Frequency of exogenous hormone therapy impacts spermiation in male Fowler's toad (Bufo fowleri)
Caitlin E. McDonough A B , Michelle W. Martin B C , Carrie K. Vance B D , Judith A. Cole C and Andrew J. Kouba B E
+ Author Affiliations
- Author Affiliations
A Beloit College, Biology Department, Beloit, 700 College St, WI 53511, USA.
B Memphis Zoo, Conservation and Research Department, Memphis, 2000 Prentiss Place, TN 38112, USA.
C University of Memphis, Department of Biological Sciences, Memphis, 3774 Walker Ave, TN 38152, USA.
D Mississippi State University, Biochemistry and Molecular Biology Department, Mississippi State, 32 Creelman St, MS 39762, USA.
E Corresponding author. Email: akouba@memphiszoo.org
Reproduction, Fertility and Development 28(7) 995-1003 https://doi.org/10.1071/RD14214
Submitted: 18 June 2014 Accepted: 16 November 2014 Published: 14 January 2015
Abstract
Amphibians are experiencing a global extinction crisis and captive assurance colonies, along with reintroduction programs, are necessary to prevent further losses. Assisted reproductive technologies (ART), such as hormone-stimulated gamete collection and in vitro fertlisation (IVF), are conservation methods that can be used to increase reproductive output for breeding and reintroduction programs when animals fail to breed naturally. In order to maximise the production of offspring using ART, it is important to establish the physiological limitations on the frequency that hormone therapy can be used to collect gametes for IVF or assisted breeding. The present study examined the effects of the frequency of hormone-induced spermiation on sperm quantity and quality in Fowler’s toad (Bufo fowleri) by comparing four levels of hormone injection frequencies: twice a week, once a week, every other week, and every 3 weeks. Sperm release was induced with an intraperitoneal injection of 300 IU human chorionic gonadotropin (hCG). Spermatozoa were collected at three time points after injection (5, 7 and 9 h) and sperm concentration, motility and quality of forward progressive movement were measured. A significant decrease in sperm concentration (P < 0.01) was observed with the most frequent treatment (twice a week hormone injections). However, there was no negative effect of the treatments on sperm motility (P = 0.06) or forward movement (P = 0.06). We also observed a significant decrease in the concentration (P < 0.01), motility (P = 0.02) and quality of forward progressive movement (P = 0.01) of spermatozoa at the 9 h collection compared with earlier collection times. These results have clear implications for amphibian captive breeding programs, where more frequent hormone-induced spermiation could have a negative effect on male performance. We recommend that hormone injections be spaced a minimum of 2 weeks apart to optimise the health of the animals, assisted breeding, IVF or collection of gametes for genome resource banking.
Additional keywords: amphibian, human chorionic gonadotropin, reproduction, spermatozoa.
References
Browne, R. K., Seratt, J., Vance, C., and Kouba, A. (2006). Hormonal priming, induction of ovulation and in-vitro fertilization of the endangered Wyoming toad (Bufo baxteri). Reprod. Biol. Endocrinol. 4, 34.| Hormonal priming, induction of ovulation and in-vitro fertilization of the endangered Wyoming toad (Bufo baxteri).Crossref | GoogleScholarGoogle Scholar | 16790071PubMed |
Carey, C. (2000). Infectious disease and worldwide declines of amphibian populations, with comments on emerging diseases in coral reef organisms and in humans. Environ. Health Perspect. 108, 143–150.
| 10698730PubMed |
Clulow, J., Mahony, M., Browne, R., Pmering, M., and Clark, A. (1999). Applications of assisted reproductive technologies (ART) to endangered anuran amphibians. In ‘Declines and Disappearances of Australian Frogs’. (Ed. A. Campbell.) pp. 219–225. (Environment Australia: Canberra.)
Clulow, J., Clulow, S., Guo, J., French, A. J., Mahony, M. J., and Archer, M. (2012). Optimisation of an oviposition protocol employing human chorionic and pregnant mare serum gonadotropins in the barred frog Mixophyes fasciolatus (Myobatrachidae). Reprod. Biol. Endocrinol. 10, 60.
| Optimisation of an oviposition protocol employing human chorionic and pregnant mare serum gonadotropins in the barred frog Mixophyes fasciolatus (Myobatrachidae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhvVequ7zP&md5=d7c72cbd9204bcbbe9b3e84758561cf3CAS | 22909256PubMed |
Conti, M., Harwood, J. P., Hsueh, A. J. W., Dufau, M. L., and Catt, K. J. (1976). Gonadotropin-induced loss of hormone receptors and desensitization of adenylate cyclase in the ovary. J. Biol. Chem. 251, 7729–7731.
| 1:CAS:528:DyaE2sXltVygug%3D%3D&md5=f8786f4e7c00d19541816d02589debefCAS | 187595PubMed |
D’Occhio, M. J., and Aspden, W. J. (1996). 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. 54, 45–52.
| 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.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXhtVSisLrI&md5=cc2172fac343cdddddc4f83d355d26c6CAS |
Garde, J. J., Soler, A. J., Cassinello, J., Crespo, C., Malo, A. F., Espeso, G., Gomendio, M., and Roldan, E. R. (2003). Sperm cryopreservation in three species of endangered gazelles (Gazella cuvieri, G. dama mhorr, and G. dorcas neglecta). Biol. Reprod. 69, 602–611.
| Sperm cryopreservation in three species of endangered gazelles (Gazella cuvieri, G. dama mhorr, and G. dorcas neglecta).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXlvVerurY%3D&md5=40eba5b04b2f03ed829066a577b0e6a5CAS | 12700201PubMed |
Gascon, C., Collins, J. P., Moore, R. D., Church, D. R., McKay, J. E., and Mendelson III, J. R. (2007). ‘Amphibian Conservation Action Plan.’ (The World Conservation Union (IUCN), IUCN/SSC Amphibian Specialist Group: Gland, Switzerland.)
Germano, J. M., and Bishop, P. J. (2008). Suitability of amphibians and reptiles for translocation. Conserv. Biol. 23, 7–15.
| Suitability of amphibians and reptiles for translocation.Crossref | GoogleScholarGoogle Scholar |
Hettyey, A., Vági, B., Hévizi, G., and Török, J. (2009). Changes in sperm stores, ejaculate size, fertilization success, and sexual motivation over repeated matings in the common toad, Bufo bufo (Anura: Bufonidae). Biol. J. Linn. Soc. Lond. 96, 361–371.
| Changes in sperm stores, ejaculate size, fertilization success, and sexual motivation over repeated matings in the common toad, Bufo bufo (Anura: Bufonidae).Crossref | GoogleScholarGoogle Scholar |
International Union for Conservation of Nature (IUCN). 2012. ‘IUCN Red List of Threatened Species. Version 2012.2.’ Available at http://www.iucnredlist.org [verified 16 November 2012].
Jahnsen, T., Purvis, K., Torjesen, P. A., and Hansson, V. (1981). Temporal relationship between hCG induced desensitization of LH/hCG responsive adenyl cyclase and down regulation of LH/hCG receptors in the rat testis. Arch. Androl. 6, 155–162.
| Temporal relationship between hCG induced desensitization of LH/hCG responsive adenyl cyclase and down regulation of LH/hCG receptors in the rat testis. Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL3M3jtFChuw%3D%3D&md5=dd13259f59189cbb7ea7850446d098e6CAS | 6264875PubMed |
James, T. Y., Litvintseva, A. P., Vilgalys, R., Morgan, J. A. T., Taylor, J. W., Fisher, M. C., Berger, L., Weldon, C., du Preez, L., and Longcore, J. E. (2009). Rapid global expansion of the fungal disease chtridiomycosis into declining and healthy amphibian populations. PLoS Pathog. 5, 1–12.
| Rapid global expansion of the fungal disease chtridiomycosis into declining and healthy amphibian populations.Crossref | GoogleScholarGoogle Scholar |
JMP 2008. An example demonstrating how to analyze repeated measures models in JMP. Available at http://www.jmp.com/support/notes/30/584.html [verified 15 November 2011].
Kouba, A. J., and Vance, C. K. (2009). Applied reproductive technologies and genetic resource banking for amphibian conservation. Reprod. Fertil. Dev. 21, 719–737.
| Applied reproductive technologies and genetic resource banking for amphibian conservation.Crossref | GoogleScholarGoogle Scholar | 19567216PubMed |
Kouba, A. J., Vance, C. K., and Willis, E. L. (2009). Artificial fertilization for amphibian conservation: current knowledge and future considerations. Theriogenology 71, 214–227.
| Artificial fertilization for amphibian conservation: current knowledge and future considerations.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1cjnt1yqtg%3D%3D&md5=e9f78d48278ce8fb40eae3a46a2c903aCAS | 19026442PubMed |
Kouba, A. J., delBarco-Trillo, J., Vance, C. K., Milam, C., and Carr, M. (2012a). A comparison of human chorionic gonadotropin and luteinizing hormone releasing hormone on the induction of spermiation and amplexus in the American toad (Anaxyrus americanus). Reprod. Biol. Endocrinol. 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 | 1:CAS:528:DC%2BC38XhvVequ7zI&md5=cdab7504481d2272d7450d4367a784ecCAS | 22905699PubMed |
Kouba, A. J., Vance, C. K., Calatayud, N., Rowlison, T., Langhorne, C., and Willard, S. (2012b). Assisted reproduction technologies (ART) for amphibians. In ‘Amphibian Husbandry Resource Guide’. (Eds V. A. Poole and S. Grow.) pp. 60–118. (Amphibian Taxon Advisory Group, Association of Zoos and Aquariums: Silver Springs, MD.)
Lentini, A. (2002). ‘Husbandry Manual: Puerto Rican Crested Toad.’ (American Association of Zoos and Aquariums: Silver Springs, MD.)
Obringer, A. R., O’Brien, J. K., Saunders, R. L., Yamamoto, K., Kikuyama, S., and Roth, T. L. (2000). Characterization of the spermiation response, luteinizing hormone release and sperm quality in the American toad (Bufo americanus) and the endangered Wyoming toad (Bufo baxteri). Reprod. Fertil. Dev. 12, 51–58.
| Characterization of the spermiation response, luteinizing hormone release and sperm quality in the American toad (Bufo americanus) and the endangered Wyoming toad (Bufo baxteri).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhtlKlug%3D%3D&md5=b966ee13856b9aab0130a4e315b0e225CAS | 11194557PubMed |
Olsson, M., Madsen, T., and Shine, R. (1997). Is sperm really so cheap? Costs of reproduction in male adders, Vipera berus. Proc. Biol. Sci. 264, 455–459.
| Is sperm really so cheap? Costs of reproduction in male adders, Vipera berus.Crossref | GoogleScholarGoogle Scholar |
Rivier, C., Rivier, J., and Vale, W. (1979). Chronic effects of (D-Trp6, Pro9, NET) luteinizing hormone-releasing factor on reproductive processes in the male rate. Endocrinology 105, 1191–1201.
| Chronic effects of (D-Trp6, Pro9, NET) luteinizing hormone-releasing factor on reproductive processes in the male rate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXhsF2rsg%3D%3D&md5=709ccc0ad847bfac99dd32e299e815acCAS | 385303PubMed |
Roth, T. L., and Obringer, A. R. (2003). Reproductive research and the worldwide amphibian extinction crisis. In ‘Reproductive Science and Integrated Conservation’. (Eds W. V. Pickard, A. R. Pickard, J. C. Rodger and D. E. Wildt.) pp. 359–374. (Cambridge University Press: Cambridge, UK.)
Roth, T. L., Szymanski, D. C., and Keyster, E. D. (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 | 1:CAS:528:DC%2BC3cXhtlCguro%3D&md5=8af6c75c94bceb846f9d93a7fe74b488CAS | 20004010PubMed |
Ryser, J. (1989). Weight loss, reproductive output, and the cost of reproduction in the common frog, Rana temporaria. Oecologia 78, 264–268.
| Weight loss, reproductive output, and the cost of reproduction in the common frog, Rana temporaria.Crossref | GoogleScholarGoogle Scholar |
Shetty, K. R., and Kalkhoff, R. K. (1977). Human chorionic gonadotropin (hCG) treatment of obesity. Arch. Intern. Med. 137, 151–155.
| Human chorionic gonadotropin (hCG) treatment of obesity.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE2s7htV2ltw%3D%3D&md5=22852819b90730649bdd50d8531398b5CAS | 836112PubMed |
Silla, A. J. (2011). Effect of priming injections of lutenizing hormone-releasing hormone on spermiation and ovulation in Günther’s toadlet, Pseudophyrne guentheri. Reprod. Biol. Endocrinol. 9, 68.
| Effect of priming injections of lutenizing hormone-releasing hormone on spermiation and ovulation in Günther’s toadlet, Pseudophyrne guentheri.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmvVKrt7k%3D&md5=240b0745a2d8c2548e8024e060a067ecCAS | 21599916PubMed |
Silla, A. J., and Roberts, J. D. (2012). Investigating patterns in the spermiation response of eight Australian frogs administered human chorionic gonadotropin (hCG) and luteinizing hormone-releasing hormone (LHRHa). Gen. Comp. Endocrinol. 179, 128–136.
| Investigating patterns in the spermiation response of eight Australian frogs administered human chorionic gonadotropin (hCG) and luteinizing hormone-releasing hormone (LHRHa).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtlKjsr3J&md5=ae3472a1ed6139115693d39991e4e3b9CAS | 22909973PubMed |
Skerratt, L. F., Berger, L., Speare, R., Cashins, S., McDonald, K. R., Phillott, A. D., Hines, H. B., and Kenyon, N. (2007). Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs. EcoHealth 4, 125–134.
| Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs.Crossref | GoogleScholarGoogle Scholar |
Spencer, B. (2002). ‘Husbandry Manual: Wyoming Toad.’ (American Association of Zoos and Aquariums Association: Silver Springs, MD.)
Stuart, S. N., Chanson, J. S., Cox, N. A., Young, B. E., Rodrigues, A. S. L., Fischman, D. L., and Waller, R. W. (2004). Status and trends of amphibian declines and extinctions worldwide. Science 306, 1783–1786.
| Status and trends of amphibian declines and extinctions worldwide.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVKitb7E&md5=dcd8e1148336dcd8b30c72388110327bCAS | 15486254PubMed |
Sundaram, K., Thau, R. B., Goldstein, M., Phillips, D. M., Rivier, J., Vale, W., and Bardin, C. W. (1984). Effect of an LHRH agonist on pituitary and testicular function in rhesus monkeys. J. Reprod. Fertil. 72, 365–371.
| Effect of an LHRH agonist on pituitary and testicular function in rhesus monkeys.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXls1GhsA%3D%3D&md5=39c6a27436ad5d28bea49d966c5d28b5CAS | 6439862PubMed |
Swanson, W. F., Horohov, D. W., and Godke, R. A. (1995). Production of gonadotrophin-neutralizing immunoglobulins in cats after repeated eCG–hCG treatment and relevance for assisted reproduction in felids. J. Reprod. Fertil. 105, 35–41.
| Production of gonadotrophin-neutralizing immunoglobulins in cats after repeated eCG–hCG treatment and relevance for assisted reproduction in felids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXptVKmtrc%3D&md5=16e4a8544136e08398e8b6d9eddf40b9CAS | 7490712PubMed |
Van Der Kraak, G., Pankhurst, N. W., Peter, R. E., and Lin, H. R. (1989). Lack of antigenicity of human chorionic gonadotropin in silver carp (Hypophthalmichthys molitrix) and goldfish (Carassius auratus). Aquaculture 78, 81–86.
| Lack of antigenicity of human chorionic gonadotropin in silver carp (Hypophthalmichthys molitrix) and goldfish (Carassius auratus).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXkvFGjtLY%3D&md5=8854eb665637730ac646330cf8757607CAS |
Vickery, B. H., McRae, G. I., Briones, W., Worden, A., Seidenberg, R., Schanbacker, B. D., and Falvo, R. (1984). Effects of an LHRH agonist analog upon sexual function in male dogs. J. Androl. 5, 28–42.
| 1:CAS:528:DyaL2cXktVWisLs%3D&md5=b830d6713bf7b335ee9826474ad8192bCAS | 6231277PubMed |
Young, R. L., Fuchs, R. J., and Woltjen, M. J. (1976). Chorionic gonadotropin in weight control. JAMA 236, 2495–2497.
| Chorionic gonadotropin in weight control.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE2s%2FlsVSluw%3D%3D&md5=3813c95c8e60b2997a3dbf294e555a3eCAS | 792477PubMed |
Zippel, K. C., and Mendelson, J. R. (2008). The amphibian extinction crisis: a call to action. Herpetol. Rev. 39, 23–29.
