Which reproductive technologies are most relevant to studying, managing and conserving wildlife?
Budhan S. Pukazhenthi A B and David E. Wildt A C
+ Author Affiliations
- Author Affiliations
A Department of Reproductive Sciences, Smithsonian’s National Zoological Park, Conservation & Research Center, Front Royal, VA 22630, USA.
B Department of Reproductive Sciences, Smithsonian’s National Zoological Park, 3001 Connecticut Ave, N. W., Washington, DC 20008, USA.
C To whom correspondence should be addressed. email: dewildt@shentel.net
Reproduction, Fertility and Development 16(2) 33-46 https://doi.org/10.1071/RD03076
Submitted: 1 August 2003 Accepted: 1 October 2003 Published: 2 January 2004
Abstract
The advent of in vitro fertilisation (IVF) and embryo transfer in the 1970s led to speculation about the potential value of these and other ‘reproductive technologies’ to conserving endangered species. So far, and for the most part, assisted breeding techniques that are routine in domesticated species are not easily adapted to wildlife. Species differences in reproductive form (anatomy/morphology) and function (mechanisms regulating reproductive success) limit the practical applicability for offspring production. Thus, the limiting factor is the lack of basic knowledge about thousands of unstudied species, the foundation that is essential to allowing reproduction to be enhanced and/or controlled. There now is excellent evidence that reproductive technologies are most useful as tools for studying how different species reproduce, especially defining novel and unique mechanisms. The present paper reviews the status and relevance of various reproductive technologies that are useful or have potential for wildlife. Modern examples of progress are provided indicating how these tools are being used to understand ways that wildlife species reproduce and, in some cases, how such knowledge has been used for successful assisted breeding, improved management and conservation.
Acknowledgments
The authors thank colleagues in the Department of Reproductive Sciences, especially Drs JoGayle Howard, Steven Monfort, Janine Brown and Rebecca Spindler, who supervised many of the published studies cited throughout this paper. This work was supported, in part, by generous grants from the National Institutes of Health, the Smithsonian Institution’s Scholarly Studies Program, the Morris Animal Foundation and Friends of the National Zoo.
References
Bamberg, E. , Choi, H. S. , Möstl, E. , Wurm, W. , Lorin, D. , and Arbeiter, K. (1984). Enzymatic determination of unconjugated oestrogens in faeces for pregnancy diagnosis in mares. Equine Vet. J. 16, 537–539.
| PubMed |
Berger, J. , Testa, J. W. , Roffe, T. , and Monfort, S. L. (1999). Conservation endocrinology: a noninvasive tool to understand relationships between carnivore colonization and ecological carrying capacity. Conserv. Pract. 13, 980–989.
| Crossref | GoogleScholarGoogle Scholar |
Blanco, J. M. , Gee, G. F. , Wildt, D. E. , and Donoghue, A. M. (2002). Producing progeny from endangered birds of prey: treatment of urine-contaminated semen and a novel intramagnal insemination approach. J. Zoo Wildl. Med. 33, 1–7.
| PubMed |
Brown, J. L. (2000). Reproductive endocrine monitoring of elephants: an essential tool for assisting captive management. Zoo Biol. 19, 347–367.
| Crossref | GoogleScholarGoogle Scholar |
Brown, J. L. , Wildt, D. E. , Graham, L. H. , Byers, A. P. , Collins, L. , Barrett, S. , and Howard, J. G. (1995). Natural versus chorionic gonadotropin-induced ovarian responses in the clouded leopard (Neofelis nebulosa) assessed by fecal steroid analysis. Biol. Reprod. 53, 93–102.
| PubMed |
Brown, J. L. , Schmitt, D. L. , Bellem, A. , Graham, L. H. , and Lehnhardt, J. (1999). Hormone secretion in the Asian elephant (Elephas maximus): characterization of ovulatory and anovulatory luteinizing hormone surges. Biol. Reprod. 61, 1294–1299.
| PubMed |
Brown, J. L. , Graham, L. H. , Wielebnowski, N. , Swanson, W. F. , Wildt, D. E. , and Howard, J. G. (2001a). Understanding the basic reproductive biology of wild felids by monitoring of fecal steroids. J. Reprod. Fertil. Suppl. 57, 71–82.
| PubMed |
Brown, J. L. , Bellem, A. C. , Fouraker, M. , Wildt, D. E. , and Roth, T. L. (2001b). Comparative analysis of gonadal and adrenal activity in the black and white rhinoceros in North America by non-invasive endocrine monitoring. Zoo Biol. 20, 463–486.
| Crossref | GoogleScholarGoogle Scholar |
Campbell, K. H. S. (1999). Nuclear transfer in farm animal species. Semin. Cell Dev. Biol. 10, 245–252.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Candy, C. J. , Wood, M. J. , and Whittingham, D. G. (1995). Follicular development in cryopreserved marmoset tissue after transplantation. Hum. Reprod. 10, 2334–2338.
| PubMed |
Creel, S. R. , Creel, N. M. , Wildt, D. E. , and Monfort, S. L. (1992). Behavioral and endocrine mechanism of reproductive suppression in Serengeti dwarf mongooses. Anim. Behav. 43, 231–245.
Creel, S. R. , Creel, N. M. , Mills, M. G. L. , and Monfort, S. L. (1997). Rank and reproduction in cooperatively breeding African wild dogs: behavioral and endocrine correlates. Behav. Ecol. 8, 298–306.
Crichton, E. G. , Bedows, E. , Miller-Lindholm, A. K. , Baldwin, D. M. , and Armstrong, D. L. , et al. (2003). Efficacy of porcine gonadotropins for repeated stimulation of ovarian activity for oocyte retrieval and in vitro embryo production and cryopreservation in Siberian tigers (Panthera tigris altaica). Biol. Reprod. 68, 105–113.
| PubMed |
Critser, J. K., Riley, L. K. and Prather, R. S. (2003). Application of nuclear transfer technology to wildlife species. In
Czekala, N. M. , and Callison, L. (1996). Pregnancy diagnosis in the black rhinoceros (Diceros bicornis) by salivary hormone analysis. Zoo Biol. 15, 37–44.
| Crossref | GoogleScholarGoogle Scholar |
Donoghue, A. M., Blanco, J. M., Gee, G. F., Kirby, Y. K. and Wildt, D. E. (2003). Reproductive technologies and challenges in avian conservation and management. In
Farstad, W. (2000). Assisted reproductive technologies in canid species. Theriogenology 53, 175–186.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Garner, D. L. (2001). Sex sorting mammalian sperm: concept to application in animals. J. Androl. 22, 519–526.
| PubMed |
Garniera, J. N. , Green, D. I. , Pickard, A. R. , Shaw, H. J. , and Holt, W. V. (1998). Non-invasive diagnosis of pregnancy in wild black rhinoceros (Diceros bicornis minor) by fecal steroid analysis. Reprod. Fertil. Dev. 10, 451–468.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Gee, G. F. (1995). Artificial insemination and cryopreservation of semen from nondomesticated birds. In
Gianaroli, L. , Selman, H. A. , Magli, M. C. , Colpi, G. , Fortini, D. , and Ferraretti, A. P. (1999). Birth of a healthy infant after conception with round spermatids isolated from cryopreserved testicular tissue. Fertil. Steril. 72, 539–541.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Glatston, A. R. (1995). Sex ratios and breeding programmes. In
Greenwald, G. S. (1970). Development of ovulatory refractoriness in the rabbit to cyclic injections of human chorionic gonadotropin. Fertil. Steril. 21, 163–168.
| PubMed |
Gunasena, K. T. , Lakey, J. R. , Villines, P. M. , Bush, M. , Raath, C. , Critser, E. S. , McGann, L. E. , and Critser, J. K. (1998). Antral follicles develop in xenografted cryopreserved African elephant (Loxodonta africana) ovarian tissue. Anim. Reprod. Sci. 53, 265–275.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Harnal, V. K. , Wildt, D. E. , Bird, D. M. , Monfort, S. L. , and Ballou, J. D. (2002). Computer simulations to determine the efficacy of different genome resource banking strategies for maintaining genetic diversity. Cryobiology 44, 122–131.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Heisterman, M. , Agil, M. , Buthe, A. , and Hodges, J. K. (1998). Metabolism and excretion of oestradiol-17β and progesterone in the Sumatran rhinoceros (Dicerorhinus sumatrensis). Anim. Reprod. Sci. 53, 157–172.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Hildebrandt, T. B. , Hermes, R. , Jewgenow, K. , and Göritz, F. (2000). Ultrasonography as an important tool for the development and application of reproductive technologies in non-domestic species. Theriogenology 53, 73–84.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Hildebrandt, T. B., Brown, J. L., Hermes, R. and Göritz, F. (2003). Ultrasound for analysis of reproductive function in wildlife species. In
Hirschenhauser, K. , Mostl, E. , and Kotrschal, K. (1999). Seasonal patterns of sex steroids determined from feces in different social categories of greylag geese (Anser anser). Gen. Comp. Endocrinol. 114, 67–79.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Hodges, J. K. (1996). Determining and manipulating female reproductive parameters. In
Hodges, J. K. (2001). Reproductive technologies necessary for successful applications of genetic resource banking. In
Hodges, J. K. , Czekala, N. M. , and Lasley, B. L. (1979). Estrogen and luteinizing hormone secretion in diverse primate species from simplified urinary analysis. J. Med. Primatol. 8, 349–364.
| PubMed |
Holt, W. V. , Bennett, P. M. , Volovouev, V. , and Watson, P. F. (1996a). Genetic resource banks in wildlife conservation. J. Zool. 238, 531–534.
Holt, W. V. , Abaigar, T. , and Jabbour, H. N. (1996b). Oestrous synchronization, semen preservation and artificial insemination in the Mohor gazelle (Gazella dama mhorr) for the establishment of a genome resource bank programme. Reprod. Fertil. Dev. 8, 1215–1222.
| PubMed |
Holt, W. V., Pickard, A. R., Rodger, J. C., and Wildt, D. E. (2003).
Holt, W. V., Abaigar, T., Watson, P. F. and Wildt, D. E. (2003). Genetic resource banks for species conservation. In
Honaramooz, A. , Snedaker, A. , Boiani, M. , Scholer, H. , and Dobrinski, I. (2002). Sperm from neonatal mammalian testes grafted in mice. Nature 418, 778–781.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Howard, J. G. (1999). Assisted reproductive techniques in nondomestic carnivores. In
Howard, J. G., Marinari, P. E. and Wildt, D. E. (2003). Black-footed ferret: model for assisted reproductive technologies contributing to in situ conservation. In
Huang, Y., Wang, P., Zhang, G., Zhang, H. and Li, D. (2002). Use of artificial insemination to enhance propagation of giant pandas at the Wolong Breeding Center. In
Hutchins, M. , and Wiese, R. J. (1991). Beyond genetic and demographic management: the future of the Species Survival Plan and related American Association of Zoological Parks and Aquariums conservation efforts. Zoo Biol. 10, 285–292.
Jainudeen, M. R. , Hafez, E. S. E. , Gollnick, P. D. , and Moustafa, L. A. (1966). Anti-gonadotropins in the serum of cows following repeated therapeutic pregnant mares’ serum injections. Am. J. Vet. Res. 27, 669–675.
| PubMed |
Johnson, L. A. (2000). Sexing mammalian sperm for production of offspring: the state-of-the-art. Anim. Reprod. Sci. 60–61, 93–107.
| Crossref | GoogleScholarGoogle Scholar |
Kersey, D. C. , Brown, J. L. , Czekala, N. M. , and Monfort, S. L. (2003). Fecal steroid monitoring to study the reproductive biology of the endangered giant panda (Ailuropoda melanoleuca). Biol. Reprod. 68, 125.Suppl. 1, (Abstract)
Kirkpatrick, J. F. , McCarthy, J. C. , Gudermuth, D. F. , Shideler, S. E. , and Lasley, B. L. (1996). An assessment of the reproductive biology of Yellowstone bison (Bison bison) subpopulations using non-capture methods. Can. J. Zool. 74, 8–14.
Lanza, R. P. , Cibelli, J. B. , Diaz, F. , Moraes, C. T. , Farin, P. W. , Farin, C. E. , Hammer, C. J. , West, M. D. , and Damiani, P. (2000). Cloning of an endangered species (Bos gaurus) using interspecies nuclear transfer. Cloning 2, 79–90.
| Crossref | GoogleScholarGoogle Scholar |
Lasley, B. L. , and Kirkpatrick, J. F. (1991). Monitoring ovarian function in captive and free-ranging wildlife by means of urinary and fecal steroids. J. Zoo Wildl. Med. 22, 23–31.
Lasley, B. L. , Loskutoff, N. M. , and Anderson, G. B. (1994). The limitation of conventional breeding programs and the need and promise of assisted reproduction in nondomestic species. Theriogenology 41, 119–132.
Loskutoff, N. M. , Bartels, P. , Meintjes, M. , Godke, R. A. , and Schiewe, M. C. (1995). Assisted reproductive technologies in nondomestic ungulates: a model approach to preserving and managing genetic diversity. Theriogenology 43, 3–12.
| Crossref | GoogleScholarGoogle Scholar |
Loskutoff, N. M. (2003). Role of embryo technologies in genetic management and conservation of wildlife. In
Monfort, S. L. (2003). Non-invasive endocrine measures of reproduction and stress in wild populations. In
Monfort, S. L. , Wemmer, C. , Kepler, T. H. , Bush, M. , Brown, J. L. , and Wildt, D. E. (1990). Monitoring ovarian function and pregnancy in the Eld’s deer (Cervus eldi) by evaluating urinary steroid metabolite excretion. J. Reprod. Fertil. 88, 271–281.
| PubMed |
Monfort, S. L. , Asher, G. W. , Wildt, D. E. , Wood, T. C. , Schiewe, M. C. , Williamson, L. R. , Bush, M. , and Rall, W. F. (1993). Successful intrauterine insemination of the Eld’s deer (Cervus eldi thamin) with frozen–thawed spermatozoa. J. Reprod. Fertil. 99, 459–465.
| PubMed |
Morrow, C. J. , Wolfe, B. A. , Roth, T. L. , Wildt, D. E. , Bush, M. , Blumer, E. S. , Atkinson, M. W. , and Monfort, S. L. (2000). Comparing ovulation synchronization protocols for artificial insemination in the scimitar-horned oryx (Oryx dammah). Anim. Reprod. Sci. 59, 71–86.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
O’Brien, J. K., Crichton, E. G., Evans, K. M., Schenk, J. L., Stojanov, T., Evans, G., Maxwell, W. M. C. and Loskutoff, N. M. (2002). Sex ratio modification using sperm sorting and assisted reproductive technology: a population management strategy. In
Olson, D. , and Wiese, R. J. (2000). State of the North American African elephant population and projections for the future. Zoo Biol. 19, 311–320.
| Crossref | GoogleScholarGoogle Scholar |
Ottobre, J. , and Stouffer, R. L. (1985). Antibody production in rhesus monkeys following prolonged administration of human chorionic gonadotropin. Fertil. Steril. 43, 122–128.
| PubMed |
Paris, M. C. , White, A. , Reiss, A. , West, M. , and Schwarzenberger, F. (2002). Fecal progesterone metabolites and behavioral observations for the non-invasive monitoring of oestrous cycles in the common wombat (Vombatus ursinus) and the southern hairy-nosed wombat (Lasiorhinus latifrons). Anim. Reprod. Sci. 72, 245–257.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Paynter, S., Cooper, A., Thomas, N. and Fuller, B. (1997). Cryopreservation of multicellular embryos and reproductive tissues. In
Pelican, K. M., Wildt, D. E. and Howard, J. G. (2003). Ovarian control and assisted reproduction in felids. In
Perlman, D. L., Adelson, G., and Wilson, E. O. (1997).
Pickard, A. R. (2003). Reproductive and welfare monitoring for the management of ex situ populations. In
Pope, C. E. (2000). Embryo technology in conservation efforts for endangered felids. Theriogenology 53, 163–174.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Pope, C. E. and Loskutoff, N. M. (1999). Embryo transfer and semen technology from cattle applied to nondomestic artiodactylids. In
Pope, C. E. , Gomez, M. C. , Mikota, S. K. , and Dresser, B. L. (2000). Development of in vitro produced African wildcat (Felis silvestris) embryos after cryopreservation and transfer in domestic cat recipients. Biol. Reprod. 62, 544.Suppl. 1, (Abstract)
Pukazhenthi, B. S. , Pelican, K. , Wildt, D. E. , and Howard, J. G. (1999). Sensitivity of domestic cat (Felis catus) sperm from normospermic versus teratospermic donors to cold-induced acrosomal damage. Biol. Reprod. 61, 135–141.
| PubMed |
Roelke-Parker, M. E. , Munson, L. , Parker, C. , Kock, R. , Cleaveland, S. , Carpenter, M. , O’Brien, S. J. , Pospischil, A. , and Hofmann-Lehmann, R. (1996). A canine distemper virus epidemic in Serengeti lions (Panthera leo). Nature 379, 441–445.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Roth, T. L. , Howard, J. G. , Donoghue, A. M. , Swanson, W. F. , and Wildt, D. E. (1994). Function and culture requirements of snow leopard (Panthera uncia) spermatozoa in vitro. J. Reprod. Fertil. 101, 563–569.
| PubMed |
Roth, T. L. , Bush, L. M. , Wildt, D. E. , and Weiss, R. B. (1999). Scimitar-horned oryx (Oryx dammah) spermatozoa are functionally competent in a heterologous bovine in vitro fertilization system after cryopreservation on dry ice, in a dry shipper or over liquid nitrogen vapor. Biol. Reprod. 60, 493–498.
| PubMed |
Roy, F. , Maurel, M. C. , Combes, B. , Vaiman, D. , Cribiu, E. P. , Lantier, I. , Pebel, T. , Deletang, F. , Comnarnous, Y. , and Guillou, F. (1999). The negative effect of repeated equine chorionic gonadotropin treatment on subsequent fertility in alpine goats is due to humoral immune response involving the major histocompatibility complex. Biol. Reprod. 60, 805–813.
| PubMed |
Russell, L. D. , and Griswold, M. D. (2000). Spermatogonial transplantation: an update for the millennium. Mol. Cell. Endocrinol. 161, 117–120.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Schenk, J. L. , and DeGrofft, D. L. (2003). Insemination of cow elk with sexed frozen semen. Theriogenology 59, 514.(Abstract)
Schiewe, M. C. , Bush, M. , Phillips, L. G. , Citino, S. , and Wildt, D. E. (1991). Comparative aspects of estrus synchronization, ovulation induction and embryo cryopreservation in the scimitar-horned oryx, bongo, eland and greater kudu. J. Exp. Zool. 258, 75–88.
Schwarzenberger, F. , Walzer, C. , Tomasova, K. , Vahala, J. , Meister, J. , Goodrowe, K. L. , Zima, J. , Strauss, G. , and Lynch, M. (1998). Fecal progesterone metabolite analysis for non-invasive monitoring of reproductive function in the white rhinoceros (Ceratotherium simum). Anim. Reprod. Sci. 53, 173–190.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Shaw, J. M. , Oranratnachai, A. , and Trounson, A. O. (2000). Fundamental cryobiology of mammalian oocytes and ovarian tissue. Theriogenology 53, 59–72.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Snow, M. , Cox, S. L. , Jenkin, G. , Trounson, A. , and Shaw, J. (2002). Generation of live young from xenografted mouse ovaries. Science 297, 2227–2229.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Solti, L. , Crichton, E. G. , Loskutoff, N. M. , and Cseh, S. (2000). Economical and ecological importance of indigenous livestock and the application of assisted reproduction in their preservation. Theriogenology 53, 149–162.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Staley, A. M. , Blanco, J. M. , Dufty, A. M. , Wildt, D. E. , and Monfort, S. L. (2003). Non-invasive fecal steroid monitoring provides insight into gonadal and adrenal function in the golden eagle (Aquila chrysaetos) and peregrine falcon (Falco peregrinus). Biol. Reprod. 68, 126.Suppl. 1 (Abstract)
Steinman, K. J. , Monfort, S. L. , Jensen, E. D. , Sweeney, J. , Havlis, D. , and Robeck, T. R. (2003). A mobile endocrinology laboratory for assessing reproductive status and timing artificial insemination in captive cetaceans. Proc. Int. Assoc. Aquat. Anim. Med. 34, 45–49.
Swain, J. E. , and Miller, R. R. (2000). A postcryogenic comparison of membrane fatty acids of elephant spermatozoa. Zoo Biol. 19, 461–473.
| Crossref | GoogleScholarGoogle Scholar |
Swanson, W. F. (2001). Reproductive biotechnology and conservation of the forgotten felids: the small cats. In
Swanson, W. F. , Horohov, D. W. , and Godke, R. A. (1995). Production of exogenous gonadotropin-neutralizing immunoglobulins in cats after repeated eCG–hCG treatment and relevance for assisted reproduction in felids. J. Reprod. Fertil. 105, 35–41.
| PubMed |
Taylor, A. C. (2003). Assessing the consequences of inbreeding for population fitness: past challenges and future prospects. In
Tucker, M. J. , Wright, G. , Morton, P. C. , and Massey, J. B. (1998). Birth after cryopreservation of immature oocytes with subsequent in vitro maturation. Fertil. Steril. 70, 578–579.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Vajta, G. (2000). Vitrification of the oocytes and embryos of domestic animals. Anim. Reprod. Sci. 60–61, 357–364.
| Crossref | GoogleScholarGoogle Scholar |
Watson, P. F. and Fuller, B. J. (2001). Principles of cryopreservation of gametes and embryos. In
Watson, P. F. and Holt, W. V. (2001). Organizational issues concerning the establishment of a genetic resource bank. In
Wielebnowski, N. C. , Ziegler, K. , Wildt, D. E. , Lukas, J. , and Brown, J. L. (2002a). Impact of social management on reproductive, adrenal and behavioral activity in the cheetah (Acinonyx jubatus). Anim. Conserv. 5, 291–301.
| Crossref | GoogleScholarGoogle Scholar |
Wielebnowski, N. C. , Fletchall, N. , Carlstead, K. , Busso, J. M. , and Brown, J. L. (2002b). Non-invasive assessment of adrenal activity associated with husbandry and behavioral factors in the North American clouded leopard population. Zoo Biol. 21, 77–98.
| Crossref | GoogleScholarGoogle Scholar |
Wiese, R. J. (2000). Asian elephants are not self-sustaining in North America. Zoo Biol. 19, 299–309.
| Crossref | GoogleScholarGoogle Scholar |
Wildt, D. E. , and Wemmer, C. (1999). Sex and wildlife: the role of reproductive biology in conservation. Biodiv. Conserv. 8, 965–976.
| Crossref | GoogleScholarGoogle Scholar |
Wildt, D. E. , Bush, M. , Morton, C. , Morton, F. , and Howard, J. G. (1989). Semen characteristics and testosterone profiles in ferrets kept in long-day photoperiod, and the influence of hCG timing and sperm dilution on pregnancy rate after laparoscopic insemination. J. Reprod. Fertil. 86, 349–358.
| PubMed |
Wildt, D. E. , Rall, W. F. , Critser, J. K. , Monfort, S. L. , and Seal, U. S. (1997). Genome resource banks: ‘living collections’ for biodiversity conservation. Bioscience 47, 689–698.
Wildt, D. E., Brown, J. L. and Swanson, W. F. (1998). Reproduction in cats. In
Wildt, D. E., Ellis, S. and Howard, J. G. (2001). Linkage of reproductive sciences: from ‘quick-fix’ to ‘integrated’ conservation. In
Wildt, D. E., Ellis, S., Janssen, D. and Buff, J. (2003). Toward more effective science for conservation. In
Wilson, E. O. (1992).
Wolvecamp, M. C. J. , MacCallum, C. , Cleary, M. , Shaw, J. , Cox, S. , Jenkin, G. , and Trounsen, A. O. (2000). Novel approach to save the critically endangered northern hairy-nosed wombat (Lasiorhinus Kefftii). Theriogenology 53, 345.
Younis, A. I. , Toner, M. , Albertini, D. F. , and Biggers, J. D. (1996). Cryobiology of nonhuman primate oocytes. Hum. Reprod. 11, 156–165.
| PubMed |
