Implementing the use of a biobank in the endangered black-footed ferret (Mustela nigripes)
Rachel SantymireDavee Center for Epidemiology and Endocrinology, Lincoln Park Zoo, 2001 North Clark Street, Chicago, IL 60614, USA. Email: rsantymire@lpzoo.org
Reproduction, Fertility and Development 28(8) 1097-1104 https://doi.org/10.1071/RD15461
Submitted: 8 November 2015 Accepted: 2 February 2016 Published: 9 March 2016
Abstract
In the current global health climate, many conservation biologists are managing crisis situations, including increased species extinction rates. One strategy for securing wildlife populations into the future is to preserve biomaterials in genome resource banks (GRB; or ‘biobanks’). However, for GRBs to be successful we must understand the fundamental reproductive biology of species, along with developing assisted reproductive techniques (ARTs), including AI and semen cryopreservation. ART has been successfully used for several taxa, from amphibians to mammals, including ungulates, carnivores and primates. Not all these success stories implemented the use of a biobank, but one example that discussed herein is the black-footed ferret (Mustela nigripes) GRB. From a founder population of seven individuals, this species has been breeding in a managed setting for nearly 30 years. The goal of the breeding program is to maintain genetic integrity by ensuring each individual has the opportunity to pass his/her genes onto the next generation, while simultaneously providing animals for release into the wild. Scientists have used ART (e.g. AI) in the recovery program. Recently, semen from an individual of the founder population that was cryopreserved for up to 20 years was used successfully for AI, which improved the genetic diversity of the population. The black-footed ferret recovery program can serve as a model for other endangered species and demonstrates the usefulness of ART and GRBs to maintain highly endangered species into the future.
Additional keywords: artificial insemination, assisted reproductive technology, cryopreservation, reproduction, semen.
References
Anderson, E., Forrest, S. C., Clark, T. W., and Richardson, L. (1986). Paleobiology, biogeography, and systematics of the black-footed ferret, Mustela nigripes. Great Basin Nat. Memoirs 8, 11–62.Asher, G. W., Fisher, M. W., Fennessy, P. F., Mackintosh, C. G., Jabbour, H. N., and Morrow, C. J. (1993). Oestrous synchronization, semen collection and artificial insemination of farmed red deer (Cervus elaphus) and fallow deer (Dama dama). Anim. Reprod. Sci. 33, 241–265.
| Oestrous synchronization, semen collection and artificial insemination of farmed red deer (Cervus elaphus) and fallow deer (Dama dama).Crossref | GoogleScholarGoogle Scholar |
Atherton, R. W., Straley, M., Curry, P., Slaughter, R., Burgess, W., and Kitchin, R. M. (1989). Electroejaculation and cryopreservation of domestic ferret sperm. In ‘Conservation Biology and the Black-Footed Ferret’. (Eds U. S. Seal, S. H. Anderson, and M. A. Bodan.) pp. 177–189. (Yale University Press: New Haven, MA.)
Ballou, J. D., Earnhardt, J., and Thompson, S. (2001). ‘MateRx: Population Management Software.’ (National Zoological Park: Washington, D.C.)
Barone, M. A., Roelke, M. E., Howard, J. G., Brown, J. L., Anderson, A. E., and Wildt, D. E. (1994). Reproductive characteristics of male Florida panthers: comparative studies from Florida, Texas, Colorado, Latin America, and North American Zoos. J. Mammal. 75, 150–162.
| Reproductive characteristics of male Florida panthers: comparative studies from Florida, Texas, Colorado, Latin America, and North American Zoos.Crossref | GoogleScholarGoogle Scholar |
Blanco, J. M., Gee, G., Wildt, D. E., and Donoghue, A. M. (2000). Species variation in osmotic, cryoprotectant, and cooling rate tolerance in poultry, eagle, and peregrine falcon spermatozoa Biol. Reprod. 63, 1164–1171.
| Species variation in osmotic, cryoprotectant, and cooling rate tolerance in poultry, eagle, and peregrine falcon spermatozoaCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXmslylurs%3D&md5=46bf2618d822b5481bb7e9740e257946CAS | 10993841PubMed |
Bonduelle, M., Aytoz, A., Van Assche, E., Devroey, P., Liebaers, I., and Van Steirteghem, A. (1998). Incidence of chromosomal aberrations in children born after assisted reproduction through intracytoplasmic sperm injection. Hum. Reprod. 13, 781–782.
| Incidence of chromosomal aberrations in children born after assisted reproduction through intracytoplasmic sperm injection.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1c3otVyhsg%3D%3D&md5=6e2eedca3a62c39821a3616119fbdf4bCAS | 9619521PubMed |
Brown, J. L. (1997). Fecal steroid profiles in black-footed ferrets exposed to natural photoperiod. J. Wildl. Manage. 61, 1428–1436.
| Fecal steroid profiles in black-footed ferrets exposed to natural photoperiod.Crossref | GoogleScholarGoogle Scholar |
Carpenter, J. W. (1985). Captive breeding and management of black-footed ferrets. In ‘Black-footed Ferret Workshop Proceedings’. (Eds S. H. Anderson and D. B. Inkley.) pp. 12.1–12.13. (Wyoming Game and Fish Department: Cheyenne.)
Carr, A. (1986). Introduction. Great Basin Nat. Memoirs 9, 1–7.
Carroll, R. S., Erskine, M. S., Doherty, P. C., Lundell, L. A., and Baum, M. J. (1985). Coital stimuli controlling luteinizing hormone secretion and ovulation in the female ferret. Biol. Reprod. 32, 925–933.
| Coital stimuli controlling luteinizing hormone secretion and ovulation in the female ferret.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXktVSqt78%3D&md5=307f65962035c82fd6bfe0c0a1f7aed8CAS | 4039954PubMed |
Carvalho, C. F., Howard, J. G., Collins, L., Wemmer, C., Bush, M., and Wildt, D. E. (1991). Captive breeding of black-footed ferrets (Mustela nigripes) and comparative reproductive efficiency in 1-year-old versus 2-year-old animals. J. Zoo Wildl. Med. 22, 96–106.
Chang, M. C. (1969). Development of transferred ferret eggs in relation to the age of corpora lutea. J. Exp. Zool. 171, 459–464.
| Development of transferred ferret eggs in relation to the age of corpora lutea.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE3c%2FivF2rsw%3D%3D&md5=53c8e76091399fe2317e0e0f94f1ac6fCAS | 5349730PubMed |
Comizzoli, P. (2015). Biobanking efforts and new advances in male fertility preservation for rare and endangered species. Asian J. Androl. 17, 640–645.
| Biobanking efforts and new advances in male fertility preservation for rare and endangered species.Crossref | GoogleScholarGoogle Scholar | 25966625PubMed |
Davison, A., Birks, J. D. S., Griffiths, H., Kitchener, A. C., Biggins, D., and Butlin, R. K. (1999). Hybridization and the phylogenetic relationship between polecats and domestic ferrets in Britain. Biol. Conserv. 87, 155–161.
| Hybridization and the phylogenetic relationship between polecats and domestic ferrets in Britain.Crossref | GoogleScholarGoogle Scholar |
Di Minin, E., Laitila, J., Montesino‐Pouzols, F., Leader‐Williams, N., Slotow, R., Goodman, P. S., Conway, A. J., and Moilanen, A. (2015). Identification of policies for a sustainable legal trade in rhinoceros horn based on population projection and socioeconomic models. Conserv. Biol. 29, 545–555.
| Identification of policies for a sustainable legal trade in rhinoceros horn based on population projection and socioeconomic models.Crossref | GoogleScholarGoogle Scholar | 25331485PubMed |
Emslie, R. (2012). Ceratotherium simum. The IUCN Red List of Threatened Species 2012: e.T4185A16980466. Available at http://www.iucnredlist.org/details/4185/0 [verified 9 February 2016].
Fickel, J., Wagener, A., and Ludwig, A. (2007). Semen cryopreservation and the conservation of endangered species. Eur. J. Wildl. Res. 53, 81–89.
| Semen cryopreservation and the conservation of endangered species.Crossref | GoogleScholarGoogle Scholar |
Gao, D., Mazur, P., and Critser, J. K. (1997). Fundamental cryobiology of mammalian spermatozoa. In ‘Reproductive Tissue Banking: Scientific Principles’. (Eds A. M. Karow and J. K. Critser.) pp. 263–328. (Academic Press: London.)
Garelle, D., Marinari, P., and Lynch, C. (2015). ‘Population Analysis and Breeding and Transfer Plan for the Black-footed Ferret (Mustela nigripes)’. (Association of Zoos and Aquariums: Chicago, IL.)
Gilpin, M. E., and Soulé, M. E. (1986). Minimum viable populations: processes of species extinction. In ‘Conservation Biology: The Science of Scarcity and Diversity’. (Ed. M. E. Soulé.) pp. 19–34. (Sinauer: Sunderland, MA.)
Haigh, J. C., and Bowen, G. (1991). Artificial insemination of red deer (Cervus elephas) with frozen–thawed wapiti semen. J. Reprod. Fertil. 93, 119–123.
| Artificial insemination of red deer (Cervus elephas) with frozen–thawed wapiti semen.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK38%2FhsFSgtA%3D%3D&md5=30e616e1034e91a1a55fe2bbb06a42e5CAS | 1920280PubMed |
Holt, W. V., Abaigar, T., Watson, P. F., and Wildt, D. E. (2003). Genetic resource banks for species conservation. In ‘Reproductive Sciences and Integrated Conservation’. (Eds W. V. Holt, A. Pickard, J. C. Rodger and D. E. Wildt.) pp. 267–280.( Cambridge University Press: Cambridge, UK.)
Howard, J. G. (1993). Semen collection and analysis in nondomestic carnivores. In ‘Zoo and Wild Animal Medicine: Current Therapy III’. (Ed. M. E. Fowler.) pp. 390–399. (W. B. Saunders Co.: Philadelphia, PA.)
Howard, J. G., and Wildt, D. E. (2009). Approaches and efficacy of artificial insemination in felids and mustelids. Theriogenology 71, 130–148.
| Approaches and efficacy of artificial insemination in felids and mustelids.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1cjnt1Crug%3D%3D&md5=5921cf2b858538b3752a7fa521957232CAS | 18996580PubMed |
Howard, J. G., Hurlbut, S. L., Morton, C., Morton, F., Bush, M., and Wildt, D. E. (1989). Pregnancies in the domestic ferret after laparoscopic artificial insemination with frozen-thawed spermatozoa. J. Androl. Supplement, 51.
Howard, J. G., Bush, M., Morton, C., Morton, F., and Wildt, D. E. (1991). Comparative semen cryopreservation in ferrets (Mustela putorius furo) and pregnancies after laparoscopic intrauterine insemination with frozen–thawed spermatozoa. J. Reprod. Fertil. 92, 109–118.
| Comparative semen cryopreservation in ferrets (Mustela putorius furo) and pregnancies after laparoscopic intrauterine insemination with frozen–thawed spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3M3nvVSiug%3D%3D&md5=95fcb0d37f6273bf2463266ae25fcde0CAS | 2056481PubMed |
Howard, J., Barone, M., Byers, A., and Roth, T. (1993). Ovulation induction sensitivity and laparoscopic intrauterine insemination in the cheetah, puma and clouded leopard. J. Androl. 14, 55.
Howard, J. G., Marinari, P. E., and Wildt, D. E. (2001). Mustelid reproductive biology and integration of assisted reproductive technology in species recovery. In ‘Proceedings of the 1st International Symposium on Assisted Reproductive Technology for the Conservation and Genetic Management of Wildlife’. pp. 159–165. (XY Inc.: Omaha, NE.)
Howard, J., Marinari, P. E., and Wildt, D. E. (2003). Black-footed ferret: model for assisted reproductive technologies contributing to in situ conservation. In ‘Reproductive Sciences and Integrated Conservation’. (Eds W. V. Holt, A. Pickard, J. C. Rodger and D. E. Wildt.) pp. 249–266. (Cambridge University Press: Cambridge, UK.)
Howard, J., Santymire, R. M., Marinari, P. E., Kreeger, J. S., Williamson, L., and Wildt, D. E. (2006). Use of reproductive technology for black-footed ferret recovery. In ‘Symposium on the Status of the Black-footed Ferret and Its Habitat’. (Eds J. E. Roelle, B. J. Miller, J. L. Godbey and D. E. Biggins). pp. 28–36. (U.S. Department of the Interior: Fort Collins, CO.)
Howard, J. G., Lynch, C., Santymire, R., Marinari, P., and Wildt, D. E. (2015). Recovery of gene diversity using long-term, cryopreserved spermatozoa in the endangered black-footed ferret. Anim. Conserv. , .
| Recovery of gene diversity using long-term, cryopreserved spermatozoa in the endangered black-footed ferret.Crossref | GoogleScholarGoogle Scholar |
Huang, Y., Li, D., Zhou, Y., Zhou, Q., Li, R., Wang, C., Huang, Z., Hull, V., and Zhang, H. (2012). Factors affecting the outcome of artificial insemination using cryopreserved spermatozoa in the giant panda (Ailuropoda melanoleuca). Zoo Biol. 31, 561–573.
| Factors affecting the outcome of artificial insemination using cryopreserved spermatozoa in the giant panda (Ailuropoda melanoleuca).Crossref | GoogleScholarGoogle Scholar | 21932329PubMed |
International Species Information System (ISIS) (2004). ‘SPARKS (Single Population Analysis and Records Keeping System) V 1.5.’ (ISIS: Minneapolis, MN.)
Jabbour, H. N., Argo, C. M. G., Brinklow, B. R., Loudon, A. S. I., and Hooton, J. (1993). Conception rates following intrauterine insemination of European fallow deer (Dama dama dama) does with fresh or frozen–thawed Mesopotamian fallow deer (Dama dama mesopotamica) spermatozoa. J. Zool. (Lond.) 230, 379–384.
| Conception rates following intrauterine insemination of European fallow deer (Dama dama dama) does with fresh or frozen–thawed Mesopotamian fallow deer (Dama dama mesopotamica) spermatozoa.Crossref | GoogleScholarGoogle Scholar |
Kouba, A. J., and Vance, C. K. (2009). Applied reproductive technologies and genetic resource banking for amphibian conservation. Reprod. Fertil. Dev. 21, 719–737.
| Applied reproductive technologies and genetic resource banking for amphibian conservation.Crossref | GoogleScholarGoogle Scholar | 19567216PubMed |
Kouba, A. J., Lloyd, R. E., Houck, M. L., Silla, A. J., Calatayud, N., Trudeau, V. L., Clulow, J., Molinia, F., Langhorne, C., Vance, C., Arregui, L., Germano, J., Lermen, D., and Della Togna, G. (2013). Emerging trends for biobanking amphibian genetic resources: the hope, reality and challenges for the next decade. Biol. Conserv. 164, 10–21.
| Emerging trends for biobanking amphibian genetic resources: the hope, reality and challenges for the next decade.Crossref | GoogleScholarGoogle Scholar |
Lacy, R. C. (1995). Clarification of genetic terms and their use in the management of populations. Zoo Biol. 14, 565–577.
| Clarification of genetic terms and their use in the management of populations.Crossref | GoogleScholarGoogle Scholar |
Leibo, S. P. (1994). In vitro fertilization of oocytes by 37-year old cryopreserved bovine spermatozoa. Theriogenology 42, 1257–1262.
| In vitro fertilization of oocytes by 37-year old cryopreserved bovine spermatozoa.Crossref | GoogleScholarGoogle Scholar |
Li, B. V., and Pimm, S. L. (2015). China’s endemic vertebrates sheltering under the protective umbrella of the giant panda. Conserv. Biol. , .
| China’s endemic vertebrates sheltering under the protective umbrella of the giant panda.Crossref | GoogleScholarGoogle Scholar | 26332026PubMed |
Li, Z., Sun, X., Chen, J., Liu, X., Wisely, S. M., Zhou, Q., Renard, J. P., Leno, G. H., and Engelhardt, J. F. (2006). Full-term development of ferret embryos cloned by cell nuclear transfer. Dev. Biol. 293, 439–448.
| Full-term development of ferret embryos cloned by cell nuclear transfer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XksVOmsro%3D&md5=e52bc544055d3e7967834b0d4b993e4cCAS | 16584722PubMed |
Loskutoff, N. M. (2003). Role of embryo technologies in genetic management and conservation of wildlife. In ‘Reproductive Sciences and Integrated Conservation’. (Eds W. V. Holt, A. Pickard, J. C. Rodger and D. E. Wildt.) pp. 183–194. (Cambridge University Press: Cambridge, UK.)
Marinari, P. (2015). ‘North American Regional Black-footed Ferret Studbook.’ (Smithsonian National Zoological Park: Front Royal, VA.)
Marsh, R. E. (1984). Ground squirrels, prairie dogs, and marmots as pest on rangeland. In ‘Proceedings of the Conference for Organization and Practice of Vertebrate Pest Control’. pp. 195–208. (ICI Plant Protection Division: Fernherst, UK.)
Mead, R. A., Joseph, M. M., and Neirinckx, S. (1988). Optimal dose of human chorionic gonadotropin for inducing ovulation in the ferret. J. Reprod. Fertil. 88, 353–360.
| Optimal dose of human chorionic gonadotropin for inducing ovulation in the ferret.Crossref | GoogleScholarGoogle Scholar |
Miller, B. J., Reading, R. P., and Forrest, S. (1996). ‘Prairie Night: Black-Footed Ferrets and the Recovery of Endangered Species.’ (Smithsonian Institution: Washington, D. C.)
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 Eld’s deer (Cervus eldii thamin) with frozen–thawed spermatozoa. J. Reprod. Fertil. 99, 459–465.
| Successful intrauterine insemination of Eld’s deer (Cervus eldii thamin) with frozen–thawed spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXhvVeiu7g%3D&md5=04a0de744204679667800c4dee1869dbCAS | 8107027PubMed |
Morrell, J. M., Nubbemeyer, R., Heistermann, M., Rosenbusch, J., Kuderling, I., Holt, W., and Hodges, J. K. (1998). Artificial insemination in Callithrix jacchus using fresh or cryopreserved sperm. Anim. Reprod. Sci. 52, 165–174.
| Artificial insemination in Callithrix jacchus using fresh or cryopreserved sperm.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1cvkslertg%3D%3D&md5=0b9f9983aa1527993a0e1b22c51c968cCAS | 9776489PubMed |
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.
| Comparing ovulation synchronization protocols for artificial insemination in the scimitar-horned oryx (Oryx dammah).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjtVeqtrY%3D&md5=7c960ab7c64316e433731868d930a728CAS | 10804277PubMed |
Munson, L., Brown, J. L., Bush, M., Parker, C., Janssen, D., Reiziss, S. M., and Wildt, D. E. (1996). Genetic diversity affects testicular morphology in free-ranging lions (Panthera leo) of the Serengeti Plains and Ngorongoro Crater. J. Reprod. Fertil. 108, 11–15.
| Genetic diversity affects testicular morphology in free-ranging lions (Panthera leo) of the Serengeti Plains and Ngorongoro Crater.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XntFOlu78%3D&md5=b1f82c7efd2cf3c82831931cfc267ff5CAS | 8958822PubMed |
O’Brien, S. J., Roelke, M. E., Marker, L., Newman, A., Winkler, C. A., Meltzer, D., Colly, L., Evermann, J. F., Bush, M., and Wildt, D. E. (1985). Genetic basis for species vulnerability in the cheetah. Science 227, 1428–1434.
| Genetic basis for species vulnerability in the cheetah.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL2M7kt1Wmtg%3D%3D&md5=ce136ba82fe44b65ed091be26a15cc27CAS | 2983425PubMed |
O’Brien, S. J., Martenson, J. S., Eichelberger, M. A., Thorne, E. T., and Wright, F. (1989). Genetic variation and molecular systematics of the black-footed ferret. In ‘Conservation Biology and the Black-Footed Ferret’. (Eds U. S. Seal, S. H. Anderson and M A. Bogan.) pp. 21–33. (Yale University Press: New Haven, MA.)
Patton, M. L., Swaisgood, R. R., Czekala, N. M., White, A. M., Fetter, G. A., Montagne, J. P., Rieches, R. G., and Lance, V. A. (1999). Reproductive cycle length and pregnancy in the southern white rhinoceros (Ceratotherium simum simum) as determined by fecal pregnane analysis and observations of mating behavior. Zoo Biol. 18, 111–127.
| Reproductive cycle length and pregnancy in the southern white rhinoceros (Ceratotherium simum simum) as determined by fecal pregnane analysis and observations of mating behavior.Crossref | GoogleScholarGoogle Scholar |
Penfold, L. M., Monfort, S. L., Wolfe, B. A., Citino, S. B., and Wildt, D. E. (2005). Reproductive physiology and artificial insemination studies in wild and captive gerenuk (Litocranius walleri walleri). Reprod. Fertil. Dev. 17, 707–714.
| Reproductive physiology and artificial insemination studies in wild and captive gerenuk (Litocranius walleri walleri).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFKkt7zM&md5=77032b6b176fa8e7e8162be17ffec0e8CAS | 16364224PubMed |
Pollak, J. P., Lacy, R. C., and Ballou, J. D. (2000). ‘Population Management 2000, version 1.175.’ (Chicago Zoological Society: Brookfield, IL.)
Ptak, G., Clinton, M., Barboni, B., Muzzeddu, M., Cappai, P., Tischner, M., and Loi, P. (2002). Preservation of the wild European mouflon: the first example of genetic management using a complete program of reproductive biotechnologies. Biol. Reprod. 66, 796–801.
| Preservation of the wild European mouflon: the first example of genetic management using a complete program of reproductive biotechnologies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhvVeiu74%3D&md5=5492ca3e9304c170449272dd25e9b4abCAS | 11870088PubMed |
Pukazhenthi, B., Noiles, E., Pelican, K., Donoghue, A., Wildt, D. E., and Howard, J. G. (2000). Osmotic effects on feline spermatozoa from normospermic versus teratospermic donors. Cryobiology 40, 139–150.
| Osmotic effects on feline spermatozoa from normospermic versus teratospermic donors.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c3ltVOkug%3D%3D&md5=f4a6f2a32e8529153e71e97bdd388d12CAS | 10788313PubMed |
Reading, R. P., and Clark, T. W. (1996). Carnivore reintroductions: an interdisciplinary examination. In ‘Carnivore Behavior, Ecology, and Evolution’, Vol. 2. (Ed. J. L. Gittleman.) pp. 296–336. (Cornell University Press: Ithaca, NY.)
Roelke, M. E., Martenson, J. S., and O’Brien, S. J. (1993). The consequences of demographic reduction and genetic depletion in the endangered Florida panther. Curr. Biol. 3, 340–350.
| The consequences of demographic reduction and genetic depletion in the endangered Florida panther.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2cvjtFSrsA%3D%3D&md5=08da2d578a23ee41e47714b8b0cd537aCAS | 15335727PubMed |
Roldan, E. R. S., Gomendio, M., Garde, J. J., Espeso, G., Ledda, S., Berlinguer, F., Del Olmo, A., Soler, A. J., Arregui, L., Crespo, C., and González, R. (2006). Inbreeding and reproduction in endangered ungulates: preservation of genetic variation through the organization of genetic resource banks. Reprod. Domest. Anim. 41, 82–92.
| Inbreeding and reproduction in endangered ungulates: preservation of genetic variation through the organization of genetic resource banks.Crossref | GoogleScholarGoogle Scholar |
Sánchez-Partida, L. G., Maginnis, G., Dominko, T., Martinovich, C., McVay, B., Fanton, J., and Schatten, G. (2000). Live rhesus offspring by artificial insemination using fresh sperm and cryopreserved sperm. Biol. Reprod. 63, 1092–1097.
| Live rhesus offspring by artificial insemination using fresh sperm and cryopreserved sperm.Crossref | GoogleScholarGoogle Scholar |
Santymire, R. M., Howard, J. G., Wisely, S. M., Livieri, T. M., Kreeger, J. S., Marinari, P. E., and Wildt, D. E. (2004). Seminal characteristics of wild black-footed ferrets (Mustela nigripes). In ‘Proceedings of Defenders of Wildlife Carnivores 2004–Expanding Partnerships in Carnivore Conservation Conference’, Santa Fe, NM. (Eds A. Delach.) p. 200. (Defenders of Wildlife: Washington, D.C.) [Abstract]
Santymire, R. M., Marinari, P. E., Kreeger, J. S., Wildt, D. E., and Howard, J. G. (2006). Sperm viability in the black-footed ferret (Mustela nigripes) is influenced by seminal and medium osmolality. Cryobiology 53, 37–50.
| Sperm viability in the black-footed ferret (Mustela nigripes) is influenced by seminal and medium osmolality.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XntV2mtLk%3D&md5=c25f81748c4fbed5edf5cabe1245a3ecCAS | 16712829PubMed |
Santymire, R. M., Marinari, P. E., Kreeger, J. S., Wildt, D. E., and Howard, J. G. (2007). Slow cooling prevents cold-induced damage to sperm motility and acrosomal integrity in the black-footed ferret (Mustela nigripes). Reprod. Fertil. Dev. 19, 652–663.
| Slow cooling prevents cold-induced damage to sperm motility and acrosomal integrity in the black-footed ferret (Mustela nigripes).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2szosFKqsA%3D%3D&md5=d84da6efbb2bc570eb629543c563a9acCAS | 17601413PubMed |
Santymire, R. M., Branvold-Faber, H., and Marinari, P. E. (2014a). Recovery of the black-footed ferret. In ‘Biology and diseases of the ferret’, 3rd edn. (Eds J. G. Fox and R. P. Marini.) pp. 219–231. (Wiley, Ames, IA.)
Santymire, R. M., Livieri, T. M., Branvold-Faber, H., and Marinari, P. E. (2014b). The black-footed ferret: on the brink of recovery? In ‘Reproductive Sciences in Animal Conservation’. (Eds W. V. Holt, J. L. Brown and P. Comizzoli.) pp. 119–134. (Springer: New York, NY.)
Songsasen, N., Yu, I., Murton, S., Paccamonti, D. L., Eilts, B. E., Godke, R. A., and Leibo, S. P. (2002). Osmotic sensitivity of canine spermatozoa. Cryobiology 44, 79–90.
| Osmotic sensitivity of canine spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XltlSqtrc%3D&md5=6b545649eb71674afd6f9cf597f8cd91CAS | 12061850PubMed |
Swanson, W. F., Howard, J. G., Roth, T. L., Brown, J. L., Alvarado, T., Burton, M., Starnes, D., and Wildt, D. E. (1996). Responsiveness of ovaries to exogenous gonadotrophins and laparoscopic artificial insemination with frozen–thawed spermatozoa in ocelots (Felis pardalis). J. Reprod. Fertil. 106, 87–94.
| Responsiveness of ovaries to exogenous gonadotrophins and laparoscopic artificial insemination with frozen–thawed spermatozoa in ocelots (Felis pardalis).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XmtVCmsA%3D%3D&md5=6bc9bd1c2a6ce5a0ebfe8fc48f513b49CAS | 8667352PubMed |
Taylor, A. C. (2003). Assessing the consequences of inbreeding for population fitness: past challenges and future prospects. In ‘Reproductive Sciences and Integrated Conservation’. (Eds W. V. Holt, A. Pickard, J. C. Rodge, and D. E. Wildt.) pp. 67–81. (Cambridge University Press: Cambridge, UK.)
United States Fish and Wildlife Service (USFWS) (1988). ‘Black-footed Ferret Recovery Plan.’ (USFWS: Denver, CO.)
United States Fish and Wildlife Service (USFWS) (2013). ‘Black-footed Ferret Recovery Implementation Team 2013 Progress Report.’ (USFWS: Wellington, CO.)
Wildt, D. E. (1997). Genome resource banking: Impact on biotic conservation and society. In ‘Reproductive Tissue Banking’. (Eds A. Karow and J. Critser.) pp. 399–439. (Academic Press: New York, NY.)
Wildt, D. E., and Goodrowe, K. (1989). The potential for embryo technology in the black-footed ferret. In ‘Conservation Biology and the Black-Footed Ferret’. (Eds U. S. Seal, E. T. Thorne, S. H. Anderson and M. A. Bogan.) pp. 160–176. (Yale University Press: New Haven, CT.)
Wildt, D. E., Bush, M., Goodrowe, K. L., Packer, C., Pusey, A. E., Brown, J. L., Joslin, P., and O’Brien, S. J. (1983). Unique seminal quality in the South African cheetah and comparative evaluation in the domestic cat. Biol. Reprod. 29, 1019–1025.
| Unique seminal quality in the South African cheetah and comparative evaluation in the domestic cat.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL2c%2FltlGltA%3D%3D&md5=ebb0dd6722f2063adb6903e85e7cd31cCAS | 6640033PubMed |
Wildt, D. E., Bush, M., Goodrowe, K. L., Packer, C., Pusey, A. E., Brown, J. L., Joslin, P., and O’Brien, S. J. (1987). Reproductive and genetic consequences of founding isolated lion populations. Nature 329, 328–331.
| Reproductive and genetic consequences of founding isolated lion populations.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.
| 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.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXktFOqs7c%3D&md5=9111fea707aa05cb8efd4f658fe99411CAS | 2526874PubMed |
Wildt, D. E., Monfort, S. L., Donoghue, A. M., Johnston, L. A., and Howard, J. (1992). Embryogenesis in conservation biology: or, how to make an endangered species embryo. Theriogenology 37, 161–184.
| Embryogenesis in conservation biology: or, how to make an endangered species embryo.Crossref | GoogleScholarGoogle Scholar |
Wildt, D. E., Rall, W. F., Critser, J. K., Monfort, S. L., and Seal, U. S. (1997). Genome resource banks. Bioscience 47, 689–698.
| Genome resource banks.Crossref | GoogleScholarGoogle Scholar |
Williams, E. S., Thorne, E. T., Kwiatkowski, D. R., Anderson, S. L., and Lutz, K. (1991). Reproductive biology and management of captive black‐footed ferrets (Mustela nigripes). Zoo Biol. 10, 383–398.
| Reproductive biology and management of captive black‐footed ferrets (Mustela nigripes).Crossref | GoogleScholarGoogle Scholar |
Williams, E. S., Thorne, E. T., Kwiatkowski, D. R., Lutz, K., and Anderson, S. L. (1992). Comparative vaginal cytology of the estrus cycle of black-footed ferrets (Mustela nigripes), Siberian polecats (M. eversmanni), and domestic ferrets (M. putorius furo). J. Vet. Diagn. Invest. 4, 38–44.
| Comparative vaginal cytology of the estrus cycle of black-footed ferrets (Mustela nigripes), Siberian polecats (M. eversmanni), and domestic ferrets (M. putorius furo).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK383gvVSgtg%3D%3D&md5=46b0d693885984a9315d33567825eb29CAS | 1554767PubMed |
Wisely, S. M., Santymire, R. M., Marinari, P., Kreeger, J., Wildt, D. E., and Howard, J. G. (2005). Environment influences morphology and development for in situ and ex situ populations of the black-footed ferret (Mustela nigripes). Anim. Conserv. 8, 321–328.
| Environment influences morphology and development for in situ and ex situ populations of the black-footed ferret (Mustela nigripes).Crossref | GoogleScholarGoogle Scholar |
Wisely, S. M., Santymire, R. M., Livieri, T. M., Mueting, S. A., Wildt, D. E., and Howard, J. G. (2008). Genotypic and phenotypic consequences of reintroduction history: case study of the black-footed ferret. Conserv. Genet. 9, 389–399.
| Genotypic and phenotypic consequences of reintroduction history: case study of the black-footed ferret.Crossref | GoogleScholarGoogle Scholar |
Wisely, S. M., Ryder, O. A., Santymire, R. M., Englehardt, J. F., and Novak, B. J. (2015). Developing a road map for 21st century genetic restoration: gene pool enrichment of the black-footed ferret. J. Hered. 106, 581–592.
| Developing a road map for 21st century genetic restoration: gene pool enrichment of the black-footed ferret.Crossref | GoogleScholarGoogle Scholar | 26304983PubMed |
Wolf, K. N., Wildt, D. E., Vargas, A., Marinari, P. E., Ottinger, M. A., and Howard, J. G. (2000a). Reproductive inefficiency in male black-footed ferrets (Mustela nigripes). Zoo Biol. 19, 517–528.
| Reproductive inefficiency in male black-footed ferrets (Mustela nigripes).Crossref | GoogleScholarGoogle Scholar | 11180413PubMed |
Wolf, K. N., Wildt, D. E., Vargas, A., Marinari, P. E., Kreeger, J. S., Ottinger, M. A., and Howard, J. G. (2000b). Age dependent changes in sperm production, semen quality and testicular volume in black-footed ferrets (Mustela nigripes). Biol. Reprod. 63, 179–187.
| Age dependent changes in sperm production, semen quality and testicular volume in black-footed ferrets (Mustela nigripes).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXktl2rsL4%3D&md5=20df42b3cb8bc2251ff0cf71b3e40883CAS | 10859258PubMed |