Abstract
Small, isolated, and disturbed forest fragments potentially offer valuable habitats for small carnivore conservation. Yet the influence of resource availability—critical for survival and reproduction—on small carnivore habitat use within these modified environments is poorly understood. We conducted camera-trap surveys within a seasonally dry tropical forest fragment (148 km2) in northeastern Thailand to better understand the influence resource availability has on small carnivore habitat use within fragmented areas. Species occupancy models including both habitat and resource variables were assessed across periods of high and low resource availability (fruit abundance and rodent biomass). Species with similar resource or habitat preferences may also compete when resources are low. Therefore, we tested species with shared preferences for patterns of spatial co-occurrence and temporal overlap. Fruit availability influenced the distribution of common palm civet (Paradoxurus hermaphroditus), while rodent biomass influenced Asiatic jackal (Canis aureus), leopard cat (Prionailurus bengalensis), and small Indian civet (Viverricula indica), but only during annual periods of scarcity. In contrast, small Asian mongoose (Herpestes javanicus) was highly selective for a specific habitat (dry dipterocarp forest) regardless of seasonal fluctuations in food availability. Occupancy increased for all species during periods of resource scarcity, with leopard cat and Asiatic jackal experiencing the greatest increases (139% and 58%, respectively). Species with shared resource and habitat preferences appeared to avoid each other, either spatially or temporally. For example, leopard cat and Asiatic jackal co-occurred spatially less than would be expected, though only when rodents were scarce. Similarly, small Indian civet and small Asian mongoose, which used the same habitat and co-occurred spatially at a rate greater than expected, were active at different times. Our results indicate that seasonal resource fluctuations and interspecific interactions strongly influence the distribution of sympatric small carnivores in a fragmented forest.
Similar content being viewed by others
References
Arnold, T.W., 2010. Uninformative parameters and model selection using akaike’s information criterion. J. Wildl. Manage 74, 1175–1178.
Ashton, P.S., Reinmar, R., Kassim, A.R., 2014. On the Forests of Tropical Asia: Lest the Memory Fade. Kew Publishing.
Barlow, J., Gardner, T.A., Araujo, I.S., Avila-Pires, T.C., Bonaldo, A.B., Costa, J.E., et al., 2007. Quantifying the biodiversity value of tropical primary, secondary, and plantation forests. Proc. Natl. Acad. Sci. U. S.A. 104, 18555–18560.
Barton, K., Availableat: 2018. MuMIn: Multi-model Inference. R Package Version 1.40.4. http://CRAN.R-project.org/package=MuMIn.
Börger,.L, Dalziel, B.D., Fryxell, J.M., 2008. Are there general mechanisms of animal home range behaviour? A review and prospects for future research. Ecol. Lett. 11, 637–650.
Braczkowski, A.R., Balme, G.A., Dickman, A., Fattebert, J., Johnson, P., Dickerson, T., Macdonald, D.W., Hunter, L., 2016. Scent lure effect on camera-trap based leopard density estimates. PLoS One 11, e0151033.
Bregman, T.P., Lees, A.C., Seddon, N., MacGregor, H.E.A., Darski, B., Aleixo, A., et al., 2015. Species interactions regulate the collapse of biodiversity and ecosystem function in tropical forest fragments. Ecology 96, 2692–2704.
Bu, H., Wang, F., McShea, W.J., Lu, Z., Wang, D., Li, S., 2016. Spatial co-occurrence and activity patterns of mesocarnivores in the temperate forests of southwest China. PLoS One 11, e0164271.
Burnham, K.P., Anderson, D.R., 2002. Model Selection and Multimodel Inference: a Practical Information-theoretic Approach. Springer, New York.
Cablk, M.E., Sagebie, Heaton J.S., Valentin, C., 2008. Olfaction-based detection distance: a quantitative analysis of how far away dogs recognize torotise odor and follow it to source. Sensors 8, 2208–2222.
Carbone, C., Gittleman, J.L., 2002. A common rule for the scaling of carnivore density. Science 295, 2273–2276.
Carbone, C., Mace, G.M., Roberts, S.C., Macdonald, D.W., 1999. Energetic constraints on the diet of terrestrial carnivores. Nature 402, 286–288.
Chiang, P., Pei, K.J., Vaughan, M.R., Li, C., 2012. Niche relationships of carnivores in a subtropical primary forest in southern Taiwan. Zool. Stud. 51, 500–511.
Chutipong, W., Steinmetz, R., Savini, T., Gale, G.A., 2017. Assessing resource and predator effects on habitat use of tropical small carnivores. Assess. Large Mamm. Potential Tululujia Wildl. Reserve Southwest. Ethiop. 62, 21–36, http://dx.doi.org/10.1007/s13364-016-0283-z.
Chutipong, W., Tantipisanuh, N., Ngoprasert, D., Lynam, A.J., Steinmetz, R., Jenks, K.E., et al., 2014. Current distribution and conservation status of small carnivores in Thailand: a baseline review. Small Carniv. Conserv. 51, 96–136.
Clavel, J., Julliard, R., Devictor, V., 2011. Worldwide decline of specialist species: toward a global functional homogenization? Front. Ecol. Environ. 9, 222–228.
Crooks, K.R., Soulé, M.E., 1999. Mesopredator release and avifaunal extinctions in a fragmented system. Nature 400, 563–566.
Di Bitetti, M.S., De Angelo, C.D., Di Blanco, Y.E., Paviolo, A., 2010. Niche partitioning and species coexistence in a Neotropical felid assemblage. Acta Oecol. 36, 403–412.
Di Bitetti, M.S., Di Blanco, Y.E., Pereira, J.A., Paviolo, A., Pérez, I.J., 2009. Time partitioning favors the coexistence of sympatric crab-eating foxes (Cerdocyon thous) and Pampas foxes (Lycalopex gymnocercus). J. Mammal. 90, 479–490.
Donadio, E., Buskirk, S.W., 2006. Diet, morphology, and interspecific killing in carnivora. Am. Nat. 167, 524–536.
Efford, M.G., 2015. Secr: Spatially Explicit Capture-recapture Models. R Package Version 2.9.5. http://CRAN.R-project.org/package=secr.
Estes, JA, Terbourgh, J., Brashares, J.S., Power, M.E., Berger, J., Bond, W.J., et al., 2011. Trophic downgrading of planet Earth. Science 333, 301–306.
Fahrig, L., Rytwinski, T., 2009. Effects of roads on animal abundance: and empirical review and synthesis. Ecol. Soc. 14, 21.
Ferguson, S.H., Taylor, M.K., Born, E.W., Rosing-Asvid, A., Messier, F., 1999. Determinants of home range size for polar bears (Ursus maritimus). Ecol. Lett. 2, 311–318.
Fiske, I.J., Chandler, R.B., Royle, JA, 2011. Unmarked: Models for Data From Unmarked Animals. http://CRAN.R-project.org/package=unmarked.
Fuller, T.K., Sievert, P.R., 2001. Carnivore demography and the consequences of changes in prey availability. In: Gittleman, J.L., Funk, S.M., Macdonald, D.W., Wayne, R.K. (Eds.), Carnivore Conservation. Cambridge University Press, pp. 163–177.
Gelman, A., 2008. Scaling regression inputs by dividing by two standard deviations. Stat. Med. 27, 2865–2873.
Gerber, B.D., Karpanty, S.M., Kelly, M.U., 2012a. Evaluating the potential biases in carnivore capture-recapture studies associated with the use of lure and varying density estimation techniques using photographic-sampling data of the Malagasy civet. Pop. Ecol. 54, 43–54.
Gerber, B.D., Karpanty, S.M., Randrianantenaina, J., 2012b. Activity patterns of carnivores in the rain forests of Madagascar: implications for species coexistence. J. Mammal. 93, 667–676.
Giam, X., Clements, G.R., Aziz, S.A., Chong, K.Y., Miettinen, J., 2011. Rethinking the ‘back to wilderness’ concept for Sundaland’s forests. Biol. Conserv. 144, 3149–3152.
Gittleman, J.L., Harvey, P.H., 1982. Carnivore home-range size, metabolic needs and ecology. Behav. Ecol. Sociolbiol. 10, 57–63.
Grassman, L.I., Tewes, M.E., Silvy, N.J., Kreetiyutanont, K., 2005. Spatial organization and diet of the leopard cat (Prionailurus bengalensis) in north-central Thailand. J. Zool. 266, 45–54, http://dx.doi.org/10.1017/S095283690500659X.
Griffith, D.M., Veech, JA, Marsh, C.J., 2016. Cooccur: probabilistic species co-occurrence analysis in R. J. Stat. Softw. 69, 1–17.
Hirsch, B.T., 2010. Tradeoff between travel speed and olfactory food detection in ring-tailed coatis (Nasua nasua). Ethology 116, 671–679.
Hoyle, M., Harborne, A.R., 2005. Mixed effects of habitat fragmentation on species richness and community structure in a microarthropod microecosystem. Ecol. Entomol. 30, 684–691.
Hunter, M.D., Price, P.W., 1992. Playing chutes and ladders: heterogeneity and the relative roles of bottom-up and top-down forces in natural communities. Ecology 73, 724–732.
Karanth, K.U., Sunquist, M.E., 2000. Behavioural correlates of predation by tiger (Panthera tigris), leopard (Panthera pardus), and dhole (Cuon alpinus) in Nagarahole. India. J. Zool. 250, 255–265.
Joshi, A.R., Smith, J.L.D., Cuthbert, F.J., 1995. Influence of food distribution and predation pressure on spacing behavior in palm civets. J. Mamm. 76, 1205–1212.
Lambert, T.D., Malcolm, J.R., Zimmerman, B.L., 2006. Amazonian small mammal abundances in relation to habitat structure and resource abundance. J. Mammal. 87, 766–776.
Lanski, J., Heltai, M., 2010. Food preferences of golden jackals and sympatric red foxes in European temperate climate agricultural area (Hungary). Mammalia 74, 267–273.
Loveridge, A.J., Macdonald, D.W., 2003. Niche separation in sympatric jackals (Canis mesomelas and Canis adustus). J. Zool. 259, 143–153.
Loveridge, A.J., Valeix, M., Davidson, Z., Murindagomo, F., Fritz, H., Macdonald, D.W., 2009. Changes in home range size of African lions in relation to pride size and prey biomass in a semi-arid savanna. Ecography 32, 953–962.
MacKenzie, D.I., Nichols, J.D., Royle, JA, Pollock, K.H., Bailey, L.L., Hines, J.E., 2006. Occupancy Estimation and Modeling: Inferring Patterns and Dynamics of Species Occurrence. Elsevier, San Diego.
Mahmood, T., Hussain, I., Nadeem, M.S., 2011. Population estimates, habitat preference and the diet of small Indian mongoose (Herpestes javanicus) in Potohar Plateau, Pakistan. Pakistan J. Zool. 43, 103–111.
Mahmood, T., Niazi, F., Nadeem, M.S., 2013. Diet composition of Asiatic jackal (Canis aureus) in Margallah Hills National Park, Islamabad, Pakistan. J. Anim. Plant Sci. 23, 444–456.
Meredith, M., Ridout, M., 2017. Estimates of Coefficient of Overlapping for Animal Activity. patterns http://CRAN.R-project.org/package=overlap.
Messier, F., 1985. Social organization, spatial distribution, and population density of wolves in relation to moose density. Can. J. Zool. 63, 1068–1077.
Mitchell, M.S., Powell, RA, 2004. A mechanistic home range model for optimal use of spatially distributed resources. Ecol. Model. 177, 209–232.
Morellet, N., Bonefant, C., Börger, L., Ossi, F., Cagnacci, F., Heurich, M., Kjellander, P., Linnell, J.D., Nicoloso, S., Sustr, P., Urbano, F., Mysterud, A., 2013. Seasonality, weather and climate affect home range size in roe deer across a wide latitudinal gradient within Europe. J. Anim. Ecol. 82, 1326–1339.
Morin, P.J., 1999. Community Ecology. Blackwell Science, Inc.
Nakashima, Y., Nakabayashi, M., Sukor, JA, 2013. Space use, habitat selection, and day-beds of the common palm civet (Paradoxurus hermaphroditus) in human-modified habitats in Sabah, Borneo. J. Mammal. 94, 1169–1178.
O’Brien, T.G., Kinnaird, M.F., Wibisono, H.T., 2003. Crouching tigers, hidden prey: sumatran tiger and prey populations in a tropical forest landscape. Anim. Conserv. 6, 131–139.
Oliver, K., Ngoprasert, D., Savini, T., 2019. Slow Lori’s density in a fragmented, disturbed dry forest, north-east Thailand. Am. J. Primatol., e22957, http://dx.doi.org/10.1002/ajp.22957.
Ostfeld, R.S., Keesing, F., 2000. Pulsed resources and community dynamics of consumers in terrestrial ecosystems. Trends Ecol. Evolut. 15, 232–237.
Otis, D.L., Burnham, K.P., White, G.C., Anderson, D.R., 1978. Statistical inference from capture data on closed animal populations. Wildl. Monogr. 62, 1–135.
Packer, C., 1986. The ecology of sociality in felids. In: Rubenstein, D.I., Wrangham, R.W. (Eds.), Ecological Aspects of Social Evolution: Birds and Mammals. Princeton Univ. Press.
Palomares, F., Caro, T.M., 1999. Interspecific killing among mammalian carnivores. Am. Nat. 153, 492–508.
Pimsai, U., Pearch, M.J., Satasook, C., Bumrungsri, S., Bates, P.J.J., 2014. Murine rodents (Rodentia: murinae) of the Myanmar-Thai-Malaysian peninsula and Singapore: taxonomy, distribution, ecology, conservation status, and illustrated identification keys. Bonn Zool. Bull. 63, 15–114.
Pitman, R.T., Swanepoel, L.H., Hunter, L., Slotow, R., Balme, G.A., 2015. The importance of refugia, ecological traps, and scale for large carnivore management. Biodivers. Conserv. 24, 1975–1987.
R Development Core Team, 2016. R: a Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria http://www.R-project.org/.
Rajaratnam, R., Sunquist, M., Rajaratnam, L, Ambu, L, 2007. Diet and habitat selection of the leopard cat (Prionailurus bengalensis borneoensis) in an agricultural landscape in Sabah, Malaysian Borneo. J. Trop. Ecol. 23, 209, http://dx.doi.org/10.1017/S0266467406003841.
Reed, S.E., Bidlack, A.L., Hurt, A., Getz, W.M., 2011. Detection distance and environmental factors in conservation detection dog surveys. J. Wildl. Manage. 75, 243–251.
Ridout, M.S., Linkie, M., 2009. Estimating overlap of daily activity patterns from camera trap data. J. Agric. Biol. Environ. Stat. 14, 322–337.
Ripple, W.J., Estes, JA, Beschta, R.L., Wilmers, C.C., Ritchie, E.G., Hebblewhite, M., et al., 2014. Status and ecological effects of the world’s largest carnivores. Science 343, 1241484.
Ritchie, E.G., Johnson, C.N., 2009. Predator interactions, mesopredator release and biodiversity conservation. Ecol. Lett. 12, 982–998.
Sˇálek, M., Kreisinger, J., Sedlácek, F., Albrecht, T., 2010. Do prey densities determine preferences of mammalian predators for habitat edges in an agricultural landscape? Landsc. Urban Plan. 98, 86–91.
Salo, P., Nordström, M., Thomson, R.L., Korpimäki, E., 2008. Risk induced by a native top predator reduces alien mink movements. J. Anim. Ecol. 77, 1092–1098.
Sarawee, A., Nakhon Ratchasima. Unpublished thesis 2008. Diet and Habitat Use of Viverrid Group at Sakaerat Environmental Research Station.
Satgé, J., Teichman, K., Cristescu, B., 2017. Competition and coexistence in a small carnivore guild. Oecologia 184, 873–884.
Savini, T., Boesch, C., Reichard, U.H., 2008. Home-range characteristics and the influence of seasonality on female reproduction in white-handed gibbons (Hylobates lar)at Khao Yai National Park, Thailand. Am. J. Phys. Anthropol. 135, 1–12, http://dx.doi.org/10.1002/ajpa.20578.
Schuette, P., Wagner, A.P., Wagner, M.E., Creel, S., 2012. Occupancy patterns and niche partitioning within a diverse carnivore community exposed to anthropogenic pressures. Biol. Conserv. 158, 301–312.
Scognamillo, D., Maxit, I.E., Sunguist, M., 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.
Shehzad, W., Riaz, T., Nawaz, M.A., Miquel, C., Poillot, C., Shah, S.A., Taberlet, P., 2012. Carnivore diet analysis based on next-generation sequencing: application to the leopard cat (Prionailurus bengalensis) in Pakistan. Mol. Ecol., 1951–1965, http://dx.doi.org/10.1111/j.1365-294X.2011.05424.x.
Shenkut, M., Mebrate, A., Balakrishnan, M., 2006. Distribution and abundance of rodents in farmlands: a case study in Alleltu Woreda, Ethiopia. Ethiop. J. Sci. 29, 63–70.
Sodhi, N.S., Pin, L., Clements, R., Wanger, T.C., Hill, J.K., Hamer, K.C., Clough, Y., Tscharntke, T., Rose, M., Posa, C., Ming, T., 2010. Conserving Southeast Asian forest biodiversity in human-modified landscapes. Biol. Conserv. 143, 2375–2384, http://dx.doi.org/10.1016/j.biocon.2009.12.029.
Suwanrat, J., Artchawakom, T., Suwanwaree, P., 2011. Mammal Diversity Study Using Camera Trap at Sakaerat Environmental Research Station. Poster presented at the 32nd Thailand Wildlife Seminar, Bangkok, Thailand.
Tabarelli, M., Silva, M.J.C., Gascon, C., 2004. Forest fragmentation, synergisms and the impoverishment of Neotropical forests. Biodivers. Conserv. 13, 1419–1425.
Tantipisanuh, N., Gale, G.A, 2013. Representation of threatened vertebrates by a protected area system in Southeast Asia: the importance of non-forest habitats. Raffles Bull. Zool. 61, 359–395.
Terborgh, J., 1986. Keystone plant resources in the tropical forest. In: Soulé, M.E. (Ed.), Conservation Biology: The Science of Scarcity and Diversity. Sinauer Associates, Inc., pp. 330–344.
Thompson, C.M., Gese, E.M., 2007. Food webs and intraguild predation: community interactions of a native mesocarnivore. Ecology 88, 334–346.
Veech, J.A., 2013. A probabilistic model for analysing species co-occurrence. Glob. Ecol. Biogeogr. 22, 252–260.
Viana, D.S., Granados, J.E., Fandos, P., Pérez, J.M., Cano-Manuel, F.J., Burón, D., Fandos, G., Aguado, M.A.P., Figuerola, J., Soriguer, R.C., 2018. Linking seasonal home range size with habitat selection and movement in a mountain ungulate. Mov. Ecol. 6, 1.
Vieira, E.M., Port, D., 2007. Niche overlap and resource partitioning between two sympatric fox species in southern Brazil. J. Zool. 272, 57–63.
Wang, H., Fuller, T.K., 2003. Food habits of foursympatric carnivores in southeastern China. Mammalia 67, 513–519.
Wells, K., Kalko, E.K.V., Lakim, M.B., Pfeiffer, M., 2007. Effects of rain forest logging on species richness and assemblage composition of small mammals in Southeast Asia. J. Biogeogr. 34, 1087–1099.
White, T.C.R., 1978. The importance of a relative shortage of food in animal ecology. Oecologia 33, 71–86.
Wiens, J.A., 1993. Fat times, lean times and competition among predators. Trends Ecol. Evol. (Amst.) 8, 348–349.
Wolf, C., Ripple, W.J., 2016. Prey depletion as a threat to the world’s large carnivores. R. Soc. Open Sci. 3, 160252.
Woodroffe, R., Davies-Mostert, H., Ginsberg, J., Graf, J., Leigh, K., McCreery, K., et al., 2007. Rates and causes of mortality in Endangered African wild dogs Lycaon pictus: lessons for management and monitoring. Oryx 41, 215–223.
Wright, S.J., Duber, H.C., 2001. Poachers and forest fragmentation alter seed dispersal, seed survival, and seedling recruitment in the palm Attalea butryaceae, with implications for tropical tree diversity. Biotropica 33, 421–434.
Zhou, Y., Zhang, J., Slade, E., Zhang, L, Palomares, F., Chien, J., Wang, X., Zhang, S., 2008. Dietary shifts in relation to fruit availability among masked palm civets (Paguma lavarta) in central China. J. Mammal. 89, 435–447.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Petersen, W.J., Savini, T., Steinmetz, R. et al. Periodic resource scarcity and potential for interspecific competition influences distribution of small carnivores in a seasonally dry tropical forest fragment. Mamm Biol 95, 112–122 (2019). https://doi.org/10.1016/j.mambio.2018.11.001
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1016/j.mambio.2018.11.001