Berenty 2006: Census of Propithecus verreauxi and Possible Evidence of Population Stress

Article

Abstract

We provide a survey of a folivorous lemur, Propithecus verreauxi (sifaka), in the Berenty Reserve, southern Madagascar. Higher densities of folivores in small patches occur in either high-quality food areas or in less disturbed refugia. The skewness of sex ratio, which in lemurs is often male-biased, can be critically exacerbated in population stress. We predicted that sifaka would show higher densities in areas where protein-rich food is abundant (prediction 1a) and in refugium areas (prediction 1b). Owing to increased competition by brown and ring-tailed lemurs and decreased food production by tamarind trees, we expected an extremely male-biased sex ratio (prediction 2). In November–December 2006, we counted and sexed 206 adult/subadult sifaka (49 groups) during daily walks in different forest zones (Ankoba secondary forest, to the north, Malaza gallery/scrub areas, and spiny forest, to the south). Sifaka may have decreased in the gallery forest to concentrate in Ankoba (in a sort of out-of-Malaza). The area contains protein-rich food (prediction 1a confirmed). Sifaka are proportionally more concentrated in the spiny area than in the degraded scrub forest (prediction 1b confirmed). The sex ratio is extremely male biased, possibly due to either high sifaka density, in Ankoba, or food availability reduction, in Malaza (prediction 2 confirmed). The sifaka population seems to be under stress: researchers need to resume demographic studies, interrupted in Berenty in the mid-1980s, to preserve in situ a species that is difficult to protect ex situ.

Keywords

drought Indriidae population survey prosimian 

References

  1. Allainé, D., Brondex, F., Graziani, L., Coulon, J., & Till-Bottraud, I. (2000). Male-biased sex ratio in litters of Alpine marmots supports the helper repayment hypothesis. Behavioral Ecology, 11, 507–514.CrossRefGoogle Scholar
  2. Blumenfeld-Jones, K., Randriamboavonjy, T. M., Williams, G., Mertl-Millhollen, A. S., Pinkus, S., & Rasamimanana, H. (2006). Tamarind recruitment and long-term stability in the gallery forest at Berenty, Madagascar. In A. Jolly, R. W. Sussman, N. Koyama, & H. Rasamimanana (Eds.), Ringtailed lemur biology: Lemur catta in Madagascar (p. 69–85). New York: Springer Verlag Press.CrossRefGoogle Scholar
  3. Bonefant, C., Gaillard, J. M., Loison, A., & Klein, F. (2003). Sex-ratio variation and reproductive costs in relation to density in a forest-dwelling population of red deer (Cervus elaphus). Behavioral Ecology, 14, 862–869.CrossRefGoogle Scholar
  4. Britt, A., Randriamandratonirina, N., Glasscock, K. D., & Iambana, B. R. (2002). Diet and feeding behaviour in Indri indri in a low-altitude rain forest. Folia Primatologica, 73, 225–239.CrossRefGoogle Scholar
  5. Brockman, D. K. (1999). Reproductive behavior of female Propithecus verreauxi at Beza Mahafaly, Madagascar. International Journal of Primatology, 20, 375–398.CrossRefGoogle Scholar
  6. Chapman, C. A., Chapman, L. J., Bjorndal, K. A., & Onderdonk, D. A. (2002). Application of protein-to-fiber ratios to predict colobine abundance on different spatial scales. International Journal of Primatology, 23, 283–310.CrossRefGoogle Scholar
  7. Chiarello, A. G. (2000). Density and population size of mammals in remnants of Brazilian Atlantic forest. Conservation Biology, 14, 1649–1657.CrossRefGoogle Scholar
  8. Chiarello, A. G., & de Melo, F. R. (2001). Primate population densities and sizes in Atlantic forest remnants of northern Espiritu Santo, Brazil. International Journal of Primatology, 22, 379–396.CrossRefGoogle Scholar
  9. Clark, A. B. (1978). Sex ratio and local resource competition in a prosimian primate. Science, 201, 163–165.PubMedCrossRefGoogle Scholar
  10. Clutton-Brock, T. H., & Iason, G. R. (1986). Sex variation in mammals. Quarterly Review of Biology, 61, 339–374.PubMedCrossRefGoogle Scholar
  11. Cockburn, A. (1990). Sex ratio variation in marsupials. Australian Journal of Zoology, 37, 467–479.CrossRefGoogle Scholar
  12. Curtis, D. J. (2003). Diet and nutrition in wild mongoose lemurs (Eulemur mongoz) and their implications for the evolution of female dominance and small group size in lemurs. American Journal of Physical Anthropology, 124, 234–247.CrossRefGoogle Scholar
  13. Dittus, W. P. J. (1988). Group fission among wild toque macaques as a consequence of female resource competition and environmental stress. Animal Behavior, 36, 1626–1645.CrossRefGoogle Scholar
  14. Donati, G., Bollen, A., BorgognIni-Tarli, S. M., & Ganzhorn, J. U. (2007). Feeding over the 24-h cycle: Dietary flexibility of cathemeral collared lemurs (Eulemur collaris). Behavioral Ecology and Sociobiology, 61, 1237–1251.CrossRefGoogle Scholar
  15. Emlen, S. T., & Oring, L. W. (1977). Ecology, sexual selection and the evolution of mating systems. Science, 197, 215–223.PubMedCrossRefGoogle Scholar
  16. Feistner, A. T. C., & Schmid, J. (1999). Lemurs of the réserve naturelle intégrale d’andohahela, Madagascar. In S. M. Goodman (Ed.), A floral and faunal inventory of the réserve naturelle intégrale d’andohahela, Madagascar: With reference to elevational variation (pp. 269–283). Chicago: Fieldiana.Google Scholar
  17. Ganzhorn, J. U. (1992). Leaf chemistry and the biomass of folivorous primates in tropical forests. Test of a hypothesis. Oecologia, 91, 540–547.CrossRefGoogle Scholar
  18. Ganzhorn, J. U. (1995). Low-level forest disturbance effects on primary production, leaf chemistry, and lemur populations. Ecology, 76, 2084–2096.CrossRefGoogle Scholar
  19. Ganzhorn, J. U. (1997). Habitat characteristics and lemur species richness in Madagascar. Biotropica, 29, 331–343.CrossRefGoogle Scholar
  20. Ganzhorn, J. U., Goodman, S. M., & Dehgan, A. (2003). Effects of forest fragmentation on small mammals and lemurs. In S. M., Goodman, & J. P. Benstead (Eds.), The natural history of Madagascar (p. 1228–1234). Chicago: University of Chicago Press.Google Scholar
  21. Glessner, K. D. G., & Britt, A. (2005). Population density and home range size of Indri indri in a protected low altitude rain forest. International Journal of Primatology, 26, 855–872.CrossRefGoogle Scholar
  22. Godfrey, L. R., Samonds, K. E., Jungers, W. L., Sutherland, M. R., & Irwin, M. T. (2004). Ontogenic correlates of diet in Malagasy lemurs. American Journal of Physical Anthropology, 123, 250–276.PubMedCrossRefGoogle Scholar
  23. Gould, L. (2006). Lemur catta ecology: What we know and what we need to know. In L. Gould, & M. L. Sauther (Eds.), Lemurs: Ecology and adaptations (p. 255–274). New York: Springer.Google Scholar
  24. Gould, L., Sussman, R. W., & Sauther, M. L. (1999). Natural disasters and primate populations: The effects of a 2-year drought on a naturally occurring population of ring-tailed lemurs (Lemur catta) in Southwestern Madagascar. International Journal of Primatology, 20, 69–84.CrossRefGoogle Scholar
  25. Gould, L., Sussman, R. W., & Sauther, M. L. (2003). Demographic and life-history patterns in a population of ring-tailed lemurs (Lemur catta) at Beza Mahafaly Reserve, Madagascar: A 15-year perspective. American Journal of Physical Anthropology, 120, 182–194.PubMedCrossRefGoogle Scholar
  26. Hamilton III, W. J. (1985). Demographic consequences of a food and water shortage to desert chacma baboons, Papio ursinus. International Journal of Primatology, 6, 451–462.CrossRefGoogle Scholar
  27. Jolly, A. (1966). Lemur behavior: A Madagascar field study (p. 197). Chicago: University of Chicago Press.Google Scholar
  28. Jolly, A. (1972). Troop continuity and troop spacing in Propithecus verreauxi and Lemur catta at Berenty (Madagascar). Folia Primatologica, 17, 335–362.Google Scholar
  29. Jolly, A. (2004). Lords and lemurs. New York: Houghton Mifflin.Google Scholar
  30. Jolly, A., Dobson, A., Rasamimanana, H. M., Walker, J., O’Connor, S., Solberg, M., et al. (2002). Demography of Lemur catta at Berenty Reserve, Madagascar: Effects of troop size, habitat and rainfall. International Journal of Primatology, 23, 327–353.CrossRefGoogle Scholar
  31. Jolly, A., Gustafson, H., Oliver, W. L. R., & O’ Connor, S. M. (1982). Propithecus verreauxi population and ranging at Berenty, Madagascar, 1975 and 1980. Folia Primatologica, 39, 124–144.Google Scholar
  32. Jolly, A., Koyama, N., Rasamimanana, H., Crowley, H., & Williams, G. (2006). Berenty Reserve: A research site in southern Madagascar. In A. Jolly, R. W. Sussman, N. Koyama, & H. Rasamimanana (Eds.), Ringtailed lemur biology: Lemur catta in Madagascar (p. 32–42). New York: Springer.CrossRefGoogle Scholar
  33. Kappeler, P. (2000). Causes and consequences on unusual sex ratios among lemurs. In P. Kappeler (Ed.), Primate males (p. 55–63). Cambridge, U.K.: Cambridge University Press.Google Scholar
  34. Koyama, N., Nakamichi, M., Oda, R., Miyamoto, N., & Takahata, Y. (2001). A ten-year summary of reproductive parameters for ring-tailed lemurs at Berenty, Madagascar. Primates, 42, 1–14.CrossRefGoogle Scholar
  35. Kruuk, L. E. B., Clutton-Brock, T. H., Albon, S. D., Pemberton, J. M., & Guinness, F. E. (1999). Population density affects sex variation in red deer. Nature, 399, 459–461.PubMedCrossRefGoogle Scholar
  36. Lehman, S. M., Rajaonson, A., & Day, S. (2006a). Edge influence on lemur density and distribution in southeast Madagascar. American Journal of Physical Anthropology, 129, 232–241.PubMedCrossRefGoogle Scholar
  37. Lehman, S. M., Ratsimbazafy, J., Rajaonson, A., & Day, S. (2006b). Decline of Propithecus diadema edwardsi and Varecia variegata variegata (Primates: Lemuridae) in south-east Madagascar. Oryx, 40, 108–111.CrossRefGoogle Scholar
  38. Lewis, R. J. (2005). Sex differences in scent-marking in sifaka: Mating conflict or male services. American Journal of Physical Anthropology, 128, 389–398.PubMedCrossRefGoogle Scholar
  39. Lewis, R. J., & Kappeler, P. M. (2005a). Seasonality, body condition, and timing of reproduction in Propithecus verreauxi verreauxi. American Journal of Primatology, 66, 1–18.Google Scholar
  40. Lewis, R. J., & Kappeler, P. M. (2005b). Are Kirindy sifaka capital or income breeders? It depends. American Journal of Primatology, 63, 365–369.CrossRefGoogle Scholar
  41. Mertl-Milhollen, A., Rambeloarivony, H., Miles, W., Kaiser, V. A., Gray, L., Dorn, L. T., et al. (2006). The influence of tamarind tree quality and quantity on Lemur catta behavior. In A. Jolly, R. W. Sussman, N. Koyama, & H. Rasamimanana (Eds.), Ringtailed lemur biology: Lemur catta in Madagascar (p. 102–118). New York: Springer.CrossRefGoogle Scholar
  42. Mittermeier, R. W., Konstant, W. R., Hawkins, F., Louis, E. E., Langrand, O., Ratsimbazafy, J., et al. (2006). Lemurs of Madagascar (2nd ed.). Washington, DC: Conservation International.Google Scholar
  43. Mundry, R., & Fischer, J. (1998). Use of statistical programs for nonparametric tests of small samples often leads to incorrect P values: Examples from animal behaviour. Animal Behavior, 56, 256–259.CrossRefGoogle Scholar
  44. Nakamura, M. (2004). Predation by Eulemur fulvus fulvus on eggs of Ploceus sakalava sakalava (Aves: Ploceidae) in Ankarafantsika, Madagascar. Folia Primatologica, 75, 376–378.CrossRefGoogle Scholar
  45. Norscia, I. (2008). Pilot survey of avahi population (woolly lemurs) in littoral forest fragments of southeast Madagascar. Primates, 49, 85–88.PubMedCrossRefGoogle Scholar
  46. Norscia, I., & Borgognini-Tarli, S. M. (2008). Ranging behavior and possible correlates of pair-living in Southeastern Avahis (Madagascar). International Journal of Primatology, 29, 153–171.CrossRefGoogle Scholar
  47. Norscia, I., Carrai, V., & Borgognini-Tarli, S. M. (2006). Influence of dry season, food quality and quantity on behavior and feeding strategy of Propithecus verreauxi in Kirindy, Madagascar. International Journal of Primatology, 27, 1001–1022.CrossRefGoogle Scholar
  48. Nunn, C. L., & Pereira, M. E. (2000). Group histories and offspring sex ratios in ringtailed lemurs (Lemur catta). Behavioral Ecology and Sociobiology, 48, 18–28.CrossRefGoogle Scholar
  49. O’Connor, S. (1987). The effect of human impact on vegetation and the consequences to primates in two Riverine forests, southern Madagascar. Ph.D. thesis, University of Cambridge, Cambridge, U.K.Google Scholar
  50. Onderdonk, D. A., & Chapman, C. A. (2000). Coping with forest fragmentation: The primates of Kibale National Park, Uganda. International Journal of Primatology, 21, 587–611.CrossRefGoogle Scholar
  51. Ostner, J. (2002). Social thermoregulation in redfronted lemurs (Eulemur fulvus rufus). Folia Primatologica, 73, 175–180.CrossRefGoogle Scholar
  52. Ostner, J., & Kappeler, P. M. (2004). Male life history and the unusual adult sex ratios of redfronted lemur, Eulemur fulvus rufus, groups. Animal Behavior, 67, 249–259.CrossRefGoogle Scholar
  53. Packer, C., Collins, D. A., & Eberly, L. E. (2000). Problems with primate sex ratios. Philosophical Transactions of the Royal Society of London Series B, 355, 1627–1635.PubMedCrossRefGoogle Scholar
  54. Perret, M. (1990). Influence of social factors on sex ratio at birth, maternal investment and young survival in a prosimian primate. Behavioral Ecology and Sociobiology, 27, 447–454.CrossRefGoogle Scholar
  55. Pinkus, S., Smith, J. N. M., & Jolly, A. (2006). Feeding competition between introduced Eulemur fulvus and native Lemur catta during the birth season a Berenty Reserve, Southern Madagascar. In A. Jolly, R. W. Sussman, N. Koyama, & H. Rasamimanana (Eds.), Ringtailed lemur biology: Lemur catta in Madagascar (pp. 119–140). New York: Springer.CrossRefGoogle Scholar
  56. Pochron, S. T., Tucker, W. T., & Wright, P. C. (2004). Demography, life history, and social structure in Propithecus diadema edwardsi from 1986–2000 in Ranomafana National Park, Madagascar. American Journal of Physical Anthropology, 125, 61–72.PubMedCrossRefGoogle Scholar
  57. Pochron, S. T., & Wright, P. C. (2003). Variability in adult group compositions of a prosimian primate. Behavioral Ecology and Sociobiology, 54, 285–293.CrossRefGoogle Scholar
  58. Ralison, J. M., Ramanamanjato, J. B., & Rakotomalala-Razanahoera, M. (2006). Influence de la qualité de la forêt sur Eulemur collaris (E. Geoffroy, 1812) dans les formations littorales de Mandena et de Sainte Luce à Tolagnaro, Madagascar, en 1998–1999. In C. Schwitzer, S. Brandt, O. Ramilijaona, M. Rakotomalala-Razanahoera, D. Ackermand, T. Razakamanana, & J. U. Ganzhorn (Eds.), Proceedings of the German-Malagasy research cooperation in life and earth sciences (p. 161–167). Berlin, Germany: Concept Verlag.Google Scholar
  59. Ramanamanjato, J. B. (2000). Fragmentation effects on reptile and amphibian diversity in the littoral forest of southeastern Madagascar. In G. Rheinwals (Ed.), Isolated vertebrate communities in the tropics. Proceedings 4th International Symposium (pp. 297–308). Bonn, Germany: Bonn Zoological Monograph.Google Scholar
  60. Richard, A. F. (1974). Intra-specific variation in the social organization and ecology of Propithecus verreauxi. Folia Primatologica, 22, 178–207.CrossRefGoogle Scholar
  61. Richard, A. F. (1985). Social boundaries in a Malagasy prosimian, the Sifaka (Propithecus verreauxi). International Journal of Primatology, 6, 553–568.CrossRefGoogle Scholar
  62. Richard, A. F., & Dewar, R. E. (1991). Lemur ecology. Annual Review of Ecological Systems, 22, 145–175.CrossRefGoogle Scholar
  63. Richard, A. F., Dewar, R. E., Schwartz, M., & Ratsirarson, J. (2002). Life in the slow lane? Demography and life histories of male and female sifaka (Propithecus verreauxi verreauxi). Journal of Zoology London, 256, 421–436.Google Scholar
  64. Richard, A. F., Rakotomanga, P., & Schwartz, M. (1991). Demography of Propithecus verreauxi at Beza Mahafaly, Madagascar: Sex ratio, survival, and fertility, 1984–1988. American Journal of Physical Anthopology, 84, 307–322.CrossRefGoogle Scholar
  65. Ricklefs, R. E. (1990). Ecology (3rd ed.). New York: Chiron Press.Google Scholar
  66. Rudran, E., & Fernandez-Duque, E. (2003). Demographic changes over thirty years in a red howler population in Venezuela. International Journal of Primatology, 24, 925–947.CrossRefGoogle Scholar
  67. Shaffen, M. L. (1981). Minimum population sizes for species conservation. Bioscience, 31, 131–134.CrossRefGoogle Scholar
  68. van Schaik, C. P., & van Noordwijk, M. A. (1983). Social stress and the sex ratio of neonates and infants among non-human primates. Netherlands Journal of Zoology, 33, 249–265.CrossRefGoogle Scholar
  69. Simmen, B., Hladik, A., & Ramasiarisoa, P. (2003). Food intake and dietary overlap in native Lemur catta and Propithecus verreauxi and introduced Eulemur fulvus at Berenty, Southern Madagascar. International Journal of Primatology, 24, 949–968.CrossRefGoogle Scholar
  70. Simmen, B., Sauther, M. L., Soma, T., Rasamimanana, H., Sussman, R. W., Jolly, A., et al. (2006). Plant species fed on by Lemur catta in gallery forests of the southern domain of Madagascar. In A. Jolly, R. W. Sussman, N. Koyama, & H. Rasamimanana (Eds.), Ringtailed lemur biology: Lemur catta in Madagascar (p. 55–68). New York: Springer.CrossRefGoogle Scholar
  71. Smith, A. P., Horning, N., & Moore, D. (1997). Regional biodiversity planning and lemur conservation with GIS in Western Madagascar. Conservation Biology, 11, 498–512.CrossRefGoogle Scholar
  72. Soma, T. (2006). Tradition and novelty: Lemur catta feeding strategy on introduced tree species at Berenty Reserve. In A. Jolly, R. W. Sussman, N. Koyama, & H. Rasamimanana (Eds.), Ringtailed lemur biology: Lemur catta in Madagascar (p. 141–159). New York: Springer.CrossRefGoogle Scholar
  73. Sussman, R. W. (1974). Ecological distinctions in sympatric species of lemurs. In R. D. Martin, G. A. Doyle, & A. C. Walker (Eds.), Prosimian biology (pp. 75–108). London: Duckworth Press.Google Scholar
  74. Tarnaud, L. (2004). Ontogeny of feeding behavior of Eulemur fulvus in the dry forest of Mayotte. International Journal of Primatology, 25, 803–824.CrossRefGoogle Scholar
  75. Tattersall, I. (1982). The primates of Madagascar. New York: Columbia University Press.Google Scholar
  76. Trivers, R. L., & Willard, D. E. (1973). Natural selection of parental ability to vary sex ratio of offspring. Science, 179, 90–92.PubMedCrossRefGoogle Scholar
  77. Tutin, C. E. G., White, L. J. T., & Mackanga-Missadzou, A. (1997). The use by rain forest mammals of natural forest fragments in an equatorial African savanna. Conservation Biology, 11, 1190–1203.CrossRefGoogle Scholar
  78. Warren, R. D., & Crompton, R. H. (1997). Locomotor ecology of Lepilemur edwardsi and Avahi occidentalis. American Journal of Primatology, 104, 471–486.Google Scholar
  79. Wright, P. C. (1999). Lemur traits and Madagascar ecology: Coping with an island environment. Yearbookof Physical Anthropology, 42, 31–72.CrossRefGoogle Scholar
  80. Wronski, T., & Apio, A. (2005). Home range overlap, social vicinity and agonistic interactions denoting matrilineal organization in bushbuck, Tragelaphus scriptus. Behavioral Ecology and Sociobiology, 59, 819–828.CrossRefGoogle Scholar
  81. Yamashita, N. (2002). Diets of two lemur species in different microhabitats in Beza Mahafaly special reserve, Madagascar. International Journal of Primatology, 23, 1025–1050.CrossRefGoogle Scholar
  82. Zar, J. H. (1998). Biostatistical analysis (4th ed.). Englewood Cliffs, NJ: Prentice-Hall.Google Scholar

Copyright information

© Springer Science+Business Media, LLC 2008

Authors and Affiliations

  1. 1.Centro Interdipartimentale, Museo di Storia Naturale e del TerritorioUniversità di PisaCalci, PisaItaly

Personalised recommendations