Neighboring groups and habitat edges modulate range use in Phayre’s leaf monkeys (Trachypithecus phayrei crepusculus)

Abstract

An animal’s use of space may be strongly influenced by habitat edges and neighboring conspecifics encountered in and around its home range. Habitat edges are known to affect species density and distribution, but their impact on home range use is largely unknown. Additionally, among large animals, interactions with neighbors become particularly important as increasing home range size leads to decreasing exclusivity of resource use, but the effect of neighbors on home range use remains poorly understood. Here, we examine the influence of neighbors and habitat edges on the ranging patterns of three groups of Phayre’s leaf monkeys (Trachypithecus phayrei crepusculus) in northeast Thailand over a period of more than 2 years. The study animals occupied dry evergreen forest, and adjacent patches of dry dipterocarp forest created a habitat edge and formed barriers between some groups. We found that the use of home range interiors was 50–90% higher than the border areas, indicating concentrated use of resources within the home range. The use of peripheral areas was influenced by social organization, the presence of neighboring groups, and forest edges. While one multimale group showed no particular habitat preference, two single-male groups preferred areas bordering dry dipterocarp habitat and avoided areas bordering neighboring groups, suggesting that the threat of neighbors mediated border presence. Additionally, groups may have been attracted to the forest edge, where conspecific competitors are absent and increased sunlight may increase resource abundance and/or quality. This study revealed that the use of border areas can be modulated by neighboring groups and habitat edges, thereby adding to our understanding of home range use among territorial species in heterogeneous habitats.

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References

  1. Barrett L, Lowen CB (1998) Random walks and the gas model: spacing behaviour of grey-cheeked mangabeys. Funct Ecol 12:857–865. doi:10.1046/j.1365-2435.1998.00261.x

    Article  Google Scholar 

  2. Bauchop T, Martucci RW (1968) Ruminant like digestion of the langur monkey. Science 161:698–700. doi:10.1126/science.161.3842.698

    PubMed  Article  CAS  Google Scholar 

  3. Borries C, Larney E, Kreetiyutanont K, Koenig A (2002) The diurnal primate community in a dry evergreen forest in Phu Khieo Wildlife Sanctuary, northeast Thailand. Nat Hist Bull Siam Soc 50:75–88

    Google Scholar 

  4. Borries C, Larney E, Derby AM, Koenig A (2004) Temporary absence and dispersal in Phayre’s leaf monkeys (Trachypithecus phayrei). Folia Primatol 75:27–30. doi:10.1159/000073428

    PubMed  Article  Google Scholar 

  5. Borries C, Lu A, Ossi-Lupo K, Larney E, Koenig A (2011) Primate life histories and dietary adaptations: a comparison of Asian colobines and macaques. Am J Phys Anthropol 144:286–299. doi:10.1002/ajpa.21403

    PubMed  Article  Google Scholar 

  6. Carl KM (2009) Home range size, daily path length, and territoriality in Phayre's leaf monkeys (Trachypithecus phayrei). MA thesis, Stony Brook University

  7. Chapman CA (1990) Association patterns of spider monkeys: the influence of ecology and sex on social organization. Behav Ecol Sociobiol 26:409–414. doi:10.1007/BF00170898

    Article  Google Scholar 

  8. Chapman CA, Chapman LJ, McLaughlin RL (1989) Multiple central place foraging by spider monkeys—travel consequences of using many sleeping sites. Oecologia 79:506–511. doi:10.1007/BF00378668

    Article  Google Scholar 

  9. Crofoot MC, Gilby IC, Wikelski MC, Kays RW (2008) Interaction location outweighs the competitive advantage of numerical superiority in Cebus capucinus intergroup contests. P Natl Acad Sci USA 105:577–581. doi:10.1073/pnas.0707749105

    Article  CAS  Google Scholar 

  10. Curtin SH (1980) Dusky and banded leaf monkeys. In: Chivers DJ (ed) Malayan forest primates. Ten years in tropical rain forest. Plenum Press, New York, pp 107–145

    Google Scholar 

  11. Curtin SH, Chivers DJ (1978) Leaf-eating primates of Peninsular Malaysia: the siamang and the dusky leaf-monkey. In: Montgomery GG (ed) The ecology of arboreal folivores. Smithsonian Institution Press, Washington, pp 441–464

    Google Scholar 

  12. Damuth J (1981a) Home range overlap and species energy use among herbivorous mammals. Biol J Linn Soc 15:185–194. doi:10.1111/j.1095-8312.1981.tb00758.x

    Article  Google Scholar 

  13. Damuth J (1981b) Population density and body size in mammals. Nature 290:699–700. doi:10.1038/290699a0

    Article  Google Scholar 

  14. Desrochers A, Fortin MJ (2000) Understanding avian responses to forest boundaries: a case study with chickadee winter flocks. Oikos 91:376–384. doi:10.1034/j.1600-0706.2000.910218.x

    Article  Google Scholar 

  15. Di Bitetti MS (2001) Home-range use by the tufted capuchin monkey (Cebus apella nigritus) in a subtropical rainforest of Argentina. J Zool 253:33–45. doi:10.1017/S0952836901000048

    Article  Google Scholar 

  16. Duelli P, Studer M, Marchand I, Jakob S (1990) Population-movements of arthropods between natural and cultivated areas. Biol Conserv 54:193–207. doi:10.1016/0006-3207(90)90051-P

    Article  Google Scholar 

  17. Eason PK, Cobbs GA, Trinca KG (1999) The use of landmarks to define territorial boundaries. Anim Behav 58:85–91. doi:10.1006/anbe.1999.1133

    PubMed  Article  Google Scholar 

  18. Fisher J (1954) Evolution and bird sociality. In: Huxley J, Hardy AC, Ford EB (eds) Evolution as a process. Allen and Unwin, London, pp 71–83

    Google Scholar 

  19. Ganey JL, Balda RP (1989) Home-range characteristics of spotted owls in Northern Arizona. J Wildl Manage 53:1159–1165

    Article  Google Scholar 

  20. Ganzhorn JU (1995) Low-level forest disturbance effects on primary production, leaf chemistry, and lemur populations. Ecology 76:2084–2096. doi:10.2307/1941683

    Article  Google Scholar 

  21. Goosem M (2000) Effects of tropical rainforest roads on small mammals: edge changes in community composition. Wildl Res 27:151–163. doi:10.1071/WR98091

    Article  Google Scholar 

  22. Gorman ML, Stone RD (1990) Mutual avoidance by European moles Talpa europaea. In: MacDonald DW, Müller-Schwarze D, Natynczuk SE (eds) Chemical signals in vertebrates 5. Oxford University Press, New York, pp 367–377

    Google Scholar 

  23. Grassman LI, Tewes ME, Silvy NJ, Kreetiyutanont K (2005) Spatial organization and diet of the leopard cat (Prionailurus bengalensis) in north-central Thailand. J Zool 266:45–54. doi:10.1017/S095283690500659X

    Article  Google Scholar 

  24. Guerra-Castro E, Carmona-Suárez CA, Conde JE (2007) Activity patterns and zonation of the swimming crabs Arenaeus cribrarius and Callinectes ornatus. J Crustac Biol 27:49–58. doi:10.1651/S-2651.1

    Article  Google Scholar 

  25. Hamilton MJ, Milne BT, Walker RS, Brown JH (2007) Nonlinear scaling of space use in human hunter-gatherers. P Natl Acad Sci USA 104:4765–4769. doi:10.1073/pnas.0611197104

    Article  CAS  Google Scholar 

  26. Haynes KJ, Cronin JT (2006) Interpatch movement and edge effects: the role of behavioral responses to the landscape matrix. Oikos 113:43–54. doi:10.1111/j.0030-1299.2006.13977.x

    Article  Google Scholar 

  27. Herbinger I (2004) Inter-group aggression in wild West African chimpanzees (Pan troglodytes verus): mechanisms and functions. Ph.D. thesis, University of Leipzig, Leipzig

  28. Herbinger I, Boesch C, Rothe H (2001) Territory characteristics among three neighboring chimpanzee communities in the Taï National Park, Cote d’Ivoire. Int J Primatol 22:143–167

    Article  Google Scholar 

  29. Hooge PN, Eichenlaub B (2000) Animal movement extension to ArcView, version 2.0. Alaska Science Center—Biological Science Office, U.S. Geological Survey, Anchorage, AK

  30. Hutchinson JMC, Waser PM (2007) Use, misuse and extensions of “ideal gas” models of animal encounter. Biol Rev 82:335–359. doi:10.1111/j.1469-185X.2007.00014.x

    PubMed  Article  Google Scholar 

  31. Ims RA (1988) Spatial clumping of sexually receptive females induces space sharing among male voles. Nature 335:541–543. doi:10.1038/335541a0

    PubMed  Article  CAS  Google Scholar 

  32. Jetz W, Carbone C, Fulford J, Brown JH (2004) The scaling of animal space use. Science 306:266–268. doi:10.1126/science.1102138

    PubMed  Article  CAS  Google Scholar 

  33. Kelly RC (2005) The evolution of lethal intergroup violence. P Natl Acad Sci USA 102:15294–15298. doi:10.1073/pnas.0505955102

    Article  CAS  Google Scholar 

  34. Kelt DA, Van Vuren DH (2001) The ecology and macroecology of mammalian home range area. Am Nat 157:637–645

    PubMed  Article  CAS  Google Scholar 

  35. Kitchen DM (2004) Alpha male black howler monkey responses to loud calls: effect of numeric odds, male companion behaviour and reproductive investment. Anim Behav 67:125–139. doi:10.1016/j.anbehav.2003.03.007

    Article  Google Scholar 

  36. Kitchen DM, Cheney DL, Seyfarth RM (2004) Factors mediating inter-group encounters in savannah baboons (Papio cynocephalus ursinus). Behaviour 141:197–218. doi:10.1163/156853904322890816

    Article  Google Scholar 

  37. Koenig A, Borries C (2012) Social organization and male residence patterns in Phayre’s leaf monkeys. In: Kappeler PM, Watts DP (eds) Long-term field studies of primates. Springer, Berlin. doi:10.1007/978-3-642-22514-7_10

    Google Scholar 

  38. Koenig A, Larney E, Lu A, Borries C (2004) Agonistic behavior and dominance relationships in female Phayre’s leaf monkeys—preliminary results. Am J Primatol 64:351–357. doi:10.1002/ajp. 20084

    PubMed  Article  Google Scholar 

  39. Lambert TD, Malcolm JR, Zimmerman BL (2006) Amazonian small mammal abundances in relation to habitat structure and resource abundance. J Mammal 87:766–776

    Article  Google Scholar 

  40. Laundre JW, Loxterman J (2007) Impact of edge habitat on summer home range size in female pumas. Am Midl Nat 157:221–229. doi:10.1674/0003-0031(2007) 157[221:IOEHOS]2.0.CO;2

    Article  Google Scholar 

  41. Laurance WF, Lovejoy TE, Vasconcelos HL, Bruna EM, Didham RK, Stouffer PC, Gascon C, Bierregaard RO, Laurance SG, Sampaio E (2002) Ecosystem decay of Amazonian forest fragments: a 22-year investigation. Cons Biol 16:605–618. doi:10.1046/j.1523-1739.2002.01025.x

    Article  Google Scholar 

  42. Lehman SM, Rajaonson A, Day S (2006) Lemur responses to edge effects in the Vohibola III Classified Forest, Madagascar. Am J Primatol 68:293–299. doi:10.1002/ajp.20224

    PubMed  Article  Google Scholar 

  43. Lidicker WZJ (1999) Responses of mammals to habitat edges: an overview. Landsc Ecol 14:333–343. doi:10.1023/A:1008056817939

    Article  Google Scholar 

  44. Lima SL, Zollner PA (1996) Towards a behavioral ecology of ecological landscapes. Trends Ecol Evol 11:131–135. doi:10.1016/0169-5347(96)81094-9

    PubMed  Article  CAS  Google Scholar 

  45. Malcolm JR (1997) Biomass and diversity of small mammals in Amazonian forest fragments. In: Laurance WF, Bierregaard RO (eds) Tropical forest fragments: ecology, management, and conservation of fragmented communities. University of Chicago Press, Chicago, pp 207–222

    Google Scholar 

  46. Malcolm JR, Ray JC (2000) Influence of timber extraction routes on central African small-mammal communities, forest structure, and tree diversity. Cons Biol 14:1623–1638. doi:10.1111/j.1523-1739.2000.99070.x

    Article  Google Scholar 

  47. McNab (1963) Bioenergetics and the determination of home range size. Am Nat 97:133–140

    Article  Google Scholar 

  48. Mech LD, Harper EK (2002) Differential use of a wolf, Canis lupus, pack territory edge and core. Can Field Nat 116:315–316

    Google Scholar 

  49. Mitani JC, Watts DP, Amsler SJ (2010) Lethal intergroup aggression leads to territorial expansion in wild chimpanzees. Curr Biol 20:R507–R508. doi:10.1016/j.cub.2010.04.021

    PubMed  Article  CAS  Google Scholar 

  50. Mitchell MS, Powell RA (2004) A mechanistic home range model for optimal use of spatially distributed resources. Ecol Model 177:209–232. doi:10.1016/j.ecolmodel.2004.01.015

    Article  Google Scholar 

  51. Müller CA, Manser MB (2007) “Nasty neighbours” rather than “dear enemies” in a social carnivore. P Roy Soc B 274:959–965. doi:10.1098/rspb.2006.0222

    Article  Google Scholar 

  52. Nievergelt CM, Mutschler T, Feistner ATC (1998) Group encounters and territoriality in wild Alaotran gentle lemurs (Hapalemur griseus alaotrensis). Am J Primatol 46:251–258. doi:10.1002/(SICI)1098-2345(1998) 46:3<251::AID-AJP5>3.0.CO;2-H

    PubMed  Article  CAS  Google Scholar 

  53. Nunn CL, Barton RA (2000) Allometric slopes and independent contrasts: a comparative test of Kleiber’s law in primate ranging patterns. Am Nat 156:519–533

    Article  Google Scholar 

  54. Nunn CL, Dokey AT-W (2006) Territoriality and parasitism in primates. Biol Lett 2:351–354. doi:10.1098/rsbl.2006.0485

    PubMed  Article  Google Scholar 

  55. Onderdonk DA, Chapman CA (2000) Coping with forest fragmentation: the primates of Kibale National Park, Uganda. Int J Primatol 21:587–611. doi:10.1023/A:1005509119693

    Article  Google Scholar 

  56. Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge

    Google Scholar 

  57. R Development Core Team (2010) The R Project for Statistical Computing, version 2.11.1. Available at http://www.R-project.org

  58. Samson C, Huot J (2001) Spatial and temporal interactions between female American black bears in mixed forests of eastern Canada. Can J Zool 79:633–641. doi:10.1139/cjz-79-4-633

    Article  Google Scholar 

  59. Shillito JF (1963) Observations on the range and movements of a woodland population of the common shrew Sorex araneus L. Proc Zool Soc Lond 140:533–546. doi:10.1111/j.1469-7998.1963.tb01872.x

    Google Scholar 

  60. Sih A, Mateo J (2001) Punishment and persistence pay: a new model of territory establishment and space use. Trends Ecol Evol 16:477–479. doi:10.1016/S0169-5347(01)02251-0

    Article  Google Scholar 

  61. Smith RJ, Jungers WL (1997) Body mass in comparative primatology. J Hum Evol 32:523–559. doi:10.1006/jhev.1996.0122

    PubMed  Article  CAS  Google Scholar 

  62. Sokal RR, Rohlf FJ (1995) Biometry, 3rd edn. WH Freeman, New York

    Google Scholar 

  63. Stamps JA, Krishnan VV (2001) How territorial animals compete for divisible space: a learning-based model with unequal competitors. Am Nat 157:154–169

    PubMed  Article  CAS  Google Scholar 

  64. Stamps JA, Buechner M, Krishnan VV (1987) The effects of edge permeability and habitat geometry on emigration from patches of habitat. Am Nat 129:533–552

    Article  Google Scholar 

  65. Tabachnick BG, Fidell LS (2001) Using multivariate statistics, 4th edn. Allyn and Bacon, Boston

    Google Scholar 

  66. Temeles EJ (1994) The role of neighbors in territorial systems—when are they dear enemies? Anim Behav 47:339–350. doi:10.1006/anbe.1994.1047

    Article  Google Scholar 

  67. Terborgh J (1983) Five new world primates. A study in comparative ecology. Princeton University Press, Princeton

    Google Scholar 

  68. Waser PM (1976) Cercocebus albigena—site attachment, avoidance, and intergroup spacing. Am Nat 110:911–935

    Article  Google Scholar 

  69. Wilson EO (1975) Sociobiology, the new synthesis. Harvard University Press, Cambridge

    Google Scholar 

  70. Wilson ML, Hauser MD, Wrangham RW (2001) Does participation in intergroup conflict depend on numerical assessment, range location, or rank for wild chimpanzees? Anim Behav 61:1203–1216. doi:10.1006/anbe.2000.1706

    Article  Google Scholar 

  71. Wilson ML, Britton NF, Franks NR (2002) Chimpanzees and the mathematics of battle. P Roy Soc B 269:1107–1112. doi:10.1098/rspb.2001.1926

    Article  Google Scholar 

  72. Worton BJ (1989) Kernel methods for estimating the utilization distribution in home-range studies. Ecology 70:164–168. doi:10.2307/1938423

    Article  Google Scholar 

  73. Wrangham R, Crofoot M, Lundy R, Gilby I (2007) Use of overlap zones among group-living primates: a test of the risk hypothesis. Behaviour 144:1599–1619. doi:10.1163/156853907782512092

    Article  Google Scholar 

  74. Ydenberg RC, Giraldeau LA, Falls JB (1988) Neighbors, strangers, and the asymmetric war of attrition. Anim Behav 36:343–347. doi:10.1016/S0003-3472(88)80004-6

    Article  Google Scholar 

  75. Zhang S (1995) Sleeping habits of brown capuchin monkeys (Cebus paella) in French Guiana. Am J Primatol 36:327–335. doi:10.1002/ajp.1350360407

    Article  Google Scholar 

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Acknowledgments

We would like to thank the National Research Council of Thailand (NRCT) and the Department of National Parks, Wildlife and Plant Conservation (DNP) for the permission to conduct this study. We gratefully acknowledge the cooperation and guidance by Jarupol Prabnasuk, Kanjana Nitaya, and Kitti Kreetiyutanont (Phu Khieo Wildlife Sanctuary), Naris Bhumpakphan and Wichan Eiadthong (Kasetsart University), and Warren Brockelman (Mahidol University). For the help with data collection, we would like to thank Carola Borries, Amnoi Bprasapmu, Surachest Dtubpraserit, Eileen Larney, Emily Lloyd, Amy Lu, the late Wichian Natongbo, Guillaume Pages, Scott Suarez, Amphon Suyanang, Pia Terranova, Tara Whitty, and Araya Yamee. We are thankful for the helpful comments and suggestions on the manuscript by Carola Borries, Tara Whitty, Hamish Wilman, the three anonymous reviewers, and the Associate Editor David Watts. The project was financially supported by NSF (BCS-0215542 and BCS-0542035) and approved by Stony Brook University’s IACUC (IDs: 20031120–20061120). All work reported here was non-invasive and complied with the laws of Thailand and the USA.

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Gibson, L., Koenig, A. Neighboring groups and habitat edges modulate range use in Phayre’s leaf monkeys (Trachypithecus phayrei crepusculus). Behav Ecol Sociobiol 66, 633–643 (2012). https://doi.org/10.1007/s00265-011-1311-2

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Keywords

  • Edge effects
  • Home range use
  • Neighbor avoidance
  • Territory borders