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Predation on Lemurs in the Rainforest of Madagascar by Multiple Predator Species: Observations and Experiments

  • Sarah M. Karpanty
  • Patricia C. Wright
Chapter
Part of the Developments in Primatology: Progress and Prospects book series (DIPR)

Abstract

Predation by raptors, snakes, and carnivores is a constant risk for most wild primates (Cheney & Seyfarth, 1981; Anderson, 1986; Cheney & Wrangham, 1987; Janson & van Schaik, 1993; Cowlishaw, 1994; Isbell, 1994; Hill & Dunbar, 1998; Treves, 1999; Bearder et al., 2002; Gursky, 2002a, b; Shultz & Noë, 2002). In Madagascar, the problem may be especially severe since prosimians are the largest, most abundant and conspicuous mammals in the forest (Wright, 1998). Lemur behavior may be strongly influenced in its avoiding predation by stealthy predators, such as Henst’s goshawk (Accipiter henstii), the fossa (Cryptoprocta ferox), or the Madagascar boa constrictor (Boa manditra) (Sauther, 1989; Goodman et al., 1993a; Gould, 1996; Wright, 1998; Karpanty & Goodman, 1999; Karpanty & Grella, 2001; Fichtel & Kappeler, 2002; Goodman, 2004). Most studies of predator and prey concentrate on one taxon of predator, such as hawks or leopards (Isbell, 1990; Peres, 1990; Struhsaker & Leakey, 1990, Boesch, 1991; Shultz, 2001, 2002), while the forest reality is that an animal avoids several distinct predators simultaneously. This is certainly true in Madagascar, where day-hunting hawks and eagles hunt both sleeping nocturnal and active diurnal lemurs, and fossas and boas hunt day and night (Wright, 1998; Karpanty, 2006). Therefore, ability to develop foraging and resting strategy for risk avoidance might be a major factor in primate sociality (Janson & van Schaik, 1993; Janson & Goldsmith, 1995; Stanford, 1995).

Keywords

Predation Rate Alarm Call Playback Experiment Lemur Species Aerial Predator 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Alexander, R. (1974). The evolution of social behavior. Annu. Rev. Ecol. Syst., 5: 325–383.CrossRefGoogle Scholar
  2. Anderson, C.M. (1986). Predation and primate evolution. Primates, 27: 15–39.CrossRefGoogle Scholar
  3. Arrigo-Nelson, S.J., and Wright, P.C. (2004). Census and survey results from Ranomafana National Park: New evidence for the effects of habitat preference and disturbance on the Genus Hapalemur. Folia Primatol., 75(5): 331–334.PubMedCrossRefGoogle Scholar
  4. Balko, E., and Underwood, B. (2005) Effects of forest structure and composition on food availability for Varecia variegata at Ranomafana National Park, Madagascar. Amer. J. Primatol., 66: 45–70.CrossRefGoogle Scholar
  5. Bearder S.K., Nekaris, K.A.I., and Buzzell, A. (2002). Dangers in the night: Are some nocturnal primates afraid of the dark? In L.E. Miller (Ed.), Eat or be eaten: Predator sensitive foraging among primates (pp. 21–43). Cambridge: Cambridge Univ. Press.Google Scholar
  6. Berkelman, J. (1994). The ecology of the Madagascar buzzard Buteo brachypterus. In B. Meyburg and R. Chancellor (Eds.), Raptor conservation today (pp. 255–256). London: The Working Group on Birds of Prey and Owls.Google Scholar
  7. Boesch, C. (1991). The effects of leopard predation on grouping patterns in forest chimpanzees. Behaviour, 117: 220–242.Google Scholar
  8. Boinski, S. (1989). Birth synchrony in squirrel monkeys (Saimiri oerstedi): A strategy to reduce neonatal predation. Behav. Ecol. Sociobiol., 21: 393–400.CrossRefGoogle Scholar
  9. Cheney, D.L., and Seyfarth, R. (1981). Selective forces affecting the predator alarm calls of vervet monkeys. Behaviour, 76: 25–61.Google Scholar
  10. Cheney, D.L., and Wrangham, R.W. (1987). Predation. In B.B. Smuts, D.L. Cheney, R.M. Seyfarth, R.W. Wrangham, and T.T. Struhsaker (Eds), Primate societies (pp. 227–239). Chicago: Univ. of Chicago Press.Google Scholar
  11. Cowlishaw, G. (1994). Vulnerability to predation in baboon populations. Behaviour, 131: 293–304.Google Scholar
  12. Dollar, L., Forward, Z., and Wright, P.C. (1997). First study of Cryptoprocta ferox in the rainforests of Madagascar. Am. J. Phys. Anthro., (Suppl. 24): 102–103.Google Scholar
  13. Dollar, L. (1999). Preliminary report on the status, activity cycle, and ranging of Cryptoprocta ferox in the Malagasy rainforest, with implications for conservation. IUCN Small Carnivore Newsletter: 3–6.Google Scholar
  14. Fichtel, C., and Kappeler, P.M. (2002). Anti-predator behavior of group-living Malagasy primates: Mixed evidence for a referential alarm call system. Behav. Ecol. Sociobiology, 51: 262–275.CrossRefGoogle Scholar
  15. Ganzhorn, J.U., and Kappeler, P.M. (1996). Lemurs of the Kirindy forest. In J.U. Ganzhorn and J.P. Sorg (Eds.), Ecology and economy of a tropical dry forest in Madagascar. Primate Report, 46: 257–274.Google Scholar
  16. Garbutt, N. (1999). The mammals of Madagascar. New Haven: Yale Univ. Press.Google Scholar
  17. Goodman, S.M. (1994a). The enigma of anti-predator behavior in lemurs: Evidence of a large extinct eagle on Madagascar. Int. J. Primatol., 15: 129–134.Google Scholar
  18. Goodman, S.M. (1994b). Description of a new species of subfossil eagle from Madagascar: Stephanoatus (Aves: Falconiformes) from the deposits of Ampasambazimba. Proc. Biol. Soc. Wash., 107: 421–426.Google Scholar
  19. Goodman, S.M. (2004). Predation on lemurs. In S.M. Goodman and J. Bedstead (Eds.), The natural history of Madagascar (pp. 1221–1228). Chicago: Univ. of Chicago Press.Google Scholar
  20. Goodman, S.M., O’Connor, S., and Langrand, O. (1993a). A review of predation on lemurs: Implications for the evolution of social behavior in small, nocturnal primates. In P.M. Kappeler and J.U. Ganzhorn (Eds.), Lemur social systems and their ecological basis (pp. 51–63). New York: Plenum Press.Google Scholar
  21. Goodman, S.M., Langrand, O., and Raxworthy, C.J. (1993b). The food habits of the barn owl Tyto alba at three sites on Madagascar. Ostrich, 64: 160–171.Google Scholar
  22. Goodman, S.M., Langrand, O., and Raxworthy, C.J. (1993c). The food habits of the Madagascar long eared owl Asio madagascariensis in two habitats in southern Madagascar. Ostrich, 64: 160–171.Google Scholar
  23. Goodman, S.M., and Rakotozafy, L.M. (1995). Evidence for the existence of two species of Aquila on Madagascar during the Quaternary. Geobios, 28: 241–246.CrossRefGoogle Scholar
  24. Gould, L. (1996). Vigilance behavior during the birth and lactation season in naturally occurring ring-tailed lemurs (Lemur catta) at the Beza-Mahafaly Reserve, Madagascar. Int. J. Primatol., 17: 331–347.Google Scholar
  25. Gursky, S. (2002a). Determinants of gregariousness in the spectral tarsier (Prosimian: Tarsius spectrum). J. Zool. Lond., 256: 401–410.Google Scholar
  26. Gursky, S. (2002b). The behavioral ecology of the spectral tarsier, Tarsius spectrum. Evol. Anthropol., 11: 226–234.CrossRefGoogle Scholar
  27. Hamilton, W. (1971). Geometry for the selfish herd. J. Theor. Biol., 32: 295–311.CrossRefGoogle Scholar
  28. Hauser, M.D., and Wrangham, R.W. (1990). Recognition of predator and competitor calls in nonhuman primates and birds: A preliminary report. Ethology, 86: 116–130.CrossRefGoogle Scholar
  29. Hill, R.A., and Dunbar, R.I.M. (1998). An evaluation of the roles of predation rate and predation risk as selective pressures on primate grouping behaviour. Behaviour, 135: 411–430.Google Scholar
  30. Irwin, M.T., Johnson, S.E., and Wright, P.C. (2005). The state of lemur conservation in south-eastern Madagascar: Population and habitat assessments for diurnal and cathemeral lemurs using surveys, satellite imagery and GIS. Oryx, 39(2).Google Scholar
  31. Isbell, L. (1990). Sudden short-term increase in mortality of vervet monkeys (Cercopithecus aethiops) due to predation in Amboseli National Park, Kenya. Am. J. Primatol., 21: 41–52.CrossRefGoogle Scholar
  32. Isbell, L.A. (1994). Predation on primates: ecological patterns and evolutionary consequences. Evol. Anthropol., 61–74.Google Scholar
  33. IUCN (2005). The lemur working group report. Global Mammal Assessment. Switzerland: IUCN.Google Scholar
  34. Janson, C.H. (1992). Evolutionary ecology of primate social structure. In E.A. Smith (Ed.), Evolutionary ecology and human behavior (pp. 95–130). New York: Walter de Gruyter, Inc.Google Scholar
  35. Janson, C.H. (1998). Testing the predation hypothesis for vertebrate sociality: Prospects and pitfalls. Behaviour, 135: 389–410.Google Scholar
  36. Janson, C.H. and Goldsmith, M.L. (1995). Predicting group size in primates: Foraging costs and predation risks Behav. Ecol., 6: 326–336.CrossRefGoogle Scholar
  37. Janson, C.H., and van Schaik, C. (1993). Ecological risk aversion in juvenile primates: Slow and steady wins the race. In M.E. Pereira and L.A. Fairbanks (Eds.), Juvenile primates life history, development and behavior (pp. 57–74). Oxford: Oxford Univ. Press.Google Scholar
  38. Kappeler, P.M., and Heyman, E.W. (1996). Non-convergence in the evolution of primate life history and socioecology. Biol. J. Linn. Soc., 59: 297–326.CrossRefGoogle Scholar
  39. Karpanty, S.M. (2005). Behavioral and ecological interactions of raptors and lemurs in southeastern Madagascar: A multiple-predator approach. Doctoral dissertation. Stony Brook, New York.Google Scholar
  40. Karpanty, S.M. (2006). Direct and indirect impacts of raptor predation on lemurs in southeastern Madagascar. Int. J. Primatol., 27(1): 239–261.CrossRefGoogle Scholar
  41. Karpanty, S.M., and Goodman S.M. (1999). Diet of the Madagascar harrier-hawk, Polyboroides radiatus, in southeastern Madagascar. J. Raptor Res., 33: 313–316.Google Scholar
  42. Karpanty, S.M., and Grella, R. (2001). Lemur responses to diurnal raptor calls in Ranomafana National Park, Madagascar. Folia Primatol., 72: 100–103.PubMedCrossRefGoogle Scholar
  43. Lima, S.L. (1992). Life in a multi-predator environment: some considerations for anti-predatory vigilance. Ann. Zool. Fennici., 29: 217–226.Google Scholar
  44. 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.Google Scholar
  45. Macedonia, J.M. (1990). What is communicated in the antipredator calls of lemurs: Evidence from playback experiments with ringtailed and ruffed lemurs. Ethology, 86: 177–190.CrossRefGoogle Scholar
  46. Macedonia, J.M., and Polak, J.F. (1989). Visual assessment of avian threat in semi-captive ringtailed lemurs (Lemur catta). Behaviour, 111: 291–304.Google Scholar
  47. Matsuda, H., Abrams, P.A., and Hori, M. (1993). The effect of anti-predator behavior on exploitive competition and mutualism between predators. OIKOS, 68: 549–559.CrossRefGoogle Scholar
  48. Matsuda, H., Hori, M., and Abrams, P.A. (1994). Effects of predator-specific defence on community complexity. Evolutionary Ecology, 8: 628–638.CrossRefGoogle Scholar
  49. Matsuda, H., Hori, M., and Abrams, P.A. (1996). Effects of predator-specific defence on biodiversity and community complexity in two-trophic-level communities. Evolutionary Ecology, 10: 13–28.CrossRefGoogle Scholar
  50. Oates, J.F., Whitesides, G.H., Davies, A.F., Waterman, P.G., Green, S.M., Dasilva, G.L., and Mole, S. (1990). Determinants of variation in tropical forest primate biomass: New evidence from West Africa. Ecology, 71: 328–343.CrossRefGoogle Scholar
  51. Overdorff, D.J. (1996). Ecological correlates to social structure in two lemur species in Madagascar. Am. J. Phys. Anthro., 100: 487–506.CrossRefGoogle Scholar
  52. Overdorff, D.J., and Strait, S.G. (1995). Life history and predation in Eulemur rubriventer in Madagascar. Am. J. Phys. Anthro., 20: 164–165.Google Scholar
  53. Overdorff, D.J., Merenlender, A.M., Talata, P., Telo, A., and Forward Z.A. (1999). Life history of Eulemur fulvus rufus from 1988-1998 in southeastern Madagascar. Am. J. Phys. Anthropol., 108: 295–310.PubMedCrossRefGoogle Scholar
  54. Peres, C.A. (1990). A harpy eagle successfully captures an adult male red howler monkey. Wilson Bull., 102: 560–561.Google Scholar
  55. Peres, C.A. (1993). Structure and spatial organization of an Amazonian terre firme primate community. J. Trop. Ecol., 9: 259–276.CrossRefGoogle Scholar
  56. Pochron, S.T., Tucker, T., and Wright, P.C. (2004). Demography, life history, and social structure in Propithecus diadema edwardsi from 1986-2000 in Ranomafana National Park, Madagascar. Amer. J. Phys. Anthro., 125(1): 61–72.CrossRefGoogle Scholar
  57. Porter, L. (1998). Influences on the distribution of Lepilemur microdon in Ranomafana National Park, Madagascar. Folia Primatol., 69: 172–176.CrossRefGoogle Scholar
  58. Pulliam, H.R., and Caraco, T. (1984). Living in groups: Is there an optimal group size? In J.R. Krebs and N.B. Davies (Eds), Behavioral ecology: An evolutionary approach (pp. 122–147). Sunderland: Sinauer.Google Scholar
  59. Sauther, M.L. (1989). Antipredator behavior in troops of free-ranging Lemur catta at Beza Mahafaly Special Reserve, Madagascar. Int. J. Primatol., 10: 595–606.Google Scholar
  60. Shultz, S. (2001). Interactions between crowned eagles and monkeys in Taï National Park, Ivory Coast. Folia Primatol., 72: 248–250.PubMedCrossRefGoogle Scholar
  61. Shultz, S. (2002). Crowned eagle population density, diet, and behavior in the Taï National Park, Ivory Coast. Ibis, 144: 135–138.CrossRefGoogle Scholar
  62. Shultz, S., and Noë, R. ((2002). The consequences of crowned eagle central-place foraging on predation risk in monkeys. Proc. Roy. Soc. Lond., 269: 1797–1802.CrossRefGoogle Scholar
  63. Sih, A., Englund G., and Wooster, D. (1998). Emergent impacts of multiple predators on prey. Trends Ecol. and Evol., 13(9): 350–355.CrossRefGoogle Scholar
  64. Simons, E.L. (1997). Lemurs: Old and new. In S.M. Goodman and B.D. Patterson (Eds.), Natural change and human impact in Madagascar (pp. 142–166). Washington, DC: Smithsonian Institution Press.Google Scholar
  65. Stanford, C.B. (1995). The influence of chimpanzee predation on group size and anti-predator behaviour in red colobus monkeys. Anim. Behav., 49: 577–587.Google Scholar
  66. Struhsaker, T., and Leakey, M. (1990). Prey selectivity by crowned hawk-eagles on monkeys in the Kibale Forest, Uganda. Behav. Ecol. Sociobiol., 26: 435–443.CrossRefGoogle Scholar
  67. Tan, C.L. (1999). Group composition, home range size and diet of three sympatric bamboo lemurs (genus Hapalemur) in Ranomafana National Park, Madagascar. Int. J. Primatol., 20: 547–566.CrossRefGoogle Scholar
  68. Terborgh, J. (1983). Five New World primates. Princeton, NJ: Princeton Univ. Press.Google Scholar
  69. Terborgh, J., and Janson, C.H. (1986). The socioecology of primate groups. Ann. Rev. Ecol. System., 17: 111–135.CrossRefGoogle Scholar
  70. Treves, A. (1999). Has predation shaped the social systems of arboreal primates? Int. J. Primatol., 20: 35–67.CrossRefGoogle Scholar
  71. van Schaik, C.P. (1983). Why are diurnal primates living in groups? Behaviour, 87: 120–144.Google Scholar
  72. van Schaik, C.P., and van Hooff, J.A.R.A.M. (1983). On the ultimate causes of primate social systems. Behaviour, 85: 91–117.Google Scholar
  73. van Schaik, C.P., and Kappeler, P.M. (1993). Life history, activity period and lemur social systems. In P.M. Kappeler and J.U. Ganzhorn (Eds.), Lemur social systems and their ecological basis (pp. 241–260). New York: Plenum Press.Google Scholar
  74. van Schaik, C.P., and Kappeler, P.M. (1996). The social systems of gregarious lemurs: Lack of convergence with anthropoids due to evolutionary disequilibrium? Ethology, 102: 915–941.CrossRefGoogle Scholar
  75. Vine, I. (1973). Detection of prey flocks by predators. J. Theor. Biol., 40: 207–210.PubMedCrossRefGoogle Scholar
  76. Watson, R., and Lewis, R. (1994). Raptor studies in Madagascar’s rain forest. In B.U. Meyberg and R. Chancellor (Eds.), Raptor conservation today (pp. 283–290). London: World Working Group on Birds of Prey and Owls.Google Scholar
  77. White, L.J.T. (1994). Biomass of rain forest mammals in the Lope Reserve, Gabon. J. An. Ecol., 63: 499–512.CrossRefGoogle Scholar
  78. Wright, P.C. (1989). The nocturnal primate niche in the new world. J. Hum. Evol., 8: 635–658.CrossRefGoogle Scholar
  79. Wright, P.C. (1992). Primate ecology, rainforest conservation, and economic development: Building a national park in Madagascar. Evol. Anthropol., 1: 25–33.CrossRefGoogle Scholar
  80. Wright, P.C. (1994). Behavior and ecology of the owl monkey in the wild. In J.F. Baer, R.E. Weller, and I. Kakoma (Eds.), Aotus: The owl monkey (pp. 97–112). San Diego: Academic Press.Google Scholar
  81. Wright, P.C. (1995). Demography and life history of free-ranging Propithecus diadema edwardsi in Ranomafana National Park, Madagascar. Int. J. Primatol., 16: 835–853.Google Scholar
  82. Wright, P.C. (1997). The future of biodiversity in Madagascar A view from Ranomafana National Park. In S.M. Goodman and B.D. Patterson (Eds.), Natural change and human impact in Madagascar (pp. 381–405). Washington, DC: Smithsonian Institution Press.Google Scholar
  83. Wright, P.C. (1998). Impact of predation risk on the behaviour of Propithecus diadema edwardsi in the rain forest of Madagascar. Behaviour, 135: 483–512.Google Scholar
  84. Wright, P.C. (1999). Lemur traits and Madagascar ecology: Coping with an island environment. Yearbook Phys. Anthropology, 42: 31–72.CrossRefGoogle Scholar
  85. Wright, P.C., and Martin, L.B. (1995). Predation, pollination and torpor in two nocturnal primates: Cheirogaleus major and Microcebus rufus in the rain forest of Madagascar. In L. Alterman, M.K. Izard, and G. Doyle (Eds.), Creatures of the dark: The nocturnal prosimians (pp. 45–60). New York: Plenum Press.Google Scholar
  86. Wright, P.C., Heckscher, S.K., and Dunham, A.E. (1997). Predation on Milne-Edwards’ sifaka (Propithecus diadema edwardsi) by the fossa (Cryptoprocta ferox) in the rain forest of southeastern Madagascar. Folia Primatol., 97: 34–43.CrossRefGoogle Scholar
  87. Wright, P.C., and Andriamihaja, B. (2004). Making a rain forest national park work in Madagascar: Ranomafana National Park and its long-term research commitment. In J. Terborgh, C. van Schaik, L. Davenport, and M. Rao (Eds.), Making parks work: Strategies for preserving tropical nature (pp. 112–136). Covelo, CA: Island Press.Google Scholar
  88. Wright, P.C. Razafindratsita V., Pochron, S.T. and Jernvall, J.J. (2005). The key to Madagascar frugivores. In J.L. Dew and H. Boubli (Eds.), Tropical fruits and frugivores: Strong interactors (pp. 1–18). New York: Springer Press.Google Scholar
  89. Zuberbühler, K., Jenny, D., and Bshary R. ((1999). The predator deterrence function of primate alarm calls. Ethology, 105: 477–490.Google Scholar

Copyright information

© Springer Science+Business Media, LLC 2007

Authors and Affiliations

  • Sarah M. Karpanty
    • 1
  • Patricia C. Wright
    • 2
  1. 1.Department of Fisheries and Wildlife ScienceVirginia Polytechnic Institute and State University BlacksburgUSA
  2. 2.Institute for the Conservation, Tropical EnvironmentsSUNY-Stony BrookStony BrookUSA

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