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Insular Arctic Ground Squirrels (Spermophilus Parryii) of the North Pacific: Indigenous Or Exotic?

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Insular Arctic Ground Squirrels (Spermophilus Parryii) of the North Pacific: Indigenous Or Exotic? Journal of Mammalogy, 91(6):1401–1412, 2010 Insular arctic ground squirrels (Spermophilus parryii) of the North Pacific: indigenous or exotic? JOSEPH A. COOK,* AREN A. EDDINGSAAS,JANET L. LOXTERMAN,STEVE EBBERT, AND S. O. MACDONALD Museum of Southwestern Biology and Department of Biology, University of New Mexico, Albuquerque, NM 87131, USA (JAC, SOM) Department of Biological Sciences, Idaho State University, Pocatello, ID 83209, USA (AAE, JLL) Alaska Maritime National Wildlife Refuge, Homer, AK 99603, USA (SE) * Correspondent: [email protected] We lack critical information for oceanic archipelagos worldwide related to the origin and status of insular faunas. In southwestern Alaska, in particular, a need exists to tease apart whether specific insular populations are naturally occurring or are the result of exotic introductions by humans. We analyzed variation in mitochondrial sequences of the cytochrome-b gene and 8 nuclear microsatellite loci across 215 individuals representing 17 populations (12 insular) to refine our understanding of the history of the previously identified Southwest clade of arctic ground squirrels (Spermophilus parryii). We found significant geographic structure that suggests long-term isolation and diversification (Ushugat Island and Cold Bay), but we also documented closely related populations that are likely the result of human-mediated introductions. The latter instances (Kavalga and Unalaska islands) corroborate reports from early Alaska explorers. DOI: 10.1644/09-MAMM-A- 386.1. Key words: Alaska, Beringia, endemic, exotic, glacial refugia, island, microsatellite DNA, mitochondrial DNA E 2010 American Society of Mammalogists Introductions of exotic mammals have been a primary of the Last Glacial Maximum (LGM). Smaller ice-age refugia driver of extinctions worldwide, with an impact that is in this coastal region also have been proposed, possibly on especially acute when exotics enter island ecosystems and Kodiak Island or on the outer continental shelf that was encounter insular endemics (Quammen 1996; Whittaker and exposed by dramatically lowered sea levels (.100 m) during Ferna´ndez-Palacios 2007). Predation by exotics, for example, glacial advances (Karlstrom 1964). has been advanced as the key factor in depletion or extinction After the arrival of Europeans to the region in the 18th of insular, tropical seabirds of the Pacific (Steadman 2006). century, mammals such as Sitka black-tailed deer (Odocoileus Heavy declines of nesting seabirds on several islands of hemionus sitkensis), wapiti (Cervus canadensis), red fox southwestern Alaska (Aleutian Chain and islands south of the (Vulpes vulpes), brown rat (Rattus norvegicus), and others Alaska Peninsula) provided 1 of the earliest published were introduced by humans to islands or nearby mainland sites examples of environmental impacts on insular systems due (Bailey 1993; MacDonald and Cook 2009). The location and to introduction of exotic mammals (Dall 1870; Murie 1959; chronology of many island introductions, however, remains Turner 1886), but relatively few assessments of the impact of obscure. Arctic foxes (Vulpes lagopus) and red foxes were exotic species on high-latitude archipelagos have been moved to more than 450 islands in Alaska by fur ranchers completed (Anderson et al. 2006; Silva and Saavedra 2008). (Bailey 1993). In addition to these furbearers, fox ranchers Prior to the exploratory voyage of Vitus Bering in 1741, the ‘‘filled barrels’’ with arctic ground squirrels (Spermophilus central and western Aleutians largely were devoid of parryii) and other small rodents (e.g., root voles [Microtus terrestrial mammals (Hopkins 1967; Murie 1959), but islands oeconomus]) and released them on numerous islands (Peterson in the eastern Aleutians and south of the Alaska Peninsula 1967:123) to supplement existing prey for these fox ranches, supported a limited mammalian fauna (MacDonald and Cook especially as insular bird populations declined (Bailey 1993; 2009). These eastern islands are nearer mainland source populations and could have been colonized naturally by species dispersing from the central Beringian refugium (Waltari et al. 2007) across land and ice bridges at the close www.mammalogy.org 1401 1402 JOURNAL OF MAMMALOGY Vol. 91, No. 6 Black 1984). In the case of ground squirrels, introductions conservation efforts, but recently introduced populations might have been initiated by the indigenous Alutiiq and Aleut might be considered harmful exotics that should be removed people of the region, who highly valued them for garment to protect nesting bird populations and other aspects of North making (Black 2001; Clark 2005). Pacific insular ecosystems. Murie (1959) visited a number of islands in southwestern Alaska in 1936 and 1937 and recognized the negative impact of alien predators on insular bird populations. His subsequent MATERIALS AND METHODS reports to the United States Fish and Wildlife Service Sampling.—Island populations included in this analysis instigated efforts to eradicate exotics and establish programs extend from the Kodiak Archipelago westward along the aimed at conserving the native insular faunas (Ebbert and southern edge of the Alaska Peninsula and into the Aleutian Byrd 2002). Many of the islands initially studied by Murie Archipelago to Kavalga Island (Fig. 1). Through fieldwork later became incorporated into the Alaska Maritime National beginning in 1991 and continuing through 2003, we collected Wildlife Refuge (Ebbert and Byrd 2002). Due to declining tissue samples from ground squirrels representing 12 (32%)of populations of a number of native species, maintaining or the 37 southwestern islands believed to harbor extant restoring insular faunas is becoming a major conservation populations (Table 1). We followed guidelines approved by issue in Alaska’s archipelagos (Cook et al. 2006). Similar to the American Society of Mammalogists (Gannon et al. 2007). other archipelagos worldwide (Whittaker and Ferna´ndez- Specimens are archived in the University of Alaska Museum Palacios 2007), critical information on the origin and status of the North in Fairbanks or Museum of Southwestern Biology of these northern insular faunas is lacking (MacDonald and in Albuquerque, New Mexico. We selected 5 individuals from Cook 2007). In southwestern Alaska, in particular, a need each population for mitochondrial DNA (mtDNA) sequence exists to tease apart whether specific insular populations are analyses (total n 5 75; Appendix I) and 2–41 individuals (total naturally occurring or the result of introductions by humans. n 5 215) for nuclear (microsatellite) analyses (Appendix I). A preliminary investigation of mitochondrial sequence To test whether island populations were closely related to each variation (Eddingsaas et al. 2004) provided a broad view of other, to particular mainland populations (indicating a possible phylogeographic structure in ground squirrels throughout history of translocation), or were more distantly related Alaska and the adjoining Yukon Territory. That effort (indicating possible refugial isolation), we used analyses of suggested that southwestern Alaska populations were strongly geographic variation in mitochondrial sequences and 8 nuclear differentiated from all other ground squirrels. Within south- microsatellite loci. In general, microsatellite loci are expected western Alaska, populations on some islands are highly to be more variable than the mitochondrial cytochrome-b distinctive, suggesting that they may be insular paleoendemics (Cytb) gene in mammals and should provide finer resolution (i.e., older relictual lineages that persisted in situ since before of patterns of within- and among-population variation (Hillis the LGM). Work by Eddingsaas et al. (2004) was based on et al. 1996). relatively few specimens (n 5 20) representing southwestern Molecular methods.—We used a salt extraction method populations of ground squirrels and a single mitochondrial (Miller et al. 1988) modified by Fleming and Cook (2002) to marker. Those limitations, combined with questions surround- extract DNA from tissue (heart, liver, spleen, or muscle). The ing possible human introduction of ground squirrels onto entire Cytb gene of the mitochondria was amplified in 2 islands throughout the region, necessitate a finer-scale sections by polymerase chain reaction using primer pairs MVZ examination of insular populations based on multiple, 05 (Smith and Patton 1993)–SPERMO 06 (Eddingsaas et al. independent markers. 2004) or MVZ 14 (Smith and Patton 1993)–SPERMO 07 We tested whether the preliminary mitochondrial patterns (Eddingsaas et al. 2004). Amplification protocols are detailed uncovered by Eddingsaas et al. (2004) reflected the evolu- in Eddingsaas et al. (2004). tionary history of these populations by investigating variation Eight nuclear microsatellite loci (GS3, GS12, GS14, GS17, in a suite of nuclear loci. In addition to our primary goal of GS20, GS22, GS25, and GS26) were assayed using primers exploring the influence of LGM refugia on genetic relation- developed for the Columbian ground squirrel (Spermophilus ships among ground squirrel populations across southwestern columbianus—Stevens et al. 1997). Polymerase chain reaction Alaska, we used biogeographic analyses to identify distinctive amplification was carried out in 20-ml volumes containing clusters of island populations. We then looked at individual 50 mg of genomic DNA, 0.3 mM of deoxynucleoside islands to begin the process of discriminating introduced arctic triphosphates,
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