brought from North America by the Argentine government in the 1940s and 1950s as part of an effort to introduce economically valuable furbearers. Once survey information was geo-referenced and mapped, it was also realized that these species had some the widest distributions of any exotic species in the archi- pelago and were the least associated with human settlements. We first confirmed the presence of mink in Cape Horn County in 2001 on NavarinoIsland(RozziandSherriffs2003).Duringtransectsconductedinthe austral summer of 2004 and 2005, we sighted mink or their tracks along the