(Puma Concolor) to Migration of Their Primary Prey in Patagonia

RESEARCH ARTICLE Response of pumas (Puma concolor) to migration of their primary prey in Patagonia Maria L. Gelin1, Lyn C. Branch1*, Daniel H. Thornton2, AndreÂs J. Novaro3, Matthew J. Gould4, Anthony Caragiulo5 1 Department of Wildlife Ecology and Conservation, and School of Natural Resources and Environment, University of Florida, Gainesville, Florida, United States of America, 2 School of the Environment, Washington State University, Pullman, Washington, United States of America, 3 Programa Estepa PatagoÂnica y Andina, INIBIOMA-Universidad Nacional del Comahue-CONICET, Wildlife Conservation Society, JunõÂn de los Andes, NeuqueÂn, Argentina, 4 Department of Biology, New Mexico State University, a1111111111 Las Cruces, New Mexico, United States of America, 5 Sackler Institute for Comparative Genomics, American a1111111111 Museum of Natural History, New York, New York, United States of America a1111111111 a1111111111 * [email protected] a1111111111 Abstract Large-scale ungulate migrations result in changes in prey availability for top predators and, OPEN ACCESS as a consequence, can alter predator behavior. Migration may include entire populations of Citation: Gelin ML, Branch LC, Thornton DH, prey species, but often prey populations exhibit partial migration with some individuals Novaro AJ, Gould MJ, Caragiulo A (2017) remaining resident and others migrating. Interactions of migratory prey and predators have Response of pumas (Puma concolor) to migration been documented in North America and some other parts of the world, but are poorly stud- of their primary prey in Patagonia. PLoS ONE 12 (12): e0188877. https://doi.org/10.1371/journal. ied in South America. We examined the response of pumas (Puma concolor) to seasonal pone.0188877 migration of guanacos (Lama guanicoe) in La Payunia Reserve in northern Patagonia Editor: John Goodrich, Panthera, UNITED STATES Argentina, which is the site of the longest known ungulate migration in South America. More than 15,000 guanacos migrate seasonally in this landscape, and some guanacos also are Received: April 27, 2017 resident year-round. We hypothesized that pumas would respond to the guanaco migration Accepted: November 14, 2017 by consuming more alternative prey rather than migrating with guanacos because of the Published: December 6, 2017 territoriality of pumas and availability of alternative prey throughout the year at this site. To Copyright: © 2017 Gelin et al. This is an open determine whether pumas moved seasonally with the guanacos, we conducted camera access article distributed under the terms of the trapping in the summer and winter range of guanacos across both seasons and estimated Creative Commons Attribution License, which density of pumas with spatial mark±resight (SMR) models. Also, we analyzed puma scats to permits unrestricted use, distribution, and reproduction in any medium, provided the original assess changes in prey consumption in response to guanaco migration. Density estimates author and source are credited. of pumas did not change significantly in the winter and summer range of guanacos when Data Availability Statement: Data are available guanacos migrated to and from these areas, indicating that pumas do not follow the migra- from the Dryad database DOI 10.5061/dryad.7fb7r. tion of guanacos. Pumas also did not consume more alternative native prey or livestock Funding: The authors gratefully acknowledge when guanaco availability was lower, but rather fed primarily on guanacos and some alter- financial support and equipment from the native prey during all seasons. Alternative prey were most common in the diet during sum- Conservation Food and Health Foundation, mer when guanacos also were abundant on the summer range. The response of pumas to Pittsburgh Zoo & PPG Aquarium's PPG Conservation and Sustainability Fund, Rufford the migration of guanacos differs from sites in the western North America where entire prey Small Grants for Nature Conservation, IdeaWild, populations migrate and pumas migrate with their prey or switch to more abundant prey and the Tropical Conservation and Development when their primary prey migrates. Program, University of Florida. During this work, M. L. Gelin was supported by scholarships from BEC.AR Argentina and the School of Natural PLOS ONE | https://doi.org/10.1371/journal.pone.0188877 December 6, 2017 1 / 16 Response of pumas to prey migration Resources and the Environment, University of Introduction Florida. The funders had no role in study design, data collection and analysis, decision to publish, or Large-scale ungulate migrations associated with changes in availability of resources and risk of preparation of the manuscript. predation are widespread phenomena that influence mammal community composition, prey abundance for top predators, and fitness of predators [1±3]. In many systems with ungulate Competing interests: The authors have declared that no competing interests exist. migrations, not all individuals migrate, but even partial migrations can result in large spatial changes in prey biomass [4±7]. Predators track prey movements by undertaking migrations with them, or they can modify their foraging behavior (e.g., exhibit prey switching or incorpo- rate additional prey in the diet when large numbers of their prey migrate [3,8±10]). Some predators also hold territories throughout the year near den sites and then make long distance foraging trips to areas with migratory herbivores once these herbivores have moved away from the territory [11,12]. Predator responses to prey migration have diverse effects at the community level. For example, if predators move with prey, the distribution of carcasses for scaven- gers and decomposers also shifts [13,14]. On the other hand, if predators remain relatively stationary and switch prey or broaden their diet in response to migration, they may have significant impacts on populations of alternative prey [15,16]. Migration of native prey also may affect frequency of predation on livestock and increase human-predator conflict if livestock serve as alternative prey sources for predators [10,12,17]. Behavioral responses of carnivores to prey migration have been documented for a variety of species and ecosystems in North America (e.g., [9,12,18]), but both herbivore migrations and predator responses to these migrations are poorly studied in South America. One predator that spans both of these continents is the puma (Puma concolor), which has the largest geo- graphic range of any mammal in the western hemisphere and is a top predator from Canada to southern South America. Although pumas rely on non-migratory prey in much of their range, studies in North America have reported migration by pumas [18] and prey switching [9] in systems where their primary prey, large ungulates, migrate. In Patagonia in southern South America, pumas prey heavily on the largest native ungulate, the guanaco (Lama guanicoe), in areas where this species is still common [19±21]. Although guanaco populations have declined throughout their range and movement patterns likely have been altered, the longest known terrestrial migration for mammals in South America is seasonal migration of guanacos in northern Patagonia, Argentina [22,23]. The ecological impacts of this migration are unknown. In this study, we examined the response of pumas to this guanaco migration, which occurs in La Payunia Reserve, the protected area with the largest population of guanacos (> 25,000 individuals) across the entire range of the species. Approximately two-thirds of the population is migratory; other individuals are resident in the summer or winter range throughout the year [23±25]. Although La Payunia Reserve is one of the few sites in South America where long-distance ungulate migrations are well documented, shorter migrations and other seasonal movements of guanacos are known to occur in other areas and likely were more common in the past when guanaco populations were large and barriers to movement were less common [22,26,27]. We hypothesized that pumas respond to migration of large numbers of guanacos by switching to alternative prey, or by consuming more alternative prey along with resident guanacos, rather than migrating with guanacos because pumas generally are territorial, have broad food habits [28,29], and alternative prey are common in La Payunia and available throughout the year. We expected pumas to include more livestock as well as native prey in their diet when guanacos migrated. Ranching of goats and cattle occurred within the reserve and on neighbor- ing lands, and puma predation on livestock was a significant source of conflict. Local herders reported a higher frequency of puma attacks on livestock in areas where guanaco abundance was low, but this predation has not been explicitly linked to the guanaco migration [24]. PLOS ONE | https://doi.org/10.1371/journal.pone.0188877 December 6, 2017 2 / 16 Response of pumas to prey migration To test our hypothesis, we examined puma density in summer and winter ranges of guanacos and analyzed diet of pumas from scats to determine whether pumas shift their diet when guanacos migrate. If, in contrast to our hypothesis, pumas move with guanacos, we expected to see changes in puma density that paralleled guanaco migration. We estimated puma density from camera-trapping data with spatial mark-resight models. Spatial mark-resight models are a new tool developed to overcome important limitations of capture-recapture models related to the need to better define effective

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