Hostname: page-component-cd9895bd7-mkpzs Total loading time: 0 Render date: 2024-12-23T12:21:38.802Z Has data issue: false hasContentIssue false

Predictable timing of oestrus in the tropical bat Saccopteryx bilineata living in a Costa Rican rain forest

Published online by Cambridge University Press:  01 February 2011

Sabine Greiner*
Affiliation:
Research Group Evolutionary Ecology, Leibniz Institute for Zoo and Wildlife Research, Alfred-Kowalke-Str. 17, 10315 Berlin, Germany Freie Universität Berlin, Department Animal Behaviour, Takustr. 3, 14195 Berlin, Germany
Franz Schwarzenberger
Affiliation:
Department of Biomedical Sciences – Biochemistry, University of Veterinary Medicine, Veterinärplatz 1, 1210 Vienna, Austria
Christian C. Voigt
Affiliation:
Research Group Evolutionary Ecology, Leibniz Institute for Zoo and Wildlife Research, Alfred-Kowalke-Str. 17, 10315 Berlin, Germany Freie Universität Berlin, Department Animal Behaviour, Takustr. 3, 14195 Berlin, Germany
*
1Corresponding author. Email: [email protected]

Abstract:

Many tropical mammals reproduce seasonally, although the circum-equatorial climate is more stable and less seasonal than that of temperate zones. The mechanisms underlying seasonal reproduction in the tropics remain enigmatic. Female reproduction and its relation to environmental factors were investigated in the Neotropical bat species Saccopteryx bilineata. Colonies consist of year-round stable groups of several females that are defended each by an adult male. Females give birth to a single offspring each year and it is suggested that mating is restricted to November and December. In this study, it was asked whether females of a Costa Rican colony come into oestrus around the same time each year and whether oestrus times are synchronized. Oestrogen and progesterone metabolites were monitored from faeces between October and January in four years. Oestrus was identified in 32 females. In addition, climatic factors such as rainfall and temperature were monitored at the study site. Results indicate that (1) females exhibit monoestry, (2) oestrus dates cluster around the first half of December, (3) reproduction is strongly seasonal and highly predictable and (4) oestrus times are possibly influenced by long-term cues like photoperiod and short-term cues like sudden changes in rainfall and temperature.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

LITERATURE CITED

ANDERSON, D. P., NORDHEIM, E. V. & BOESCH, C. 2006. Environmental factors influencing the seasonality of estrus in chimpanzees. Primates 47:4350.CrossRefGoogle ScholarPubMed
ARARK, A. 1988. Callers and satellites in the natterjack toad: evolutionary stable decision rules. Animal Behaviour 36:416432.CrossRefGoogle Scholar
BASS, M. S., FINER, M., JENKINS, C. N., KREFT, H., CISNEROS-HEREDIA, D. F., MCCRACKEN, S. F., PITMAN, N. C. A., ENGLISH, P. A., SWING, K., VILLA, G., DIFIORE, A., VOIGT, C. C. & KUNZ, T. H. 2010. Global conservation significance of Ecuador's Yasuni National Park. PlosOne, doi/10.1371/journal.pone.0008767.Google Scholar
BEASLEY, L. J. & ZUCKER, I. 1984. Photoperiod influences the annual reproductive cycle of the male pallid bat (Antrozous pallidus). Journal of Reproduction and Fertility 70:567573.CrossRefGoogle ScholarPubMed
BOINSKI, S. 1987. Birth synchrony in squirrel monkeys (Saimiri oerstedi). Behavioral Ecology and Sociobiology 21:393400.CrossRefGoogle Scholar
BORCHERT, R., RENNER, S. S., CALLE, Z., NAVARRETE, D., TYE, A., GAUTIER, L., SPICHIGER, R. & VON HILDEBRAND, P. 2005. Photoperiodic induction of synchronous flowering near the equator. Nature 433:627629.CrossRefGoogle ScholarPubMed
BRADBURY, J. W. 1979. Behavioural aspects of reproduction in Chiroptera. Journal of Reproduction and Fertility 56:431438.CrossRefGoogle ScholarPubMed
BRADBURY, J. W. & EMMONS, L. 1974. Social organization of some Trinidad bats I. Emballonuridae. Zeitschrift für Tierpsychologie 36:137183.CrossRefGoogle ScholarPubMed
BRONSON, F. H. 1988. Mammalian reproductive strategies: genes, photoperiod and latitude. Reproduction Nutrition Development 28:335347.CrossRefGoogle ScholarPubMed
BRONSON, F. H. 1989. Mammalian reproductive biology. University of Chicago Press, Chicago. 336 pp.Google Scholar
BRONSON, F. H. 2009. Climate change and seasonal reproduction in mammals. Philosophical Transactions of the Royal Society of London, Series B 364:33313340.CrossRefGoogle ScholarPubMed
BUMRUNGSRI, S., BUMRUNGSRI, W. & RACEY, P. A. 2007. Reproduction in the short-nosed fruit bat in relation to environmental factors. Journal of Zoology 272:7381.CrossRefGoogle Scholar
CASPERS, B., FRANKE, S. & VOIGT, C. C. 2008. The wing sac odour of male greater sac-winged bats (Saccopteryx bilineata) as a composite trait: seasonal and individual differences. Pp. 151160 in Hurst, J. L., Beynon, R. J., Roberts, S. C. & Wyatt, T. D. (eds.). Chemical signals in vertebrates XI. Springer, New York.CrossRefGoogle Scholar
CASPERS, B. A., SCHROEDER, F. C., FRANKE, S., STREICH, W. J. & VOIGT, C. C. 2009. Odour-based species recognition in two sympatric species of sac-winged bats (Saccopteryx bilineata, S. leptura): combining chemical analyses, behavioural observations and odour preference tests. Behavioral Ecology and Sociobiology 63:741749.CrossRefGoogle Scholar
COLWELL, R. K. 1974. Predictability, constancy, and contingency of periodic phenomena. Ecology 55:11481153.CrossRefGoogle Scholar
CUMMING, G. S. & BERNARD, R. T. F. 1997. Rainfall, food abundance and timing of parturition in African bats. Oecologia 111:309317.CrossRefGoogle ScholarPubMed
DUNBAR, R. I. M. 1980. Demographic and life history variables of a population of Gelada baboons (Theropithecus gelada). Behavioral Ecology and Sociobiology 7:253265.CrossRefGoogle Scholar
FEDIGAN, L. M. & ROSE, L. M. 1995. Interbirth interval variation in three sympatric species of Neotropical monkey. American Journal of Primatology 37:924.CrossRefGoogle ScholarPubMed
GWINNER, E. & DITTAMI, J. 1985. Photoperiodic responses in temperate zone and equatorial Stonechats: a contribution to the problem of photoperiodism in tropical organisms. Pp. 279294 in Follett, B. K., Ishii, S. & Chandola, A. (eds.). The endocrine system and the environment. Springer Verlag, Berlin.Google Scholar
HAU, M. 2001. Timing of breeding in variable environments: tropical birds as model systems. Hormones and Behavior 40:281290.CrossRefGoogle ScholarPubMed
HAU, M., WIKELSKI, M. & WINGFIELD, J. C. 1998. A neotropical forest bird can measure the slight changes in tropical photoperiod. Proceedings of the Royal Society of London B 265:8995.CrossRefGoogle Scholar
HAU, M., WIKELSKI, M. & WINGFIELD, J. C. 2000. Visual and nutritional food cues fine-tune timing of reproduction in a neotropical rainforest bird. Journal of Experimental Zoology 286:494504.3.0.CO;2-3>CrossRefGoogle Scholar
HAU, M., PERFITO, N. & MOORE, I. T. 2008. Timing of breeding in tropical birds: mechanisms and evolutionary implications. Ornitologia Neotropical 19:3959.Google Scholar
HECKEL, G., VOIGT, C. C., MAYER, F. & VON HELVERSEN, O. 1999. Extra-harem paternity in the white-lined bat Saccopteryx bilineata (Emballonuridae). Behaviour 136:11731185.CrossRefGoogle Scholar
HEIDEMAN, P. D. & BRONSON, F. H. 1993. Sensitivity of Syrian-Hamsters (Mesocricetus auratus) to amplitudes and rates of photoperiod change typical of the tropics. Journal of Biological Rhythms 8:325337.CrossRefGoogle ScholarPubMed
HEIDEMAN, P. D. & BRONSON, F. H. 1994. An endogenous circannual rhythm of reproduction in a tropical bat, Anoura geoffroyi, is not entrained by photoperiod. Biology of Reproduction 50:607614.CrossRefGoogle Scholar
HEIDEMAN, P. D., DEORAJ, P. & BRONSON, F. H. 1992. Seasonal reproduction of a tropical bat, Anoura geoffroyi, in relation to photoperiod. Journal of Reproduction and Fertility 96:765773.CrossRefGoogle ScholarPubMed
HOWARD, R. D. 1980. Mating behaviour and mating success in wood frog Rana sylvatica. Animal Behaviour 28:705716.CrossRefGoogle Scholar
IMS, R. A. 1990. The ecology and evolution of reproductive synchrony. Tree 5:135140.Google ScholarPubMed
JERRETT, D. P. 1979. Female reproductive patterns in non-hibernating bats. Journal of Reproduction and Fertility 56:369378.CrossRefGoogle Scholar
KAPPELER, P. M. & VAN SCHAIK, C. P. 2004. Sexual selection in primates: review and selective preview. Pp. 323 in Kappeler, P. M. & van Schaik, C. P. (eds.). Sexual selection in primates. Cambridge University Press, Cambridge.CrossRefGoogle Scholar
KAVANAGH, M. 1983. Birth seasonality in Cercopithecus aethiops. A social advantage from synchrony? Pp. 8998 in Seth, P. K. (ed.). Perspectives in primate biology. Today and Tomorrows, New Delhi.Google Scholar
KUMMER, H. 1968. Social organization of Hamadryas baboons. Bibliotheca Primatologica 6:1189.Google Scholar
MCCRACKEN, G. F. & WILKINSON, G. S. 2000. Bat mating systems. Pp. 321362 in Crichton, E. G. & Krutzsch, P. H. (eds.). Reproductive biology of bats. Academic Press, London.CrossRefGoogle Scholar
MCLEAN, J. A. & SPEAKMAN, J. R. 1999. Energy budgets of lactating and non-reproductive brown long-eared bats (Plecotus auritus) suggest females use compensation in lactation. Functional Ecology 13:360372.CrossRefGoogle Scholar
MILLER, A. H. 1965. Capacity for photoperiodic response and endogenous factors in the reproductive cycles of an equatorial sparrow. Proceedings of the National Academy of Science, USA 54:97101.CrossRefGoogle ScholarPubMed
NELSON, R. J., BADURA, L. L. & GOLDMAN, B. D. 1990. Mechanisms of seasonal cycles of behavior. Annual Review of Psychology 41:81108.CrossRefGoogle ScholarPubMed
NOWAK, R. 1994. Walker's bats of the world. John Hopkins University Press, Baltimore. 288 pp.Google Scholar
PEREIRA, M. E. 1991. Asynchrony within estrous synchrony among ringtailed lemurs (Primates: Lemuridae). Physiology and Behavior 49:4752.CrossRefGoogle ScholarPubMed
PERFITO, N., TRAMONTIN, A. D., MEDDLE, S. L., SHARP, P., AFIK, D., GEE, J., ISHII, S., KIKUCHI, M. & WINGFIELD, J. C. 2004. Reproductive development according to elevation in a seasonally breeding male songbird. Oecologia 140:201210.CrossRefGoogle Scholar
PORTER, T. A. & WILKINSON, G. S. 2001. Birth synchrony in greater spear-nosed bats (Phyllostomus hastatus). Journal of Zoology 253:383390.CrossRefGoogle Scholar
RACEY, P. A. 1978. The effect of photoperiod on the initiation of spermatogenesis in pipistrelle bats, Pipistrellus pipistrellus. Pp. 255258 in Olembo, R. J., Castelino, J. B. & Mutere, F. A. (eds.). Proceedings of the fourth international bat research conference. Kenya National Academy of Arts and Sciences. Nairobi.Google Scholar
RACEY, P. A. 1982. Ecology of bat reproduction. Pp. 5793 in Kunz, T. H. (ed.). Ecology of bats. Plenum Press, New York.CrossRefGoogle Scholar
RACEY, P. A. & ENTWISTLE, A. C. 2000. Life history and reproductive strategies of bats. Pp. 363401 in Crichton, E. G. & Krutzsch, P. H. (eds.). Reproductive biology of bats. Academic Press, London.CrossRefGoogle Scholar
RIDLEY, M. 1986. The number of males in a primate troop. Animal Behaviour 34:18481858.CrossRefGoogle Scholar
RISSMAN, E. F., NELSON, R. J., BLANK, J. L. & BRONSON, F. H. 1987. Reproductive response of a tropical mammal, the musk shrew (Suncus murinus), to photoperiod. Journal of Reproduction and Fertility 81:563566.CrossRefGoogle ScholarPubMed
SANFORD, R. L., PAABY, P., LUVALL, J. C. & PHILLIPS, E. 1994. Climate, geomorphology, and aquatic systems. Pp. 1933 in McDade, L. A., Bawa, K. S., Hespenheide, H. A. & Hartshorn, G. S. (eds.). La Selva: ecology and natural history of a Neotropical rain forest. University of Chicago Press, Chicago.Google Scholar
SCHWARZENBERGER, F., FREDRIKSSON, G., SCHALLER, K. & KOLTER, L. 2004. Fecal steroid analysis for monitoring reproduction in the sun bear (Helarctos malayanus). Theriogenology 62:16771692.CrossRefGoogle ScholarPubMed
SIMMONS, N. B. 2005. An Eocene big bang for bats. Science 307:527528.CrossRefGoogle ScholarPubMed
STRIER, K. B. 1991. Demography and conservation in an endangered primate, Brachyteles arachnoides. Conservation Biology 5:214218.CrossRefGoogle Scholar
VAN HORN, R. N. 1975. Primate breeding season – photoperiodic regulation in captive Lemur catta. Folia Primatologica 24:203220.CrossRefGoogle ScholarPubMed
VOIGT, C. C. & SCHWARZENBERGER, F. 2008. Reproductive endocrinology of a small tropical bat (female Saccopteryx bilineata; Emballonuridae) monitored by fecal hormone metabolites. Journal of Mammalogy 89:5057.CrossRefGoogle Scholar
VOIGT, C. C. & VON HELVERSEN, O. 1999. Storage and display of odor in male Saccopteryx bilineata Emballonuridae. Behavioral Ecology and Sociobiology 47:2940.CrossRefGoogle Scholar
VOIGT, C. C., CASPERS, B. & SPECK, S. 2005. Bats, bacteria, and bat smell: sex-specific diversity of microbes in a sexually selected scent organ. Journal of Mammalogy 86:745749.CrossRefGoogle Scholar
VOIGT, C. C., STREICH, W. J. & DEHNHARD, M. 2007. Assessment of fecal testosterone metabolite analysis in free-ranging Saccopteryx bilineata (Chiroptera: Emballonuridae). Acta Chiropterologica 9:463475.CrossRefGoogle Scholar
WALLIS, J. 1985. Synchrony of estrous swelling in captive groupliving chimpanzees (Pan troglodytes). International Journal of Primatology 6:335350.CrossRefGoogle Scholar
WAYNE, N. L. & RISSMAN, E. F. 1991. Tropical photoperiods affect reproductive development in the musk shrew, Suncus murinus. Physiology and Behavior 50:549553.CrossRefGoogle ScholarPubMed
WIKELSKI, M., HAU, M. & WINGFIELD, J. C. 2000. Seasonality of reproduction in a neotropical rain forest bird. Ecology 81:24582472.CrossRefGoogle Scholar
WINGFIELD, J. C., HAHN, T. P., LEVIN, R. & HONEY, P. 1992. Environmental predictability and control of gonadal cycles in birds. Journal of Experimental Zoology 261:214231.CrossRefGoogle Scholar
YANCEY, F. F., GOETZE, J. R. & JONES, C. 1998. Saccopteryx bilineata. Mammalian Species 581:15.Google Scholar
ZINNER, D. P., SCHWIBBE, M. H. & KAUMANNS, W. 1994. Cycle synchrony and probability of conception in female hamadryas baboons Papio hamadryas. Behavioral Ecology and Sociobiology 35:175183.CrossRefGoogle Scholar