Attempts to Mitigate Aggression and Reproductive Behavior in Male Cownose Rays (Rhinoptera bonasus) Through Implantation of a Gonadotropin Releasing Hormone (GNRH) Agonist Deslorelin
Abstract
Gonadotropin-releasing hormone (GnRH) agonists, such as deslorelin (Suprelorin®, Peptech Animal Health, Virbac, Australia), are commonly used among mammals for reproductive management and behavioral mitigation.1 However, little work has been done to advance our understanding of GnRH agonists in elasmobranchs, particularly rays. Deslorelin has been used with mixed results in a few female stingray species,2 with fewer attempts in male rays in either reproductive management or behavioral mitigation.3,4 Male cownose rays (Rhinoptera bonasus) in large groups at times can display aggressive behaviors toward other males and even females, such as chasing and biting. This can lead to accidental, self-inflicted trauma to the subordinate rays attempting to flee, such as rostral or ocular abrasions and ulcerations. Long-term health can also be impacted by chronic stress.
A pilot study was initiated whereby three adult male cownose rays were implanted with either one (two rays) or two (one ray) 9.4-mg deslorelin implants. Another male ray was not implanted and considered the “control” male. Blood was collected from each ray prior to implantation, two weeks post-, two months post-, and then monthly post-implantation for the next 12 months to evaluate plasma testosterone concentrations. Plasma testosterone was measured via enzyme immunoassay, which was validated for this species. The three males that received the implants all had higher testosterone concentrations than the control animal from two weeks to 12 months post-implantation. The ray receiving two 9.4-mg implants displayed dose-response 50–100% higher concentrations compared to the two rays receiving only one 9.4-mg implant. Control testosterone concentrations were similar to previously published results for the species5 with 21.0–113.4, 51.9±31.8 (min–max, mean±SD) ng/ml. The highest concentrations were observed from June through August, which corresponded with increased aggression and breeding behavior suggestive of the breeding season. Testosterone concentrations in the two rays with a single implant were 60.2–289.8, 186.5±58.8 ng/ml. For the ray with two 9.4-mg implants, testosterone concentrations were 221.2–408.8, 297.6±59.0 ng/ml. Implanted rays displayed increased aggressive behaviors (chasing and biting), appeared to have increased appetites, and were more assertive during feeding sessions. Reproductive behavior, including mating attempts and swollen clasper glands, was observed outside of breeding season and persisted throughout the year. Female rays continued to be chased through the year, some sustaining self-inflicted rostral abrasions requiring medical management.
Typically, deslorelin has a two-phase effect: an acute stimulatory phase producing temporary enhancement of testosterone production in males, followed by a chronic suppressive phase when the hypothalamic-pituitary-gonadal axis is downregulated, leading to a reduction in hormone production.1 This was not the case in male cownose rays. The deslorelin implants produced a persistent stimulation of testosterone production with no sign of suppression after one year. The same effect was observed in male freshwater stingrays (Potamotrygon sp.).4 Taxa differences in down-regulating effects of GnRH have also been reported in ungulates.6,7 Based on the continued and sometimes enhanced unwanted aggressive behaviors, deslorelin is not recommended in male cownose rays for behavior mitigation.
Acknowledgments
The authors wish to thank H. Walters and the shark team for their dedicated care and behavioral monitoring of the cownose rays; P. Toledo, V. Jemec, K. Gross, and A. Ingrisano for sample collection and processing; and J. Gillis and K. Mowle for sample analyses. Deslorelin implants were provided by the AZA Reproductive Management Center.
*Presenting author
Literature Cited
1. Agnew MK, Asa CS, Franklin AD, McDonald MM, Cowl VB. Deslorelin (Suprelorin) use in North American and European zoos and aquariums: taxonomic scope, dosing, and efficacy. J Zoo Wildl Med. 2021;52:427–436.
2. Janse M, Luten HA. Contraception within an elasmobranch captive breeding programme: a case report on the eagle ray Aetobatus ocellatus using gonadotrophin-releasing hormone (GnRH) agonist deslorelin (Suprelorin). J Fish Biol. 2019;94:196–199.
3. Daly J, Jones R. The use of reproductive technologies in breeding programs for elasmobranchs in aquaria. In: Smith M, Warmolts D, Thoney D, Hueter R, Murray M, Ezcurra J, eds. The Elasmobranch Husbandry Manual II: Recent Advances in the Care of Sharks, Rays and Their Relatives. Columbus, OH: Ohio Biology Survey; 2017:363–374.
4. Sailler A, Laidebeure S, Lécu A. No more sex in the river? Evaluation of two chemical contraception methods in male freshwater stingrays (Potamotrygon sp.). EAZWV Annual Conference Proceedings; Emmen, Netherlands; 2022:78.
5. Sheldon JD, Allender MC, George RH, Bulman F, Abney K. Reproductive hormone patterns in male and female cownose rays (Rhinoptera bonasus) in an aquarium setting and correlation to ultrasonographic staging. J Zoo Wildl Med. 2018;49:638–647.
6. D’Occhio MJ, Aspden WJ. Characteristics of luteinizing hormone (LH) and testosterone secretion, pituitary responses to LH-releasing hormone (LHRH), and reproductive function in young bulls receiving the LHRH agonist deslorelin: effect of castration on LH responses to LHRH. Biol Reprod. 1996;54:45–52.
7. Penfold LM, Ball R, Burden I, et al. Case studies in antelope aggression control using GnRH agonist. Zoo Biol. 2002;21:435–448.