Abstract
Dolichotis patagonum (common name: mara) is a large sized rodent, endemic of Argentina, which raises its juveniles in burrows. It has recently been categorized as vulnerable. This is the first study to evaluate D. patagonum interactions with potential predators in the surroundings of the dens. We monitored 20 burrows, using camera-traps, with a total of 5644 camera-days, obtained over two years (2015 and 2016). Five potential predator species were detected (Lycalopex griseus, Puma concolor, Leopardus geoffroyi, Salvator sp. and Chaetophractus villosus). L. griseus and L. geoffroyi were the species with the highest frequency of visits. Both species were photographed attacking the juveniles. Four out of five potential predator species registered presented agonistic interactions with adults of mara. Overlap between all species analyzed and mara was low to moderate, and potential predator visits to the surrounding of the burrows did not vary according to the presence of juveniles. Our results suggest that in this system, predators behave as opportunistic predators of mara’s juveniles. Mara’s social and reproductive behavior varies along the distribution range of the species, therefore it is of great ecological value to analyze and understand the variations of its interactions with predators in different regions and environments.
Funding source: Universidad Nacional de San Luis
Award Identifier / Grant number: PROICO 2-2818
Acknowledgements
We thank the many volunteers, who collaborated in the data collection; the staff of Sierra de las Quijadas National Park, especially Park Ranger Daniel Figueroa for his unconditional support and helpful advice; Lorena Tribe for her assistance. Thanks are also due to the Instituto Multidisciplinario de Investigaciones Biológicas (IMIBIO)-CCT San Luis; the PPBio Argentina collaborative research network; and to the Universidad Nacional de San Luis.
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Author contributions: Ailin Gatica was responsible for the main idea, and contributed with the general design, execution, coordination of field activities, data ordering and analysis, and writing of the manuscript. Ana Ochoa contributed by aiding in the conceptual design, data gathering, data analysis and writing of the manuscript. Antonio Mangione contributed with the assessment of experimental design and revisions of the manuscript.
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Research funding: This study was supported by PROICO 2-2818 from the Secretaría de Ciencia y Tecnología -Facultad de Química, Bioquímica y Farmacia, Universidad Nacional de San Luis.
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Conflict of interest statement: The authors declare that they have no conflicts of interest regarding this article.
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Research ethics: This research has been approved and authorized by Argentinian National Parks Administration (APN) of Argentina, which is the competent authority in our country for the authorization of research works in these territories. Permissions numbers giving by APN: DRC262 and DRC 315.
References
Abba, A. and Cassini, M. (2008). Ecology and conservation of three species of armadillos in the Pampas region, Argentina. In: Loughry, W. and Vizcaíno, S. (Eds.), The biology of the Xenarthra. University Press of Florida, Gainesville, pp. 300–305.Search in Google Scholar
Abba, A.M., Nabte, M.J., and Udrizar Sauthier, D.E. (2010). New data on armadillos (Xenarthra: Dasypodidae) for Central Patagonia, Argentina. Edentata 11: 11–17, https://doi.org/10.1896/020.011.0103.Search in Google Scholar
Alonso Roldán, V., Bossio, L., and Galván, D.E. (2015). Sources of variation in a two-step monitoring protocol for species clustered in conspicuous points: Dolichotis patagonum as a case study. PloS One 10: e0128133, https://doi.org/10.1371/journal.pone.0128133.Search in Google Scholar
Alonso Roldán, V. and Udrizar Sauthier, D.E. (2016). Madrigueras de Dolichotis patagonum como recurso para otros vertebrados en Península Valdés. Mastozool. Neotrop. 23: 515–520.Search in Google Scholar
Alonso Roldán, V., Udrizar Sauthier, D.E., Giannoni, S.M., and Campos, C.M. (2019). Dolichotis patagonum. Categorización 2019 de los mamíferos de Argentina según su riesgo de extinción, Available at: <http://cma.sarem.org.ar>.Search in Google Scholar
APN. (2017). Actualización del Plan de Gestión del Parque Nacional Sierra de las Quijadas. Administración de Parques Nacionales, Available at: <https://sib.gob.ar/archivos/PG_PNSQ_2017_VERSION_FINAL.pdf>.Search in Google Scholar
Azevedo, F.C., Lemos, F.G., Freitas-Junior, M.C., Rocha, D.G., and Azevedo, F.C.C. (2018). Puma activity patterns and temporal overlap with prey in a human-modified landscape at Southeastern Brazil. J. Zool. 305: 246–255, https://doi.org/10.1111/jzo.12558.Search in Google Scholar
Baldi, R. (2007). Breeding success of the endemic mara Dolichotis patagonum in relation to habitat selection: conservation implications. J. Arid Environ. 68: 9–19, https://doi.org/10.1016/j.jaridenv.2006.03.025.Search in Google Scholar
Blumstein, D.T. (1998). Quantifying predation risk for refuging animals: a case study with golden marmots. Ethology 104: 501–516.10.1111/j.1439-0310.1998.tb00086.xSearch in Google Scholar
Camp, M.J., Rachlow, J.L., Woods, B.A., Johnson, T.R., and Shipley, L.A. (2012). When to run and when to hide: the influence of concealment, visibility, and proximity to refugia on perceptions of risk. Ethology 118: 1–8, https://doi.org/10.1111/eth.12000.Search in Google Scholar
Campos, C.M., Tognelli, M.F., and Ojeda, R.A. (2001). Dolichotis patagonum. Mamm. Species 652: 1–5, https://doi.org/10.1644/1545-1410(2001)652<0001:dp>2.0.co;2.10.1644/1545-1410(2001)652<0001:DP>2.0.CO;2Search in Google Scholar
Canevari, M. and Vaccaro, O. (2007). Guía de mamíferos del sur de América del Sur. L.O.L.A., Buenos Aires.Search in Google Scholar
Castillo Sánchez, L.L., Álvarez, M.C., Nuñez, M.B., Kaufmann, C.A., Alcaraz, A.P., Ochoa, A.C., and Gatica, A. (2021). ¿Potencial depredación intragremio? Puma concolor y Lycalopex gymnocercus en el ecotono Chaco-Monte, San Luis, República Argentina. Notas sobre Mamíferos Sudamericanos, Available at: <https://www.sarem.org.ar/wp-content/uploads/2021/04/SAREM_NotasMamSud_3-2021_CastilloSanchez.pdf>.10.31687/saremNMS.21.3.3Search in Google Scholar
Craig, C.L. and Freeman, C.R. (1991). Effects of predator visibility on prey encounter: a case study on aerial web weaving spiders. Behav. Ecol. Sociobiol. 29: 249–254, https://doi.org/10.1007/bf00163981.Search in Google Scholar
Del Vitto, L.A., Petenatti, E.M., Nellar, M.M., and Petenatti, M.E. (1994). Las áreas naturales protegidas de San Luis, Argentina. Multequina 3: 141–156.Search in Google Scholar
Di Bitetti, M.S., Di Blanco, Y.E., Pereira, J.A., Paviolo, A.N., and Jimenez Perez, I. (2009). Time partitioning favors the coexistence of sympatric crab-eating foxes (Cerdocyon thous) and pampas foxes (Lycalopex gymnocercus). J. Mammal. 90: 479–490, https://doi.org/10.1644/08-mamm-a-113.1.Search in Google Scholar
Donadio, E., Novaro, A.J., Buskirk, S.W., Wurstten, A., Vitali, M.S., and Monteverde, M.J. (2010). Evaluating a potentially strong trophic interaction: pumas and wild camelids in protected areas of Argentina. J. Zool. 280: 33–40, https://doi.org/10.1111/j.1469-7998.2009.00638.x.Search in Google Scholar
Emsens, W.J., Hirsch, B.T., Kays, R., and Jansen, P.A. (2014). Prey refuges as predator hotspots: ocelot (Leopardus pardalis) attraction to agouti (Dasyprocta punctata) dens. Acta Theriol. 59: 257–262, https://doi.org/10.1007/s13364-013-0159-4.Search in Google Scholar
Faria-Corrêa, M., Balbueno, R.A., Vieira, E.M., and Freitase, T.R.O. (2009). Activity, habitat use, density, and reproductive biology of the crab-eating fox (Cerdocyon thous) and comparison with the pampas fox (Lycalopex gymnocercus) in a Restinga area in the southern Brazilian Atlantic Forest. Mamm. Biol. 74: 220–229, https://doi.org/10.1016/j.mambio.2008.12.005.Search in Google Scholar
Fitzgerald, L.A. (1992). La Historia Natural de Tupinambis. Rev. Un. Nac. Asunción 3: 71–72.Search in Google Scholar
Gatica, A. and Mangione, A.M. (2018). Behavioral response of the mara (Dolichotis patagonum) to food density in Argentina. Rev. Mex. Mastozool. 8: 40–47.10.22201/ie.20074484e.2018.1.2.259Search in Google Scholar
Gatica, A., Denkiewicz, N.M., and Ochoa, A.C. (2019). Breeding behavior of mara [Dolichotis patagonum (Zimmermann, 1780)] in the Monte-Chaco ecotone of Argentina. Mamm. Stud. 44: 233–241, https://doi.org/10.3106/ms2019-0006.Search in Google Scholar
Gatica, A., Ochoa, A.C., Denkiewicz, N.M., and Mangione, A.M. (2020). Wildlife associated with burrows of Dolichotis patagonum in central west Argentina. Neotrop. Biol. Conserv. 15: 399–407, https://doi.org/10.3897/neotropical.15.e54979.Search in Google Scholar
Genovart, M., Negre, N., Tavecchia, G., Bistuer, A., Parpal, L., and Oroet, D. (2010). The young, the weak and the sick: evidence of natural selection by predation. PloS One 5: e9774, https://doi.org/10.1371/journal.pone.0009774.Search in Google Scholar PubMed PubMed Central
Gómez, H., Wallace, R.B., Ayala, G., and Tejada, R. (2005). Dry season activity periods of some Amazonian mammals. Stud. Neotrop. Fauna Environ. 40: 91–95, https://doi.org/10.1080/01650520500129638.Search in Google Scholar
Grillet, P., Cheylan, M., Thirion, J.M., Dore, F., Bonnet, X., Dauge, C., Chollet, S., and Marchand, M.A. (2010). Rabbit burrows or artificial refuges are a critical habitat component for the threatened lizard, Timon lepidus (Sauria, Lacertidae). Biol. Conserv. 19: 2039–2051, https://doi.org/10.1007/s10531-010-9824-y.Search in Google Scholar
Guerisoli, M.M., Caruso, N., Vidal, E.M.L., and Lucherini, M. (2019). Habitat use and activity patterns of Puma concolor in a human dominated landscape of Central Argentina. J. Mammal. 100: 202–211, https://doi.org/10.1093/jmammal/gyz005.Search in Google Scholar
Haitao Yang, H.D., Smith, J.L.D., Feng, L., Wang, T., and Ge, J. (2019). Prey selection of Amur tigers in relation to the spatiotemporal overlap with prey across the Sino–Russian border. Wildl. Biol. 2019: 1–11, https://doi.org/10.2981/wlb.00508.Search in Google Scholar
Harmsen, B.J., Foster, R.J., Silver, S.C., Ostro, L.E.T., and Doncaster, C.P. (2011). Jaguar and puma activity patterns in relation to their main prey. Mamm. Biol. 76: 320–324, https://doi.org/10.1016/j.mambio.2010.08.007.Search in Google Scholar
Holling, C.S. (1959). Some characteristics of simple types of predation and parasitism. Can. Entomol. 91: 385–397, https://doi.org/10.4039/ent91385-7.Search in Google Scholar
Houngbégnon, F.G.A., Cornelis, D., Vermeulen, C., Sonké, B., Ntie, S., Fayolle, A., Fonteyn, D., Lhoest, S., Evrard, Q., Yapi, F., et al.. (2020). Daily activity patterns and co-occurrence of duikers revealed by an intensive camera trap survey across Central African rainforests. Animals 10: 2200, https://doi.org/10.3390/ani10122200.Search in Google Scholar PubMed PubMed Central
Lima, S.L. and Dill, L.M. (1990). Behavioral decisions made under the risk of predation: a review and prospectus. Can. J. Zool. 68: 619–640, https://doi.org/10.1139/z90-092.Search in Google Scholar
Mares, M.A. and Ojeda, R.A. (1982). Patterns of diversity and adaptation in South American hystricognath rodents. In: Mares, M.A. and Genoways, H.H. (Eds.), Mammalian biology in South America. Special Publications Series Pymatuning Laboratory of Ecology, University of Pittsburgh, Pittsburgh, pp. 393–432.Search in Google Scholar
Meredith, M. and Ridout, M. (2020). Overview of the overlap package, Available at: <https://cran.r-project.org/web/packages/overlap/vignettes/overlap.pdf>.Search in Google Scholar
Montaño, R.R., Cuéllar, R.L., Fitzgerald, L.A., Mendoza, F., Soria, F., Fiorello, C.V., Deem, S.L., and Noss, A.J. (2013). Activity and ranging behavior of the red tegu lizard Tupinambis rufescens in the bolivian chaco. South Am. J. Herpetol. 8: 81–88, https://doi.org/10.2994/sajh-d-13-00016.1.Search in Google Scholar
Núñez, M.B. and Mangione, A. (2008). Determining micro- and mesofaunal composition through the analysis of South American grey fox’s feces in two different semiarid habitats. Ecol. Austral 18: 205–212.Search in Google Scholar
Otto, S., Rall, B., and Brose, U. (2007). Allometric degree distributions facilitate food- web-stability. Nature 450: 1226–1229, https://doi.org/10.1038/nature06359.Search in Google Scholar PubMed
Palacios, R., Walker, R.S., and Novaro, A.J. (2012). Differences in diet and trophic interactions of Patagonian carnivores between areas with mostly native or exotic prey. Mamm. Biol. 77: 183–189, https://doi.org/10.1016/j.mambio.2012.01.001.Search in Google Scholar
Pankhurst, S.H. (1998). The social organisation of the mara at Whipsnade Wild Animal Park, Ph.D. thesis. Cambridge, University of Cambridge.Search in Google Scholar
Pereira, J.A. (2010). Activity pattern of Geoffroy’s cats (Leopardus geoffroyi) during a period of food shortage. J. Arid Environ. 74: 1106–1109, https://doi.org/10.1016/j.jaridenv.2010.03.017.Search in Google Scholar
Pereira, J.A., Di Bitetti, M.S., Fracassi, N.G., Paviolo, A., De Angelo, C.D., Di Blanco, Y.E., and Novaro, A.J. (2011). Population density of Geoffroy’s cat in scrublands of Central Argentina. J. Zool. 283: 37–44, https://doi.org/10.1111/j.1469-7998.2010.00746.x.Search in Google Scholar
Preisser, E.L. and Orrock, J.L. (2012). The allometry of fear: interspecific relationships between body size and response to predation risk. Ecosphere 3: 1–27, https://doi.org/10.1890/es12-00084.1.Search in Google Scholar
R Core Team. (2020). R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, Available at: <https://www.R-project.org/>.Search in Google Scholar
Sazima, I. and D’Angelo, G.B. (2013). Range of animal food types recorded for the tegu lizard (Salvator merianae) at an urban park in South-Eastern Brazil. Herpetol. Notes 6: 427–430.Search in Google Scholar
Scognamillo, D., Maxit, I.E., Sunquist, M., and Polisar, J. (2003). Coexistence of jaguar (Panthera onca) and puma (Puma concolor) in a mosaic landscape in the Venezuelan llanos. J. Zool. 259: 269–279, https://doi.org/10.1017/s0952836902003230.Search in Google Scholar
Sidell, B.P. (2002). Moonrise 3.5 software (32 bit), Available at: <https://moonrise.informer.com/3.5/>.Search in Google Scholar
Sih, A. (1984). The behavioral response race between predator and prey. Am. Nat. 123: 143–150, https://doi.org/10.1086/284193.Search in Google Scholar
Sinclair, A., Mduma, S., and Brashares, J. (2003). Patterns of predation in a diverse predator-prey system. Nature 425: 288–290, https://doi.org/10.1038/nature01934.Search in Google Scholar
Srbek-Araujo, A.C., Jardim Guimarães, L., and Costa-Braga, D. (2020). Activity pattern of the black-and-white Tegu, Salvator merianae (Squamata, Teiidae), in an Atlantic Forest remnant in Southeastern Brazil. Herpetol. Notes 13: 93–99.Search in Google Scholar
Stevenson, R.D. (1985). The relative importance of behavioral and physiological adjustments controlling body temperature in terrestrial ectotherms. Am. Nat. 126: 362–386, https://doi.org/10.1086/284423.Search in Google Scholar
Taber, A.B. (1987). The behavioral ecology of the mara Dolichotis patagonum, Ph.D. thesis. Oxford, University of Oxford.Search in Google Scholar
Taber, A.B. and Macdonald, D.W. (1992a). Communal breeding in the mara, Dolichotis patagonum. J. Zool. 227: 439–452, https://doi.org/10.1111/j.1469-7998.1992.tb04405.x.Search in Google Scholar
Taber, A.B. and Macdonald, D.W. (1992b). Spatial organization and monogamy in the mara Dolichotis patagonum. J. Zool. 227: 417–438, https://doi.org/10.1111/j.1469-7998.1992.tb04404.x.Search in Google Scholar
Turner, A.M. and Montgomery, S.L. (2003). Spatial and temporal scales of predator avoidance: experiments with fish and snails. Ecology 84: 616–622, https://doi.org/10.1890/0012-9658(2003)084[0616:satsop]2.0.co;2.10.1890/0012-9658(2003)084[0616:SATSOP]2.0.CO;2Search in Google Scholar
Vieira, E.M. and Port, D. (2007). Niche overlap and resource partitioning between two sympatric fox species in Southern Brazil. J. Zool. 272: 57–63, https://doi.org/10.1111/j.1469-7998.2006.00237.x.Search in Google Scholar
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