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Growth, development, and parental care in the western tarsier (Tarsius bancanus) in captivity: Evidence for a “slow” life-history and nonmonogamous mating system

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Abstract

I studied reproduction, prenatal and postnatal growth rates, behavioral ontogeny, and parental care in nine captive births to two wild-caught pairs of Tarsius bancanusover a 5-year period. T. bancanusinvariably gives birth to a single infant of approximately 20% maternal body mass after an extremely long gestation period. The fetal growth rate is among the slowest recorded for any mammal and the relative postnatal growth rate to physical maturity is the lowest in a sample of 26 prosimian species examined. These life-history variables, and a slow rate of reproduction, contribute to an extremely low г max in this and other species of Tarsius.The relative rate of behavioral development, especially foraging and locomotor behaviors, is extremely rapid for a specialized predator. Infants attained nutritional independence at approximately 80 days and perfected hunting skills without apparent help from either parent. Mothers were very protective of their young and kept fathers from having contact with infants through heightened agonism after birth, and thus , there was no evidence of direct paternal care. The data suggest that there is an energetic/dietary basis for slow pre- and postnatal growth rates, but an extremely large neonatal brain size enables the rapid behavioral development and neuromuscular coordination necessary for this specialized predator to attain early nutritional independence. The captive and field data also suggest that extremely restrictive conditions exist for the purported monogamous mating system of T. bancanusand that an alternative mating system is more likely.

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References

  • Banks, E. (1949).Bomean Mammals, Government Printing Office, Kuching.

    Google Scholar 

  • Bearder, S. K. (1987). Lorises, bushbabies, and tarsiers: Diverse societies in solitary foragers. In Smuts, B. B., Cheney, D. L., Seyfarth, R. M., Wrangham, R. W., and Strusaker, T. T. (eds.),Primate Societies, University of Chicago Press, Chicago, pp. 11–24.

    Google Scholar 

  • Catchpole, H. R., and Fulton, J. F. (1943). The oestrous cycle inTarsius: Observations on a captive pair.J. Mammal. 24: 90–93.

    Article  Google Scholar 

  • Chapman, C., Walker, S., and Lefebvre, L. (1990). Reproductive strategies of primates: The influence of body size and diet on litter size.Primates 31: 1–13.

    Article  Google Scholar 

  • Clutton-Brock, T. H. (1991).The Evolution of Parental Care, Princeton University Press, Princeton, NJ.

    Google Scholar 

  • Cole, L. C. (1954). The population consequences of life history phenomena.Q. Rev. Biol. 29: 103–137.

    Article  PubMed  CAS  Google Scholar 

  • Crompton, R., and Andau, P. (1987). Ranging, activity rhythms and sociality in free-rangingTarsius bancanus: A preliminary report.Int. J. PrimatoL 8: 43–71.

    Article  Google Scholar 

  • Doyle, G. A. (1979). Development of behavior in prosimians with special reference to the lesser bushbaby,Galago senegalensis moholi. In Doyle, G. A., and Martin, R. D. (eds.),The Study of Prosimian Behavior, Academic Press, New York, pp. 158–206.

    Google Scholar 

  • Dunbar, R. I. (1988).Primate Social Systems, Comstock, Cornell University Press, Ithaca, NY.

    Google Scholar 

  • Erlich, A., and MacBride, L. (1989). Mother-infant interactions in captive slow lorises (Nyctecebus coucang).Am. J. Primatol 19: 217–228.

    Article  Google Scholar 

  • Fogden, M. P. (1974). A preliminary field study of the western tarsier,Tarsius bancanus Horsfield. In Martin, R. D., Doyle, G. A., and Walker, A. C. (eds.),Prosimian Biology, Duckworth, London, pp. 151–166.

    Google Scholar 

  • Hanwell, A., and Peaker, M. (1977). Physiological effects of lactation on the mother.Symp. Zool. Soc. Lond. 41: 297–312.

    Google Scholar 

  • Haring, D., and Wright, P. (1989). Hand-raising a Philippine Tarsier,Tarsius syrichta.Zoo Biol 8: 265–274.

    Article  Google Scholar 

  • Harvey, P. H., and Clutton-Brock, T. H. (1985). Life history variation in primates.Evolution 39: 559–591.

    Article  Google Scholar 

  • Harvey, P. H., and Pagel, M. D. (1991).The Comparative Method in Evolutionary Biology, Oxford University Press, Oxford.

    Google Scholar 

  • Harvey, P. H., Promislow, D. E. L., and Read, A. F. (1989). Causes and correlations of life history differences among mammals. In Standen, V., and Foley, R. (eds.),Comparative Socioecology, Blackwell Scientific, Oxford, pp. 305–313.

    Google Scholar 

  • Izard, M., Wright, P., and Simons, E. (1985). Gestation length inTarsius bancanus.Am. J. Phys. Anthropol. 9: 327–331.

    Google Scholar 

  • Izard, M. K., Weisensteel, K. A., and Ange, R. L. (1988). Reproduction in the slow loris (Nyctecebus coucang).Am. J. PrimatoL 16: 331–339.

    Article  Google Scholar 

  • Kleiman, D. G. (1977). Monogamy in mammals.Q. Rev. Biol. 52: 39–69.

    Article  PubMed  CAS  Google Scholar 

  • Kleiman, D. G., and Malcom, J. R. (1981). The evolution of male parental investment in mammals. In Gubernick, D. J., and Klopfer, P. H. (eds.),Parental Care in Mammals, Plenum Press, New York, pp. 347–387.

    Google Scholar 

  • Knowlton, N. (1979). Reproductive synchrony, parental investment and the evolutionary dynamics of sexual selection.Anim. Behav. 27: 1022–1033.

    Article  Google Scholar 

  • Leutenegger, W. (1973). Maternal-fetal weight relationships in primates.Folia PrimatoL 20: 280–293.

    Article  PubMed  CAS  Google Scholar 

  • MacKinnon, J., and MacKinnon, K. (1980). The behavior of wild spectral tarsiers.Int. J. PrimatoL 1: 361–379.

    Article  Google Scholar 

  • May, R. M., and Rubenstein, D. I. (1985). Reproductive strategies. In Austin, C. R., and Short, R. V. (eds.),Reproductive Fitness, Cambridge University Press, Cambridge, pp. 1–23.

    Google Scholar 

  • McNab, B. K. (1986). The influence of food habits on the energetics of eutherian mammals.EcoL Monogr. 56: 1–19.

    Article  Google Scholar 

  • McNab, B. K. (1988). Complications inherent in scaling the basal metabolic rate of metabolism in mammals.Q. Rev. Biol. 63: 25–54.

    Article  PubMed  CAS  Google Scholar 

  • McNab, B. K., and Wright, P. (1987). Temperature regulation and oxygen consumption in the Philippine tarsier,Tarsius syrichta.Physiol. Zool. 60: 596–600.

    Google Scholar 

  • Millar, J. S. (1981). Pre-partum reproductive characteristics of eutherian mammals.Evolution 35: 1149–1163.

    Article  Google Scholar 

  • Müller, E. F. (1985). Basal metabolic rates in primates — the possible role of phylogenetic and ecological factors.Comp. Biochem. Physiol. 81A: 707–711.

    Article  Google Scholar 

  • Musser, G. G., and Dagasto, M. (1987). The identity ofTarsius pumilus, a pygmy species endemic to the montane mossy forests of Central Sulawesi.Am. Mus. Novitat. 2867: 1–53.

    Google Scholar 

  • Napier, J., and Walker, A. C. (1967). Vertical clinging and leaping — a newly recognized category of locomotor behavior in primates.Folia Primalol. 6: 204–219.

    Article  CAS  Google Scholar 

  • Niemitz, C. (1974). A contribution to the postnatal behavioral development ofTarsius bancanus, Horsfield, 1821, studied in two cases.Folia Primalol. 21: 250–276.

    Article  CAS  Google Scholar 

  • Niemitz, C. (1979a). Results of a field study on the western tarsier (Tarsius bancanus borneanus Horsfield, 1821) in Sarawak.Sarawak Mus. J. 27: 171–228.

    Google Scholar 

  • Niemitz, C. (1979b). Outline of the behavior ofTarsius bancanus. In Doyle, G. A., and Martin, R. D. (eds.),The Study of Prosimian Behavior, Academic Press, New York, pp. 631–660.

    Google Scholar 

  • Niemitz, C. (1984a). Locomotion and posture inTarsius bancanus. In Niemitz, C. (ed.),The Biology of Tarsiers, Gustav Fischer Verlag, New York, pp. 191–225.

    Google Scholar 

  • Niemitz, C. (1984b). An investigation and review of the territorial behavior and social organization of the genusTarsius. In Niemitz, C. (ed.),The Biology of Tarsiers, Gustav Fischer Verlag, New York, pp. 117–127.

    Google Scholar 

  • Niemitz, C. (1984c). Vocal communication of two tarsier species (Tarsius bancanus andTarsius spectrum). In Niemitz, C. (ed.),The Biology of Tarsiers, Gustav Fischer Verlag, New York, pp. 129–142.

    Google Scholar 

  • Niemitz, C., Nietsche, A., Warter, S., and Rumpler, Y. (1991).Tarsius dianae: A new primate species from central Sulawesi (Indonesia).Folia Primalol. 56: 105–116.

    Article  CAS  Google Scholar 

  • Peters, A., and Preuschoft, H. (1984). External biomechanics of leaping inTarsius and its morphological and kinematic consequences. In Niemitz, C. (ed.),The Biology of Tarsiers, Gustav Fischer Verlag, New York, pp. 227–256.

    Google Scholar 

  • Preuschoft, H., Fritz, M., and Niemitz, C. (1979). Biomechanics of the trunk in primates and problems of leaping inTarsius. In Morbeck, M. E., Preuschoft, H., and Gomberg, N. (eds.),Environment, Behavior and Morphology: Dynamic Interaction in Primates, Gustav Fischer Verlag, New York, pp. 327–345.

    Google Scholar 

  • Rasmussen, D. T., and Izard, M. K. (1988). Scaling of growth and life history traits relative to body size, brain size, and metabolic rate in lorises and galagos (Lorisidae, Primates).Am. J. Phys. Anthropol. 75: 357–367.

    Article  PubMed  CAS  Google Scholar 

  • Richard, A., and Nicoll, M. (1987). Primate social dominance and basal metabolism in a Malagasy primate,Propilhecus verrauxi.Am. J. PrimatoL 12: 309–314.

    Article  Google Scholar 

  • Ricklefs, R. E. (1967). A graphical method of fitting equations to growth curves.Ecology 48: 978–983.

    Article  Google Scholar 

  • Roberts, M., and Baker, A. J. (1986). Foraging behavior of the western tarsier,Tarsius bancanus, in captivity. Paper presented at 65th Ann. Mtg. Amer. Soc. Mammal., Orono, Maine, 20 pp.

  • Roberts, M., and Cunningham, B. (1986). Space and substrate use in captive western tarsiers,Tarsius bancanus.Int. J. PrimatoL 7: 113–130.

    Article  Google Scholar 

  • Roberts, M. and Kohn, F. (1993). Habitat use, foraging behavior and activity patterns in reproducing Western tarsiers,Tarsius bancanus in captivity.Zoo Biology 12: 217–232.

    Article  Google Scholar 

  • Robinson, J. G., and Redford, K. H. (1986). Intrinsic rate of natural increase in neotropical forest mammals: Relationship to phylogeny and diet.Oecologia 68: 516–520.

    Article  Google Scholar 

  • Ross, C. (1988). The intrinsic rate of natural increase and reproductive effort in primates.J. Zool. (Land.) 214: 199–219.

    Article  Google Scholar 

  • Ulmer, F. A. (1963). Observations on the tarsier in captivity.Zool. Gart. 27: 106–121.

    Google Scholar 

  • van Horn, R. N., and Eaton, G. G. (1979). Reproductive physiology and behavior of prosimians. In Doyle, G. A., and Martin, R. D. (eds.),The Study of Prosimian Biology, Academic Press, London, pp. 79–122.

    Google Scholar 

  • van Schaik, C. P., van Noordwijk, M. A., Wasone, M. A., and Sitriono, E. (1983). Party size and early detection in Sumatran forest primates.Primates 24: 211–221.

    Article  Google Scholar 

  • Wittenberger, J. F., and Tilson, R. L. (1980). The evolution of monogamy: Hypotheses and evidence.Annu. Rev. EcoL Syst. 11: 197–232.

    Article  Google Scholar 

  • Wright, P. C. (1990). Patterns of paternal care in primates.Int. J. Primatol. 11: 89–102.

    Article  Google Scholar 

  • Wright, P., Izard, M., and Simons, E. (1986a). Reproductive cycles inTarsius bancanus.Am. J. Primatol. 11: 207–215.

    Article  Google Scholar 

  • Wright, P., Toyama, L. and Simons, E. (1986b). Courtship and copulation inTarsius bancanus.Folia PrimatoL 46: 142–148.

    Article  PubMed  CAS  Google Scholar 

  • Zimmermann, E. (1989). Aspects of reproduction and behavioral and vocal development in Senegal bushbabies (Galago senegalensis.Int. J. Primatol. 10: 1–16.

    Article  Google Scholar 

  • Zuckerman, S. (1932). The menstrual cycle of the primates. VI. Further observations on the breeding of primates, with special reference to the suborders Lemuroidea and Tarsoidea.Proc. Zool. Soc. Lond. 1932: 1059–1075.

    Google Scholar 

  • Zullinger, E. M., Ricklefs, R. E., Redford, K. H., and Mace, G. M. (1984). Fitting sigmoidal equations to mammalian growth curves.J. Mammal. 65: 607–636.

    Article  Google Scholar 

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  1. Department of Zoological Research, National Zoological Park, 20008, Washington, D.C

    Miles Roberts

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Roberts, M. Growth, development, and parental care in the western tarsier (Tarsius bancanus) in captivity: Evidence for a “slow” life-history and nonmonogamous mating system. Int J Primatol 15, 1–28 (1994). https://doi.org/10.1007/BF02735232

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