Spermiation response to exogenous hormone therapy in hibernated and non-hibernated boreal toads (Anaxyrus boreas boreas)
Andrew J. Kouba A , Cecilia J. Langhorne B , Scott T. Willard B , Theodore Smith C and Carrie K. Kouba
B *
+ Author Affiliations
- Author Affiliations
A Wildlife, Fisheries, and Aquaculture Department, Mississippi State University, Mississippi State, MS 39762, USA.
B Biochemistry, Molecular Biology, Entomology and Plant Pathology Department, Mississippi State University, Mississippi State, MS 39762, USA.
C Native Aquatic Species Restoration Facility, Colorado Parks and Wildlife, Alamosa, CO 81101, USA.
Reproduction, Fertility and Development 34(5) 453-460 https://doi.org/10.1071/RD21033
Published online: 1 November 2021
© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)
Abstract
Conservation programs for threatened high- elevation amphibian species rely on hibernation to trigger appropriate male reproductive behaviours and gametogenesis. Although common practice and anecdotal observations have supported the practice of hibernation, there is limited empirical evidence documenting the effects on reproduction in these species. In this study, the effect of hibernation on sperm quantity and quality was evaluated for the alpine species Anaxyrus boreas boreas. Hibernated (n = 19) and non-hibernated (n = 21) male toads were administered 10 IU g−1 body weight (BW) human chorionic gonadotropin (hCG) and spermic urine was collected over 24 h. Hibernation had no effect on the number of males undergoing spermatogenesis, but hibernated males produced sperm in higher concentrations. Sperm quality was measured in terms of total motility, forward progressive motility and quality of forward progression. Although there was no difference in the total sperm motility of samples from hibernated and non-hibernated toads, the percentage of sperm exhibiting forward progressive motility and the quality of forward progression was significantly greater from hibernated toads. These results support our hypothesis that hibernation impacts both sperm quantity and quality in male boreal toads. This study will better inform captive breeding management decisions for threatened alpine species, in imminent danger of extinction.
Keywords: alpine-species, anuran, assisted-reproduction, brumation, chorionic gonadotropin, hormone, over-wintering, spermatogenesis.
References
Bondarenko, V, and Cosson, J (2019). Structure and beating behavior of the sperm motility apparatus in aquatic animals. Theriogenology 135, 152–163.| Structure and beating behavior of the sperm motility apparatus in aquatic animals.Crossref | GoogleScholarGoogle Scholar | 31216506PubMed |
Brizzi R, Corti C (2006) Reproductive cycles of the European amphibians: a brief history of studies on the role of exogenous and endogenous factors. In ‘Herpetologia Bonnensis II: Proceedings of the 13th Congress of the Societas Europaea Herpetologica, 27 September–2 October 2005, Bonn, Germany’. (Eds M Vences, J Köhler, T Ziegler, W Böhme) Vol. 27, p. 30. (Societas Europaea Herpetologica, Alexander Koenig Museum: Bonn, Germany)
Browne, RK, Seratt, J, Vance, C, and Kouba, A (2006). Hormonal priming, induction of ovulation and in-vitro fertilization of the endangered Wyoming toad (Bufo baxteri. Reproductive Biology and Endocrinology 4, 34.
| Hormonal priming, induction of ovulation and in-vitro fertilization of the endangered Wyoming toad (Bufo baxteri.Crossref | GoogleScholarGoogle Scholar | 16790071PubMed |
Byrne, PG, and Silla, AJ (2010). Hormonal induction of gamete release, and in-vitro fertilisation, in the critically endangered Southern Corroboree Frog, Pseudophryne corroboree. Reproductive Biology and Endocrinology 8, 144.
| Hormonal induction of gamete release, and in-vitro fertilisation, in the critically endangered Southern Corroboree Frog, Pseudophryne corroboree.Crossref | GoogleScholarGoogle Scholar | 21114857PubMed |
Calatayud, NE, Langhorne, CJ, Mullen, AC, Williams, CL, Smith, T, Bullock, L, Kouba, AJ, and Willard, ST (2015). A hormone priming regimen and hibernation affect oviposition in the boreal toad (Anaxyrus boreas boreas. Theriogenology 84, 600–607.
| A hormone priming regimen and hibernation affect oviposition in the boreal toad (Anaxyrus boreas boreas.Crossref | GoogleScholarGoogle Scholar | 26025241PubMed |
Carey, C (1993). Hypothesis concerning the causes of the disappearance of Boreal Toads from the Mountains of Colorado. Conservation Biology 7, 355–362.
| Hypothesis concerning the causes of the disappearance of Boreal Toads from the Mountains of Colorado.Crossref | GoogleScholarGoogle Scholar |
Chen, W, Zhang, LX, and Lu, X (2011). Higher pre-hibernation energy storage in anurans from cold environments: a case study on a temperate frog Rana chensinensis along a broad latitudinal and altitudinal gradients. Annales Zoologici Fennici 48, 214–220.
| Higher pre-hibernation energy storage in anurans from cold environments: a case study on a temperate frog Rana chensinensis along a broad latitudinal and altitudinal gradients.Crossref | GoogleScholarGoogle Scholar |
Chen, X, Ren, C, Teng, Y, Shen, Y, Wu, M, Xiao, H, and Wang, H (2021). Effects of temperature on growth, development and the leptin signaling pathway of Bufo gargarizans. Journal of Thermal Biology 96, 102822.
| Effects of temperature on growth, development and the leptin signaling pathway of Bufo gargarizans.Crossref | GoogleScholarGoogle Scholar | 33627262PubMed |
Corn, PS (2005). Climate change and amphibians. Animal Biodiversity and Conservation 28, 59–67.
Duellman WE, Trueb L (1994) Introduction to the amphibia. In ‘Biology of amphibians’. (Eds WE Duellman, L Trueb). (John Hopkins University Press Ltd: London, UK/Baltimore, MD, USA)
Elmberg, J (1991). Ovarian cyclicity and fecundity in boreal common frogs Rana temporaria L. along a climatic gradient. Functional Ecology 5, 340–350.
| Ovarian cyclicity and fecundity in boreal common frogs Rana temporaria L. along a climatic gradient.Crossref | GoogleScholarGoogle Scholar |
Hammerson GS (1999) ‘Amphibians and reptiles in Colorado’. 2nd edn. p. 484. (University Press of Colorado and Colorado Division of Wildlife: Denver, CO, USA)
Hartel, T, Sas, I, Pernetta, AP, and Geltsh, IC (2007). The reproductive dynamics of temperate amphibians: a review. North-Western Journal of Zoology 3, 127–145.
Kouba, AJ, delBarco-Trillo, J, Vance, CK, Milam, C, and Carr, M (2012). A comparison of human chorionic gonadotropin and luteinizing hormone releasing hormone on the induction of spermiation and amplexus in the American toad (Anaxyrus americanus. Reproductive Biology and Endocrinology 10, 59.
| A comparison of human chorionic gonadotropin and luteinizing hormone releasing hormone on the induction of spermiation and amplexus in the American toad (Anaxyrus americanus.Crossref | GoogleScholarGoogle Scholar | 22905699PubMed |
Kouba, AJ, and Vance, CK (2009). Applied reproductive technologies and genetic resource banking for amphibian conservation. Reproduction, Fertility and Development 21, 719–737.
| Applied reproductive technologies and genetic resource banking for amphibian conservation.Crossref | GoogleScholarGoogle Scholar |
Langhorne, CJ, Calatayud, NE, Kouba, CK, Willard, ST, Smith, T, Ryan, PL, and Kouba, AJ (2021). Efficacy of hormone stimulation on sperm production in an alpine amphibian (Anaxyrus boreas boreas) and the impact of short-term storage on sperm quality. Zoology 146, 125912.
| Efficacy of hormone stimulation on sperm production in an alpine amphibian (Anaxyrus boreas boreas) and the impact of short-term storage on sperm quality.Crossref | GoogleScholarGoogle Scholar | 33743452PubMed |
Loeffler C (Ed.) (2001) ‘Conservation plan and agreement for the management and recovery of the southern Rocky Mountain population of the boreal toad (Bufo boreas boreas)’. p. 76 + appendices. (Boreal Toad Recovery Team, Colorado Division of Wildlife: Denver, CO, USA)
Lofts, B (1964). Seasonal changes in the functional activity of the interstitial and spermatogenetic tissues of the green frog, Rana esculenta. General and Comparative Endocrinology 4, 550–562.
| Seasonal changes in the functional activity of the interstitial and spermatogenetic tissues of the green frog, Rana esculenta.Crossref | GoogleScholarGoogle Scholar | 14217824PubMed |
Mann, RM, Hyne, RV, and Choung, CB (2010). Hormonal induction of spermiation, courting behavior and spawning in the Southern bell frog, Litoria raniformis. Zoo Biology 29, 774–782.
| Hormonal induction of spermiation, courting behavior and spawning in the Southern bell frog, Litoria raniformis.Crossref | GoogleScholarGoogle Scholar | 20549714PubMed |
McDonough, CE, Martin, MW, Vance, CK, Cole, JA, and Kouba, AJ (2016). Frequency of exogenous hormone therapy impacts spermiation in male Fowler’s toad (Bufo fowleri. Reproduction, Fertility and Development 28, 995–1003.
| Frequency of exogenous hormone therapy impacts spermiation in male Fowler’s toad (Bufo fowleri.Crossref | GoogleScholarGoogle Scholar |
Pinder AW, Storey KB, Uitsch GR (1992) Estivation and hibernation. In ‘Environmental physiology of the amphibians’. (Eds ME Feder, WW Burggren) pp. 250–274. (University of Chicago Press: Chicago, IL, USA)
Rastogi RK, Iela L, di Meglio M, Di Fiore MM, D’Aniello B, Pinelli C, et al. (2005) Hormonal regulation of reproductive cycles in amhibians. In ‘Amphibian biology. Volume 6: Endocrinology’. (Ed H Heatwole) pp. 2045–2177. (Surrey Beatty and Sons: Chipping Norton, NSW, Australia)
Rastogi RK, Pinelli C, Polese G, D’Aniello B, Chieffi-Baccari G (2011) Hormones and reproductive cycles in anuran amphibians. In ‘Hormones and reproduction of vertebrates. Volume 2: amphibians’. (Eds DO Norris, KH Lopez) pp. 171–185. (Academic Press: London, UK)
Roth, TL, Szymanski, DC, and Keyster, ED (2010). Effects of age, weight, hormones, and hibernation on breeding success in boreal toads (Bufo boreas boreas. Theriogenology 73, 501–511.
| Effects of age, weight, hormones, and hibernation on breeding success in boreal toads (Bufo boreas boreas.Crossref | GoogleScholarGoogle Scholar | 20004010PubMed |
Santana, FE, Swaisgood, RR, Lemm, JM, Fisher, RN, and Clark, RW (2015). Chilled frogs are hot: hibernation and reproduction of the Endangered mountain yellow-legged frog Rana muscosa. Endangered Species Research 27, 43–51.
| Chilled frogs are hot: hibernation and reproduction of the Endangered mountain yellow-legged frog Rana muscosa.Crossref | GoogleScholarGoogle Scholar |
Silla, AJ, McFadden, MS, and Byrne, PG (2020). Hormone-induced sperm-release in the critically endangered Booroolong frog (Litoria booroolongensis): effects of gonadotropin-releasing hormone and human chorionic gonadotropin. Conservation Physiology 7, coy080.
| Hormone-induced sperm-release in the critically endangered Booroolong frog (Litoria booroolongensis): effects of gonadotropin-releasing hormone and human chorionic gonadotropin.Crossref | GoogleScholarGoogle Scholar |
Stevenson, LA, Roznik, EA, Greenspan, SE, Alford, RA, and Pike, DA (2020). Host thermoregulatory constraints predict growth of an amphibian chytrid pathogen (Batrachochytrium dendrobatidis. Journal of Thermal Biology 87, 102472.
| Host thermoregulatory constraints predict growth of an amphibian chytrid pathogen (Batrachochytrium dendrobatidis.Crossref | GoogleScholarGoogle Scholar | 31999604PubMed |
Storey KB (Ed.) (2000) Turning down the fires of life: metabolic regulation of hibernation and estivation. In ‘Molecular mechanisms of metabolic arrest’. pp. 1–21. (BIOS Scientific Publishers: Oxford, UK)
Storey, KB, and Storey, JM (1992). Natural freeze tolerance in ectothermic vertebrates. Annual Review of Physiology 54, 619–637.
| Natural freeze tolerance in ectothermic vertebrates.Crossref | GoogleScholarGoogle Scholar | 1562185PubMed |
Tsai P-S (2011) Neuroendocrine control of reproduction in amphibians. In ‘Hormones and reproduction of vertebrates. Volume 2: amphibians’. (Eds DO Norris, KH Lopez) pp. 21–37. (Academic Press: London, UK)
Wright KM, Whitaker BR (2001) Reproduction. In ‘Amphibian medicine and captive husbandry’. pp. 285–299. (Kreiger Publishing Company: Malabar, FL, USA)
