Suppression of ovarian activity in a captive African Lion Panthera leo after deslorelin treatment

Main Article Content

Daniela Paes de Almeida Ferreira Braga
Cristiane Schilbach Pizzutto
https://orcid.org/0000-0002-4357-5133
Derek Andrew Rosenfield
https://orcid.org/0000-0001-5546-8872
Priscila Viau Furtado
https://orcid.org/0000-0002-5138-3676
Cláudio A. Oliveira
https://orcid.org/0000-0002-4143-7212
Sandra Helena Ramiro Corrêa
Pedro Nacib Jorge-Neto
https://orcid.org/0000-0002-5894-0148
Marcelo Alcindo de Barros Vaz Guimarães

Abstract

Abstract: With the intent to evaluate the efficiency of a contraceptive treatment for cyclic ovarian suppression in African Lionesses Panthera leo using a Gonadotrophin-Releasing Hormone (GnRH) agonist bioimplant, noninvasive fecal steroid assay associated with the observation of the behavioral estrus were employed for a period of 36 months.  Five captive adult females, maintained with a vasectomized male, subcutaneously received a 9.4mg deslorelin acetate implant.  The treatment initially stimulated behavioral estrus along with ovarian activity, demonstrated by an estrogen increase in two lionesses.  A rise in progesterone concentration in two other animals suggested possible treatment-induced ovulation.  After the initial period, deslorelin prevented ovarian activity for at least 22 months.  Two females exhibited signs of behavioral estrus after 22 and 31 months.  A third lioness with an increased estrogen concentration did not exhibit behavioral estrus signs or a consequent progesterone surge until 33 months after implantation, suggesting a possible resumption of ovarian activity.  One female did not exhibit any behavioral estrus signs nor a rise in steroid levels after the “treatment-induced” estrus throughout the entire experiment (36 months).  One lioness died after 15 months without exhibiting signs of estrus or an increased progesterone level, however, the estrogen concentration increased 12 months post-implantation, suggesting resumed ovarian activity.  The study showed that long-term treatment with a GnRH agonist can be extremely effective as a contraceptive treatment in African lionesses, however, the duration of contraception may vary among individuals and may bear the risk of permanent loss of normal ovarian activity.


 

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Communications

References

Asa, C., S. Boutelle, & K. Bauman (2012). AZA Wildlife Contraception Center Programme for Wild Felids and Canids. Reproduction in Domestic Animals 47(SUPPL. 6): 377–380. https://doi.org/10.1111/rda.12004 DOI: https://doi.org/10.1111/rda.12004

Barnes, S.A., J. Andrew Teare, S. Staaden, L. Metrione & L.M. Penfold (2016). Characterization and manipulation of reproductive cycles in the jaguar (Panthera onca). General and Comparative Endocrinology 225: 95–103. https://doi.org/10.1016/j.ygcen.2015.09.012 DOI: https://doi.org/10.1016/j.ygcen.2015.09.012

Bertschinger, H.J., C.S. Asa, P.P. Calle, J.A. Long, K. Bauman, K. DeMatteo, W. Jöchle, T.E. Trigg & A. Human (2001). Control of reproduction and sex related behaviour in exotic wild carnivores with the GnRH analogue deslorelin: preliminary observations. Journal of Reproduction and Fertility (Supplement) 57: 275–283.

Bertschinger, H.J., M.A. de B.V. Guimarães, T.E. Trigg & A. Human (2008). The use of deslorelin implants for the long-term contraception of lionesses and tigers. Wildlife Research 35(6): 525. https://doi.org/10.1071/WR07141 DOI: https://doi.org/10.1071/WR07141

Bertschinger, H.J., T.E. Trigg, W. Jöchle & A. Human (2002). Induction of contraception in some African wild carnivores by downregulation of LH and FSH secretion using the GnRH analogue deslorelin. Reproduction (Supplement) 60: 41–52.

Brown, J.L., D.E. Wildt, L.H. Graham, A.P. Byers, L. Collins, S. Barrett & J. Howard (1995). Natural versus chorionic gonadotropin-induced ovarian responses in the Clouded Leopard (Neofelis nebulosa) assessed by fecal steroid analysis. Biology of Reproduction 53(1): 93–102. https://doi.org/10.1095/biolreprod53.1.93 DOI: https://doi.org/10.1095/biolreprod53.1.93

Brown, J.L., L.H. Graham, N. Wielebnowski, W.F. Swanson, D.E. Wildt & J.G. Howard (2001). Understanding the basic reproductive biology of wild felids by monitoring of faecal steroids. Journal of Reproduction and Fertility (Supplement) 57: 71–82.

Brown, J.L, S.K. Wasser, D.E. Wildt & L.H. Graham (1994). Comparative aspects of steroid hormone metabolism and ovarian activity in felids, measured noninvasively in feces. Biology of Reproduction 51(4): 776–786. https://doi.org/10.1095/biolreprod51.4.776 DOI: https://doi.org/10.1095/biolreprod51.4.776

Castle, P.E. & J. Dean (1996). Molecular genetics of the zona pellucida: implications for immunocontraceptive strategies. Journal of Reproduction and Fertility (Supplement) 50: 1–8.

Conn, P.M. & W.F. Crowley (1994). Gonadotropin-releasing hormone and its analogs. Annual Review of Medicine 45(1): 391–405. https://doi.org/10.1146/annurev.med.45.1.391 DOI: https://doi.org/10.1146/annurev.med.45.1.391

D’Occhio, M.J. & J.E. Kinder (1995). Failure of the LH-releasing hormone agonist, deslorelin, to prevent development of a persistent follicle in heifers synchronized with norgestomet. Theriogenology 44(6): 849–857. https://doi.org/10.1016/0093-691X(95)00270-I DOI: https://doi.org/10.1016/0093-691X(95)00270-I

D’Occhio, M.J., G. Fordyce, T.R. Whyte, T.F. Jubb, L.A. Fitzpatrick, N.J. Cooper, W.J. Aspden, M.J. Bolam & T.E. Trigg (2002). Use of GnRH agonist implants for long-term suppression of fertility in extensively managed heifers and cows. Animal Reproduction Science 74(3–4): 151–162. https://doi.org/10.1016/S0378-4320(02)00189-6 DOI: https://doi.org/10.1016/S0378-4320(02)00189-6

Fontaine, C. (2015). Long-term contraception in a small implant. Journal of Feline Medicine and Surgery 17(9): 766–771. https://doi.org/10.1177/1098612X15594990 DOI: https://doi.org/10.1177/1098612X15594990

Gong, J.G., B.K. Campbell, T.A. Bramley, C.G. Gutierrez, A.R. Peters & R. Webb (1996). Suppression in the secretion of follicle-stimulating hormone and luteinizing hormone, and ovarian follicle development in heifers continuously Infused with a gonadotropin-releasing hormone agonist. Biology of Reproduction 55(1): 68–74. https://doi.org/10.1095/biolreprod55.1.68 DOI: https://doi.org/10.1095/biolreprod55.1.68

Gong, J.G., T.A. Bramley, C.G. Gutierrez, A.R. Peters & R. Webb (1995). Effects of chronic treatment with a gonadotrophin-releasing hormone agonist on peripheral concentrations of FSH and LH, and ovarian function in heifers. Reproduction 105(2): 263–270. https://doi.org/10.1530/jrf.0.1050263 DOI: https://doi.org/10.1530/jrf.0.1050263

Gonzalez, S.J., J.G. Howard, J. Brown, H. Grajales, J. Pinzón, H. Grajales, J. Pinzón, H. Monsalve, M.A. Moreno & C.J. Escobar (2017). Reproductive analysis of male and female captive jaguars (Panthera onca) in a Colombian zoological park. Theriogenology 89: 192–200. https://doi.org/10.1016/j.theriogenology.2016.09.049 DOI: https://doi.org/10.1016/j.theriogenology.2016.09.049

Graham, L.H., A.P. Byers, D.L. Armstrong, N.M. Loskutoff, W.F. Swanson, D.E. Wildt & J.L. Brown (2006). Natural and gonadotropin-induced ovarian activity in tigers (Panthera tigris) assessed by fecal steroid analyses. General and Comparative Endocrinology 147(3): 362–370. https://doi.org/10.1016/j.ygcen.2006.02.008 DOI: https://doi.org/10.1016/j.ygcen.2006.02.008

Graham, L.H., W.F. Swanson & J.L. Brown (2000). Chorionic gonadotropin administration in domestic cats causes an abnormal endocrine environment that disrupts oviductal embryo transport. Theriogenology 54(7): 1117–1131. https://doi.org/10.1016/S0093-691X(00)00420-9 DOI: https://doi.org/10.1016/S0093-691X(00)00420-9

Grandy, J.W. & A.T. Rutberg (2002). An animal welfare view of wildlife contraception. Reproduction (Cambridge, England) Supplement 60: 1–7.

Jewgenow, K., M. Dehnhard, T.B. Hildebrandt & F. Göritz (2006). Contraception for population control in exotic carnivores. Theriogenology 66(6–7): 1525–1529. https://doi.org/10.1016/j.theriogenology.2006.01.027 DOI: https://doi.org/10.1016/j.theriogenology.2006.01.027

Jorge-Neto, P.N., T.C. Luczinski, G.R. Araújo, J.A. Salomão Júnior, A.S. Traldi, J.A.M. Santos, L.A. Requena, M.C.M. Gianni, T. Deco-Souza, C.S. Pizzutto & H. Baldassarre (2020). Can jaguar (Panthera onca) ovulate without copulation? Theriogenology 147: 57–61. https://doi.org/10.1016/j.theriogenology.2020.02.026 DOI: https://doi.org/10.1016/j.theriogenology.2020.02.026

Jorge-Neto, P.N., C.S. Pizzutto, G.R. Araújo, T. Deco-Souza, L.C. Silva, J.A. Salomão Jr. & H. Baldassare (2018a). Copulatory behavior of the Jaguar Panthera onca (Mammalia: Carnivora: Felidae). Journal of Threatened Taxa 10(15): 12933–12939. https://doi.org/10.11609/jott.4218.10.15.12933-12939 DOI: https://doi.org/10.11609/jott.4218.10.15.12933-12939

Jorge Neto, P.N., L.A. Requena, C.S. Pizzuto & H. Baldassarre (2018b). Laparoscopic Ovum Pick-Up (LOPU): From animal production to conservation. SPERMOVA 8(1): 61–67. https://doi.org/10.18548/aspe/0006.07 DOI: https://doi.org/10.18548/aspe/0006.07

Melson, B.E., J.L. Brown, H.M. Schoenemann, G.K. Tarnavsky & J.J. Reeves (1986). Elevation of serum testosterone during chronic LHRH agonist treatment in the bull. Journal of Animal Science 62(1): 199–207. https://doi.org/10.2527/jas1986.621199x DOI: https://doi.org/10.2527/jas1986.621199x

Monfort, S.L., S.K. Wasser, K.L. Mashburn, M. Burke, B.A. Brewer & S.R. Creel (1997). Steroid metabolism and validation of noninvasive endocrine monitoring in the African Wild Dog (Lycaon pictus). Zoo Biology 16(6): 533–548. https://doi.org/10.1002/(SICI)1098-2361(1997)16:6<533::AID-ZOO6>3.0.CO;2-B DOI: https://doi.org/10.1002/(SICI)1098-2361(1997)16:6<533::AID-ZOO6>3.0.CO;2-B

Munson, L. (2006). Contraception in felids. Theriogenology 66(1): 126–134. https://doi.org/10.1016/j.theriogenology.2006.03.016 DOI: https://doi.org/10.1016/j.theriogenology.2006.03.016

Munson, L., J.E. Bauman, C.S. Asa, W. Jöchle & T.E. Trigg (2001). Efficacy of the GnRH analogue deslorelin for suppression of oestrous cycles in cats. Journal of Reproduction and Fertility. Supplement 57: 269–273.

Packer, C., A. Loveridge, S. Canney, T. Caro, S.T. Garnett, M Pfeifer, K.K. Zander, A. Swanson, D. MacNulty, G. Balme, H. Bauer, C.M. Begg, K.S. Begg, S.Bhalla, C. Bissett, T. Bodasing, H. Brink, A. Burger, A.C. Burton, B. Clegg, S. Dell, A. Delsink, T. Dickerson, S.M.Dloniak, D. Druce, L. Frank, P. Funston, N. Gichohi, R. Groom, C. Hanekom, B. Heath, L. Hunter, H.H. DeIongh, C.J. Joubert, S.M. Kasiki, B. Kissui, W. Knocker, B. Leathem, P.A. Lindsey, S.D. Maclennan, J.W. McNutt, S.M. Miller, S. Naylor, P. Nel, C. Ng’weno, K. Nicholls, J.O. Ogutu, E. Okot-Omoya, B.D. Patterson, A. Plumptre, J. Salerno, K. Skinner, R. Slotow, E.A. Sogbohossou, K.J. Stratford, C. Winterbach, H. Winterbach, S. Polasky (2013). Conserving large carnivores: dollars and fence. Ecology Letters 16(5): 635–641. https://doi.org/10.1111/ele.12091 DOI: https://doi.org/10.1111/ele.12091

Pelican, K.M., J.L. Brown, D.E. Wildt, M.A. Ottinger & J.G. Howard (2005). Short term suppression of follicular recruitment and spontaneous ovulation in the cat using levonorgestrel versus a GnRH antagonist. General and Comparative Endocrinology 144(2): 110–121. https://doi.org/10.1016/j.ygcen.2005.04.014 DOI: https://doi.org/10.1016/j.ygcen.2005.04.014

Rosenfield, D.A. (2016). Wildlife population control comprehensive and critical literature review on contraceptive methods in wildlife - mammals. Universidade de São Paulo, São Paulo, 219pp. https://doi.org/10.11606/D.10.2016.tde-05102016-134221 DOI: https://doi.org/10.11606/D.10.2016.tde-05102016-134221

Schaller, G.B. (1972). Behavior within the group, pp. 83–166. In: Schaller, G.B. (ed.). The Serengeti Lion. A study of predator-prey relations. University of Chicago Press, Chicado, 504pp.

Schmidt, A.M., D.L. Hess, M.J. Schmidt & C.R. Lewis (1993). Serum concentrations of oestradiol and progesterone and frequency of sexual behaviour during the normal oestrous cycle in the snow leopard (Panthera uncia). Reproduction 98(1): 91–95. https://doi.org/10.1530/jrf.0.0980091 DOI: https://doi.org/10.1530/jrf.0.0980091

Schmidt, A.M., D.L. Hess, M.J. Schmidt, R.C. Smith & C.R. Lewis (1988). Serum concentrations of oestradiol and progesterone, and sexual behaviour during the normal oestrous cycle in the leopard (Panthera pardus). Journal of Reproduction and Fertility 82(1): 43–49. https://doi.org/10.1530/jrf.0.0820043 DOI: https://doi.org/10.1530/jrf.0.0820043

Schramm, R.D., M.B. Briggs & J.J. Reeves (1994). Spontaneous and induced ovulation in the lion (Panthera leo). Zoo Biology 13(4): 301–307. https://doi.org/10.1002/zoo.1430130403 DOI: https://doi.org/10.1002/zoo.1430130403

Seal, U.S., R.L. Tilson, E.D. Plotka, N.J. Reindl & M.F. Seal (1987). Behavioral indicators and endocrine correlates of estrus and anestrus in Siberian tigers, pp. 244–250. In: Tilson, R. & U. Seal (Eds.). Tigers of The World: The Biology, Biopolitics, Management, And Conservation of An Endangered Species. Noyes Publications, Park Ridge, 540pp.

Sgai, M.G.F.G., C.S. Pizzutto, P. Viau, C.A. Oliveira & M.A. de B.V Guimarães (2015). Estudo endócrino reprodutivo e do comportamento sócio-sexual de sagui-de-tufo-preto (Callithrix penicillata) mantido em cativeiro. Pesquisa Veterinária Brasileira 35(3): 304–310. https://doi.org/10.1590/S0100-736X2015000300015 DOI: https://doi.org/10.1590/S0100-736X2015000300015

Sheriff, M.J., B. Dantzer, B. Delehanty, R. Palme & R. Boonstra (2011). Measuring stress in wildlife: techniques for quantifying glucocorticoids. Oecologia 166(4): 869–887. https://doi.org/10.1007/s00442-011-1943-y DOI: https://doi.org/10.1007/s00442-011-1943-y

Sinhorini, J.A., C.S. Pizzutto & R. Palme (2020). ACTH Stimulation Induced Self-Mutilation Behavior in the Golden Conure (Guaruba guarouba). Animals 10(3): 418. https://doi.org/10.3390/ani10030418 DOI: https://doi.org/10.3390/ani10030418

Umapathy, G., S.D. Sontakke, K. Srinivasu, T. Kiran, S.D. Kholkute & S. Shivaji (2007). Estrus behavior and fecal steroid profiles in the Asiatic lion (Panthera leo persica) during natural and gonadotropin-induced estrus. Animal Reproduction Science 101(3–4): 313–325. https://doi.org/10.1016/j.anireprosci.2006.09.014 DOI: https://doi.org/10.1016/j.anireprosci.2006.09.014

Van Meter, P.E., J.A. French, K. Bidali, M.L. Weldele, J.L Brown & K.E. Holekamp (2008). Non-invasive measurement of fecal estrogens in the spotted hyena (Crocuta crocuta). General and Comparative Endocrinology 155(2): 464–471. https://doi.org/10.1016/j.ygcen.2007.08.002 DOI: https://doi.org/10.1016/j.ygcen.2007.08.002

Wielebnowski, N. & J.L. Brown (1998). Behavioral correlates of physiological estrus in cheetahs. Zoo Biology 17(3): 193–209. https://doi.org/10.1002/(SICI)1098-2361(1998)17:3<193::AID-ZOO4>3.0.CO;2-4 DOI: https://doi.org/10.1002/(SICI)1098-2361(1998)17:3<193::AID-ZOO4>3.0.CO;2-4

Wildt, D.E., C.C. Platz, P.K. Chakraborty & S.W.J. Seager (1979). Oestrous and ovarian activity in a female jaguar (Panthera onca). Reproduction 56(2): 555–558. https://doi.org/10.1530/jrf.0.0560555 DOI: https://doi.org/10.1530/jrf.0.0560555

Woodroffe, R (2001). Strategies for carnivore conservation: lessons from contemporary extinctions, pp. 61–92. In: Gittleman, J.L., S.M. Funk, D.W. MacDonald, & R.K. Wayne (eds.). Carnivore conservation. Cambridge University Press, 690pp.

Woodroffe, R. & L.G. Frank (2005). Lethal control of African Lions (Panthera leo): local and regional population impacts. Animal Conservation 8(1): 91–98. https://doi.org/10.1017/S1367943004001829 DOI: https://doi.org/10.1017/S1367943004001829

Wright, P.J., J.P. Verstegen, K. Onclin, W. Jöchle, A.F. Armour, G.B. Martin & T.E. Trigg (2001). Suppression of the oestrous responses of bitches to the GnRH analogue deslorelin by progestin. Journal of Reproduction and Fertility. Supplement 57: 263–268.

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