Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Circumventing the natural, frequent oestrogen waves of the female cheetah (Acinonyx jubatus) using oral progestin (Altrenogest)

Adrienne E. Crosier A C , Pierre Comizzoli B , Diana C. Koester A and David E. Wildt A
+ Author Affiliations
- Author Affiliations

A Smithsonian Conservation Biology Institute, 1500 Remount Road, Front Royal, VA 22630, USA.

B Smithsonian Conservation Biology Institute, National Zoological Park, 3001 Connecticut Ave., NW, Washington, DC 20008, USA.

C Corresponding author. Email: crosiera@si.edu

Reproduction, Fertility and Development - https://doi.org/10.1071/RD16007
Submitted: 7 January 2016  Accepted: 15 June 2016   Published online: 3 August 2016

Abstract

Cheetah are induced ovulators, experiencing short, variable oestrogen waves year-round. Exogenous gonadotrophin administration induces ovulation, but success is variable and often improves if ovaries are quiescent. After affirming the presence of short-term oestrogenic waves, we examined the effect of the timing of administration of exogenous equine and human chorionic gonadotrophins (eCG–hCG) within the oestrogen concentration pattern on subsequent follicle development and oocyte and corpus luteum quality. We also investigated ovarian suppression using an oral progestin (Altrenogest, 7 days) and assessed whether Altrenogest moderated adrenal activity by reducing glucocorticoid metabolites. All cheetahs exhibited short (every ~7–10 days), sporadic, year-round increases in faecal oestradiol punctuated by unpredictable periods (4–10 weeks) of baseline oestradiol (anoestrous). Gonadotrophin (eCG–hCG) efficacy was not affected by oestradiol ‘wave’ pattern if administered ≥3 days after an oestrogen peak. Such cheetahs produced normative faecal progestagen patterns and higher numbers (P < 0.06) of mature oocytes than females given gonadotrophins ≤2 days after an oestradiol peak. Altrenogest supplementation expanded the interval between oestradiol peaks to 12.9 days compared with 7.3 days without progestin pretreatment. Altrenogest-fed females excreted less (P < 0.05) glucocorticoid metabolites than non-supplemented counterparts. Results show that Altrenogest is effective for suppressing follicular activity, may contribute to reduced glucocorticoid production and may result in more effective ovulation induction via gonadotrophin therapy.

Additional keywords: gonadotrophin, oestradiol, ovary, ovulation, progesterone.


References

Bó, G. A., Baruselli, P. S., Moreno, D., Cutaia, L., Caccia, M., Tríbulo, R., Tríbulo, H., and Mapletoft, R. J. (2002). The control of follicular wave development for self-appointed embryo transfer programs in cattle. Theriogenology 57, 53–72.
The control of follicular wave development for self-appointed embryo transfer programs in cattle.CrossRef | 11775981PubMed | open url image1

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.
Natural versus chorionic gonadotropin-induced ovarian responses in the clouded leopard (Neofelis nebulosa) assessed by fecal steroid analysis.CrossRef | 1:CAS:528:DyaK2MXmt12itL8%3D&md5=2dcae6162fd0bd6397504e55d425b6edCAS | 7669862PubMed | open url image1

Brown, J. L., Wildt, D. E., Wielebnowski, N., Goodrowe, K. L., Graham, L. H., Wells, S., and Howard, J. G. (1996). Reproductive activity in captive female cheetahs (Acinonyx jubatus) assessed by faecal steroids. J. Reprod. Fertil. 106, 337–346.
Reproductive activity in captive female cheetahs (Acinonyx jubatus) assessed by faecal steroids.CrossRef | 1:CAS:528:DyaK28XitFKnt7o%3D&md5=c11dc5ad7e9933821180095a9577f4edCAS | 8699419PubMed | open url image1

Caro, T. M. (1994). ‘Cheetahs of the Serengeti Plains Group Living in an Asocial Species’. (The University of Chicago Press: ChicagoXXX.)

Chastain, C. B., Graham, C. L., and Nichols, C. E. (1981). Adrenocortical suppression in cats given megestrol acetate. Am. J. Vet. Res. 42, 2029–2035.
| 1:CAS:528:DyaL38XotVWqsA%3D%3D&md5=62dac741aba4918938ea08def0e63196CAS | 6280517PubMed | open url image1

Collins, C. W., Monfort, S. L., Vick, M. M., Wolfe, B. A., Weiss, R. B., Keefer, C. L., and Songsasen, N. (2014). Oral and injectable synthetic progestagens effectively manipulate the estrous cycle in the Przewalski’s horse (Equus ferus przewalskii). Anim. Reprod. Sci. 148, 42–52.
Oral and injectable synthetic progestagens effectively manipulate the estrous cycle in the Przewalski’s horse (Equus ferus przewalskii).CrossRef | 1:CAS:528:DC%2BC2cXoslCqtLw%3D&md5=9e5410d39a68544ccb11364dba523506CAS | 24856195PubMed | open url image1

Crosier, A. E., Pukazhenthi, B. S., Henghali, J. N., Howard, J., Dickman, A. J., Marker, L., and Wildt, D. E. (2006). Cryopreservation of spermatozoa from wild-born Namibian cheetahs (Acinonyx jubatus) and influence of glycerol on cryosurvival. Cryobiology 52, 169–181.
Cryopreservation of spermatozoa from wild-born Namibian cheetahs (Acinonyx jubatus) and influence of glycerol on cryosurvival.CrossRef | 1:CAS:528:DC%2BD28Xit1yqtrk%3D&md5=8174beb719d6d5181979addb0db790e1CAS | 16412415PubMed | open url image1

Crosier, A. E., Marker, L., Howard, J., Pukazhenthi, B. S., Henghali, J. N., and Wildt, D. E. (2007). Ejaculate traits in the Namibian cheetah (Acinonyx jubatus): influence of age, season and captivity. Reprod. Fertil. Dev. 19, 370–382.
Ejaculate traits in the Namibian cheetah (Acinonyx jubatus): influence of age, season and captivity.CrossRef | 17257524PubMed | open url image1

Crosier, A. E., Henghali, J. N., Howard, J. G., Pukazhenthi, B. S., Terrell, K. A., Marker, L. L., and Wildt, D. E. (2009). Improved quality of cryopreserved cheetah (Acinonyx jubatus) spermatozoa after centrifugation through Accudenz. J. Androl. 30, 298–308.
Improved quality of cryopreserved cheetah (Acinonyx jubatus) spermatozoa after centrifugation through Accudenz.CrossRef | 19023140PubMed | open url image1

Crosier, A. E., Comizzoli, P., Baker, T., Davidson, A., Munson, L., Howard, J. G., Marker, L. L., and Wildt, D. E. (2011). Increasing age influences uterine integrity, but not ovarian function or oocyte quality, in the cheetah (Acinonyx jubatus). Biol. Reprod. 85, 243–253.
Increasing age influences uterine integrity, but not ovarian function or oocyte quality, in the cheetah (Acinonyx jubatus).CrossRef | 1:CAS:528:DC%2BC3MXpslOntbs%3D&md5=734d41800109350ffd58dec95a87da24CAS | 21565998PubMed | open url image1

Edwards, K. M., and Mills, P. J. (2008). Effects of estrogen verses estrogen and progesterone on cortisol and interleukin-6. Maturitas 61, 330–333.
Effects of estrogen verses estrogen and progesterone on cortisol and interleukin-6.CrossRef | 1:CAS:528:DC%2BD1cXhsFChtL3P&md5=2b864f931a38a5b5ef4562279631cd19CAS | 19010617PubMed | open url image1

Gonzalez-Bulnes, A., Veiga-Lopez, A., Garcia, P., Garcia-Garcia, R. M., Ariznavarreta, C., Sanchez, M. A., Tresguerres, J. A., Cocero, M. J., and Flores, J. M. (2005). Effects of progestagens and prostaglandin analogues on ovarian function and embryo viability in sheep. Theriogenology 63, 2523–2534.
Effects of progestagens and prostaglandin analogues on ovarian function and embryo viability in sheep.CrossRef | 1:CAS:528:DC%2BD2MXks1CktbY%3D&md5=9e0d8c8afef3580632f6a8da45e22863CAS | 15910932PubMed | open url image1

Graham, L. H., and Brown, J. L. (1996). Cortisol metabolism in the domestic cat and implications for non-invasive monitoring of adrenocortical function in endangered felids. Zoo Biol. 15, 71–82.
Cortisol metabolism in the domestic cat and implications for non-invasive monitoring of adrenocortical function in endangered felids.CrossRef | 1:CAS:528:DyaK28Xit1yhtLs%3D&md5=0202c302e56d0bf14f96d524e9a53252CAS | open url image1

Graham, L. H., Swanson, W. F., and Brown, J. L. (2000). Chorionic gonadotropin administration in domestic cats causes an abnormal endocrine environment that disrupts oviductal embryo transport. Theriogenology 54, 1117–1131.
Chorionic gonadotropin administration in domestic cats causes an abnormal endocrine environment that disrupts oviductal embryo transport.CrossRef | 1:CAS:528:DC%2BD3MXhtlCnug%3D%3D&md5=e3b565e621b89bb62da283def26a7d99CAS | 11131330PubMed | open url image1

Graham, L., Schwarzenberger, F., Möstl, E., Galama, W., and Savage, A. (2001). A versatile enzyme immunoassay for the determination of progesterone in feces and serum. Zoo Biol. 20, 227–236.
A versatile enzyme immunoassay for the determination of progesterone in feces and serum.CrossRef | 1:CAS:528:DC%2BD3MXmvVagtbY%3D&md5=9707dad7a2f54dfe42b83d25e2d0012dCAS | open url image1

Graham, L. H., Byers, A. P., Armstrong, D. L., Luskutoff, N. M., Swanson, W. F., Wildt, D. E., and Brown, J. L. (2006). Natural and gonadotropin-induced ovarian activity in tigers (Panthera tigris) assessed by fecal steroid analyses. Gen. Comp. Endocrinol. 147, 362–370.
Natural and gonadotropin-induced ovarian activity in tigers (Panthera tigris) assessed by fecal steroid analyses.CrossRef | 1:CAS:528:DC%2BD28XltFOls74%3D&md5=ba40d96f8131568f1d3934e22c90277cCAS | 16564049PubMed | open url image1

Herrick, J. R., Bond, J. B., Campbell, M., Levens, G., Moore, T., Benson, K., D’Agostino, J., West, G., Okeson, D. M., Coke, R., Portacio, S. C., Leiske, K., Kreider, C., Polumbo, P. J., and Swanson, W. F. (2010). Fecal endocrine profiles and ejaculate traits in black-footed cats (Felis nigripes) and sand cats (Felis margarita). Gen. Comp. Endocrinol. 165, 204–214.
Fecal endocrine profiles and ejaculate traits in black-footed cats (Felis nigripes) and sand cats (Felis margarita).CrossRef | 1:CAS:528:DC%2BD1MXhsVKht7zI&md5=c57e935df963065a984c75bc453d9241CAS | 19576217PubMed | open url image1

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 | 1:STN:280:DC%2BD1cjnt1Crug%3D%3D&md5=5921cf2b858538b3752a7fa521957232CAS | 18996580PubMed | open url image1

Howard, J. G., Roth, T. L., Byers, A. P., Swanson, W. F., and Wildt, D. E. (1997). Sensitivity to exogenous gonadotropins for ovulation induction and laparoscopic artificial insemination in the cheetah and clouded leopard. Biol. Reprod. 56, 1059–1068.
Sensitivity to exogenous gonadotropins for ovulation induction and laparoscopic artificial insemination in the cheetah and clouded leopard.CrossRef | 1:CAS:528:DyaK2sXitFKlsrg%3D&md5=bfc41b4c80bc9f5efe0522cb04234a14CAS | 9096891PubMed | open url image1

IUCN (2015) ‘The IUCN Red List of Threatened Species. Version 2015.2’. Available at http://www.iucnredlist.org/details/219/0 [Downloaded 4 July 2015; Verified 20 June 2016].

Koester, D. C., Freeman, E., Brown, J. L., Wildt, D. E., Terrell, K. A., Franklin, A. D., and Crosier, A. E. (2015). Motile sperm output by male cheetahs (Acinonyx jubatus) managed ex situ is influenced by public exposure and number of care-givers. Plos 1 10, e0135847.
Motile sperm output by male cheetahs (Acinonyx jubatus) managed ex situ is influenced by public exposure and number of care-givers.CrossRef | 26332582PubMed | open url image1

Marker, L. (2013). ‘International Studbook Cheetah (Acinonyx jubatus)’. (Cheetah Conservation Fund: Otjiwarongo, Namibia.)

Munson, L., Gardner, A., Mason, R. J., Chassy, L. M., and Seal, U. S. (2002). Endometrial hyperplasia and mineralization in zoo felids treated with melengestrol acetate contraceptives. Vet. Pathol. 39, 419–427.
Endometrial hyperplasia and mineralization in zoo felids treated with melengestrol acetate contraceptives.CrossRef | 1:CAS:528:DC%2BD38XlvVKnt7s%3D&md5=eed3445e9701fa0229191ab05395f321CAS | 12126144PubMed | open url image1

Munson, L., Terio, K. A., Worley, M., Jago, M., Bagot-Smith, A., and Marker, L. (2005). Extrinsic factors significantly affect patterns of disease in free-ranging and captive cheetah (Acinonyx jubatus) populations. J. Wildl. Dis. 41, 542–548.
Extrinsic factors significantly affect patterns of disease in free-ranging and captive cheetah (Acinonyx jubatus) populations.CrossRef | 16244064PubMed | open url image1

Pelican, K. M., Brown, J. L., Wildt, D. E., Ottinger, M. A., and Howard, J. G. (2005). Short term suppression of follicular recruitment and spontaneous ovulation in the cat using levonorgestrel versus a GnRH antagonist. Gen. Comp. Endocrinol. 144, 110–121.
Short term suppression of follicular recruitment and spontaneous ovulation in the cat using levonorgestrel versus a GnRH antagonist.CrossRef | 1:CAS:528:DC%2BD2MXhtVynurjN&md5=3985a1c878a8a47d8a4933b719e245c6CAS | 15979618PubMed | open url image1

Pelican, K. M., Wildt, D. E., Pukazhenthi, B. S., and Howard, J. G. (2006). Ovarian control for assisted reproduction in the domestic cat and wild felids. Theriogenology 66, 37–48.
Ovarian control for assisted reproduction in the domestic cat and wild felids.CrossRef | 1:CAS:528:DC%2BD28XlsFKrsL0%3D&md5=999c7f1f8960ddee90a64b56be819ddbCAS | 16630653PubMed | open url image1

Pelican, K. M., Wildt, D. E., Ottinger, M. A., and Howard, J. G. (2008). Priming with progestin, but not GnRH antagonist, induces a consistent endocrine response to exogenous gonadotropins in induced and spontaneously ovulating cats. Domest. Anim. Endocrinol. 34, 160–175.
Priming with progestin, but not GnRH antagonist, induces a consistent endocrine response to exogenous gonadotropins in induced and spontaneously ovulating cats.CrossRef | 1:CAS:528:DC%2BD1cXptlaktw%3D%3D&md5=7a1348a5cebdf93bbdf73fd6381f0d26CAS | 17369001PubMed | open url image1

Pierce, B. N., Clarke, I. J., Turner, A. I., Rivalland, E. T., and Tilbrook, A. J. (2009a). Cortisol disrupts the ability of estradiol-17 beta to induce the LH surge in ovariectomized ewes. Domest. Anim. Endocrinol. 36, 202–208.
Cortisol disrupts the ability of estradiol-17 beta to induce the LH surge in ovariectomized ewes.CrossRef | 1:CAS:528:DC%2BD1MXktlygtbo%3D&md5=948b7ae432bfd70dd8b8997c0c7f3f03CAS | 19185443PubMed | open url image1

Pierce, B. N., Stackpole, C. A., Breen, K. M., Clarke, I. J., Karsch, F. J., Rivalland, E. T., Turner, A. I., Caddy, D. J., Wagenmaker, E. R., Oakley, A. E., and Tilbrook, A. J. (2009b). Estradiol enables cortisol to act directly upon the pituitary to suppress pituitary responsiveness to GnRH in sheep. Neuroendocrinology 89, 86–97.
Estradiol enables cortisol to act directly upon the pituitary to suppress pituitary responsiveness to GnRH in sheep.CrossRef | 1:CAS:528:DC%2BD1MXhtFSmsLY%3D&md5=2de2475e6ffd176f04456790a93f31ddCAS | 18714145PubMed | open url image1

Robeck, T. R., Gill, C., Doescher, B. M., Sweeney, J., De Laender, P., Van Elk, C. E., and O’Brien, J. K. (2012). Altrenogest and progesterone therapy during pregnancy in bottlenose dolphins (Tursiops truncatus) with progesterone insufficiency. J. Zoo Wildl. Med. 43, 296–308.
Altrenogest and progesterone therapy during pregnancy in bottlenose dolphins (Tursiops truncatus) with progesterone insufficiency.CrossRef | 22779233PubMed | open url image1

Santymire, R. M., Brown, J. L., Stewart, R. A., Santymire, R. C., Wildt, D. E., and Howard, J. G. (2011). Reproductive gonadal steroidogenic activity in the fishing cat (Prionailurus viverrinus) assessed by fecal steroid analyses. Anim. Reprod. Sci. 128, 60–72.
Reproductive gonadal steroidogenic activity in the fishing cat (Prionailurus viverrinus) assessed by fecal steroid analyses.CrossRef | 1:CAS:528:DC%2BC3MXhsVamsr%2FE&md5=662c418768a9cb400dcc85e12065e053CAS | 21975304PubMed | open url image1

Spitz, I. M. (2003). Progesterone antagonists and progesterone receptor modulators: an overview. Steroids 68, 981–993.
Progesterone antagonists and progesterone receptor modulators: an overview.CrossRef | 1:CAS:528:DC%2BD3sXps1Olu7s%3D&md5=0bee25f11cfb549a5b359f9c4f1a7f2dCAS | 14667991PubMed | open url image1

Stewart, R. A., Pelican, K., Brown, J. L., Wildt, D. E., Ottinger, M. A., and Howard, J. G. (2010). Oral progestin induces rapid, reversible suppression of ovarian activity in the cat. Gen. Comp. Endocrinol. 166, 409–416.
Oral progestin induces rapid, reversible suppression of ovarian activity in the cat.CrossRef | 1:CAS:528:DC%2BC3cXjtVCgurw%3D&md5=83d637be7731b9d8933daa76ee280f7dCAS | 20051246PubMed | open url image1

Stewart, R. A., Pelican, K. M., Crosier, A. E., Pukazhenthi, B. S., Wildt, D. E., Ottinger, M. A., and Howard, J. G. (2012). Oral progestin priming increases ovarian sensitivity to gonadotropin stimulation and improves luteal function in the cat. Biol. Reprod. 87, 137.
Oral progestin priming increases ovarian sensitivity to gonadotropin stimulation and improves luteal function in the cat.CrossRef | 23100619PubMed | open url image1

Stewart, R. A., Crosier, A. E., Pelican, K. M., Pukazhenthi, B. S., Sitzmann, B. D., Porter, T. E., Wildt, D. E., Ottinger, M. A., and Howard, J. G. (2015). Progestin priming before gonadotrophin stimulation and AI improves embryo development and normalises luteal function in the cat. Reprod. Fertil. Dev. 27, 360–371.
Progestin priming before gonadotrophin stimulation and AI improves embryo development and normalises luteal function in the cat.CrossRef | 1:CAS:528:DC%2BC2MXhslegtro%3D&md5=a4938d1134a72c1f8a8825a079a1d708CAS | 24300570PubMed | open url image1

Stoops, M. A., West, G. D., Roth, T. L., and Lung, N. P. (2014). Use of urinary biomarkers of ovarian function and altrenogest supplementation to enhance captive breeding success in the Indian rhinoceros (Rhinoceros unicornis). Zoo Biol. 33, 83–88.
Use of urinary biomarkers of ovarian function and altrenogest supplementation to enhance captive breeding success in the Indian rhinoceros (Rhinoceros unicornis).CrossRef | 1:CAS:528:DC%2BC2cXlvFSmt7g%3D&md5=494d41bffed28e111846057dba3cf92eCAS | 24375460PubMed | open url image1

Sun, Y., Fang, M., Davies, H., and Hu, Z. (2014). Mifepristone: a potential clincial agent based on its anti-progesterone and anti-glucocorticoid properties. Gynecol. Endocrinol. 30, 169–173.
Mifepristone: a potential clincial agent based on its anti-progesterone and anti-glucocorticoid properties.CrossRef | 1:CAS:528:DC%2BC2cXjt1amtr8%3D&md5=cd82a4b366cffbca6840baa55ad874d0CAS | 24205903PubMed | open url image1

Swanson, W. F., Howard, J. G., Roth, T. L., Brown, J. L., Alvarado, T., Burton, M., Starnes, D., and Wildt, D. E. (1996a). 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 | 1:CAS:528:DyaK28XmtVCmsA%3D%3D&md5=6bc9bd1c2a6ce5a0ebfe8fc48f513b49CAS | 8667352PubMed | open url image1

Swanson, W. F., Roth, T. L., Graham, K., Horohov, D. W., and Godke, R. A. (1996b). Kinetics of the humoral immune response to multiple treatments with exogenous gonadotropins and relation to ovarian responsiveness in domestic cats. Am. J. Vet. Res. 57, 302–307.
| 1:CAS:528:DyaK28XitVyitrY%3D&md5=c56d6aef3fb5108863109e16459392c7CAS | 8669759PubMed | open url image1

Swanson, W. F., Penfold, L. M., Brown, J. L., Munson, L., and Wildt, D. E. (1997). Normality of the maternal environment in domestic cats treated with gonadotropin-releasing hormone and exogenous gonadotropins. Biol. Reprod. 56, 131. open url image1

Terio, K. A., Marker, L., and 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.
Evidence for chronic stress in captive but not free-ranging cheetahs (Acinonyx jubatus) based on adrenal morphology and function.CrossRef | 1:CAS:528:DC%2BD2cXmsVShurs%3D&md5=ad35a3187b651130fad7e5ff8f0f2056CAS | 15362825PubMed | open url image1

Wielebnowski, N., and Brown, J. L. (1998). Behavioral correlates of physiological estrus in cheetahs. Zoo Biol. 17, 193–209.
Behavioral correlates of physiological estrus in cheetahs.CrossRef | open url image1

Wielebnowski, N., Fletchall, N., Carlstead, K., Busso, J. M., and Brown, J. L. (2002a). Noninvasive assessment of adrenal activity associated with husbandry and behavior factors in the North American clouded leopard population. Zoo Biol. 21, 77–98.
Noninvasive assessment of adrenal activity associated with husbandry and behavior factors in the North American clouded leopard population.CrossRef | open url image1

Wielebnowski, N. C., Ziegler, K., Wildt, D. E., Lukas, J., and Brown, J. L. (2002b). Impact of social management on reproductive, adrenal and behavioural activity in the cheetah (Acinonyx jubatus). Anim. Conserv. 5, 291–301.
Impact of social management on reproductive, adrenal and behavioural activity in the cheetah (Acinonyx jubatus).CrossRef | open url image1

Wildt, D. E., Guthrie, S. C., and Seager, S. W. J. (1978). Ovarian and behavioral cyclicity of the laboratory maintained cat. Horm. Behav. 10, 251–257.
Ovarian and behavioral cyclicity of the laboratory maintained cat.CrossRef | 1:STN:280:DyaE1M%2Fks1ynug%3D%3D&md5=e02ba788b566fccbcb1ed175af4d32e2CAS | 568595PubMed | open url image1

Wildt, D. E., Platz, C. C., Seager, S. W., and Bush, M. (1981). Induction of ovarian activity in the cheetah (Acinonyx jubatus). Biol. Reprod. 24, 217–222.
Induction of ovarian activity in the cheetah (Acinonyx jubatus).CrossRef | 1:CAS:528:DyaL3MXhtFGjs7g%3D&md5=3da3ca31cfe3f968f23259b66694739fCAS | 6781547PubMed | open url image1

Wildt, D. E., Bush, M., Howard, J. G., O’Brien, S. J., Meltzer, D., Van Dyk, A., Ebedes, H., and Brand, D. J. (1983). Unique seminal quality in the South African cheetah and a comparative evaluation in the domestic cat. Biol. Reprod. 29, 1019–1025.
Unique seminal quality in the South African cheetah and a comparative evaluation in the domestic cat.CrossRef | 1:STN:280:DyaL2c%2FltlGltA%3D%3D&md5=ebb0dd6722f2063adb6903e85e7cd31cCAS | 6640033PubMed | open url image1

Wildt, D. E., Brown, J. L., Bush, M., Barone, M. A., Cooper, K. A., Grisham, J., and Howard, J. G. (1993). Reproductive status of cheetahs (Acinonyx jubatus) in North American zoos: the benefits of physiological surveys for strategic planning. Zoo Biol. 12, 45–80.
Reproductive status of cheetahs (Acinonyx jubatus) in North American zoos: the benefits of physiological surveys for strategic planning.CrossRef | open url image1

Wildt, D. E., Swanson, W., Brown, J. L., Sliwa, A., and Vargas, A. (2010). Felids ex situ: managed programmes, research, and species recovery. In ‘Biology and Conservation of Wild Felids’. (Eds D. W. Macdonald and A. J. Loveridge.) pp. 217–236. (Oxford University Press: Oxford.)

Wood, T. C., and Wildt, D. E. (1997). Effect of the quality of the cumulus–oocyte complex in the domestic cat on the ability of oocytes to mature, fertilize, and develop into blastocysts in vitro. J. Reprod. Fertil. 110, 355–360.
Effect of the quality of the cumulus–oocyte complex in the domestic cat on the ability of oocytes to mature, fertilize, and develop into blastocysts in vitro.CrossRef | 1:CAS:528:DyaK2sXlvFKrsL0%3D&md5=6976a4bcbc93b404b4a8c75108bb50c8CAS | 9306990PubMed | open url image1

Young, K. M., Walker, S. L., Lanthier, C., Waddell, W. T., Monfort, S. L., and Brown, J. L. (2004). Noninvasive monitoring of adrenocortical activity in carnivores by fecal glucocorticoid analyses. Gen. Comp. Endocrinol. 137, 148–165.
Noninvasive monitoring of adrenocortical activity in carnivores by fecal glucocorticoid analyses.CrossRef | 1:CAS:528:DC%2BD2cXkt1ajsr8%3D&md5=2f34f687c84ead60c7406c9feb0a44a2CAS | 15158127PubMed | open url image1



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