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Mammal Research

, Volume 62, Issue 1, pp 21–36 | Cite as

Assessing resource and predator effects on habitat use of tropical small carnivores

  • Wanlop Chutipong
  • Robert Steinmetz
  • Tommaso Savini
  • George A. Gale
Original Paper

Abstract

Habitat use of animals is influenced by a combination of factors including food abundance and interactions with other species. Animals typically must forage while simultaneously avoiding predation from multiple potential predators, but habitat use in tropical forest ecosystems that assesses effects of both predation risk and resources has rarely been conducted. We used camera traps and occupancy analyses to document small mammalian carnivore occurrence in relation to food abundance and interactions with large predators. We hypothesized that habitat use of six small mammalian carnivores (≤15 kg) would be influenced by (1) abundance of resources (fruit, rodents, and streams) and/or (2) large predators. Predictions regarding food and habitat resources were only supported for one species (crab-eating mongoose, Urva urva), which was positively associated with rodents and streams. Three small carnivores (masked palm civet Paguma larvata, common palm civet Paradoxurus hermaphroditus, yellow-throated marten Martes flavigula) were affected negatively by leopard and mesopredators as predicted. Counter to our predictions, two species (masked palm civet and yellow-throated marten) showed spatial avoidance of tiger suggesting that an apex predator might also pose predation risk to small carnivores. The focal small carnivores and large predators of this study appeared to have moderately to highly overlapping temporal activity indicating no temporal avoidance. In conclusion, food resources appeared to have minimal effects for six small carnivores in this ecosystem probably due to continuous resource availability. Predation risk appeared to affect some species in terms of spatial occupancy but not in temporal activity, indicating perhaps complex, but not entirely negative interactions between larger carnivores and this guild of small carnivores. The mechanisms which facilitate co-occurrence between small carnivores and large predators may, however, operate at finer spatiotemporal scales than we investigated here.

Keywords

Habitat use Predation risk Small carnivores Species interactions Thailand 

Notes

Acknowledgments

Permission to conduct research in Thung Yai Naresuan Wildlife Sanctuary was provided by the Department of National Parks, Wildlife and Plant Conservation. We wish to also acknowledge all rangers of Thung Yai for their help and generosity during fieldwork. Thanks are also due to E. Chirngsaarrd and V. Panyaporn, the former superintendents, M. Kaengketkarn, chief assistant, and present superintendent, W. O-chakul. We are grateful to N. Seuaturien, T. Dawreung, A. Kamjing, and S. Tarawanaruk for their extensive assistance with fieldwork. We thank A.J. Lynam for comments on earlier drafts of this manuscript and Orien Richmond for kindly providing the R script for using the delta method and for coaching us on SIF calculations. We thank three anonymous reviewers for their constructive comments that improved the manuscript.

Compliance with ethical standard

Funding

This study was funded by the TRF/BIOTEC Special Program for Biodiversity Research and Training grant (BRT T351001 and BRT R353008), the National Science and Technology Development Agency (CMPO P-11-00592), WWF Thailand, the Rufford Small Grant for Nature Conservation (RSG 10504-1), and Office of the Thai Higher Education Commission (Strategic Scholarships Fellowships Frontier Research Networks).

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with animals performed by any of the authors.

Supplementary material

13364_2016_283_MOESM1_ESM.docx (138 kb)
ESM 1 (DOCX 137 kb)

References

  1. Abramov A, Timmins RJ, Roberton S, Long B, Than Zaw, Duckworth JW (2008) Martes flavigula. The IUCN red list of threatened species 2008: e.T41649A10528335. Downloaded on 21 May 2016Google Scholar
  2. Aroon S (2008) Diet and habitat use of viverrid group at Sakaerat Environmental Research Station, Nakhon Ratchasima. Dissertation, Suranaree University of TechnologyGoogle Scholar
  3. Austin SC, Tewes ME, Grassman LI Jr, Silvy NJ (2007) Ecology and conservation of the leopard cat Prionailurus bengalensis and clouded leopard Neofelis nebulosa in Khao Yai National Park, Thailand. Acta Zool Sin 53:1–14Google Scholar
  4. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, New YorkGoogle Scholar
  5. Choudhury A et al (2015) Herpestes urva. The IUCN red list of threatened species 2015: e.T41618A45208308 Accessed 25 December 2015Google Scholar
  6. Chua MAH, Sivasothi N, Meier R (2016) Population density, spatiotemporal use and diet of the leopard cat (Prionailurus bengalensis) in a human-modified succession forest landscape of Singapore. Mamm Res. doi: 10.1007/s13364-015-0259-4 Google Scholar
  7. Chuang S-A, Lee L-L (1997) Food habits of three carnivore species (Viverricula indica, Herpestes urva, and Melogale moschata) in Fushan Forest, northern Taiwan. J Zool 243:71–79CrossRefGoogle Scholar
  8. Chutipong W et al (2014) Current distribution and conservation status of small carnivores in Thailand: a baseline review. Small Carniv Conserv 51:96–136Google Scholar
  9. Chutipong W, Steinmetz R, Savini T, Gale GA (2015) Sleeping site selection in two Asian viverrids: effects of predation risk, resource access and habitat characteristics. Raffles Bull Zool 63:516–528Google Scholar
  10. Donadio E, Buskirk SW (2006) Diet, morphology, and interspecific killing in Carnivora. Am Nat 167:524–536CrossRefPubMedGoogle Scholar
  11. Duckworth JW (1997) Small carnivores in Laos: a status review with notes on ecology, behavior and conservation. Small Carniv Conserv 16:1–21Google Scholar
  12. Duckworth JW, Wozencraft C, Kanchanasaka B (2008a) Paguma larvata. The IUCN red list of threatened species 2008: e.T41692A10517976. Downloaded on 21 May 2016Google Scholar
  13. Duckworth JW, Widmann P, Custodio C, Gonzalez JC, Jennings A, Veron G (2008b) Paradoxurus hermaphroditus. The IUCN red list of threatened species 2008: e.T41693A10518525. Downloaded on 21 May 2016Google Scholar
  14. Duckworth, JW, Wozencraft C, Wang Y-X, Kanchanasaka B, Long B (2015) Viverra zibetha. The IUCN red list of threatened species 2015: e.T41709A81522305. Downloaded on 21 May 2016Google Scholar
  15. Efford MG (2015) secr: spatially explicit capture-recapture models. R package version 2.9.5. URL http://CRAN.R-project.org/package=secr
  16. Elmhagen B, Rushton SP (2007) Trophic control of mesopredators in terrestrial ecosystems: top-down or bottom-up? Ecol Lett 10:197–206CrossRefPubMedGoogle Scholar
  17. Fieberg J, Johnson DH (2015) MMI: multimodel inference or models with management implications? J Wildl Manage 79:708–718CrossRefGoogle Scholar
  18. Fiske IJ, Chandler RB (2011) unmarked: an R package for fitting hierarchical models of wildlife occurrence and abundance. J Stat Soft 43:1–23CrossRefGoogle Scholar
  19. Francis CM (2008) A field guide to the mammals of Southeast Asia. New Holland Publishers, UKGoogle Scholar
  20. Grassman LI Jr (1998) Movements and fruit selection of two Paradoxurinae species in a dry evergreen forest in Southern Thailand. Small Carniv Conserv 19:25–29Google Scholar
  21. Grassman LI Jr (1999) Ecology and behavior of the Indochinese leopard in Kaeng Krachan National Park, Thailand. Nat Hist Bull Siam Soc 47:77–93Google Scholar
  22. Grassman LI Jr, Tewes ME, Silvy NJ, Kreetiyutanont K (2005a) Spatial organization and diet of the leopard cat (Prionailurus bengalensis) in north-central Thailand. J Zool 266:45–54CrossRefGoogle Scholar
  23. Grassman LI Jr, Tewes ME, Silvy NJ (2005b) Ranging, habitat use and activity patterns of binturong Arctictis binturong and yellow-throated marten Martes flavigula in north-central Thailand. Wildl Biol 11:49–57CrossRefGoogle Scholar
  24. Harihar A, Pandav B, Goyal SP (2011) Responses of leopard Panthera pardus to the recovery of a tiger Panthera tigris population. J Appl Ecol 48:806–814CrossRefGoogle Scholar
  25. Harmsen BJ et al (2009) Spatial and temporal interactions of sympatric jaguars (Panthera onca) and pumas (Puma concolor) in a Neotropical forest. J Mammal 90:612–620CrossRefGoogle Scholar
  26. Hayward MW et al (2006) Prey preferences of the leopard (Panthera pardus). J Zool 270:298–313Google Scholar
  27. Hines JE (2006) PRESENCE. Software to estimate patch occupancy and related parameters. USGS-PWRC. http://www.mbr-pwrc.usgs.gov/software/presence.html
  28. Hunter MD, Price PW (1992) Playing chutes and ladders: heterogeneity and the relative roles of bottom-up and top-down forces in natural communities. Ecology 73:724–732Google Scholar
  29. Jackson CH (2011) Multi-state models for panel data: the msm package for R. J Stat Softw 38:1–29CrossRefGoogle Scholar
  30. Jennings AP, Zubaid A, Veron G (2010) Home ranges, movements and activity of the short-tailed mongoose (Herpestes brachyurus) on Peninsular Malaysia. Mammalia 74:43–50CrossRefGoogle Scholar
  31. Jennings AP, Veron G (2011) Predicted distributions and ecological niches of 8 civet and mongoose species in Southeast Asia. J Mammal 92:316–327CrossRefGoogle Scholar
  32. Joshi AR, Smith JLD, Cuthbert FJ (1995) Influence of food distribution and predation pressure on spacing behavior in palm civets. J Mammal 76:1205–1212CrossRefGoogle Scholar
  33. Kamler JF, Johnson A, Vongkhamheng C, Bousa A (2012) The diet, prey selection, and activity of dholes (Cuon alpinus) in northern Laos. J Mammal 93:627–633CrossRefGoogle Scholar
  34. Kitamura S, Yumoto T, Poonswad P, Chuailua P, Plongmai K, Maruhashi T, Noma N (2002) Interactions between fleshy fruits and frugivores in a tropical seasonal forest in Thailand. Oecol 133:559–572Google Scholar
  35. Lam WY, Hedges L, Clements GR (2014) First record of a clouded leopard predating on a binturong. Cat News 60:33Google Scholar
  36. Langham N (1983) Distribution and ecology of small mammals in three rain forest localities of Peninsula Malaysia with particular references to Kedah Peak. Biotropica 15:199–206CrossRefGoogle Scholar
  37. Lynam AJ et al (2013) Terrestrial activity patterns of wild cats from camera-trapping. Raffles Bull Zool 61:407–415Google Scholar
  38. MacKenzie DI et al (2006) Occupancy estimation and modeling: inferring patterns and dynamics of species occurrence. Elsevier, San DiegoGoogle Scholar
  39. Mazerolle MJ (2015) AICcmodavg: model selection and multimodel inference based on (Q)AIC(c). R package version 2.0-3. URL http://CRAN.R-project.org/package=AICcmodavg
  40. Morrison ML, Marcot BG, Mannan RW (2006) Wildlife–habitat relationships: concepts and applications, 3rd edn. University of Wisconsin Press, Madison, Wisconsin, USAGoogle Scholar
  41. Nakashima Y, Inoue E, Inoue-Murayama M, Sukor JA (2010) High potential of a disturbance-tolerant frugivore, the common palm civet Paradoxurus hermaphroditus (Viverridae), as a seed disperser for large-seeded plants. Mammal Stud 35:209–215CrossRefGoogle Scholar
  42. 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 94:1169–1178CrossRefGoogle Scholar
  43. Nakhasathien S, Stewart-Cox B (1990) Nomination of the Thung Yai-Huai Kha Khaeng Wildlife Sanctuary to be a UNESCO World Heritage Site. Wildlife Conservation Division, Royal Forest Department, BangkokGoogle Scholar
  44. Nichols JD et al (2008) Multi-scale occupancy estimation and modelling using multiple detection methods. J Appl Ecol 45:1321–1329CrossRefGoogle Scholar
  45. Odden M, Wegge P, Fredriksen T (2010) Do tigers displace leopards? If so, why? Ecol Res 25:875–881CrossRefGoogle Scholar
  46. Palomares F, Caro TM (1999) Interspecific killing among mammalian carnivores. Am Nat 153:492–508CrossRefGoogle Scholar
  47. Phetdee A (2000) Feeding habits of the tiger (Panthera tigris Linnaeus) in Huai Kha Khaeng Wildlife Sanctuary by fecal analysis. Kasetsart University, ThesisGoogle Scholar
  48. R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org/
  49. Rabinowitz AR (1990) Notes on the behavior and movements of leopard cats, Felis bengalensis in a dry tropical forest mosaic in Thailand. Biotropica 22:397–403CrossRefGoogle Scholar
  50. Rabinowitz AR (1991) Behaviour and movements of sympatric civet species in Huai Kha Khaeng Wildlife Sanctuary, Thailand. J Zool 223:281–298CrossRefGoogle Scholar
  51. Rabinowitz AR, Walker SR (1991) The carnivore community in a dry tropical forest mosaic in Huai Kha Khaeng Wildlife Sanctuary, Thailand. J Trop Ecol 7:37–47CrossRefGoogle Scholar
  52. 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 23:209–217CrossRefGoogle Scholar
  53. Richards SA, Whittingham MJ, Stephens PA (2011) Model selection and model averaging in behavioural ecology: the utility of the IT-AIC framework. Behav Ecol Sociobiol 65:77–89CrossRefGoogle Scholar
  54. Richmond OMW, Hines JE, Beissinger SR (2010) Two-species occupancy models: a new parameterization applied to co-occurrence of secretive rails. Ecol Appl 20:2036–2046CrossRefPubMedGoogle Scholar
  55. Ridout MS, Linkie M (2009) Estimating overlap of daily activity patterns from camera trap data. J Agric Biol Environ Stat 14:322–337Google Scholar
  56. Ritchie EG, Johnson CN (2009) Predator interactions, mesopredator release and biodiversity conservation. Ecol Lett 12:982–998CrossRefPubMedGoogle Scholar
  57. Ross S, Munkhtsog B, Harris S (2012) Determinants of mesocarnivore range use: relative effects of prey and habitat properties on Pallas’s cat home-range size. J Mammal 93:1292–1300CrossRefGoogle Scholar
  58. Ross J et al (2015) Prionailurus bengalensis. The IUCN red list of threatened species 2015: e.T18146A50661611. Downloaded on 21 May 2016Google Scholar
  59. Salo P, Nordström M, Thomson RL, Korpimäki E (2008) Risk induced by a native top predator reduces alien mink movements. J Anim Ecol 77:1092–1098CrossRefPubMedGoogle Scholar
  60. Schipper J, Hoffmann M, Duckworth JW, Conroy J (2008) The 2008 IUCN red listings of the world’s small carnivores. Small Carniv Conserv 39:29–34Google Scholar
  61. Schoener TW (1974) Resource partitioning in ecological communities. Science 185:27–39CrossRefPubMedGoogle Scholar
  62. Schreiber A, Wirth R, Riffle M, Van Rompaey H (1989) Weasels, civets, mongooses, and their relatives: an action plan for the conservation of mustelids and viverrids. IUCN, Gland, SwitzerlandGoogle Scholar
  63. Shine R, Harlow PS, Keogh JS, Boeadi NI (1998) The influence of sex and body size on food habits of a giant tropical snake, Python reticulatus. Funct Ecol 12:248–258CrossRefGoogle Scholar
  64. Simcharoen S (2008) Ecology of the leopard (Panthera pardus Linn.) in Huai Kha Khaeng Wildlife Sanctuary. Kasetsart University, BangkokGoogle Scholar
  65. Steinmetz R, Chutipong W, Seuaturien N (2006) Collaborating to conserve large mammals in Southeast Asia. Conserv Biol 20:1391–1401CrossRefPubMedGoogle Scholar
  66. Steinmetz R, Seuaturien N, Chutipong W (2013a) Tigers, leopards, and dholes in a half-empty forest: assessing species interactions in a guild of threatened carnivores. Biol Conserv 163:68–78CrossRefGoogle Scholar
  67. Steinmetz R, Garshelis DL, Chutipong W, Seuaturien N (2013b) Foraging ecology and coexistence of Asiatic black bears and sun bears in a seasonal tropical forest in Southeast Asia. J Mammal 94:1–18CrossRefGoogle Scholar
  68. St-Pierre C, Ouellet J-P, Crête M (2006) Do competitive intraguild interactions affect space and habitat use by small carnivores in a forested landscape? Ecography 29:487–496CrossRefGoogle Scholar
  69. Sunarto S, Kelly MJ, Parakkasi K, Hutajulu MB (2015) Cat coexistence in central Sumatra: ecological characteristics, spatial and temporal overlap, and implications for management. J Zool 296:104–115CrossRefGoogle Scholar
  70. Su Su, Sale J (2007) Niche differentiation between common palm civet Paradoxurus hermaphroditus and small Indian civet Viverricula indica in regenerating degraded forest, Myanmar. Small Carniv Conserv 36:30–34Google Scholar
  71. Than Zaw et al (2008) Status and distribution of small carnivores in Myanmar. Small Carniv Conserv 38:2–28Google Scholar
  72. Thompson CM, Gese EM (2007) Food webs and intraguild predation: community interactions of a native mesocarnivore. Ecology 88:334–346CrossRefPubMedGoogle Scholar
  73. van de Bult M (2003) The vegetation and flora of the Western Forest Complex using rapid ecological assessment and vegetation type description in the WEFCOM area. Western Forest Complex Ecosystem Management Project, National Park, Wildlife and Plant Conservation Department, BangkokGoogle Scholar
  74. Walker S, Rabinowitz A (1992) The small mammal community of a dry-tropical forest in central Thailand. J Trop Ecol 8:57–71CrossRefGoogle Scholar
  75. Wang H, Fuller TK (2003) Food habits of four sympatric carnivores in southeastern China. Mammalia 67:513–519Google Scholar
  76. Wang Y, Allen ML, Wilmers CC (2015) Mesopredator spatial and temporal responses to large predators and human development in the Santa Cruz Mountains of California. Biol Conserv 190:23–33CrossRefGoogle Scholar
  77. Webb EL (2007) Botanical exploration of Thung Yai Naresuan Wildlife Sanctuary, Western Thailand. National Geographic Research and Exploration Grant (No. 6798-00). The Asian Institute of Technology, Pathum ThaniGoogle Scholar
  78. Wood BJ, Chung GF (2003) A critical review of the development of rat control in Malaysian agriculture since 1960s. Crop Prot 22:445–461CrossRefGoogle Scholar
  79. Zhou Y-B et al (2008) Dietary shifts in relation to fruit availability among masked palm civets (Paguma larvata) in central China. J Mammal 89:435–447CrossRefGoogle Scholar
  80. Zhou Y-B et al (2011) Diet of an opportunistically frugivorous carnivore, Martes flavigula, in subtropical forest. J Mammal 92:611–619CrossRefGoogle Scholar

Copyright information

© Mammal Research Institute, Polish Academy of Sciences, Białowieża, Poland 2016

Authors and Affiliations

  1. 1.Conservation Ecology ProgramKing Mongkut’s University of Technology ThonburiBangkokThailand
  2. 2.WWF ThailandBangkokThailand

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