Animal Reproduction (AR)
https://animal-reproduction.org/article/doi/10.1590/1984-3143-AR2024-0049
Animal Reproduction (AR)
Thematic Section: 40th Annual Meeting of the Association of Embryo Technology in Europe (AETE)

40 ‘wild’ years: the current reality and future potential of assisted reproductive technologies in wildlife species

Gabriela Mastromonaco

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Abstract

Over the past 40 years, assisted reproductive technologies (ARTs) have grown significantly in scale and innovation, from the bovine embryo industry’s shift from in vivo derived to in vitro produced embryos and the development of somatic cell-based approaches for embryo production. Domestic animal models have been instrumental in the development of ARTs for wildlife species in support of the One Plan Approach to species conservation that integrates in situ and ex situ population management strategies. While ARTs are not the sole solution to the biodiversity crisis, they can offer opportunities to maintain, and even improve, the genetic composition of the captive and wild gene pools over time. This review focuses on the application of sperm and embryo technologies (artificial insemination and multiple ovulation/in vitro produced embryo transfer, respectively) in wildlife species, highlighting impactful cases in which significant progress or innovation has transpired. One of the key messages following decades of efforts in this field is the importance of collaboration between researchers and practitioners from zoological, academic, governmental, and private sectors.

Keywords

assisted reproduction, embryo technologies, biodiversity conservation, wildlife species

References

Aardema H, Vethaak A, Kamstra JH, Legler J. Farm animals as a critical link between environmental and human health impacts of micro-and nanoplastics. Micropl and Nanopl. 2024;4(5):5. http://doi.org/10.1186/s43591-024-00082-w.

Acevedo C, Barfield JP. Review: reproductive physiology of bison and application of assisted reproductive technologies to their conservation. Animal. 2023;17(Suppl 1):100842. http://doi.org/10.1016/j.animal.2023.100842. PMid:37567664.

Allen WRT, Wilsher S. Historical aspects of equine embryo transfer. J Equine Vet Sci. 2020;89:102987. http://doi.org/10.1016/j.jevs.2020.102987. PMid:32563443.

Anzalone DA, Palazzese L, Iuso D, Martino G, Loi P. Freeze-dried spermatozoa: an alternative biobanking option for endangered species. Anim Reprod Sci. 2018;190:85-93. http://doi.org/10.1016/j.anireprosci.2018.01.010. PMid:29397252.

Baldrighi JM, Sá Filho MF, Siqueira AF, Visintin JA, Baruselli PS, Assumpção MEOA. Temporal evaluation of follicular dynamics and endocrine patterns of Holstein (Bos taurus), Gir (Bos indicus), and Murrah (Bubalus bubalis) heifers kept under the same nutritional, management and environmental conditions. Theriogenology. 2022;190:8-14. http://doi.org/10.1016/j.theriogenology.2022.07.006. PMid:35863098.

Ballou JD. Strategies for maintaining genetic diversity in captive populations through reproductive technology. Zoo Biol. 1984;3(4):311-23. http://doi.org/10.1002/zoo.1430030404.

Beirão J, Boulais M, Gallego V, O’Brien JK, Peixoto S, Robeck TR, Cabrita E. Sperm handling in aquatic animals for artificial reproduction. Theriogenology. 2019;133:161-78. http://doi.org/10.1016/j.theriogenology.2019.05.004. PMid:31108371.

Bison Integrated Genomics (BIG) Project. [homepage on the Internet]. Parks Canada; 2022 [cited 2024 March 9]. Available from: https://www.bigproject.ca/.

Blanco JM, Wildt DE, Höfle U, Voelker W, Donoghue AM. Implementing artificial insemination as an effective tool for ex situ conservation of endangered avian species. Theriogenology. 2009;71(1):200-13. http://doi.org/10.1016/j.theriogenology.2008.09.019. PMid:19004491.

BusinessWire. [homepage on the internet]. BioSpace, 2023. Colossal biosciences joins BioRescue in its mission to save the northern white rhino from extinction; 2023 [cited 2024 March 20]. Available from: https://www.biospace.com/article/releases/colossal-biosciences-joins-biorescue-in-its-mission-to-save-the-northern-white-rhino-from-extinction/.

Byers O, Lees C, Wilcken J, Schwitzer C. The One Plan Approach: the philosophy and implementation of CBSG’s approach to integrated species conservation planning. In: Gusset M, Dick G, editors. Towards integrated species conservation. Vol. 14. Switzerland: World Association of Zoos and Aquariums Magazine. [serial on the internet]. 2013 [cited 2024 March 9]. p. 2-5. Available from: https://www.waza.org/wp-content/uploads/2019/02/waza_mag_14.pdf.

Cabeza JP, Gambini A. Advancements and challenges in in vitro reproductive technologies for the conservation of equine species. Theriogenology Wild. 2023;2:100036. http://doi.org/10.1016/j.therwi.2023.100036.

Chatiza FP, Bartels P, Nedambale TL, Wagenaar GM. Sperm-egg interaction and functional assessment of springbok, impala and blesbok cauda epididymal spermatozoa using a domestic cattle in vitro fertilization system. Anim Reprod Sci. 2013;143(1-4):8-18. http://doi.org/10.1016/j.anireprosci.2013.11.001. PMid:24284137.

Crosier AE, Comizzoli P, Koester DC, Wildt DE. Circumventing the natural, frequent oestrogen waves of the female cheetah (Acinonyx jubatus) using oral progestin (Altrenogest). Reprod Fertil Dev. 2017;29(8):1486-98. http://doi.org/10.1071/RD16007. PMid:27483379.

Crosier AE, Henghali JN, Howard J, Pukazhenthi BS, Terrell KA, Marker LL, Wildt DE. Improved quality of cryopreserved cheetah (Acinonyx jubatus) spermatozoa after centrifugation through Accudenz. J Androl. 2009;30(3):298-308. http://doi.org/10.2164/jandrol.108.006239. PMid:19023140.

Diwan AD, Harke SN, Gopalkrishna, Panche AN. Gopalkrishna, Panche AN. Cryobanking of fish and shellfish egg, embryos and larvae: an overview. Front Mar Sci. 2020;7:251. http://doi.org/10.3389/fmars.2020.00251.

Dominko T, Mitalipova M, Haley B, Beyhan Z, Memili E, McKusick B, First NL. Bovine oocyte cytoplasm supports development of embryos produced by nuclear transfer of somatic cell nuclei from various mammalian species. Biol Reprod. 1999;60(6):1496-502. http://doi.org/10.1095/biolreprod60.6.1496. PMid:10330111.

Dresser BL. Cryobiology, embryo transfer, and artificial insemination in ex situ animal conservation programs. In: Wilson EO, Peter FM, editors. Biodiversity. Washington (DC): National Academies Press; 1988. Chapter 34, p. 296-308.

Dresser BL. Embryo transfer in exotic bovids. Int Zoo Yearb. 1986;24(1):138-42. http://doi.org/10.1111/j.1748-1090.1985.tb02529.x.

Duarte GS, Galindo DJ, Baldini MHM, da Fonseca JF, Duarte JMB, Oliveira MEF. Transcervical artificial insemination in the brown brocket deer (Subulo gouazoubira): a promising method for assisted reproduction in deer. Sci Rep. 2023;13(1):17369. http://doi.org/10.1038/s41598-023-43392-4. PMid:37833322.

Duszewska AM, Baraniewicz-Kołek M, Wojdan J, Barłowska K, Bielecki W, Gręda P, Niżański W, Olech W. Establishment of a wisent (Bison bonasus) germplasm bank. Animals (Basel). 2022;12(10):1239. http://doi.org/10.3390/ani12101239. PMid:35625085.

Ferraz MAMM, Ferronato GA. Opportunities involving microfluidics and 3D culture systems to the in vitro embryo production. Anim Reprod. 2023;20(2):e20230058. http://doi.org/10.1590/1984-3143-ar2023-0058. PMid:37638255.

Ferraz MAMM, Nagashima JB, Noonan MJ, Crosier AE, Songsasen N. Oviductal extracellular vesicles improve post-thaw sperm function in red wolves and cheetahs. Int J Mol Sci. 2020;21(10):3733. http://doi.org/10.3390/ijms21103733. PMid:32466321.

Ferré LB, Kjelland ME, Strøbech LB, Hyttel P, Mermillod P, Ross PJ. Review: recent advances in bovine in vitro embryo production: reproductive biotechnology history and methods. Animal. 2020;14(5):991-1004. http://doi.org/10.1017/S1751731119002775. PMid:31760966.

Gambini A, Duque Rodríguez M, Rodríguez MB, Briski O, Flores Bragulat AP, Demergassi N, Losinno L, Salamone DF. Horse ooplasm supports in vitro preimplantation development of zebra ICSI and SCNT embryos without compromising YAP1 and SOX2 expression pattern. PLoS One. 2020;15(9):e0238948. http://doi.org/10.1371/journal.pone.0238948. PMid:32915925.

Gambini A, Maserati M. A journey through horse cloning. Reprod Fertil Dev. 2017;30(1):8-17. http://doi.org/10.1071/RD17374. PMid:29539299.

Hayashi K, Saitou M. Generation of eggs from mouse embryonic stem cells and induced pluripotent stem cells. Nat Protoc. 2013;8(8):1513-24. http://doi.org/10.1038/nprot.2013.090. PMid:23845963.

Hayashi M, Zywitza V, Naitou Y, Hamazaki N, Goeritz F, Hermes R, Holtze S, Lazzari G, Galli C, Stejskal J, Diecke S, Hildebrandt TB, Hayashi K. Robust induction of primordial germ cells of white rhinoceros on the brink of extinction. Sci Adv. 2022;8(49):eabp9683. http://doi.org/10.1126/sciadv.abp9683. PMid:36490332.

Herrick JR. Assisted reproductive technologies for endangered species conservation: developing sophisticated protocols with limited access to animals with unique reproductive mechanisms. Biol Reprod. 2019;100(5):1158-70. http://doi.org/10.1093/biolre/ioz025. PMid:30770538.

Hildebrandt TB, Holtze S, Colleoni S, Hermes R, Stejskal J, Lekolool I, Ndeereh D, Omondi P, Kariuki L, Mijele D, Mutisya S, Ngulu S, Diecke S, Hayashi K, Lazzari G, de Mori B, Biasetti P, Quaggio A, Galli C, Goeritz F. In vitro fertilization program in white rhinoceros. Reproduction. 2023;166(6):383-99. http://doi.org/10.1530/REP-23-0087. PMid:37877686.

Holt WV, Fazeli A. Sperm storage in the female reproductive tract. Annu Rev Anim Biosci. 2016;4(1):291-310. http://doi.org/10.1146/annurev-animal-021815-111350 PMid:26526545.

Imbler S. [homepage on the Internet]. USA: The New York TImes; 2021. Meet Elizabeth Ann, the first cloned black-footed ferret; 2021 [cited 2024 February 18]. Available from: https://www.nytimes.com/2021/02/18/science/black-footed-ferret-clone.html.

Kahrl AF, Snook RR, Fitzpatrick JL. Fertilization mode differentially impacts the evolution of vertebrate sperm components. Nat Commun. 2022;13(1):6809. http://doi.org/10.1038/s41467-022-34609-7. PMid:36357384.

Kaneko T, Ito H, Sakamoto H, Onuma M, Inoue-Murayama M. Sperm preservation by freeze-drying for the conservation of wild animals. PLoS One. 2014;9(11):e113381. http://doi.org/10.1371/journal.pone.0113381. PMid:25409172.

Katayama M, Fukuda T, Kaneko T, Nakagawa Y, Tajima A, Naito M, Ohmaki H, Endo D, Asano M, Nagamine T, Nakaya Y, Saito K, Watanabe Y, Tani T, Inoue-Murayama M, Nakajima N, Onuma M. Induced pluripotent stem cells of endangered avian species. Commun Biol. 2022;5(1):1049. http://doi.org/10.1038/s42003-022-03964-y. PMid:36280684.

Kersey DC, Wildt DE, Brown JL, Snyder RJ, Huang Y, Monfort SL. Endocrine milieu of perioestrus in the giant panda (Ailuropoda melanoleuca), as determined by non-invasive hormone measures. Reprod Fertil Dev. 2010;22(6):901-12. http://doi.org/10.1071/RD09178. PMid:20591324.

Korody ML, Ford SM, Nguyen TD, Pivaroff CG, Valiente-Alandi I, Peterson SE, Ryder OA, Loring JF. Rewinding extinction in the northern white rhinoceros: genetically diverse induced pluripotent stem cell bank for genetic rescue. Stem Cells Dev. 2021;30(4):177-89. http://doi.org/10.1089/scd.2021.0001. PMid:33406994.

Kouba AJ, Vance CK, Willis EL. Artificial fertilization for amphibian conservation: current knowledge and future considerations. Theriogenology. 2009;71(1):214-27. http://doi.org/10.1016/j.theriogenology.2008.09.055. PMid:19026442.

Kouba AJ, Vance CK. Applied reproductive technologies and genetic resource banking for amphibian conservation. Reprod Fertil Dev. 2009;21(6):719-37. http://doi.org/10.1071/RD09038. PMid:19567216.

Kydd J, Boyle MS, Allen WR, Shephard A, Summer PM. Transfer of exotic equine embryos to domestic horses and donkeys. Equine Vet J. 1985;17(S3):80-3. http://doi.org/10.1111/j.2042-3306.1985.tb04601.x.

Li J, Song W, Pan G, Zhou J. Advances in understanding the cell types and approaches used for generating induced pluripotent stem cells. J Hematol Oncol. 2014;7(1):50. http://doi.org/10.1186/s13045-014-0050-z. PMid:25037625.

Lindeberg H, Nikitkina E, Nagy S, Musidray A, Shiryaev G, Kumpula J, Holand Ø. Potential applications of assisted reproductive technologies (ART) in reindeer (Rangifer tarandus). Anim Reprod Sci. 2021;235:106890. http://doi.org/10.1016/j.anireprosci.2021.106890. PMid:34847527.

Locatelli Y, Hendriks A, Vallet JC, Baril G, Duffard N, Bon N, Ortiz K, Scala C, Maurel MC, Mermillod P, Legendre X. Assessment LOPU-IVF in Japanese sika deer (Cervus nippon nippon) and application to Vietnamese sika deer (Cervus nippon pseudaxis) a related subspecies threatened with extinction. Theriogenology. 2012;78(9):2039-49. http://doi.org/10.1016/j.theriogenology.2012.07.025. PMid:23043947.

Lueders I, Luther I, Scheepers G, van der Horst G. Improved semen collection method for wild felids: urethral catheterization yields high sperm quality in African lions (Panthera leo). Theriogenology. 2012;78(3):696-701. http://doi.org/10.1016/j.theriogenology.2012.02.026. PMid:22538007.

Mastromonaco GF, González-Grajales LA, Filice M, Comizzoli P. Somatic cells, stem cells, and induced pluripotent stem cells: how do they now contribute to conservation? In: Holt WV, Brown JL, Comizzoli P, editors. Reproductive sciences in animal conservation. advances in experimental medicine and biology. New York: Springer; 2014. p. 385-427. http://doi.org/10.1007/978-1-4939-0820-2_16.

Mastromonaco GF, Songsasen N. Reproductive technologies for the conservation of wildlife and endangered species. In: Presicce GA, editor. Reproductive technologies in animals. Cambridge: Academic Press; 2020. Chapter 7, p. 99-117.

Mastromonaco GF. A quarter century of CANDES: the state of embryo technologies in companion animals, non-domestic and endangered species. Theriogenology Wild. 2024;4:100069. http://doi.org/10.1016/j.therwi.2023.100069.

Matsumura T, Katagiri K, Yao T, Ishikawa-Yamauchi Y, Nagata S, Hashimoto K, Sato T, Kimura H, Shinohara T, Sanbo M, Hirabayashi M, Ogawa T. Generation of rat offspring using spermatids produced through in vitro spermatogenesis. Sci Rep. 2023;13(1):12105. http://doi.org/10.1038/s41598-023-39304-1. PMid:37495678.

Melo LM, Silva SB, Magalhães LC, Cortez JV, Kumar S, Duarte JMB, Rola LD, Chaves MS, Freitas VJF. The use of somatic cell nuclear transfer to obtain interspecific cloned embryos from brown brocket deer karyoplast and bovine cytoplast: embryo development and nuclear gene expression. Theriogenology Wild. 2022;1:100001. http://doi.org/10.1016/j.therwi.2022.100001.

Menkhorst E, Selwood L. Vertebrate extracellular preovulatory and postovulatory egg coats. Biol Reprod. 2008;79(5):790-7. http://doi.org/10.1095/biolreprod.108.068551. PMid:18614703.

Nagashima JB, Songsasen N. Canid reproductive biology: norm and unique aspects in strategies and mechanisms. Animals (Basel). 2021;11(3):653. http://doi.org/10.3390/ani11030653. PMid:33804569.

Novak BJ, Ryder OA, Houck ML, Putnam AS, Walker K, Russell L, Russell B, Walker S, Arenivas SS, Aston L, Veneklasen G, Ivy JA, Koepfli K-P, Rusnak A, Simek J, Zhuk A, Phelan R. Endangered Przewalski’s horse, Equus przewalskii, cloned from historically cryopreserved cells. bioRxiv 2024;1-17. http://doi.org/10.1101/2023.12.20.572538.

O’Brien JK, Robeck TR. Development of sperm sexing and associated assisted reproductive technology for sex preselection of captive bottlenose dolphins (Tursiops truncatus). Reprod Fertil Dev. 2006;18(3):319-29. http://doi.org/10.1071/RD05108. PMid:16554007.

O’Brien JK, Steinman KJ, Schmitt T, Robeck TR. Semen collection, characterisation and artificial insemination in the beluga (Delphinapterus leucas) using liquid-stored spermatozoa. Reprod Fertil Dev. 2008;20(7):770-83. http://doi.org/10.1071/RD08031. PMid:18842179.

Ogorevc J, Orehek S, Dovč P. Cellular reprogramming in farm animals: an overview of iPSC generation in the mammalian farm animal species. J Anim Sci Biotechnol. 2016;7(1):10. http://doi.org/10.1186/s40104-016-0070-3. PMid:26900466.

Palomino JM, Mastromonaco GF, Cervantes MP, Mapletoft RJ, Anzar M, Adams GP. Effect of season and superstimulatory treatment on in vivo and in vitro embryo production in wood bison (Bison bison athabascae). Reprod Domest Anim. 2020;55(1):54-63. http://doi.org/10.1111/rda.13580. PMid:31661568.

Peippo J, Lindeberg H, Mutikainen M, Harmama T-M, Kumpula J, Holand O. In vitro production of the first reindeer (Rangifer tarandus tarandus) blastocysts. In: Proceedings of the 35th annual meeting of the European Embryo Transfer Association; 2019 Sep 12-14; Murcia, Spain. Murcia: AETE; 2019. p. 746.

Pennington PM, Marshall KL, Capiro JM, Felton RG, Durrant BS. Ovulation induction in anovulatory southern white rhinoceros (Ceratotherium simum simum) without altrenogest. Conserv Physiol. 2019;7(1):coz033. http://doi.org/10.1093/conphys/coz033. PMid:31249689.

Perry S. Developing assisted reproduction for reptiles, what’s next? Clin Theriogenology. 2021;13:383. https://doi.org/10.58292/ct.v13.9315.

Prieto MT, Sanchez-Calabuig MJ, Hildebrandt TB, Santiago-Moreno J, Saragusty J. Sperm cryopreservation in wild animals. Eur J Wildl Res. 2014;60(6):851-64. http://doi.org/10.1007/s10344-014-0858-4.

Pukazhenthi BS, Wildt DE. Which reproductive technologies are most relevant to studying, managing and conserving wildlife? Reprod Fertil Dev. 2004;16(1-2):33-46. http://doi.org/10.1071/RD03076. PMid:14972101.

Revive & Restore. [homepage on the internet]. Revive & Restore; 2024. The genetic rescue toolkit; 2024 [cited 2024 March 10]. Available from: https://reviverestore.org/what-we-do/genetic-rescue-toolkit

Robeck TR, Montano GA, Steinman KJ, Smolensky P, Sweeney J, Osborn S, O’Brien JK. Development and evaluation of deep intra-uterine artificial insemination using cryopreserved sexed spermatozoa in bottlenose dolphins (Tursiops truncatus). Anim Reprod Sci. 2013;139(1-4):168-81. http://doi.org/10.1016/j.anireprosci.2013.04.004. PMid:23660366.

Robeck TR, Steinman KJ, Gearhart S, Reidarson TR, McBain JF, Monfort SL. Reproductive physiology and development of artificial insemination technology in killer whales (Orcinus orca). Biol Reprod. 2004;71(2):650-60. http://doi.org/10.1095/biolreprod.104.027961. PMid:15115725.

Robeck TR, Steinman KJ, Greenwell M, Ramirez K, Van Bonn W, Yoshioka M, Katsumata E, Dalton L, Osborn S, O’Brien JK. Seasonality, estrous cycle characterization, estrus synchronization, semen cryopreservation, and artificial insemination in the Pacific white-sided dolphin (Lagenorhynchus obliquidens). Reproduction. 2009;138(2):391-405. http://doi.org/10.1530/REP-08-0528. PMid:19494046.

Rola LD, Buzanskas ME, Melo LM, Chaves MS, Freitas VJF, Duarte JMB. Assisted reproductive technology in neotropical deer: a model approach to preserving genetic diversity. Animals (Basel). 2021a;11(7):1961. http://doi.org/10.3390/ani11071961. PMid:34209061.

Rola LD, Zanetti EDS, Del Collado M, Peroni EFC, Duarte JMB. Collection and in vitro maturation of Mazama gouazoubira (brown brocket deer) oocytes obtained after ovarian stimulation. Zygote. 2021b;29(3):216-22. http://doi.org/10.1017/S0967199420000787. PMid:33446301.

Roth TL. That was then, this is now – over two decades of progress in rhinoceros reproductive science and technology. Theriogenology Wild. 2024;4:100065. http://doi.org/10.1016/j.therwi.2023.100065.

Silla AJ, Calatayud NE, Trudeau VL. Amphibian reproductive technologies: approaches and welfare considerations. Conserv Physiol. 2021;9(1):coab011. http://doi.org/10.1093/conphys/coab011. PMid: 33763231.

Sontakke SD. Monitoring and controlling ovarian activities in wild ungulates. Theriogenology. 2018;109:31-41. http://doi.org/10.1016/j.theriogenology.2017.12.008. PMid:29254686.

Stewart RA, Pelican KM, Crosier AE, Pukazhenthi BS, Wildt DE, Ottinger MA, Howard J. Oral progestin priming increases ovarian sensitivity to gonadotropin stimulation and improves luteal function in the cat. Biol Reprod. 2012;87(6):137. http://doi.org/10.1095/biolreprod.112.104190. PMid:23100619.

Strange A, Alberio R. Review: a barnyard in the lab: prospect of generating animal germ cells for breeding and conservation. Animal. 2023;17(Suppl 1):100753. http://doi.org/10.1016/j.animal.2023.100753. PMid:37567650.

Swanson WF, Penfold LM. Captive wildlife breeding: mammals & birds. In: Skinner MK, editor. Encyclopedia of Reproduction. 2nd ed. Cambridge: Academic Press; 2018. p. 782-90. http://doi.org/10.1016/B978-0-12-809633-8.20631-6.

Swegen A, Appeltant R, Williams SA. Cloning in action: can embryo splitting, induced pluripotency and somatic cell nuclear transfer contribute to endangered species conservation? Biol Rev Camb Philos Soc. 2023;98(4):1225-49. http://doi.org/10.1111/brv.12951. PMid:37016502.

Swengel SR, Tuite ML. Recent advances in scheduling strategies and practical techniques in crane artificial insemination. In: North American Crane Workshop Proceedings; 1997 Jan 10-13; Biloxi, United States. Biloxi: North American Crane; 1997. p. 46-55.

Thitaram C, Brown JL. Monitoring and controlling ovarian activity in elephants. Theriogenology. 2018;109:42-7. http://doi.org/10.1016/j.theriogenology.2017.12.009. PMid:29287954.

Thongphakdee A, Berg DK, Tharasanit T, Thongtip N, Tipkantha W, Punkong C, Tongthainan D, Noimoon S, Maikeaw U, Kajornklin N, Siriaroonrat B, Comizzoli P, Kamolnorranath S. The impact of ovarian stimulation protocol on oocyte quality, subsequent in vitro embryo development, and pregnancy after transfer to recipients in Eld’s deer (Rucervus eldii thamin). Theriogenology. 2017;91:134-44. http://doi.org/10.1016/j.theriogenology.2016.12.021. PMid:28215678.

Thongphakdee A, Sukparangsi W, Comizzoli P, Chatdarong K. Reproductive biology and biotechnologies in wild felids. Theriogenology. 2020;150:360-73. http://doi.org/10.1016/j.theriogenology.2020.02.004. PMid:32102745.

Thongphakdee A, Tipkantha W, Punkong C, Chatdarong K. Monitoring and controlling ovarian activity in wild felids. Theriogenology. 2018;109:14-21. http://doi.org/10.1016/j.theriogenology.2017.12.010. PMid:29258698.

Toosi BM, Tribulo A, Lessard C, Mastromonaco GF, McCorkell RB, Adams GP. Superovulation and embryo transfer in wood bison (Bison bison athabascae). Theriogenology. 2013;80(5):542-51. http://doi.org/10.1016/j.theriogenology.2013.05.020. PMid:23831114.

United Parks & Resorts. [homepage on the Internet]. United Parks & Resorts; 2024. Species preservation laboratory; 2024 [cited 2024 March 9]. Available from: https://seaworld.org/conservation/species-preservation-laboratory/primary-research/.

Van Eenennaam JP, Linares-Casenave J, Muguet J-B, Doroshov SI. Induced spawning, artificial fertilization, and egg incubation techniques for green sturgeon. N Am J Aquaculture. 2008;70(4):434-45. http://doi.org/10.1577/A07-073.1.

Wildt DE, Schiewe MC, Schmidt PM, Goodrowe KL, Howard JG, Phillips LG, O’Brien SJ, Bush M. Developing animal model systems for embryo technologies in rare and endangered wildlife. Theriogenology. 1986;25(1):33-51. http://doi.org/10.1016/0093-691X(86)90182-2.

Wyse J, Latif S, Gurusinghe S, McCormick J, Weston LA, Stephen CP. Phytoestrogens: a review of their impacts on reproductive physiology and other effects upon grazing livestock. Animals (Basel). 2022;12(19):2709. http://doi.org/10.3390/ani12192709. PMid:36230450.

Zhu H, Shao X, Chen Z, Wei C, Lei M, Ying S, Yu J, Shi Z. Induction of out-of-season egg laying by artificial photoperiod in Yangzhou geese and the associated endocrine and molecular regulation mechanisms. Anim Reprod Sci. 2017;180:127-36. http://doi.org/10.1016/j.anireprosci.2017.03.009. PMid:28342689.

Zwiefelhofer ML, Shury T, Zwiefelhofer EM, Singh J, Mastromonaco GF, Adams GP. Strategies for oocyte collection and in vitro embryo production in free-roaming bison herds. Conserv Physiol. 2022b;10(1):coac058. http://doi.org/10.1093/conphys/coac058. PMid: 35966755.

Zwiefelhofer ML, Singh J, Zwiefelhofer EM, Mastromonaco GF, Adams GP. Influence of ovarian follicular wave synchronization and single-dose eCG superstimulation on oocyte collection and in vitro embryo production in bison during the ovulatory and anovulatory seasons. Theriogenology. 2022a;187:238-46. http://doi.org/10.1016/j.theriogenology.2022.04.023. PMid:35660373.

Zywitza V, Rusha E, Shaposhnikov D, Ruiz-Orera J, Telugu N, Rishko V, Hayashi M, Michel G, Wittler L, Stejskal J, Holtze S, Göritz F, Hermes R, Wang J, Izsvák Z, Colleoni S, Lazzari G, Galli C, Hildebrandt TB, Hayashi K, Diecke S, Drukker M. Naïve-like pluripotency to pave the way for saving the northern white rhinoceros from extinction. Sci Rep. 2022;12(1):3100. http://doi.org/10.1038/s41598-022-07059-w. PMid:35260583.
 


Submitted date:
04/18/2024

Accepted date:
06/25/2024

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