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Vertebrate reproductive science and technology
REVIEW

Non-surgical sterilisation methods may offer a sustainable solution to feral horse (Equus caballus) overpopulation

Sally Elizabeth Hall A B , Brett Nixon A and R. John Aitken A B
+ Author Affiliations
- Author Affiliations

A Priority Research Centre for Reproductive Science, School of Environmental and Life Sciences, Life Sciences Building, University of Newcastle, Callaghan, NSW 2308, Australia.

B Invasive Animals Cooperative Research Centre, Building 22, University of Canberra, University Drive South, Bruce, ACT 2617, Australia.

C Corresponding author. Email: sally.e.hall@uon.edu.au

Reproduction, Fertility and Development 29(9) 1655-1666 https://doi.org/10.1071/RD16200
Submitted: 13 May 2016  Accepted: 9 September 2016   Published: 5 October 2016

Abstract

Feral horses are a significant pest species in many parts of the world, contributing to land erosion, weed dispersal and the loss of native flora and fauna. There is an urgent need to modify feral horse management strategies to achieve public acceptance and long-term population control. One way to achieve this is by using non-surgical methods of sterilisation, which are suitable in the context of this mobile and long-lived species. In this review we consider the benefits of implementing novel mechanisms designed to elicit a state of permanent sterility (including redox cycling to generate oxidative stress in the gonad, random peptide phage display to target non-renewable germ cells and the generation of autoantibodies against proteins essential for conception via covalent modification) compared with that of traditional immunocontraceptive approaches. The need for a better understanding of mare folliculogenesis and conception factors, including maternal recognition of pregnancy, is also reviewed because they hold considerable potential in providing a non-surgical mechanism for sterilisation. In conclusion, the authors contend that non-surgical measures that are single shot and irreversible may provide a sustainable and effective strategy for feral horse control.

Additional keywords: fertility, immunocontraception, oxidative stress, primordial germ cells, spermatozoa.


References

Adhikari, D., Gorre, N., Risal, S., Zhao, Z., Zhang, H., Shen, Y., and Liu, K. (2012). The safe use of a PTEN inhibitor for the activation of dormant mouse primordial follicles and generation of fertilizable eggs. PLoS One 7, e39034.
The safe use of a PTEN inhibitor for the activation of dormant mouse primordial follicles and generation of fertilizable eggs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xps1Ojtrg%3D&md5=9d1e8944ba07269aae9a747e68deeb4eCAS | 22761722PubMed |

Aitken, R. J. (2002). Immunocontraceptive vaccines for human use. J. Reprod. Immunol. 57, 273–287.
Immunocontraceptive vaccines for human use.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XnvVOms7c%3D&md5=3a7300a6183e46316a0528959225a16aCAS | 12385848PubMed |

Aitken, R. J., inventor. (19 June 2006). University of Newcastle, assignee. Method for reducing the reproductive potential of a female animal. Australian patent application no. 2006903307.

Aitken, R. J. (2008). Just how safe is assisted reproductive technology for treating male factor infertility? Expert Rev. Obstet. Gynecol. 3, 267–271.
Just how safe is assisted reproductive technology for treating male factor infertility?Crossref | GoogleScholarGoogle Scholar |

Aitken, R. J. (2015). Reagents for the sterilization of pest animal species. In ‘Research Portfolio Summary 2014–15’. (Ed. Invasive Animals Cooperative Research Centre.) pp. 46–47. (Invasive Animals Cooperative Research Centre: Canberra.)

Aitken, R. J., and Baker, M. A. (2006). Oxidative stress, sperm survival and fertility control. Mol. Cell. Endocrinol. 250, 66–69.
Oxidative stress, sperm survival and fertility control.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XksVGjtrc%3D&md5=b1e09b6c8f4378de50b6a02201a2af7aCAS | 16412557PubMed |

Aitken, R. J., and Clarkson, J. S. (1987). Cellular basis of defective sperm function and its association with the genesis of reactive oxygen species by human spermatozoa. J. Reprod. Fertil. 81, 459–469.
Cellular basis of defective sperm function and its association with the genesis of reactive oxygen species by human spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXltlyjsw%3D%3D&md5=be1bb7ef5d0b7b96d59fd9455b5a8bb6CAS | 2828610PubMed |

Aitken, R. J., and Curry, B. J. (2011). Redox regulation of human sperm function: from the physiological control of sperm capacitation to the etiology of infertility and DNA damage in the germ line. Antioxid. Redox Signal. 14, 367–381.
Redox regulation of human sperm function: from the physiological control of sperm capacitation to the etiology of infertility and DNA damage in the germ line.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1SjsA%3D%3D&md5=68be2c48411648e59daccf46e462f772CAS | 20522002PubMed |

Aitken, R. J., and De Iuliis, G. N. (2010). On the possible origins of DNA damage in human spermatozoa. Mol. Hum. Reprod. 16, 3–13.
On the possible origins of DNA damage in human spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsFOhtrrN&md5=4699fb6f6741c0db6253571d53025554CAS | 19648152PubMed |

Aitken, R. J., and Richardson, D. W. (1981). Mechanism of sperm‐binding inhibition by anti‐zona antisera. Gamete Res. 4, 41–47.
Mechanism of sperm‐binding inhibition by anti‐zona antisera.Crossref | GoogleScholarGoogle Scholar |

Aitken, R. J., Koopman, P., and Lewis, S. E. (2004). Seeds of concern. Nature 432, 48–52.
Seeds of concern.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXpt1eitrc%3D&md5=16ceca320a277612c92fec60068e7fe8CAS | 15525979PubMed |

Aitken, R. J., Gibb, Z., Mitchell, L. A., Lambourne, S. R., Connaughton, H. S., and De Iuliis, G. N. (2012). Sperm motility is lost in vitro as a consequence of mitochondrial free radical production and the generation of electrophilic aldehydes but can be significantly rescued by the presence of nucleophilic thiols. Biol. Reprod. 87, 110.
Sperm motility is lost in vitro as a consequence of mitochondrial free radical production and the generation of electrophilic aldehydes but can be significantly rescued by the presence of nucleophilic thiols.Crossref | GoogleScholarGoogle Scholar | 22933515PubMed |

Aitken, R. J., Smith, T. B., Lord, T., Kuczera, L., Koppers, A. J., Naumovski, N., Connaughton, H., Baker, M. A., and Iuliis, G. N. (2013). On methods for the detection of reactive oxygen species generation by human spermatozoa: analysis of the cellular responses to catechol oestrogen, lipid aldehyde, menadione and arachidonic acid. Andrology 1, 192–205.
On methods for the detection of reactive oxygen species generation by human spermatozoa: analysis of the cellular responses to catechol oestrogen, lipid aldehyde, menadione and arachidonic acid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXislOmtrg%3D&md5=09ab72ad2fbb22a9821bcde4ff065516CAS | 23316012PubMed |

Alexander, N. J., and Anderson, D. J. (1979). Vasectomy: consequences of autoimmunity to sperm antigens. Fertil. Steril. 32, 253–260.
Vasectomy: consequences of autoimmunity to sperm antigens.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL3c%2FisVykuw%3D%3D&md5=f77e3e719367bb1c63c39ff452f293b3CAS | 114428PubMed |

Allen, W. R. (1982). Immunological aspects of the endometrial cup reaction and the effect of xenogeneic pregnancy in horses and donkeys. J. Reprod. Fertil. Suppl. 31, 57–94.
| 1:CAS:528:DyaL3sXhsFyqur4%3D&md5=0bd635c3bc0915fe2375b9049262e40bCAS | 6962845PubMed |

Allen, W. R., and Wilsher, S. (2009). A review of implantation and early placentation in the mare. Placenta 30, 1005–1015.
A review of implantation and early placentation in the mare.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsVGls7fI&md5=198ec5eaabbf1c13cd5820f756284370CAS | 19850339PubMed |

Altuntas, C. Z., Johnson, J. M., and Tuohy, V. K. (2006). Autoimmune targeted disruption of the pituitary–ovarian axis causes premature ovarian failure. J. Immunol. 177, 1988–1996.
Autoimmune targeted disruption of the pituitary–ovarian axis causes premature ovarian failure.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XmvFClsLg%3D&md5=0bd21ffdba56e928cdd11351ff905553CAS | 16849513PubMed |

Amory, J. K., Hong, S., Yu, X., Muller, C. H., Faustman, E., and Goldstein, A. (2014). Melphalan, alone or conjugated to an FSH-β peptide, kills murine testicular cells in vitro and transiently suppresses murine spermatogenesis in vivo. Theriogenology 82, 152–159.
Melphalan, alone or conjugated to an FSH-β peptide, kills murine testicular cells in vitro and transiently suppresses murine spermatogenesis in vivo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXmsVCnu7s%3D&md5=fd581287f7c2a9285b8a097b68f87cd3CAS | 24746827PubMed |

Andreoni, F. (1998). ‘Evaluating Environmental Consequences of Feral Horses in Guy Fawkes River National Park.’ (Department of Ecosystem Management, University of New England: Armidale, NSW.)

Asa, C. S., and Porton, I. J. (2005). ‘Wildlife Contraception: Issues, Methods, and Applications.’ (JHU Press.)

Asa, C. S., Porton, I. J., Baker, A., and Plotka, E. (2010). Contraception as a management tool for controlling surplus animals. In ‘Wild Mammals in Captivity: Principles and Techniques for Zoo Management’. 2nd edn. (Eds D. Kleiman, K. Thompson and C. Kirk Baer.) pp. 469–482. (The University of Chicago Press: Chicago and London.)

Bakalov, V. K., Anasti, J. N., Calis, K. A., Vanderhoof, V. H., Premkumar, A., Chen, S., Furmaniak, J., Smith, B. R., Merino, M. J., and Nelson, L. M. (2005). Autoimmune oophoritis as a mechanism of follicular dysfunction in women with 46,XX spontaneous premature ovarian failure. Fertil. Steril. 84, 958–965.
Autoimmune oophoritis as a mechanism of follicular dysfunction in women with 46,XX spontaneous premature ovarian failure.Crossref | GoogleScholarGoogle Scholar | 16213850PubMed |

Ballou, J. D., Traylor-Holzer, K., Turner, A., Malo, A. F., Powell, D., Maldonado, J., and Eggert, L. (2008). Simulation model for contraceptive management of the Assateague Island feral horse population using individual-based data. Wildl. Res. 35, 502–512.
Simulation model for contraceptive management of the Assateague Island feral horse population using individual-based data.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1KrtLjO&md5=d97399f8aa77c4c375dba635433f4458CAS |

Barber, M. R., and Fayrer-Hosken, R. A. (2000). Possible mechanisms of mammalian immunocontraception. J. Reprod. Immunol. 46, 103–124.
Possible mechanisms of mammalian immunocontraception.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXhsFGltrc%3D&md5=ec381dab4b4c2e07c48906615c058237CAS | 10706942PubMed |

Bazer, F. W., Ott, T. L., and Spencer, T. E. (1994). Pregnancy recognition in ruminants, pigs and horses: signals from the trophoblast. Theriogenology 41, 79–94.
Pregnancy recognition in ruminants, pigs and horses: signals from the trophoblast.Crossref | GoogleScholarGoogle Scholar |

Bechert, U., Bartell, J., Kutzler, M., Menino, A., Bildfell, R., Anderson, M., and Fraker, M. (2013). Effects of two porcine zona pellucida immunocontraceptive vaccines on ovarian activity in horses. J. Wildl. Manage. 77, 1386–1400.
Effects of two porcine zona pellucida immunocontraceptive vaccines on ovarian activity in horses.Crossref | GoogleScholarGoogle Scholar |

Beever, E. A., and Brussard, P. F. (2004). Community- and landscape-level responses of reptiles and small mammals to feral-horse grazing in the Great Basin. J. Arid Environ. 59, 271–297.
Community- and landscape-level responses of reptiles and small mammals to feral-horse grazing in the Great Basin.Crossref | GoogleScholarGoogle Scholar |

Beever, E., and Herrick, J. (2006). Effects of feral horses in Great Basin landscapes on soils and ants: direct and indirect mechanisms. J. Arid Environ. 66, 96–112.
Effects of feral horses in Great Basin landscapes on soils and ants: direct and indirect mechanisms.Crossref | GoogleScholarGoogle Scholar |

Berman, D. (1991) ‘The Ecology of Feral Horses in Central Australia.’ (University of New England: Armidale, NSW.)

Berman, D. M., and Jarman, P. (1987). Feral horses in the Northern Territory, Vol. 1. Ecology of feral horses in Central Australia and their interaction with cattle. University of New England, Report to Conservation Commission of the Northern Territory, Alice Springs.

Bohring, C., and Krause, W. (2003). Immune infertility: towards a better understanding of sperm (auto)‐immunity The value of proteomic analysis. Hum. Reprod. 18, 915–924.
Immune infertility: towards a better understanding of sperm (auto)‐immunity The value of proteomic analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXkslOqu7Y%3D&md5=85548fbcc045ee0607da7c8e111ba3a8CAS | 12721162PubMed |

Bomford, M., and O’Brien, P. (1997). Potential use of contraception for managing wildlife pests in Australia. In ‘Contraception in Wildlife Management’. (Ed. J. S. Wintermute) pp. 205–214. (US Department of Agriculture)

Botha, A. E., Schulman, M. L., Bertschinger, H. J., Guthrie, A. J., Annandale, C. H., and Hughes, S. B. (2008). The use of a GnRH vaccine to suppress mare ovarian activity in a large group of mares under field conditions. Wildl. Res. 35, 548–554.
The use of a GnRH vaccine to suppress mare ovarian activity in a large group of mares under field conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1KrtLjE&md5=bbdce95698c3b2bc4baaf7645ff5a252CAS |

Bradshaw, C. J., Field, I. C., Bowman, D. M., Haynes, C., and Brook, B. W. (2007). Current and future threats from non-indigenous animal species in northern Australia: a spotlight on World Heritage Area Kakadu National Park. Wildl. Res. 34, 419–436.
Current and future threats from non-indigenous animal species in northern Australia: a spotlight on World Heritage Area Kakadu National Park.Crossref | GoogleScholarGoogle Scholar |

Campbell, G. L., Marfin, A. A., Lanciotti, R. S., and Gubler, D. J. (2002). West Nile virus. Lancet Infect. Dis. 2, 519–529.
West Nile virus.Crossref | GoogleScholarGoogle Scholar | 12206968PubMed |

Chapple, R. (2005). The politics of feral horse management in Guy Fawkes River National Park, NSW. Aust. Zool. 33, 233–246.
The politics of feral horse management in Guy Fawkes River National Park, NSW.Crossref | GoogleScholarGoogle Scholar |

Cheng, A. C., and Currie, B. J. (2005). Melioidosis: epidemiology, pathophysiology, and management. Clin. Microbiol. Rev. 18, 383–416.
Melioidosis: epidemiology, pathophysiology, and management.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXksVymtbk%3D&md5=f57c19cc1556dfe91435998783bc23d9CAS | 15831829PubMed |

Clement, R. F., Doyle, K. A., and Murray, J. G. (1990). The significance of a major outbreak of quarantinable disease to the Australian horse industries. Aust. Vet. J. 67, 77–78.
The significance of a major outbreak of quarantinable disease to the Australian horse industries.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3c3mt1GitQ%3D%3D&md5=93ea1c590674a7936d19f32e5f258f46CAS | 2344342PubMed |

Csurhes, S., Paroz, G., and Markula, A. (2009). ‘Pest Animal Risk Assessment: Feral Horse.’ (Queensland Government.)

Dawson, M., Lane, C., and Saunders, G. (2006). XXX. In ‘Proceedings of the National Feral Horse Management Workshop’, August 2006, Canberra, ACT. (Eds M. Dawson, C. Lane and G. Saunders) pp. 1–82. (Invasive Animals Cooperative Research Centre.)

De Iuliis, G. N., Wingate, J. K., Koppers, A. J., McLaughlin, E. A., and Aitken, R. J. (2006). Definitive evidence for the nonmitochondrial production of superoxide anion by human spermatozoa. J. Clin. Endocrinol. Metab. 91, 1968–1975.
Definitive evidence for the nonmitochondrial production of superoxide anion by human spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XkslCnu7Y%3D&md5=7ec82d5f52b071ec3e92ff574514ec7dCAS | 16507629PubMed |

Decourt, C., Tillet, Y., Caraty, A., Franceschini, I., and Briant, C. (2008). Kisspeptin immunoreactive neurons in the equine hypothalamus: interactions with GnRH neuronal system. J. Chem. Neuroanat. 36, 131–137.
Kisspeptin immunoreactive neurons in the equine hypothalamus: interactions with GnRH neuronal system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVWmtrbO&md5=0fa915f0f747092934ad12ea1cfa4bafCAS | 18761083PubMed |

Dell’Omo, G., and Palmery, M. (2002). Fertility control in vertebrate pest species. Contraception 65, 273–275.
Fertility control in vertebrate pest species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XjvVSnsbo%3D&md5=86e4941329486924181bb62c2ab05ca9CAS | 12020776PubMed |

Dixit, V. P., Lohiya, N. K., Arya, M., and Agrawal, M. (1975). Reversible changes in the testes and epididymides of dog treated with alpha-chlorohydrin. Acta Biol. Med. Ger. 34, 1851–1856.
| 1:CAS:528:DyaE28Xhs1SjsLw%3D&md5=0a7a93c62b32107f429ec470e524c3feCAS | 1241929PubMed |

Dobbie, W. R., Berman, D. M., and Braysher, M. L. (1993). ‘Managing Vertebrate Pests: Feral Horses.’ (Australian Government Publishing Services: Canberra, ACT.)

Donovan, C. E., Hazzard, T., Schmidt, A., LeMieux, J., Hathaway, F., and Kutzler, M. A. (2013). Effects of a commercial canine gonadotropin releasing hormone vaccine on estrus suppression and estrous behavior in mares. Anim. Reprod. Sci. 142, 42–47.
Effects of a commercial canine gonadotropin releasing hormone vaccine on estrus suppression and estrous behavior in mares.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsFeqtbjF&md5=bd3ef037ce7f612ce2636799bd59ec5dCAS | 24083943PubMed |

Dyer, C. A., Raymond-Whish, S., Schmuki, S., Fisher, T., Pyzyna, B., Bennett, A., and Mayer, L. P. (2013). Accelerated follicle depletion in vitro and in vivo in Sprague-Dawley rats using the combination of 4-vinylcyclohexene diepoxide and triptolide. J. Zoo Wildl. Med. 44, S9–S17.
Accelerated follicle depletion in vitro and in vivo in Sprague-Dawley rats using the combination of 4-vinylcyclohexene diepoxide and triptolide.Crossref | GoogleScholarGoogle Scholar | 24437079PubMed |

Dyring, J. (1990). The impact of feral horses (Equus caballus) on sub-alpine and montane environments in Australia. PhD Thesis, University of Canberra.

Ealy, A. D., Eroh, M. L., and Sharp, D. C. (2010). Prostaglandin H synthase Type 2 is differentially expressed in endometrium based on pregnancy status in pony mares and responds to oxytocin and conceptus secretions in explant culture. Anim. Reprod. Sci. 117, 99–105.
Prostaglandin H synthase Type 2 is differentially expressed in endometrium based on pregnancy status in pony mares and responds to oxytocin and conceptus secretions in explant culture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtlyjt7nI&md5=151ef991c8ec735187089c68b6ab55feCAS | 19443143PubMed |

Eberhardt, L., Majorowicz, A., and Wilcox, J. (1982). Apparent rates of increase for two feral horse herds. J. Wildl. Manage. 46, 367–374.
Apparent rates of increase for two feral horse herds.Crossref | GoogleScholarGoogle Scholar |

Eidne, K. A., Henery, C. C., and Aitken, R. J. (2000). Selection of peptides targeting the human sperm surface using random peptide phage display identify ligands homologous to ZP3. Biol. Reprod. 63, 1396–1402.
Selection of peptides targeting the human sperm surface using random peptide phage display identify ligands homologous to ZP3.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXnslCksL4%3D&md5=adc927d452aaa823a318fd70e042e42dCAS | 11058544PubMed |

Elhay, M., Newbold, A., Britton, A., Turley, P., Dowsett, K., and Walker, J. (2007). Suppression of behavioural and physiological oestrus in the mare by vaccination against GnRH. Aust. Vet. J. 85, 39–45.
Suppression of behavioural and physiological oestrus in the mare by vaccination against GnRH.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXivF2hurs%3D&md5=8c13b12299105a8b1c4545d4544c66f1CAS | 17300452PubMed |

English, A. (2000). Report on the cull of feral horses in Guy Fawkes River National Park in October 2000. University of Sydney, Sydney.

English, A. W. (2006). A report on the management of feral horses in National Parks in New South Wales. NSW National Parks & Wildlife Service, Sydney.

Fagerstone, K. (2002). Wildlife fertility control. USDA National Wildlife Research Center, Staff Publications, Paper 489. Available at http://digitalcommons.unl.edu/icwdm_usdanwrc/489/ [verified 19 September 2016].

Fagerstone, K. A., Miller, L. A., Killian, G., and Yoder, C. A. (2010). Review of issues concerning the use of reproductive inhibitors, with particular emphasis on resolving human‐wildlife conflicts in North America. Integr. Zool. 5, 15–30.
Review of issues concerning the use of reproductive inhibitors, with particular emphasis on resolving human‐wildlife conflicts in North America.Crossref | GoogleScholarGoogle Scholar | 21392318PubMed |

Feh, C. (2012). Delayed reversibility of PZP (porcine zona pellucida) in free-ranging Przewalski’s horse mares. In ‘International Wild Equid Conference. Vienna, Austria: University of Veterinary Medicine’, 18–22 September 2012. p. 69. Available at https://www.vetmeduni.ac.at/fileadmin/v/fiwi/Konferenzen/Wild_Equid_Conference/IWEC_book_of_abstracts_final.pdf [verified 21 September 2016]

Finch, A. R., Caunt, C. J., Armstrong, S. P., and McArdle, C. A. (2009). Agonist-induced internalization and downregulation of gonadotropin-releasing hormone receptors. Am. J. Physiol. Cell Physiol. 297, C591–C600.
Agonist-induced internalization and downregulation of gonadotropin-releasing hormone receptors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXht1yktbjM&md5=09b5ee23347253fc15084d5cbd921373CAS | 19587220PubMed |

Fitzgerald, B. P., Peterson, K. D., and Silvia, P. J. (1993). Effect of constant administration of a gonadotropin-releasing hormone agonist on reproductive activity in mares: preliminary evidence on suppression of ovulation during the breeding season. Am. J. Vet. Res. 54, 1746–1751.
| 1:CAS:528:DyaK3sXms1alu70%3D&md5=3406ecdcf9a9dd5767b7d8c7dd34bb0bCAS | 8250402PubMed |

Forges, T., Monnier‐Barbarino, P., Faure, G., and Bene, M. (2004). Autoimmunity and antigenic targets in ovarian pathology. Hum. Reprod. Update 10, 163–175.
Autoimmunity and antigenic targets in ovarian pathology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjt1aqtrc%3D&md5=32e94792d4975f67f32b703771ca67b8CAS | 15073145PubMed |

Frank, H.-G., Bose, P., Albieri-Borges, A., Borges, M., Greindl, A., Neulen, J., Pötgens, A. J., and Kaufmann, P. (2005). Evaluation of fusogenic trophoblast surface epitopes as targets for immune contraception. Contraception 71, 282–293.
Evaluation of fusogenic trophoblast surface epitopes as targets for immune contraception.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXisFGqtLo%3D&md5=b1199f7fab65981f31f48c2ce1ed6c41CAS | 15792647PubMed |

Garrott, R. A. (1995). Effective management of free-ranging ungulate populations using contraception. Wildl. Soc. Bull. 23, 445–452.

Garrott, R. A., and Oli, M. K. (2013). A critical crossroad for BLM’s wild horse program. Science 341, 847–848.
A critical crossroad for BLM’s wild horse program.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsVOisr3M&md5=662c502ee9e64095853426fd418f4dd5CAS | 23970685PubMed |

Garza, K. M., and Tung, K. (1995). Frequency of molecular mimicry among T cell peptides as the basis for autoimmune disease and autoantibody induction. J. Immunol. 155, 5444–5448.
| 1:CAS:528:DyaK2MXpsF2itrc%3D&md5=93fa4d083793e02c1a2bfe3026415861CAS | 7594562PubMed |

Gibb, Z., Lambourne, S. R., and Aitken, R. J. (2014). The paradoxical relationship between stallion fertility and oxidative stress. Biol. Reprod. 91, 77.
The paradoxical relationship between stallion fertility and oxidative stress.Crossref | GoogleScholarGoogle Scholar | 25078685PubMed |

Gray, M. E., and Cameron, E. Z. (2010). Does contraceptive treatment in wildlife result in side effects? A review of quantitative and anecdotal evidence. Reproduction 139, 45–55.
Does contraceptive treatment in wildlife result in side effects? A review of quantitative and anecdotal evidence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXovVWntQ%3D%3D&md5=99df274b52916317293d5e4515c8702bCAS | 19656957PubMed |

Gray, M. E., Thain, D. S., Cameron, E. Z., and Miller, L. A. (2010). Multi-year fertility reduction in free-roaming feral horses with single-injection immunocontraceptive formulations. Wildl. Res. 37, 475–481.
Multi-year fertility reduction in free-roaming feral horses with single-injection immunocontraceptive formulations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsVCht7%2FI&md5=72e6b21b45da639652fa95a06cfe068eCAS |

Gupta, S. K., and Bansal, P. (2010). Vaccines for immunological control of fertility. Reprod. Med. Biol. 9, 61–71.
Vaccines for immunological control of fertility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXptFyru7k%3D&md5=4e464c70a0f0024b86b0c95f6e25bbf9CAS |

Gutierrez, P. L. (2000). The metabolism of quinone-containing alkylating agents: free radical production and measurement. Front. Biosci. 5, D629–D638.
| 1:CAS:528:DC%2BD3cXltlOksrw%3D&md5=5e6fd8cc4b2358827a2925e2b10df3d5CAS | 10877994PubMed |

Hampson, B. A., Zabek, M. A., Pollitt, C. C., and Nock, B. (2011). Health and behaviour consequences of feral horse relocation. Rangeland J. 33, 173–180.
Health and behaviour consequences of feral horse relocation.Crossref | GoogleScholarGoogle Scholar |

Hanoux, V., Pairault, C., Bakalska, M., Habert, R., and Livera, G. (2007). Caspase-2 involvement during ionizing radiation-induced oocyte death in the mouse ovary. Cell Death Differ. 14, 671–681.
Caspase-2 involvement during ionizing radiation-induced oocyte death in the mouse ovary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjt1Sku7w%3D&md5=b155c81ffa674601618b35b3af48691bCAS | 17082817PubMed |

Hardy, C. M., Hinds, L. A., Kerr, P. J., Lloyd, M. L., Redwood, A. J., Shellam, G. R., and Strive, T. (2006). Biological control of vertebrate pests using virally vectored immunocontraception. J. Reprod. Immunol. 71, 102–111.
Biological control of vertebrate pests using virally vectored immunocontraception.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD28ris1aluw%3D%3D&md5=5ecae936065cca815d0e54bd68ecc8b5CAS | 16870262PubMed |

Herbert, C. A., and Trigg, T. E. (2005). Applications of GnRH in the control and management of fertility in female animals. Anim. Reprod. Sci. 88, 141–153.
Applications of GnRH in the control and management of fertility in female animals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXpslygtro%3D&md5=60e4190a2fdcf0ad5d74453a4397e0b1CAS | 16102921PubMed |

Hinds, L. (2006). Fertility control of large herbivores: a brief overview of the options. In ‘Proceedings of the National Feral Horse Management Workshop,’ August 2006, Canberra. (Eds M. J. Dawson, C. Lane and G. Saunders.) pp. 60–64. (Invasive Animals Cooperative Research Centre: Canberra)

Hobbs, N. T., Bowden, D. C., and Baker, D. L. (2000). Effects of fertility control on populations of ungulates: general, stage-structured models. J. Wildl. Manage. 64, 473–491.
Effects of fertility control on populations of ungulates: general, stage-structured models.Crossref | GoogleScholarGoogle Scholar |

Hone, J. (1999). On rate of increase(r): patterns of variation in Australian mammals and the implications for wildlife management. J. Appl. Ecol. 36, 709–718.
On rate of increase(r): patterns of variation in Australian mammals and the implications for wildlife management.Crossref | GoogleScholarGoogle Scholar |

Hoyer, P. B., Devine, P. J., Hu, X., Thompson, K. E., and Sipes, I. G. (2001). Ovarian toxicity of 4-vinylcyclohexene diepoxide: a mechanistic model. Toxicol. Pathol. 29, 91–99.
Ovarian toxicity of 4-vinylcyclohexene diepoxide: a mechanistic model.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhtl2mtbw%3D&md5=3e760cc7a975c00a1db95c41658fafd7CAS | 11215690PubMed |

Humphrys, S., and Lapidge, S. J. (2008). Delivering and registering species-tailored oral antifertility products: a review. Wildl. Res. 35, 578–585.
Delivering and registering species-tailored oral antifertility products: a review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1KrtLjN&md5=db1c67d8991b854ba69235450537cdacCAS |

Hunt, R. J., Claridge, A. W., Fleming, P. J., Cunningham, R. B., Russell, B. G., and Mills, D. J. (2014). Use of an ungulate‐specific feed structure as a potential tool for controlling feral goats in Australian forest ecosystems. Ecol. Manage. Restor. 15, 231–238.
Use of an ungulate‐specific feed structure as a potential tool for controlling feral goats in Australian forest ecosystems.Crossref | GoogleScholarGoogle Scholar |

Imboden, I., Janett, F., Burger, D., Crowe, M., Hässig, M., and Thun, R. (2006). Influence of immunization against GnRH on reproductive cyclicity and estrous behavior in the mare. Theriogenology 66, 1866–1875.
Influence of immunization against GnRH on reproductive cyclicity and estrous behavior in the mare.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVGjtLzP&md5=1643afd4ece63827781984329806b9e1CAS | 16780942PubMed |

Jakubowski, H. (2010) The role of paraoxonase 1 in the detoxification of homocysteine thiolactone. In ‘Paraoxonases in Inflammation, Infection, and Toxicology’. (Ed. S. T. Reddy.) pp. 113–127. (Springer: Los Angeles.)

Janett, F., Stump, R., Burger, D., and Thun, R. (2009). Suppression of testicular function and sexual behavior by vaccination against GnRH (Equity™) in the adult stallion. Anim. Reprod. Sci. 115, 88–102.
Suppression of testicular function and sexual behavior by vaccination against GnRH (Equity™) in the adult stallion.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXptl2hsrk%3D&md5=5271bbf28fc92371c50786a6e4a4de08CAS | 19128902PubMed |

Keating, A. F. J., Mark, C., Sen, N., Sipes, I. G., and Hoyer, P. B. (2009). Effect of phosphatidylinositol-3 kinase inhibition on ovotoxicity caused by 4-vinylcyclohexene diepoxide and 7,12-dimethylbenz[a]anthracene in neonatal rat ovaries. Toxicol. Appl. Pharmacol. 241, 127–134.
Effect of phosphatidylinositol-3 kinase inhibition on ovotoxicity caused by 4-vinylcyclohexene diepoxide and 7,12-dimethylbenz[a]anthracene in neonatal rat ovaries.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtlCrsLvK&md5=b618298c8006e7fcdd6a06c6cf5f2cf2CAS |

Killian, G., Miller, L., Diehl, N., Rhyan, J., and Thain, D. (2006). Long-term efficacy of three contraceptive approaches for population control of wild horses. In ‘Proceedings of the 22nd Vertebrate Pest Conference’, University of California, Davis. (Eds. R. M. Timm and J. M. O’Brien.) pp. 67–71.

Killian, G., Thain, D., Diehl, N. K., Rhyan, J., and Miller, L. (2008). Four-year contraception rates of mares treated with single-injection porcine zona pellucida and GnRH vaccines and intrauterine devices. Wildl. Res. 35, 531–539.
Four-year contraception rates of mares treated with single-injection porcine zona pellucida and GnRH vaccines and intrauterine devices.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1KrtLjJ&md5=f2b89fe308801b46a276490b0a63fa96CAS |

Kim, S.-J., Jung, H.-J., and Lim, C.-J. (2013). Reactive oxygen species-dependent down-regulation of tumor suppressor genes PTEN, USP28, DRAM, TIGAR, and CYLD under oxidative stress. Biochem. Genet. 51, 901–915.
Reactive oxygen species-dependent down-regulation of tumor suppressor genes PTEN, USP28, DRAM, TIGAR, and CYLD under oxidative stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtVGqt7%2FI&md5=51eb88cf9097678b572818c9d7ff29f3CAS | 23832602PubMed |

Kirkpatrick, J. F. (2007). Viewpoint: measuring the effects of wildlife contraception: the argument for comparing apples with oranges. Reprod. Fertil. Dev. 19, 548–552.
Viewpoint: measuring the effects of wildlife contraception: the argument for comparing apples with oranges.Crossref | GoogleScholarGoogle Scholar | 17524299PubMed |

Kirkpatrick, J. F., and Turner, A. (2002). Reversibility of action and safety during pregnancy of immunization against porcine zona pellucida in wild mares (Equus caballus). Reprod. Suppl. 60, 197–202.
| 1:CAS:528:DC%2BD38XnsFGksLs%3D&md5=d5245223beb224620d527d214095b594CAS | 12220160PubMed |

Kirkpatrick, J. F., and Turner, A. (2007). Immunocontraception and increased longevity in equids. Zoo Biol. 26, 237–244.
Immunocontraception and increased longevity in equids.Crossref | GoogleScholarGoogle Scholar | 19360577PubMed |

Kirkpatrick, J. F., and Turner, A. (2008). Achieving population goals in a long-lived wildlife species (Equus caballus) with contraception. Wildl. Res. 35, 513–519.
Achieving population goals in a long-lived wildlife species (Equus caballus) with contraception.Crossref | GoogleScholarGoogle Scholar |

Kirkpatrick, J. F., Liu, I. K., and Turner, J. W. (1990). Remotely-delivered immunocontraception in feral horses. Wildl. Soc. Bull. 18, 326–330.

Kirkpatrick, J. F., Turner, J. W., Liu, I. K., and Fayrer-Hosken, R. (1996). Applications of pig zona pellucida immunocontraception to wildlife fertility control. J. Reprod. Fertil. Suppl. 50, 183–189.
| 1:STN:280:DyaK2s7gsFGhsQ%3D%3D&md5=6658465d5c0f1a5262f09c5e9a39195dCAS | 8984182PubMed |

Kirkpatrick, J. F., Lyda, R. O., and Frank, K. M. (2011). Contraceptive vaccines for wildlife: a review. Am. J. Reprod. Immunol. 66, 40–50.
Contraceptive vaccines for wildlife: a review.Crossref | GoogleScholarGoogle Scholar | 21501279PubMed |

Kirkpatrick, J. F., Rutberg, A. T., Coates-Markle, L., and Fazio, P. M. (2012). ‘Immunocontraceptive Reproductive Control Utilizing Porcine Zona Pellucida (PZP) in Federal Wild Horse Populations.’ (Science and Conservation Center: Billings, MT.)

Klein, C., Scoggin, K. E., Ealy, A. D., and Troedsson, M. H. (2010). Transcriptional profiling of equine endometrium during the time of maternal recognition of pregnancy. Biol. Reprod. 83, 102–113.
Transcriptional profiling of equine endometrium during the time of maternal recognition of pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXotlWqtLc%3D&md5=1b419d6818297531edee2c1dd396b791CAS | 20335638PubMed |

Kutzler, M., and Wood, A. (2006). Non-surgical methods of contraception and sterilization. Theriogenology 66, 514–525.
Non-surgical methods of contraception and sterilization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XntVyrt74%3D&md5=04dade9923737367415e8c99dee384b6CAS | 16757019PubMed |

Lapidge, S. J., Eason, C. T., and Humphrys, S. T. (2010). A review of chemical, biological and fertility control options for the camel in Australia. Rangeland J. 32, 95–115.
A review of chemical, biological and fertility control options for the camel in Australia.Crossref | GoogleScholarGoogle Scholar |

Levin, P. S., Ellis, J., Petrik, R., and Hay, M. E. (2002). Indirect effects of feral horses on estuarine communities. Conserv. Biol. 16, 1364–1371.
Indirect effects of feral horses on estuarine communities.Crossref | GoogleScholarGoogle Scholar |

Liu, I. K. M., Bernoco, M., and Feldman, M. (1989). Contraception in mares heteroimmunized with pig zonae pellucidae. J. Reprod. Fertil. 85, 19–29.
Contraception in mares heteroimmunized with pig zonae pellucidae.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1M7isFCqtg%3D%3D&md5=817a976e22db800f25660fecab55a114CAS |

Long, J. L. (2003). ‘Introduced Mammals of the World: Their History, Distribution and Influence.’ (CSIRO Publishing.)

Madosky, J. M., Rubenstein, D. I., Howard, J. J., and Stuska, S. (2010). The effects of immunocontraception on harem fidelity in a feral horse (Equus caballus) population. Appl. Anim. Behav. Sci. 128, 50–56.
The effects of immunocontraception on harem fidelity in a feral horse (Equus caballus) population.Crossref | GoogleScholarGoogle Scholar |

Mask, T. A., Schoenecker, K. A., Kane, A. J., Ransom, J. I., and Bruemmer, J. E. (2015). Serum antibody immunoreactivity to equine zona protein after SpayVac vaccination. Theriogenology 84, 261–267.
Serum antibody immunoreactivity to equine zona protein after SpayVac vaccination.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXmtFSjtbw%3D&md5=0b11eddd78b8916b23acd0349ebddb45CAS | 25922172PubMed |

Massei, G., and Cowan, D. (2014). Fertility control to mitigate human–wildlife conflicts: a review. Wildl. Res. 41, 1–21.
Fertility control to mitigate human–wildlife conflicts: a review.Crossref | GoogleScholarGoogle Scholar |

Mayer, L. P., Pearsall, N. A., Christian, P. J., Devine, P. J., Payne, C. M., McCuskey, M. K., Marion, S. L., Sipes, I. G., and Hoyer, P. B. (2002). Long-term effects of ovarian follicular depletion in rats by 4-vinylcyclohexene diepoxide. Reprod. Toxicol. 16, 775–781.
Long-term effects of ovarian follicular depletion in rats by 4-vinylcyclohexene diepoxide.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XotVChsLY%3D&md5=5f676b9a4a26f7d9cfd9debbfaf71e43CAS | 12401505PubMed |

McLaughlin, E. A., and Aitken, R. J. (2011). Is there a role for immunocontraception? Mol. Cell. Endocrinol. 335, 78–88.
Is there a role for immunocontraception?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXit1Ggsrs%3D&md5=e75ec380f0d86db7a9795ba5bb2aed3cCAS | 20412833PubMed |

McLaughlin, E. A., and McIver, S. C. (2009). Awakening the oocyte: controlling primordial follicle development. Reproduction 137, 1–11.
Awakening the oocyte: controlling primordial follicle development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXovVKgsL4%3D&md5=7af5e1f556872d2760f76cca1467643bCAS | 18827065PubMed |

McLaughlin, E. A., Holland, M. K., and Aitken, R. J. (2003). Contraceptive vaccines. Expert Opin. Biol. Ther. 3, 829–841.
Contraceptive vaccines.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXls1ynt78%3D&md5=973096101bbf400ea4639f7de8e604f3CAS | 12880382PubMed |

Meirow, D., and Nugent, D. (2001). The effects of radiotherapy and chemotherapy on female reproduction. Hum. Reprod. Update 7, 535–543.
The effects of radiotherapy and chemotherapy on female reproduction.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MnotFKisQ%3D%3D&md5=bb64f96ddc14dccdcfcf88fe417e3800CAS | 11727861PubMed |

Meloen, R. H., Puijk, W. C., and Slootstra, J. W. (2000). Mimotopes: realization of an unlikely concept. J. Mol. Recognit. 13, 352–359.
Mimotopes: realization of an unlikely concept.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXosFOisbo%3D&md5=5c7dfe0dee7e3faa7527574d8d6db46bCAS | 11114068PubMed |

Miller, L. A., Gionfriddo, J. P., Fagerstone, K. A., Rhyan, J. C., and Killian, G. J. (2008). The single‐shot GnRH immunocontraceptive vaccine (GonaCon™) in white‐tailed deer: comparison of several GnRH preparations. Am. J. Reprod. Immunol. 60, 214–223.
The single‐shot GnRH immunocontraceptive vaccine (GonaCon™) in white‐tailed deer: comparison of several GnRH preparations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFKrsbzP&md5=3901ceb9e6a7c521ae1c0054a8d49aa7CAS | 18782282PubMed |

Moazamian, R., Polhemus, A., Connaughton, H., Fraser, B., Whiting, S., Gharagozloo, P., and Aitken, R. J. (2015). Oxidative stress and human spermatozoa: diagnostic and functional significance of aldehydes generated as a result of lipid peroxidation. Mol. Hum. Reprod. 21, 502–515.
Oxidative stress and human spermatozoa: diagnostic and functional significance of aldehydes generated as a result of lipid peroxidation.Crossref | GoogleScholarGoogle Scholar | 25837702PubMed |

Mugnier, S., Dell’Aquila, M. E., Pelaez, J., Douet, C., Ambruosi, B., De Santis, T., Lacalandra, G. M., Lebos, C., Sizaret, P.-Y., and Delaleu, B. (2009). New insights into the mechanisms of fertilization: comparison of the fertilization steps, composition, and structure of the zona pellucida between horses and pigs. Biol. Reprod. 81, 856–870.
New insights into the mechanisms of fertilization: comparison of the fertilization steps, composition, and structure of the zona pellucida between horses and pigs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtlWrtr%2FK&md5=35fb701f39c6e2f59ea4ba12b4ce7b36CAS | 19587333PubMed |

Muller, L. I., Warren, R. J., and Evans, D. L. (1997). Theory and practice of immunocontraception in wild mammals. Wildl. Soc. Bull. 25, 504–514.

National Research Council (2013). ‘Using Science to Improve the BLM Wild Horse and Burro Program: A Way Forward.’ (National Academies Press: Washington, DC.)

Naz, R. K., and Saver, A. E. (2016). Immunocontraception for animals: current status and future perspective. Am. J. Reprod. Immunol. 75, 426–439.
Immunocontraception for animals: current status and future perspective.Crossref | GoogleScholarGoogle Scholar | 26412331PubMed |

Nimmo, D. G., and Miller, K. K. (2007). Ecological and human dimensions of management of feral horses in Australia: a review. Wildl. Res. 34, 408–417.
Ecological and human dimensions of management of feral horses in Australia: a review.Crossref | GoogleScholarGoogle Scholar |

Nimmo, D. G., Miller, K. K., and Adams, R. (2007). Managing feral horses in Victoria: a study of community attitudes and perceptions. Ecol. Manage. Restor. 8, 237–243.
Managing feral horses in Victoria: a study of community attitudes and perceptions.Crossref | GoogleScholarGoogle Scholar |

Nixon, B., Aitken, R., and McLaughlin, E. (2007). New insights into the molecular mechanisms of sperm–egg interaction. Cell. Mol. Life Sci. 64, 1805–1823.
New insights into the molecular mechanisms of sperm–egg interaction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXovFagtLo%3D&md5=7abdc8afe78db4dfff330dac3e82476bCAS | 17447007PubMed |

Nuñez, C. M., Adelman, J. S., Mason, C., and Rubenstein, D. I. (2009). Immunocontraception decreases group fidelity in a feral horse population during the non-breeding season. Appl. Anim. Behav. Sci. 117, 74–83.
Immunocontraception decreases group fidelity in a feral horse population during the non-breeding season.Crossref | GoogleScholarGoogle Scholar |

Nuñez, C. M., Adelman, J. S., and Rubenstein, D. I. (2010). Immunocontraception in wild horses (Equus caballus) extends reproductive cycling beyond the normal breeding season. PLoS One 5, e13635.
Immunocontraception in wild horses (Equus caballus) extends reproductive cycling beyond the normal breeding season.Crossref | GoogleScholarGoogle Scholar | 21049017PubMed |

Paterson, M., Wilson, M. R., Morris, K. D., Duin, M., and Aitken, R. (1998). Evaluation of the contraceptive potential of recombinant human ZP3 and human ZP3 peptides in a primate model: their safety and efficacy. Am. J. Reprod. Immunol. 40, 198–209.
Evaluation of the contraceptive potential of recombinant human ZP3 and human ZP3 peptides in a primate model: their safety and efficacy.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1cvjs1ymtA%3D%3D&md5=24284b16d89edbc35821898b97b2299eCAS | 9764365PubMed |

Powell, D. M., and Monfort, S. L. (2001). Assessment: effects of porcine zona pellucida immunocontraception on estrous cyclicity in feral horses. J. Appl. Anim. Welf. Sci. 4, 271–284.
Assessment: effects of porcine zona pellucida immunocontraception on estrous cyclicity in feral horses.Crossref | GoogleScholarGoogle Scholar |

Powers, J. G., Baker, D. L., Davis, T. L., Conner, M. M., Lothridge, A. H., and Nett, T. M. (2011). Effects of gonadotropin-releasing hormone immunization on reproductive function and behavior in captive female Rocky Mountain elk (Cervus elaphus nelsoni). Biol. Reprod. 85, 1152–1160.
Effects of gonadotropin-releasing hormone immunization on reproductive function and behavior in captive female Rocky Mountain elk (Cervus elaphus nelsoni).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhs1ShsLbP&md5=af04e07a1ca50c0db9bba53cbb47792eCAS | 21753192PubMed |

Powers, J. G., Monello, R. J., Wild, M. A., Spraker, T. R., Gionfriddo, J. P., Nett, T. M., and Baker, D. L. (2014). Effects of GonaCon immunocontraceptive vaccine in free‐ranging female Rocky Mountain elk (Cervus elaphus nelsoni). Wildl. Soc. Bull. 38, 650–656.
Effects of GonaCon immunocontraceptive vaccine in free‐ranging female Rocky Mountain elk (Cervus elaphus nelsoni).Crossref | GoogleScholarGoogle Scholar |

Prasad, S. V., Skinner, S. M., Carino, C., Wang, N., Cartwright, J., and Dunbar, B. S. (2000). Structure and function of the proteins of the mammalian zona pellucida. Cells Tissues Organs 166, 148–164.
Structure and function of the proteins of the mammalian zona pellucida.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjtVyrurc%3D&md5=64f3c0a4d522f2c28f36ba598c896750CAS | 10729725PubMed |

Pujianto, D. A., Curry, B. J., and Aitken, R. J. (2010). Prolactin exerts a prosurvival effect on human spermatozoa via mechanisms that involve the stimulation of Akt phosphorylation and suppression of caspase activation and capacitation. Endocrinology 151, 1269–1279.
Prolactin exerts a prosurvival effect on human spermatozoa via mechanisms that involve the stimulation of Akt phosphorylation and suppression of caspase activation and capacitation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXjvVKqt7g%3D&md5=db6fff8a0e913d29c7793b23f1219528CAS | 20032052PubMed |

Ransom, J. I., Cade, B. S., and Hobbs, N. T. (2010). Influences of immunocontraception on time budgets, social behavior, and body condition in feral horses. Appl. Anim. Behav. Sci. 124, 51–60.
Influences of immunocontraception on time budgets, social behavior, and body condition in feral horses.Crossref | GoogleScholarGoogle Scholar |

Ransom, J. I., Roelle, J. E., Cade, B. S., Coates‐Markle, L., and Kane, A. J. (2011). Foaling rates in feral horses treated with the immunocontraceptive porcine zona pellucida. Wildl. Soc. Bull. 35, 343–352.
Foaling rates in feral horses treated with the immunocontraceptive porcine zona pellucida.Crossref | GoogleScholarGoogle Scholar |

Ransom, J. I., Hobbs, N. T., and Bruemmer, J. (2013). Contraception can lead to trophic asynchrony between birth pulse and resources. PLoS One 8, e54972.
Contraception can lead to trophic asynchrony between birth pulse and resources.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXisVeltb0%3D&md5=f94cf4c045923626db2349f0e09e1ecdCAS | 23383018PubMed |

Ransom, J. I., Powers, J. G., Garbe, H. M., Oehler, M. W., Nett, T. M., and Baker, D. L. (2014). Behavior of feral horses in response to culling and GnRH immunocontraception. Appl. Anim. Behav. Sci. 157, 81–92.
Behavior of feral horses in response to culling and GnRH immunocontraception.Crossref | GoogleScholarGoogle Scholar |

Reddy, P., Liu, L., Adhikari, D., Jagarlamudi, K., Rajareddy, S., Shen, Y., Du, C., Tang, W., Hämäläinen, T., and Peng, S. L. (2008). Oocyte-specific deletion of Pten causes premature activation of the primordial follicle pool. Science 319, 611–613.
Oocyte-specific deletion of Pten causes premature activation of the primordial follicle pool.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1Knt78%3D&md5=4104c46dae1a475be80e079bee69a497CAS | 18239123PubMed |

Roberts, R. M., Xie, S., and Mathialagan, N. (1996). Maternal recognition of pregnancy. Biol. Reprod. 54, 294–302.
Maternal recognition of pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XltF2qtg%3D%3D&md5=ca2fd586a53ff93fb571f23f4c0175beCAS | 8788179PubMed |

Rolls, E. C. (1969). ‘They All Ran Wild: The Story of Pests on the Land in Australia.’ (Angus and Robertson: Sydney.)

Sabeur, K., Ball, B., Nett, T., Ball, H., and Liu, I. (2003). Effect of GnRH conjugated to pokeweed antiviral protein on reproductive function in adult male dogs. Reproduction 125, 801–806.
Effect of GnRH conjugated to pokeweed antiviral protein on reproductive function in adult male dogs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXltFeltLw%3D&md5=12ae9f42d270f17cf35dd562a059c23fCAS | 12773102PubMed |

Samoylov, A., Cox, N., Cochran, A., Wolfe, K., Donovan, C., Kutzler, M., Petrenko, V., Baker, H., and Samoylova, T. (2012). Generation and characterization of phage‐GnRH chemical conjugates for potential use in cat and dog immunocontraception. Reprod. Domest. Anim. 47, 406–411.
Generation and characterization of phage‐GnRH chemical conjugates for potential use in cat and dog immunocontraception.Crossref | GoogleScholarGoogle Scholar | 23279551PubMed |

Samoylov, A., Cochran, A., Schemera, B., Kutzler, M., Donovan, C., Petrenko, V., Bartol, F., and Samoylova, T. (2015). Humoral immune responses against gonadotropin releasing hormone elicited by immunization with phage-peptide constructs obtained via phage display. J. Biotechnol. 216, 20–28.
Humoral immune responses against gonadotropin releasing hormone elicited by immunization with phage-peptide constructs obtained via phage display.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhs1OrtLjP&md5=c13bf3850424b1f429e47abbff110812CAS | 26456116PubMed |

Samoylova, T. I., Cox, N. R., Cochran, A. M., Samoylov, A. M., Griffin, B., and Baker, H. J. (2010). ZP-binding peptides identified via phage display stimulate production of sperm antibodies in dogs. Anim. Reprod. Sci. 120, 151–157.
ZP-binding peptides identified via phage display stimulate production of sperm antibodies in dogs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmtFWrtr8%3D&md5=1c4048e812039068c70721dad68198f6CAS | 20434854PubMed |

Samoylova, T. I., Cochran, A. M., Samoylov, A. M., Schemera, B., Breiteneicher, A. H., Ditchkoff, S. S., Petrenko, V. A., and Cox, N. R. (2012). Phage display allows identification of zona pellucida-binding peptides with species-specific properties: novel approach for development of contraceptive vaccines for wildlife. J. Biotechnol. 162, 311–318.
Phage display allows identification of zona pellucida-binding peptides with species-specific properties: novel approach for development of contraceptive vaccines for wildlife.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhslejsLnE&md5=d3658d056d7278c8cc7f95a5acea23c2CAS | 23079080PubMed |

Schanbacher, B. D., and Pratt, B. R. (1985). Response of a cryptorchid stallion to vaccination against luteinising hormone releasing hormone. Vet. Rec. 116, 74–75.
Response of a cryptorchid stallion to vaccination against luteinising hormone releasing hormone.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL2M7ktlOqtQ%3D%3D&md5=2aeece308d57c58e88ddc820bc9f0aedCAS | 2858139PubMed |

Silva, C. A., Yamakami, L. Y. S., Aikawa, N. E., Araujo, D. B., Carvalho, J. F., and Bonfá, E. (2014). Autoimmune primary ovarian insufficiency. Autoimmun. Rev. 13, 427–430.
Autoimmune primary ovarian insufficiency.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtlKitbo%3D&md5=b33092e06d9eb674a169f4398163ddccCAS | 24418305PubMed |

Skinner, S. M., Mills, T., Kirchick, H. J., and Dunbar, B. S. (1984). Immunization with zona pellucida proteins results in abnormal ovarian follicular differentiation and inhibition of gonadotropin-induced steroid secretion. Endocrinology 115, 2418–2432.
Immunization with zona pellucida proteins results in abnormal ovarian follicular differentiation and inhibition of gonadotropin-induced steroid secretion.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXhsl2hsA%3D%3D&md5=c4109b950e0ee69e62e6e6b0fe17acbfCAS | 6437799PubMed |

Sobinoff, A. P., Pye, V., Nixon, B., Roman, S. D., and McLaughlin, E. A. (2010). Adding insult to injury: effects of xenobiotic-induced preantral ovotoxicity on ovarian development and oocyte fusibility. Toxicol. Sci. 118, 653–666.
Adding insult to injury: effects of xenobiotic-induced preantral ovotoxicity on ovarian development and oocyte fusibility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsVKjsbjJ&md5=e8235a5c02aba56c33a68689fb19184eCAS | 20829426PubMed |

Sobinoff, A. P., Pye, V., Nixon, B., Roman, S. D., and McLaughlin, E. A. (2012). Jumping the gun: smoking constituent BaP causes premature primordial follicle activation and impairs oocyte fusibility through oxidative stress. Toxicol. Appl. Pharmacol. 260, 70–80.
Jumping the gun: smoking constituent BaP causes premature primordial follicle activation and impairs oocyte fusibility through oxidative stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XjtF2htLs%3D&md5=2d16aa2032af10ee929ac19c15f92a35CAS | 22342234PubMed |

Spencer, T. E., and Bazer, F. W. (2004). Conceptus signals for establishment and maintenance of pregnancy. Reprod. Biol. Endocrinol. 49, 195–209.

Stout, T. A., and Allen, W. R. (2001). Role of prostaglandins in intrauterine migration of the equine conceptus. Reproduction 121, 771–775.
Role of prostaglandins in intrauterine migration of the equine conceptus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXktVait7w%3D&md5=67b91ddaef85d757cee82266a67a9a90CAS | 11427165PubMed |

Stout, T. A. E., and Colenbrander, B. (2004). Suppressing reproductive activity in horses using GnRH vaccines, antagonists or agonists. Anim. Reprod. Sci. 82–83, 633–643.
Suppressing reproductive activity in horses using GnRH vaccines, antagonists or agonists.Crossref | GoogleScholarGoogle Scholar |

Swegen, A., and Aitken, R. J. (2016). Prospects for immunocontraception in feral horse population control: exploring novel targets for an equine fertility vaccine. Reprod. Fertil. Dev. 28, 853–863.
Prospects for immunocontraception in feral horse population control: exploring novel targets for an equine fertility vaccine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XotFKkt7s%3D&md5=51829b7f0e3e08ee771f91647ca492acCAS |

Symanski, R. (1994). Contested realities: feral horses in outback Australia. Ann. Assoc. Am. Geogr. 84, 251–269.
Contested realities: feral horses in outback Australia.Crossref | GoogleScholarGoogle Scholar |

Tung, K. S., Garza, K. M., and Lou, Y.-h. (1999). Induction of pathogenic autoimmune T-cell and autoantibody responses through T-cell epitope mimicry. In ‘Autoimmune Reactions’. (Ed. S. Paul) pp. 99–112. (Humana Press: Totowa, NJ)

Tung, K., Agersborg, S., Bagavant, H., Garza, K., and Wei, K. (2002). Autoimmune ovarian disease induced by immunization with zona pellucida (ZP3) peptide. Curr. Protoc. Immunol. 15, 17.
| 18432873PubMed |

Turkstra, J. A., Van Der Meer, F. J. U. M., Knaap, J., Rottier, P. J. M., Teerds, K. J., Colenbrander, B., and Meloen, R. H. (2005). Effects of GnRH immunization in sexually mature pony stallions. Anim. Reprod. Sci. 86, 247–259.
Effects of GnRH immunization in sexually mature pony stallions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXit1Cjtbo%3D&md5=972417554dad48c0958eb37ae1584ba4CAS | 15766804PubMed |

Turner, A., and Kirkpatrick, J. (2002). Effects of immunocontraception on population, longevity and body condition in wild mares (Equus caballus). Reprod. Suppl. 60, 187–195.
| 1:CAS:528:DC%2BD38XnsFGksLo%3D&md5=f78a4e2dd30ff4ab9364c797cf96e245CAS | 12220158PubMed |

Turner, J. W., Liu, I. K. M., Flanagan, D. R., Rutberg, A. T., and Kirkpatrick, J. F. (2001). Immunocontraception in feral horses: one inoculation provides one year of infertility. J. Wildl. Manage. 65, 235–241.
Immunocontraception in feral horses: one inoculation provides one year of infertility.Crossref | GoogleScholarGoogle Scholar |

Turner, J. W., Rutberg, A. T., Naugle, R. E., Kaur, M. A., Flanagan, D. R., Bertschinger, H. J., and Liu, I. K. M. (2008). Controlled-release components of PZP contraceptive vaccine extend duration of infertility. Wildl. Res. 35, 555–562.
Controlled-release components of PZP contraceptive vaccine extend duration of infertility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1KrtLbL&md5=86cbb6175241086e093d3110bf37e74eCAS |

Wang, G., Li, H., and Firoze Khan, M. (2012). Differential oxidative modification of proteins in MRL+/+ and MRL/lpr mice: increased formation of lipid peroxidation-derived aldehyde-protein adducts may contribute to accelerated onset of autoimmune response. Free Radic. Res. 46, 1472–1481.
Differential oxidative modification of proteins in MRL+/+ and MRL/lpr mice: increased formation of lipid peroxidation-derived aldehyde-protein adducts may contribute to accelerated onset of autoimmune response.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhs1Wgt77O&md5=0b0ae0f6737a78cf8e8673689eb6d36aCAS | 22950782PubMed |

Warren, R. J., Fayrer-Hosken, R. A., Muller, L. I., Willis, L. P., and Goodloe, R. B. (1993). Research and field applications of contraceptives in white-tailed deer, feral horses, and mountain goats. In ‘Contraceptive Wildlife Management’. (Ed. J. Wintermute.) 133–145. (UD Department of Agriculture.)

Zabek, M. A., Berman, D. M., Wright, J., Blomberg, S., and Collins, W. C. (2014a). Understanding population dynamics of the feral horse in a coniferous environment in southeast Queensland. In ‘Proeedings of the 16th Australasian Vertebrate Pest Conference’, 2014, Brisbane, Queensland. (Ed. M. Gentle). p. 142.

Zabek, M. A., Wright, J., Berman, D. M., Hampton, J. O., and Collins, C. W. (2014b). Assessing the efficacy of medetomidine and tiletamine–zolazepam for remote immobilisation of feral horses (Equus caballus). Wildl. Res. 41, 615–622.
Assessing the efficacy of medetomidine and tiletamine–zolazepam for remote immobilisation of feral horses (Equus caballus).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXltFehsr0%3D&md5=75e0efb8ef2609fe195beb39167076fdCAS |

Zalba, S. M., and Cozzani, N. C. (2004). The impact of feral horses on grassland bird communities in Argentina. Anim. Conserv. 7, 35–44.
The impact of feral horses on grassland bird communities in Argentina.Crossref | GoogleScholarGoogle Scholar |