Spermatogenesis and plasma testosterone levels under field conditions, in males of the common toad (Rhinella arenarum Hensel, 1867), from the Monte Desert, Argentina

Lorena Quiroga, Eduardo Sanabria, Graciela Jahn, Miguel Fornés

Abstract


The reproductive function in anurans depends on interactions between the hypothalamus, adenohypophysis and gonads, which are mediated by an endocrine circuit. We studied the relationship between reproductive and histological parameters, variation in spermatogenic activity, and plasma testosterone concentration cycle for a population of Rhinella arenarum under field conditions in the Monte Desert of Argentina. We captured 28 adult male R. arenarum from December 2009 to November 2010, and define two seasons (wet and dry seasons). We performed histological analyses of the testes and used radioimmunoassay to determine plasma testosterone concentrations. Our results showed no difference in testicular volume between the wet and dry seasons, but found that changes in the fat body mass were higher in the dry season. The spematogenic cycle was characterized by the prominent presence of spermatogonia at the end of the dry season and the wet season. We also observed a higher percentage of primary spermatocytes in the wet season. In addition, we found that R. arenarum showed a continuous spermatogenic cycle, and spermatogenesis produced a high percentage of sperm bundles in the dry season, concordant with high levels of testosterone. Testosterone levels were highest during the dry season (33.89 ± 7.85 ng/ml). Our data indicate that plasma testosterone showed a “dissociation” from reproductive activity such that the two parameters are asynchronous during the reproductive season. The characteristics of the reproductive cycle of R. arenarum allow this species the plasticity to colonize different environments, from tropical regions to deserts.

Keywords


Argentina; Rhinella arenarum; reproduction; spermatogenesis; testosterone

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References


Arzabe C. (1999). Reproductive activity patterns of anurans in two different altitudinal sites within the Brazilian Caatinga. Revista Brasileira de Zoologia, 16: 851–864. https://doi.org/10.1590/S0101-81751999000300022

Brown G.P., Kelehear C. & Shine R. (2011). Effects of seasonal aridity on the ecology and behavior of invasive cane toads in the Australian wet-dry tropics. Functional Ecology, 25: 1339–1347. https://doi.org/10.1111/j.1365-2435.2011.01888.x

Burgos M.H. & Mancini R.E. (1948). Ciclo espermatogénico de Bufo arenarum Hensel. Revista de la Sociedad Argentina de Biología, 24: 322–336.

Bustos-Obregon E. & Alliende C. (1973). Spermatogonial renewal in amphibian testis. I. Mitotic activity in the breeding season. Archives of Biology (Brussels), 84: 329–339.

Bustos-Obregon E., Alliende C & Scrniede P. (1973). Spermatogonial renewal in amphibian testis. II. Seasonal variations and effect of temperature. Archives of Biology (Liège), 84: 465–473.

Cabrera A.L. (1976). Enciclopedia Argentina de Agricultura y Jardinería. Editorial ACME S.A.C.I, Buenos Aires.

Callard I.P., Callard G.V., Lance V., Bolaffi J.L. & Rosset J.S. (1978). Testicular regulation in nonmammalian vertebrates. Biology of Reproduction, 18: 16–43. https://doi.org/10.1095/biolreprod18.1.16

Canosa L.F. & Ceballos N.R. (2002). Seasonal changes in testicular steroidogenesis in the toad Bufo arenarum H. General and Comparative Endocrinology, 125: 426–434. https://doi.org/10.1006/gcen.2001.7768

Canosa L.F., Pozzi A.G., Rosemblit C. & Ceballos N.R. (2003). Steroid production in toads. Journal of Steroid Biochemistry & Molecular Biology, 85: 227–223. https://doi.org/10.1016/S0960-0760(03)00234-6

Carvalho J.E., Navas C.A. & Pereira I.C. (2010). Energy and water in aestivating amphibians. In: Navas C.A. & Carbalho J.E. (eds) Progress in Molecular and Subcellular Biology: 141–170. São Paulo, Brazil. https://doi.org/10.1007/978-3-642-02421-4_7

Caretta A., Ortega A. & Ortíz Maldonado A. (2004). Probabilidades de daño por viento zonda en la floración de frutales, vid y olivos Mendoza, Argentina. Revista de la facultad de Ciencias Agrarias, 36: 49–58.

Cei J.M. (1949). Generalidades sobre el ciclo sexual y el predominio de la espermato-génesis anual continua en varios batracios de la región chaqueña. Acta Zoológica Lilloana, 75: 27–544.

Cei J.M. (1980). Amphibians of Argentina. Monographs 2. Monitore Zoologico Italiano (NS), Italy.

Chieffi G., Rastogi R.K., Milone M. & Iela L. (1980). Amphibian reproduction: reproductive physiology in the male Rana esculenta L. Bolletino di Zoologia, 47: 63–70. https://doi.org/10.1080/11250008009440321

Crews D. & Moore M. (1986). Evolution of mechanisms controlling mating behavior. Science, 231: 121–125. https://doi.org/10.1126/science.3941893

Crump M.L. (2015). Anuran reproductive modes: evolving perspectives. Journal of Herpetology, 49: 1–16. https://doi.org/10.1670/14-097

De Assis V.R., Navas C.A., Mendonca M.T. & Gomes F.R. (2012). Vocal and territorial behavior in the Smith frog (Hypsiboas faber): Relationships with plasma levels of corticosterone and testosterone. Comparative Biochemistry and Physiology Part A, 163: 265–271. https://doi.org/10.1016/j.cbpa.2012.08.002

Delgado M.J., Gutiérrez P. & Alonso M. (1989). Seasonal cicles in testicular activity in the frog, Rana perezi. General and Comparative Endocrinology, 73: 1–11.

Denari D. & Ceballos N.R. (2005). 11β-Hydroxysteroid dehydrogenase in the testis of Bufo arenarum: Changes in its seasonal activity. General and Comparative Endocrinology, 143: 113–120. https://doi.org/10.1016/j.ygcen.2005.03.006

De Oliveira C. & Vicentini C.A. (1998). Descricao anatomica dos testículos e corpos adiposos de Scinax fuscovarius (Anura, Hylidae). Biociências, 6: 79–98.

De Oliveira C., Sant’Anna A.C., Munhoz de Omena P., De Souza Santos L.R. & Zieri R. (2003). Morphological considerations on the seminiferous structures and testes of anuran amphibians: Bufo crucufer, Physalaemus cuvieri and Scinax fuscovarius. Biociências, 11: 39–46.

De Souza Santos L.R. (2006). Ciclo reproductivo de machos de Dendropsophus minutus (Anura, Hylidae). PhD Thesis, Universidade Estadual Paulista. Sao Paulo, Brazil.

De Souza Santos L.R. & De Oliveira C. (2008). Histological aspects and structural characteristics of the testes of Dendropsophus minutus (Anura, Hylidae). Micron, 39: 1266–1270. https://doi.org/10.1016/j.micron.2008.03.006

Duellman W.E. & Trueb L. (1994). Biology of Amphibians. The Johns Hopkins University Press, Baltimore and London.

Dunham A.E. (1983). Realized niche overlap, resource abundance and intensity of interspecific competition. In: Huey R.B., Pianka E.R. & Schoener T.W. (eds) Lizard Ecology. Harvard University Press, Cambridge, USA. https://doi.org/10.4159/harvard.9780674183384.c15

Emerson S.B. & Hess D.L. (1996). The role of androgens in opportunistic breeding, tropical frogs. General and Comparative Endocrinology, 103: 220–230. https://doi.org/10.1006/gcen.1996.0113

Fernández S.N. & Ramos I. (2003). Endocrinology of reproduction. In: Jamieson B.G.M. (ed.) Reproductive Biology and Phylogeny of Anura: 73–117. Science Publishers, Enfield, London.

Fitzpatrick L.C. (1976). Life history patterns of storage and utilization of lipids for energy in amphibians. American Zoology, 16: 725–732. https://doi.org/10.1093/icb/16.4.725

Gallardo J.M; (1987). Anfibios de Argentina, Guía para su identificación. Biblioteca Mosaico. Argentina.

Hammer Ø., Harper D.A. & Ryan P.D. (2001). PAST: Paleontological Statistics Software Package for Education and Data Analysis. Paleontología Electrónica, 4: 1–9. Available from http://palaeo-electronica.org/2001_1/past/issue1_01.htm [accessed 16 April 2018].

Harvey L.A., Propper C.R., Woodley S. & Moore M. (1997). Reproductive endocrinology of the explosively breeding desert spadefoot toad, Scaphiopus couchii. General and Comparative Endocrinology, 105: 102–113. https://doi.org/10.1006/gcen.1996.6805

Hau M. (2007). Regulation of male traits by testosterone: implications for the evolution of vertebrate life histories. Biossays, 29: 133–144. https://doi.org/10.1002/bies.20524

Heyer W.R., Donelly M.A., McDiarmid R.W., Hayek L.C. & Foster M.S. (2001). Medición y monitoreo de la diversidad biológica, métodos estandarizados para anfibios. Editorial Universitaria de la Patagonia. Argentina.

Huang W.S. & Yu J.Y. (2005). Reproductive characteristics of Bufo bankorensis at two elevations in Taiwan. Zoological Science, 22: 111–117. https://doi.org/10.2108/zsj.22.111

Huang W.S., Lin J.Y. & Yu J.Y. (1997). Male reproductive cycle of the toad Bufo melanostictus in Taiwan. Zoological Science, 14: 497–503. https://doi.org/10.2108/zsj.14.497

Itoh M., Inoue M. & Ishii S. (1990). Annual cycle of pituitary and plasma gonadotropins and sex steroids in a wild population of the toad, Bufo japonicus. General and Comparative Endocrinology, 78: 242–253. https://doi.org/10.1016/0016-6480(90)90011-A

Jørgensen C.B. (1992). Growth and reproduction. In: Feder M.E. & Burggren W.W. (eds) Environmental Physiology of the Amphibians: 439–466. The University of Chicago Press, USA.

Kordonowy L., Lombardo K.D., Green H.L., Dawson M.D., Bolton E.A., LaCourse S. & MacManes M.D. (2017). Physiological and biochemical changes associated with acute experimental dehydration in the desert adapted mouse, Peromyscus eremicus. Physiological Reports, 5: e13218. https://doi.org/10.14814/phy2.13218

Krohmer R.W., Grassman M. & Crews D. (1987). Annual reproductive cycle in the male red-sided garter snake, Thamnophis sirtalis parietalis: field and laboratory studies. General and Comparative Endocrinology, 68: 64–75. https://doi.org/10.1016/0016-6480(87)90061-X

Lavilla E.O. & Rouges M. (1992). Reproducción y desarrollo de anuros Argentinos. Asociación Herpetológica Argentina. Serie divulgación, 5: 1–66.

Licht P., McCreery B.R., Barnes R. & Pang R. (1983). Seasonal and stress related changes in plasma gonadotropins, sex stedoids, and corticosterone in the bullfrog, Rana catesbeiana. General and Comparative Endocrinology, 50: 124–145.

Long D.R. (1987). A comparison of energy substrates and reproductive patterns of two anurans, Acris crepitans and Bufo woodhousei. Comparative Biochemistry and Physiology, Part A, 87: 81–91. https://doi.org/10.1016/0300-9629(87)90429-4

Long D.R. (1989). Energetics and reproduction in female Scaphiopus multiplicatus from western Texas. Journal of Herpetology, 23: 176–179. https://doi.org/10.2307/1564026

Madelaire C.B. & Gomes F.R. (2016). Breeding under unpredictable conditions: annual variation in gonadal maturation, energetic reserves and plasma levels of androgens and corticosterone in anurans from the Brazilian semi-arid. General and Comparative Endocrinology, 228: 9–16. https://doi.org/10.1016/j.ygcen.2016.01.011

Madelaire C.B., Sokolova I. & Gomes F.R. (2017). Seasonal patterns of variation in steroid plasma levels and immune parameters in anurans from Brazilian semiarid area. Physiological and Biochemical Zoology, 90: 415–433. https://doi.org/10.1086/691202

Medina M.F., Ramos I., Crespo C.A., González-Calvar S. & Fernández S.N. (2004). Changes in serum sex steroid levels throughout the reproductive cycle of Bufo arenarum females. General and Comparative Endocrinology, 136: 143–151. https://doi.org/10.1016/j.ygcen.2003.11.013

Mendonça M.T., Licht P., Ryan M.J. & Barnes R. (1985). Changes in hormone levels in relation to breeding behavior in male bullfrogs (Rana catesbeiana) at the individual and population levels. General and Comparative Endocrinology, 58: 270–279.

Montero R. & Pisanó A. (1990). Spermatogenic cycle of two species of Telmatobius the Argentine northeast. Amphibia-Reptilia, 11: 97–110.

Montero R. & Pisanó A. (1992). El ciclo espermatogénico anual de Hyla pulchella andina: un análisis numérico. Acta Zoológica Lilloana, 41: 173–180.

Navas C.A., Gomes F.R. & Carvalho J.E. (2008). Thermal relationship and exercise physiology in anuran amphibians: integration and evolutionary implications. Comparative Biochemistry & Physiology Part A, 151: 344–362. https://doi.org/10.1016/j.cbpa.2007.07.003

Perotti M.G. (1997). Modos reproductivos y variables reproductivas cuantitativas en un ensamble de anuros del chaco semiárido, Salta, Argentina. Revista Chilena de Historia Natural, 70: 277–288.

Quiroga L.B. & Sanabria E.A. (2012). Variation in reproductive parameters of Rhinella arenarum (Hensel, 1867) (Anura: Bufonidae) between the reproductive and post-reproductive periods. Belgian Journal of Zoology, 142: 68–73.

Quiroga L., Sanabria E. & Acosta J. (2009). Size- and sex-dependent variation in diet of Rhinella arenarum (Anura: Bufonidae) in a wetland of San Juan, Argentina. Journal of Herpetology, 43: 311–317. https://doi.org/10.1670/07-117R2.1

Rasband W. (2008). Image J, version 1.41. National Institutes of Health, Bethesda, Maryland. U.S. http://imagej.nih.gov/ij/

Rastogi R.K. (1976). Seasonal cycle in anuran (Amphibia) testis: The endocrine and environmental controls. Bolletino di Zoologia, 43: 151–172. https://doi.org/10.1080/11250007609434893

Rastogi R.K., Iela L., Saxena P.K. & Chieffi G. (1976). The control of espermatogenesis in the green frog Rana esculenta. Journal of Experimental Zoology, 196: 151–166.

Rastogi R.K., Iela L., Delrio G., Di Meglio M., Russo A. & Chieffi G. (1978). Environmental influence on testicular activity in the green frog, Rana esculenta. Journal of Experimental Zoology, 206: 49–64. https://doi.org/10.1002/jez.1402060106

Rastogi R.K., Iela L., Delrio G. & Bagnara J.T. (1986). Reproduction in the Mexican leaf frog, Pachymedusa dacnicolor. II The male. General and Comparative Endocrinology, 62: 23–35. https://doi.org/10.1016/0016-6480(86)90090-0

Rastogi R.K., Bagnara J.T., Iela L. & Krasovich M.A. (1988). Reproduction in the Mexican leaf frog, Pachymedusa dacnicolor. IV. Spermatogenesis: a light and ultrasonic study. Journal of Morphology, 197: 277–302. https://doi.org/10.1002/jmor.1051970304

Rastogi R.K., Di Mateo L., Minucci S., Di Meglio M. & Iela L. (1990). Regulation of primary spermatogonial proliferation in the frog (Rana esculenta): an experimental analysis. Journal of Zoology, 220: 201–211. https://doi.org/10.1111/j.1469-7998.1990.tb04303.x

Sanabria E.A. & Quiroga L.B. (2011). Thermal parameters changes in males of Rhinella arenarum (Anura: Bufonidae) related to reproductive periods. Revista de Biología tropical, 59: 347–353.

Sanabria E.A., Quiroga L.B. & Acosta J.C. (2005). Patrones de actividad temporal estacional y uso de microhábitat de una población de adultos de Bufo arenarum, en los humedales de Zonda, San Juan, Argentina. Boletín de la Sociedad Herpetológica Mexicana, 13: 61–65.

Sasso-Cerri E., De Faria F.P., Freymüller E. & Miraglia S.M. (2004). Testicular morphological changes the seasonal reproductive cycle in the Bullfrog Rana catesbeiana. Journal of Experimental Zoology Part A, 301: 249–260. https://doi.org/10.1002/jez.a.20023

Seymour R.S. (1973). Energy metabolism of dormant spadefoot toads (Scaphiopus). Copeia, 1973: 435–445. https://doi.org/10.2307/1443107

Shalan A.G., Bradshaw S.D., Withers P.C., Thompson G., Bayomy M.F.F., Bradshaw F.J. & Stewart T. (2004). Spermatogenesis and plasma testosterone levels in western Australian burrowing desert frogs, Cyclorana platycephala, Cyclorana maini, and Neobatrachus sutor, during aestivation. General and Comparative Endocrinology, 136: 90–100. https://doi.org/10.1016/j.ygcen.2003.12.005

Specker J.L. & Moore F.L. (1980). Annual cycle of plasma androgens and testicular composition in the rough-skinned newt, Taricha granulosa. General and Comparative Endocrinology, 42: 297–303. https://doi.org/10.1016/0016-6480(80)90158-6

Stebbins R.C. & Cohen N.W. (1997). A Natural History of Amphibians. Princeton University Press, USA.

Tieleman B.I., Williams J.B. & Buschur M.E. (2002). Physiological adjustments to arid and mesic environments in larks (Alaudidae). Physiological and Biochemical Zoology, 75: 305–313. https://doi.org/10.1086/341998

Tsiora A. & Kyriakopoulou-Sklavounou P. (2001). Male reproductive cycle of the water frog Rana epeirotica in northwestern Greece. Amphibia-Reptilia 22: 291–302. https://doi.org/10.1163/156853801317050089

Wells D.W. (2007). The Ecology and Behavior of Amphibians. The Universiy of Chicago Press, Chicago, USA. https://doi.org/10.7208/chicago/9780226893334.001.0001

Whitford W.G. (2002). Ecology of Desert Systems. Academic Press, New Mexico State University, Las Cruces, USA.

Woolbright L.L. (1989). Sexual dimorphism in Eleutherodactylus coqui: selection pressures and growth rates. Herpetologica, 45: 68–74.




DOI: https://doi.org/10.26496/bjz.2018.20

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