International Journal of Primatology

, Volume 23, Issue 3, pp 677–693

Sex Differences in Feeding, Height, and Space Use in Hapalemur griseus

  • Christina Grassi
Article
  • 141 Downloads

Abstract

I investigated sex differences in feeding ecology in a wild group of Hapalemur griseus, gray bamboo lemur, in southeastern Madagascar. Males and females differed in daily dietary diversity, height use while feeding, and spatial position within the group. Based on all-occurrences of feeding bouts and 15-min point samples, the adult female had significantly higher daily dietary diversity indices than those of males. The female also fed at significantly lower heights than the males did. There are also significant differences between age classes with the subadult male exhibiting the lowest dietary diversity and feeding at the greatest heights. During feeding, the female stayed in closest proximity to both juveniles, whereas adult males were peripheral. In contrast, the males moved closer in proximity to the female when resting and traveling. These sex differences could be explained 1) by the metabolic cost of reproduction for females, 2) as strategies to mitigate the cost of feeding competition between males and females, 3) by male role performance as a predator detector, and 4) by different social priorities of males and females.

Hapalemur griseus feeding ecology reproductive physiology spatial relations age differences 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

REFERENCES

  1. Altmann, J. (1980). Baboon Mothers and Infants, Harvard University Press, Cambridge.Google Scholar
  2. Ancrenaz, M., Lackman-Ancrenaz, I., and Mundy, N. (1994). Field observations of aye-ayes (Daubentonia madagascariensis) in Madagascar. Folia Primatol. 62: 22–36.Google Scholar
  3. Baldellou, M., and Henzi, S. (1992). Vigilance, predator detection and the presence of supernumary males in vervet monkey troops. Anim. Behav. 43: 451–461.Google Scholar
  4. Berkovitch, F. (1987). Female weight and reproductive condition in a population of olive baboons. Am. J. Primatol. 12: 189–195.Google Scholar
  5. Boesch, C., and Boesch, H. (1990).Tool use and tool making in wild chimpanzees.Folia Primatol. 54: 86–99.Google Scholar
  6. Boinski, S. (1988). Sex differences in the foraging behavior of squirrel monkeys in a seasonal habitat. Behav. Ecol. Sociobiol. 23: 177–186.Google Scholar
  7. Byrne, R.W., and Byrne, J.M. (1993). Complex leaf-gathering skills of mountain gorillas (Gorilla g. beringei): Variability and standardization. Am. J. Primatol. 31: 241–261.Google Scholar
  8. Byrne, R. W., Whiten, A., Henzi, S. P., and McCulloch, F. N. (1993). Nutritional constraints on mountain baboons (Papio urninus): Implications for baboon socioecology. Behav. Ecol. Sociobiol. 33: 233–246.Google Scholar
  9. Chapman, C. A. (1987). Flexibility in the diets of three species of neotropical species of Costa Rican primate. Folia Primatol. 49: 90–115.Google Scholar
  10. Clutton-Brock, T. H. (1977). Some aspects of intraspecific variation in feeding and ranging behavior in Primates. In Clutton-Brock, T. H. (ed.), Primate Ecology: Studies of Feeding and Ranging Behavior in Lemurs, Monkeys and Apes, Academic Press, London, pp. 539–556.Google Scholar
  11. Clutton-Brock, T. H., and Harvey, P. (1977). Species differences in feeding and ranging behavior in Primates. In Clutton-Brock, T. H. (ed.), Primate Ecology: Studies of Feeding and Ranging Behavior in Lemurs, Monkeys and Apes, Academic Press, London, pp. 557–584.Google Scholar
  12. Cords, M. (1995). Predator vigilance costs of allogrooming in wild blue monkeys. Behaviour 132: 559–569.Google Scholar
  13. Cowlishaw, G. (1994). Behavioural patterns in baboon group encounters: The role of resource competition and male reproductive strategies. Behaviour 132: 75–86.Google Scholar
  14. Dasilva, G. L. (1992). The western black-and-white colobus as a low energy strategist: Activity budgets, energy expenditure and energy intake. J. Anim. Ecol. 61: 79–91.Google Scholar
  15. Erhart, B. E., and Overdorff, D. J. (1998). Group leadership and feeding priority in wild Propithecus diadema edwardsi and Eulemur fulvus rufus. Am. J. Primatol. 45: 178–179.Google Scholar
  16. Fedigan, L. M., and Baxter, M. J. (1984). Sex differences and social organization in free-ranging spider monkeys (Ateles geoffroyi). Primates 25: 279–294.Google Scholar
  17. Fossey, D., and Harcourt, A. H. (1977). Feeding ecology of free-ranging mountain gorilla (Gorilla gorilla beringei). In Clutton-Brock, T. H. (ed.), Primate Ecology: Studies of Feeding and Ranging Behavior in Lemurs, Monkeys and Apes, Academic Press, London, pp. 415–447.Google Scholar
  18. Fragazy, D.M. (1986). Time budgets and foraging behavior in wedge-capped capuchins (Cebus olivaceus): Age and sex differences. In Taub, D. M., and King, F. A. (eds.), Current Perspectives in Primate Social Dynamics, Van Nostrand Reinhold, New York, pp. 159–174.Google Scholar
  19. Gaulin, S. J., and Sailer, L. D. (1985). Are females the ecological sex? Am. Anthropol. 87: 111–119.Google Scholar
  20. Gautier-Hion, A. (1980). Seasonal variation of diet related to species and sex in a community of Cercopithecus monkeys. J. Anim. Ecol. 49: 237–269.Google Scholar
  21. Ghiglieri, M. P. (1984). The Chimpanzees of Kibale Forest, Columbia University Press, New York.Google Scholar
  22. Gould, L. (1996). Vigilance behaviour during the birth and lactation seasona in naturally occurring ring-tailed lemurs (Lemur catta) at the Beza-Mahafaly Reserve, Madagascar. Int. J. Primatol. 17: 331–354.Google Scholar
  23. Grassi, C. (1997). The feeding ecology of the gentle gray bamboo lemur, Hapalemur griseus, in Southeastern Madagascar, Masters Thesis, The University of Texas at Austin, Austin, TX.Google Scholar
  24. Harrison, M. J. (1983). Age and sex differences in the diet and feeding strategies of the green monkey, Cercopithecus sabaeus. Anim. Behav. 31: 969–977.Google Scholar
  25. Hemingway, C. A. (1995). Feeding and reproductive strategies of the Milne-Edward's Sifaka, Propithecus diadema edwardsi, PhD Dissertation, Duke Univerisity, Durham, NC.Google Scholar
  26. Hiraiwa-Hasegawa, M. (1989). Sex differences in the behavioral development of chimpanzees at Mahale. In Heltne, P. G., and Marquardt, L. A. (eds.), Understanding Chimpanzees. Cambridge University Press, Cambridge, pp. 104–115.Google Scholar
  27. Isbell, L. A., and Young, T. P. (1993). Social and ecological influences on activity budgeta of vervet monkeys and their implications for group living. Behav. Ecol. Sociobiol. 32: 377–385.Google Scholar
  28. Janson, C. (1990a). Social correlates of individual spatial choice in foraging groups of brown capuchin monkeys, Cebus apella. Anim. Behav. 40: 910–921.Google Scholar
  29. Janson, C. (1990b). Ecological consequences of individual space choice in foraging groups of brown capuchin monkeys, Cebus apella. Anim. Behav. 40: 922–934.Google Scholar
  30. Jolly, A. (1984). The puzzle of female feeding priority. In Small, M. E. (ed.), Female Primates: Studies by Women Primatologists, Alan R. Liss, New York, pp. 197–215.Google Scholar
  31. Kappeler, P. M. (1996). Causes and consequences of life-history variation among Strepsirhine primates. Am. Nat. 148: 868–891.Google Scholar
  32. Kappeler, P. M., and Heymann, E.W. (1996). Nonconvergence in the evolution of primate life history and socio-ecology. Biol. J. Linn. Soc. 59: 297–326.Google Scholar
  33. Kubzdela, K. S., Richard, A. F., and Pereira, M. (1992). Social relations in semi-free-ranging sifakas (Propithecus verreauxi coquereli) and the question of female dominance. Am. J. Primatol. 28: 139–145.Google Scholar
  34. Lawes, M. J., and Henzi, S. P. (1995). Inter-group encounters in blue monkeys: How territorial must a territorial species be? Anim. Behav. 49: 239–242.Google Scholar
  35. Lawes, M. J., and Piper, S. E. (1992). Activity patterns in free-ranging Samango monkeys (Cercopithecus mitis erythrarcus Peters, 1852) at the southern range limit. Folia Primatol. 59: 186–202.Google Scholar
  36. Leighton, D. R. (1987). Gibbons: Territoriality and monogamy. In Smuts, B. B., Cheney, D. L., Seyfarth, R., Wrangham, R., and Struhsaker, T. (eds.), Primate Societies, University of Chicago Press, Chicago, pp. 135–145.Google Scholar
  37. Mittermeier, R. A., Tattersall, I., Konstant, W., Meyers, D., and Mast, R. (1994). Lemurs of Madagascar, Conservation International, Washington, DC.Google Scholar
  38. Mutschler, T. (1999). Folivory in a small-bodied lemur: The nutrition of the Alaotran gentle lemur (Hapalemur griseus alaotrensis). In Rakotosamimanana, B., Rasamimanana, H., Ganzhorn, J., and Goodman, S. (eds.), New Directions in Lemur Studies, Kluwer Academic/Plenum, New York, pp. 221–239.Google Scholar
  39. Mutschler, T., Feistner, A., and Nievergelt, C. (1998). Preliminary field data on group size, diet and activity in the Alaotran gentle lemur Hapalemur griseus alaotrensis. Folia Primatol. 69: 325–330.Google Scholar
  40. Nash, L. (1993). Juveniles in nongregarious primates. In Periera, M., and Fairbanks, L. (eds.), Juvenile Primates: Life History, Development, and Behavior, Oxford University Press, New York, pp. 119–137.Google Scholar
  41. Nunes, A. (1995).Foraging and ranging patterns in white-bellied spider monkeys.Folia Primatol. 65: 85–99.Google Scholar
  42. Oates, J. F. (1977). The guereza and its food. In Clutton-Brock, T. H. (ed.), Primate Ecology: Studies of Feeding and Ranging Behavior in Lemurs, Monkeys and Apes, Academic Press, London, pp. 275–321.Google Scholar
  43. Overdorff, D. J. (1996). Ecological correlates to social structure in two lemur species in Madagascar. Am. J. Phys. Anthropol. 100: 487–506.Google Scholar
  44. Overdorff, D. J. (1998). Are Eulemur species pair-bonded? Social organization and mating strategies in Eulemur fulvus rufus from from 1988- 1995 in southeastern Madagascar. Am. J. Phys. Anthropol. 105: 153–166.Google Scholar
  45. Overdorff, D. J., and Erhart, E. M. (1998). Group movements in wild Propithecus diadema edwardsi and Eulemur fulvus rufus. Am. J. Primatol. 45: 198.Google Scholar
  46. Overdorff, D. J., Strait, S. G., and Telo, A. (1998). Seasonal variation in activity and diet in a small bodied folivorous primate, Hapalemur griseus, in southeastern Madagaascar. Am. J. Primatol.Google Scholar
  47. Periera, M. E., Strohecker, R., Cavigelli, S., Hughes, C., and Pearson, D. (1999). Metabolic strategy and social behavior in Lemuridae. In Rakotosamimanana, B., Rasamimanana, H., Ganzhorn, J., and Goodman, S. (eds.), New Directions in Lemur Studies, Kluwer Academic/ Plenum, New York, pp. 93–118.Google Scholar
  48. Pollock, J. I. (1977). The ecology and sociology of feeding in Indri indri. In Clutton-Brock, T. H. (ed.), Primate Ecology: Studies of Feeding and Ranging Behavior in Lemurs, Monkeys and Apes, Academic Press, London, pp. 37–69.Google Scholar
  49. Pollock, J. I. (1979a). Female dominance in Indri indri. Folia Primatol. 31: 143–164.Google Scholar
  50. Pollock, J. I. (1979b). Spatial distribution and ranging behavior in lemurs. In Doyle, G. A., Martin. R.D. (eds.), The Study of Prosimian Behavior, Academic Press, NewYork, pp. 359–409.Google Scholar
  51. Portman, O. (1970). Nutritional requirements of non-human primates. In Harris, R. (ed.), Feeding and Nutrition of Non-human Primates, Academic Press, New York, pp. 87–116.Google Scholar
  52. Rakotondravony, D., Goodman, S., and Soarimalala, V. (1998). Predation on Hapalemur griseus by Boa manditra (Boidae) in the Littoral Forest of Eastern Madagascar. Folia Primatol. 69: 405–408.Google Scholar
  53. Remis, M. J. (1995). Effects of body size and social context on the arboreal activities of lowland gorillas in the Central African Republic. Am. J. Phys. Anthropol. 97: 413–433.Google Scholar
  54. Remis, M. J. (1997). Western lowland gorillas (Gorilla gorilla gorilla) as seasonal frugivores: Use of variable resources. Am. J. Primatol. 43: 87–109.Google Scholar
  55. Rhine, R. J., Forthman, D. L., Stillwell-Barnes, R., Westlund, B., and Westlund, H. (1981). Movement patterns of yellow baboons (Papio cynocephalus): Sex differences in juvenile development toward adult patterns. Am. J. Phys. Anthropol. 55: 473–484.Google Scholar
  56. Rholf, F. J. (1993). NTYSIS-pc Numerical Taxonomy and Multivariate Analysis System v. 180, Applied Biostatistics (Exeter Software), Setauket, NY.Google Scholar
  57. Richard, A. F., and Nicoll, M. E. (1987). Female social dominance and basal metabolism in a Malagasy primate, Propithecus verreauxi. Am. J. Primatol. 12: 309–314.Google Scholar
  58. Rodman, P. S., and Mitani, J. (1987). Orangutans: Sexual dimorphism in a solitary species. In Smuts, B. B., Cheney, D. L., Seyfarth, R., Wrangham, R., and Struhsaker, T. (eds.), Primate Societies, University of Chicago Press, Chicago, pp. 146–154.Google Scholar
  59. Rose, L., and Fedigan, L. (1995). Vigilance in white-faced capuchins, Cebus capucinus in Costa Rica. Anim. Behav. 49: 63–70.Google Scholar
  60. Rylands, A. B. (1993). The ecology of the lion tamarins: Leontopithecus: Some intrageneric differences and comparisons with other callitrichids. In Rylands, A.B. (ed.), Marmosets and Tamarins: Systematics, Behaviour, and Ecology, Oxford University Press, Oxford, pp. 296–313.Google Scholar
  61. Rylands, A. B. (1996). Habitat and evolution of social and reproductive behavior in Callitrichidae. Am. J. Primatol. 38: 5–18.Google Scholar
  62. Sauther, M. L. (1993). Resource competition in wild populations of ringtailed lemurs (Lemur catta): Implications for female dominance. In Kappeler, P. M., and Ganzhorn, J. U. (eds.), Lemur Social Sytems and Their Ecological Basis, Plenum, New York, pp. 135–152.Google Scholar
  63. Shatz, G. E., and Malcomber, S. T. (1993). Botanical research at Ranomafana National Park: Baseline data for long-term ecological monitoring. Ranomafana NationalPark Biodiversity Symposium, Stony Brook, NY.Google Scholar
  64. Smith, C. C. (1977). Feeding behavior and social organization in Howling Monkeys. In Clutton-Brock, T. H. (ed.), Primate Ecology: Studies of Feeding and Ranging Behavior in Lemurs, Monkeys and Apes, Academic Press, London, pp. 97–126.Google Scholar
  65. Srivastava, A. (1992). Use of resources by free-ranging female langurs (Presbytis entellus) during different reproductive phases. Folia Primatol. 59: 157–162.Google Scholar
  66. Sterling, E. J. (1993). Patterns of range use and social organization in aye-ayes (Daubentonia madagascariensis) on Nosy Be. In Kappeler, P. M., and Ganzhorn, J.U. (eds.), Lemur Social Sytems and Their Ecological Basis, Plenum, New York, pp. 1–10.Google Scholar
  67. Stevenson, P., Quinones, M., and Ahumada, J. (1994). Ecological strategies of woolly monkeys (Lagothrix lagotricha) at Tinigua National Park, Columbia. Am. J. Primatol. 32: 123–140.Google Scholar
  68. Strier, K. B. (1989). Effects of patch size in feeding assiciation in Muriquis (Brachyteles arachnoides). Folia Primatol. 52: 70–77.Google Scholar
  69. Strier, K. B. (1993). Growing up in a patrifocal society: Sex differences in the spatial relations of immature muriquis. In Periera, M., and Fairbanks, L. (eds.), Juvenile Primates: Life History, Development, and Behavior, Oxford University Press, New York, pp. 138–147.Google Scholar
  70. Symington, M. M. (1988). Food competition and foraging party size in the black spider monkey (Ateles paniscus chamek). Behaviour 105: 117–133.Google Scholar
  71. Tattersall, I. (1982). The Primates of Madagascar, Columbia University Press, New York.Google Scholar
  72. Tenaza, R., and Fuentes, A. (1995). Monandrous social ogranization of pigtailed langurs (Simias concolor) in the Pagai Islands, Indonesia. Int. J. Primatol. 16: 295–310.Google Scholar
  73. Terborgh, J. (1983). Five New World Primates, Princeton Univeristy Press, Princeton.Google Scholar
  74. Tilden, C. D., and Oftedal, O. T. (1995). The bioenergetics of reproduction in prosimian primates: Is it related to female dominance? In Alterman, L., Doyle, G. A., and Izard, M. K. (eds.), Creatures of the Dark: The Nocturnal Prosimians, Plenum, New York, pp. 119–131.Google Scholar
  75. van Noordwijk, M. A., Hemelrijk, C., Herremans, L., and Sterck, E. (1993). Spatial position and behavioral sex differences in juvenile long-tailed macaques In Periera, M., and Fairbanks, L. (eds.), Juvenile Primates: Life History, Development, and Behavior, Oxford University Press, New York, pp. 77–85.Google Scholar
  76. 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.Google Scholar
  77. van Schaik, C. P., and van Noordwijk, M. A. (1989). The special role of male Cebus monkeys in predation avoidance and its effect on group composition. Behav. Ecol. Sociobiol. 24: 265–276.Google Scholar
  78. Watts, D. P. (1988). Environmental influences on mountain gorilla time budgets. Am. J. Primatol. 15: 195–211.Google Scholar
  79. White, F. J., and Burgman, M. A. (1990). Social organization of the pygmy chimpanzee (Pan paniscus): Mulivariate analysis of intracommunity associations. Am. J. Phys. Anthropol. 83: 193–201.Google Scholar
  80. White, F. J., Overdorff, D. J., Balko, E., and Wright, P. (1995). Distribution of ruffed lemurs (Varecia variegata) in Ranomafana National Park, Madagascar. Folia Primatol. 64: 124–131.Google Scholar
  81. Wrangham, R.W. (1977). Feeding behavior of chimpanzees in Gombe National Park, Tanzania. In Clutton-Brock, T. H. (ed.), Primate Ecology: Studies of Feeding and Ranging Behavior in Lemurs, Monkeys and Apes, Academic Press, London, pp. 504–538.Google Scholar
  82. Wrangham, R. W., and Smuts, B. B. (1980). Sex differences in the behavioural ecology of chimpanzees in the Gombe National Park, Tanzania. J. Reprod. Fert. Suppl. 28: 13–31.Google Scholar
  83. Wright, P. (1984). Biparental care in Aotus trivergatus and Callicebus moloch. In Small, M. E. (ed.), Female Primates: Studies byWomen Primatologists, Alan R. Liss, New York, pp. 59–75.Google Scholar
  84. Wright, P. (1986). Diet, ranging behavior, and activity pattern of the gentle lemur (Hapalemur griseus) in Madagascar. Am. J. Phys. Anthropol. 69: 203.Google Scholar
  85. Wright, P. (1988). Comparative ecology of three sympatric bamboo lemurs in Madagascar. Am. J. Phys. Anthropol. 78: 327.Google Scholar
  86. Wright, P. (1992). Primate ecology, rainforest conservation, and economic development: Building a national park in Madagascar. Evol. Anthropol. 1: 25–33.Google Scholar
  87. Wright, P. (1998). Impact of predation risk on the behaviour of Propithecus diadema edwardsi in the rain forest of Madagascar. Behaviour 135: 483–512.Google Scholar
  88. Wright, P. (1999). Lemur traits and Madagascar ecology: Coping with an island environment. Am. J. Phys. Anthropol. 42(Suppl. 29): 31–72.Google Scholar
  89. Young, A. L., Richard, A. F., and Aiello, L. (1990). Female dominance and maternal investment in Steprsirhine primates. Am. Nat. 135: 473–488.Google Scholar
  90. Young, T. P., and Isbell, L. A. (1991). Sex differences in giraffe feeding ecology: Energetic and social constraints. Ethology 87: 79–89.Google Scholar
  91. Zuberbuhler, K., Noe, R., and Seyfarth, R. (1997). Diana monkey long-distance calls: Messages for conspecifics and predators. Anim. Behav. 53: 589–604.Google Scholar

Copyright information

© Plenum Publishing Corporation 2002

Authors and Affiliations

  • Christina Grassi
    • 1
  1. 1.Department of AnthropologyThe University of Texas at AustinAustin

Personalised recommendations