Reproductive history and absence of predators are important determinants of reproductive fitness: the cheetah controversy revisited
Bettina Wachter
Leibniz Institute for Zoo and Wildlife Research, Alfred-Kowalke-Str. 17, D-10315 Berlin, Germany
Search for more papers by this authorSusanne Thalwitzer
Leibniz Institute for Zoo and Wildlife Research, Alfred-Kowalke-Str. 17, D-10315 Berlin, Germany
Search for more papers by this authorHeribert Hofer
Leibniz Institute for Zoo and Wildlife Research, Alfred-Kowalke-Str. 17, D-10315 Berlin, Germany
Search for more papers by this authorJohann Lonzer
Leibniz Institute for Zoo and Wildlife Research, Alfred-Kowalke-Str. 17, D-10315 Berlin, Germany
Search for more papers by this authorThomas B. Hildebrandt
Leibniz Institute for Zoo and Wildlife Research, Alfred-Kowalke-Str. 17, D-10315 Berlin, Germany
Search for more papers by this authorRobert Hermes
Leibniz Institute for Zoo and Wildlife Research, Alfred-Kowalke-Str. 17, D-10315 Berlin, Germany
Search for more papers by this authorBettina Wachter
Leibniz Institute for Zoo and Wildlife Research, Alfred-Kowalke-Str. 17, D-10315 Berlin, Germany
Search for more papers by this authorSusanne Thalwitzer
Leibniz Institute for Zoo and Wildlife Research, Alfred-Kowalke-Str. 17, D-10315 Berlin, Germany
Search for more papers by this authorHeribert Hofer
Leibniz Institute for Zoo and Wildlife Research, Alfred-Kowalke-Str. 17, D-10315 Berlin, Germany
Search for more papers by this authorJohann Lonzer
Leibniz Institute for Zoo and Wildlife Research, Alfred-Kowalke-Str. 17, D-10315 Berlin, Germany
Search for more papers by this authorThomas B. Hildebrandt
Leibniz Institute for Zoo and Wildlife Research, Alfred-Kowalke-Str. 17, D-10315 Berlin, Germany
Search for more papers by this authorRobert Hermes
Leibniz Institute for Zoo and Wildlife Research, Alfred-Kowalke-Str. 17, D-10315 Berlin, Germany
Search for more papers by this authorEditor Corey Bradshaw
Abstract
Re-introduction programs rely on reproductively sound individuals and high offspring survival once captively bred species are released into their natural habitat. Some species involved in captive breeding programs reproduce poorly: one prominent example is the cheetah (Acinonyx jubatus). Here we use the cheetah as a case study to test predictions from all current hypotheses explaining this phenomenon by monitoring postemergence cub survival and assessing the reproductive status of free-ranging and captive female cheetahs in Namibia with ultrasonography. We show that reproductive activity and health of cheetah females is determined by reproductive history and age rather than innate rhythms, captive stress, or lack of genetic diversity, and that postemergence cub survival under natural conditions in a predator-free habitat is high. Our results suggest that management practices of captive breeding and re-introduction programs should encourage early reproduction in females to induce long-lasting and healthy reproductive performance. With this practice, re-introduction projects might increase their chances of success.
References
- Brown, J.L., Wildt D.E., Wielebnowski N. et al . (1996) Reproductive activity in captive female cheetahs (Acinonyx jubatus) assessed by faecal steroids. J Reprod Fertil 106, 337–346.
- Caughley, G. (1994) Directions in conservation biology. J Anim Ecol 63, 215–244.
- Caro, T. (1994) Cheethas of the Serengeti plains: group living in an asocial species. The University of Chicago Press, Chicago , USA .
- Caro, T.M., Laurenson K.M. (1994) Ecological and genetic factors in conservation: a cautionary tale. Science 263, 485–486.
-
Courchamp, F.,
Berec L.,
Gascoigne J. (2008) Allee effects in ecology and conservation. Oxford University Press,
Oxford
,
UK
.
10.1093/acprof:oso/9780198570301.001.0001 Google Scholar
- Crosier, A.E., Pukazhenthi B.S., Henghali J.N. et al . (2006) Cryopreservation of spermatozoa from wild-born Namibian cheetahs (Acinonyx jubatus) and influence of glycerol on cryosurvival. Cryobiology 52, 169–181.
- Ebenhard, T. (1995) Conservation breeding as a tool for saving animal species from extinction. Trends Ecol Evol 10, 438–443.
- Fickel, J., Wagener A., Ludwig A. (2007) Semen cryopreservation and the conservation of endangered species. Eur J Wildl Res 53, 81–89.
-
Frankham, R.,
Ballou J.D.,
Briscoe D.A. (2002) Introduction to conservation genetics. Cambridge University Press,
Cambridge
,
UK
.
10.1046/j.1365-294X.2003.01702.x Google Scholar
- Frankham, R. (2008) Genetic adaptation to captivity in species conservation programs. Mol Ecol 17, 325–333.
- Heppell, S.S., Caswell H., Crowder L.B. (2000) Life histories and elasticity patterns: perturbation analysis for species with minimal demographic data. Ecology 81, 654–665.
- Hermes, R., Hildebrandt T.B., Göritz F., Jewgenow K., Lengwinat T., Hofmann R.R. (2000) Ultrasonography of the ovaries and uterus and grey scale analysis of the endometrium during embryonic diapause in European roe deer (Capreolus capreolus). Acta Theriol 45, 559–572.
- Hermes, R., Hildebrandt T.B., Göritz F. (2004) Reproductive problems directly attributable to long-term captivity—asymmetric reproductive aging. Anim Reprod Sci 82–83, 49–60.
- Hermes, R., Hildebrandt T.B., Walzer C. et al . (2006) The effect of long non-reproductive periods on the genital health in captive female white rhinoceroses (Ceratotherium simum simum, C.s. cottoni). Theriogenology 65, 1492–1515.
- Hildebrandt, T.B., Göritz F., Pratt N.C. et al . (2000a) Ultrasonography of the urogenital tract in elephants (Loxodonta africana and Elephas maximus): an important tool for assessing female reproductive function. Zoo Biol 19, 321–332.
- Hildebrandt, T.B., Hermes R., Jewgenow K., Göritz F. (2000b) Ultrasonography as an important tool for the development and application of reproductive technologies in non-domestic species. Theriogenology 53, 73–84.
- Jurke, M.H., Czekala N.M., Lindburg D.G. Millard S.E. (1997) Fecal corticoid metabolite measurement in the cheetah (Acinonyx jubatus). Zoo Biol 16, 133–147.
-
Kleinman, D.G.,
Stanley Price M.R.,
Beck B.B. (1994) Criteria for reintroduction. Pages
287–303
in
P.J.S. Olney,
G.M. Mace,
A.T.C. Feistner, editors. Creative conservation: interactive management of wild and captive animals. Chapman and Hall,
London
.
10.1007/978-94-011-0721-1_14 Google Scholar
- Kraaijeveld-Smit, F.J.L., Griffiths R.A., Moore R.D., Beebee T.J.C. (2006) Captive breeding and the fitness of reintroduction species: a test of the response to predators in a threatened amphibian. J Appl Ecol 43, 360–365.
- Laurenson, K.M. (1992) Reproductive strategies of wild female cheetahs. PhD thesis. University of Cambridge.
- Laurenson, K.M. (1994) High juvenile mortality in cheetahs (Acinonyx jubatus) and its consequences for maternal care. J Zool Lond 234, 387–408.
- Laurenson, K.M., Caro T.M., Gros P., Wielebnowski N. (1995) Controversial cheetahs? Nature 377, 392–392.
- Lu, Z., Pan W., Zhu X., Wang D., Wang H. (2000) What has the panda taught us? Pages 325–334 in A. Entwistle, N. Dunstone, editors. Priorities for the conservation of mammalian diversity: has the panda had its day? Cambridge University Press, Cambridge .
- Marker, L.L., Dickman A.J., Jeo R.M., Mills M.G.L., Macdonald D.W. (2003) Demography of the Namibian cheetah, Acinonyx jubatus jubatus. Biol Conserv 114, 413–425.
- Marker-Kraus, L., Grisham J. (1993) Captive breeding of cheetahs in North American Zoos: 1987–1991. Zoo Biol 12, 5–18.
- Mendelsohn, J., Jarvis A., Roberts C., Robertson T. (2002) Atlas of Namibia—a portrait of the land and its people. David Philip Publishers, Cape Town , RSA .
- Merola, M. (1994) A reassessment of homozygosity and the case for inbreeding depression in the cheetah, Acinonyx jubatus: implications for conservation. Conserv Biol 8, 961–971.
- Munson, L. (1993) Disease of captive cheetahs (Acinonyx jubatus): results of the cheetah research council pathology survey, 1989–1992. Zoo Biol 12, 105–124.
- O’Brien, S.J., Roelke M.E., Marker L. et al . (1985) Genetic basis for species vulnerability in the cheetah. Science 227, 1428–1434.
- O’Brien, S.J., Wildt D.E., Goldman D., Merril C.R., Bush M. (1983) The cheetah is depauperate in genetic variation. Science 221, 459–462.
- O’Brien, S.J. (1994) The cheetah's conservation controversy. Conserv Biol 8, 1153–1155.
- Olson, D., Wiese R.J. (2000) State of the North American African elephant population and projections for the future. Zoo Biol 19, 311–320.
- Schmidt, P.M., Chakraborty P.K., Wildt D.E. (1983) Ovarian activity, circulating hormones and sexual behavior in the cat. II. Relationships during pregnancy, parturition, lactation and the postpartum estrus. Biol Reprod 28, 657–671.
- Seddon, P.J., Soorae P.S., Launay F. (2005) Taxonomic bias in reintroduction projects. Anim Conserv 8, 51–58.
- Suleman, M.A., Wango E., Farah I.O., Hau J. (2000) Adrenal cortex and stomach lesions associated with stress in wild male African green monkeys (Cercopithecus aethiops) in the post-capture period. J Med Primatol 29, 338–342.
- Terio, K.A., Marker L., Overstrom E.W., Brown J.L. (2003) Analysis of ovarian and adrenal activity in Namibian cheetahs. S Afr J Wildl Res 33, 71–78.
- Terio, K.A., Marker L., Munson L. (2004) Evidence for chronic stress in captive but not free-ranging cheetahs (Acinonyx jubatus) based on adrenal morphology and function. J Wildl Dis 40, 259–266.
- Thalwitzer, S. (2007) Reproductive activity in cheetah females, cub survival and health in male and female cheetahs on Namibian farmland. PhD thesis. Freie Universität Berlin.
- Wielebnowski, N. (1996) Reassessing the relationship between juvenile mortality and genetic monomorphism in captive cheetah. Zoo Biol 15, 353–369.
- Wildt, D.E., Brown J.L., Bush M. et al . (1993) Reproductive status of cheetahs (Acinonyx jubatus) in North American Zoos: the benefits of physiological surveys for strategic planning. Zoo Biol 12, 45–80.
- Williams, S.E., Hoffman E.A. (2009) Minimizing genetic adaptation in captive breeding programs: a review. Biol Conserv 142, 2388–2400.
