Abstract
The present study was undertaken to develop a comprehensive understanding of how environmental cues and sex steroids relate with cyclic changes in spermatogenesis in freshwater spotted snakehead Channa punctatus that is nutritious and economically important. The seasonal histological changes in testis and annual profile of gonadosomatic index (GSI) of C. punctatus delineated the testicular cycle into four phases: regressed (December–March), preparatory (April–June), spawning (July and August) and postspawning (September–November). Among environmental variables, correlation and regression analyses exhibited an important relationship between photoperiod and testicular weight while role of rainfall was seen confined to spawning. The seasonal profile of plasma sex steroids when correlated with cyclic changes in spermatogenesis in spotted snakehead, testosterone (T) seems to be involved in controlling the major events of spermatogenesis from renewal of stem cells to spawning of spermatozoa. Another important androgen prevalent in teleosts, 11-ketotestosterone (11-KT), was high during preparatory phase, suggesting that 11-KT in addition to T plays an important role in progression of spermatogenesis and spermiation in C. punctatus. However, 11-KT was not seen to be associated with milt production and release of spermatozoa during spawning. Plasma profile of estradiol-17β (E2) during different reproductive phases revealed the involvement of E2 in repopulation of stem cells during postspawning phase and in maintaining quiescence of testis during regressed phase.
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Alvarado MV, Carrillo M, Felip A (2015) Melatonin-induced changes in kiss/gnrh gene expression patterns in the brain of male sea bass during spermatogenesis. Comp Biochem Physiol A 185:69–79
Amano M, Iigo M, Ikuta K et al (2004) Disturbance of plasma melatonin profile by high dose melatonin administration inhibits testicular maturation of precocious male masu salmon. Zool Sci 21:79–85
Amer M, Miura T, Miura C, Yamauchi K (2001) Involvement of sex steroid hormones in the early stages of spermatogenesis in Japanese huchen (Hucho perryi). Biol Reprod 65:1057–1066
Baggerman B (1980) Photoperiod and endogenous control of the annual reproductive cycle in teleost fishes. In: Ali MA (ed) Environmental physiology of fishes. Plenum, New York, pp 533–567
Bhattacharyya S, Maitra S (2006) Environmental correlate of the testicular events in a major carp Catla catla in an annual reproductive cycle. Biol Rhythm Res 37:87–110
Breton B, Billard R (1977) Effects of photoperiod and temperature on plasma gonadotropin and spermatogenesis in the rainbow trout Salmo gairdnerii Richardson. Ann Biol Anim Biochim Biophys 17:331–340
Bruton M (1979) The breeding biology and early development of Clarias gariepinus (Pisces: Clariidae) in Lake Sibaya, South Africa, with a review of breeding in species of the subgenus Clarias (Clarias). Trans Zool Soc Lond 35:1–45
Carreau S, de Vienne C, Galeraud-Denis I (2008) Aromatase and estrogens in man reproduction: a review and latest advances. Adv Med Sci 53:139–144
Chang C, Lee M, Chen G (1994) Estradiol-17beta associated with the sex reversal in protandrous black porgy, Acanthopagrus schlegeli. J Exp Zool 268:53–58
Chaves-Pozo E, Mulero V, Meseguer J, García Ayala A (2005) An overview of cell renewal in the testis throughout the reproductive cycle of a seasonal breeding teleost, the gilthead seabream (Sparus aurata L). Biol Reprod 72:593–601
Chaves-Pozo E, Liarte S, Vargas-Chacoff L et al (2007) 17Beta-estradiol triggers postspawning in spermatogenically active gilthead seabream (Sparus aurata L.) males. Biol Reprod 76:142–148
Courtenay W, Williams J (2004) Snakeheads (Pisces, Channidae)–a biological synopsis and risk assessment. U.S. Geological Survey Circular 1251, U.S Geological Survey, Denver, CO, vi + 143 pp
de Vlaming V (1974) Environmental and endocrine control of teleost reproduction. In: Schreck C (ed) Control of sex in fishes. Virginia Polytechnic Institute and State University, Blacksburg, pp 13–83
de Vlaming V (1975) Effects of photoperiod and temperature on gonadal activity in the cyprinid teleost, Notemigonus crysoleucas. Biol Bull 148:402–415
El-Gharabawy M, Fahmy A, Assem S (2007) Steroid hormone in serum of male Mugil cephalus from lake Quaron in relation to ultrastructure of steroidogenic secreting tissue. Egypt J Aquat Res 33:156–178
Falcón J, Migaud H, Muñoz-cueto JA, Carrillo M (2010) Current knowledge on the melatonin system in teleost fish. Gen Comp Endocrinol 165:469–482
Fenwick J (1970) The pineal organ: photoperiod and reproductive cycles in the goldfish, Carassius auratus L. J Endocrinol 46:101–111
Fostier A (1983) The gonadal steroids. In: Hoar W, Randall D, Donaldson E (eds) Fish physiology, Vol IX A, reproduction: endocrine tissues and hormones. Academic Press, New York, pp 277–372
Fraile B, Sáez F, Vicentini C et al (1993) Effects of photoperiod on spermatogenesis in Gambusia affinis holbrooki (Teleostei: Poecilidae) during the period of testicular quiescence. J Zool 230:651–658
Gam L, Leow C, Baie S (2006) Proteomic analysis of snakehead fish (Channa striata) muscle tissue. Malays J Biochem Mol Biol 14:25–32
García-Allegue R, Madrid JA, Sánchez-Vázquez FJ (2001) Melatonin rhythms in European sea bass plasma and eye: influence of seasonal photoperiod and water temperature. J Pineal Res 31:68–75
Garg S, Sundararaj B (1985) Response of the testes and seminal vesicles of the catfish Heteropneustes fossilis (Bloch) to various combinations of photoperiod and temperature. Physiol Zool 58:616–627
Hess R (2003) Estrogen in the adult male reproductive tract: a review. Reprod Biol Endocrinol 1:52
Iigo M, Aida K (1995) Effects of season, temperature, and photoperiod on plasma melatonin rhythms in the goldfish, Carassius auratus. J Pineal Res 18:62–68
Kaptaner B, Kankaya E (2013) Analysis of germ cell proliferation, apoptosis, and androgenesis in the Lake Van fish (Chalcalburnus tarichi) during testicular development. Fish Physiol Biochem 39:1665–1679
Kobayashi Y, Nozu R, Nakamura M (2011) Role of estrogen in spermatogenesis in initial phase males of the three-spot wrasse (Halichoeres trimaculatus): effect of aromatase inhibitor on the testis. Dev Dyn 240:116–121
Kramer DL (1978) Reproductive seasonality in the fishes of a tropical stream. Ecology 59:976–985
Lam T (1983) Environmental influences on gonadal activity in fish. In: Hoar W, Randall D, Donalson E (eds) Fish physiology, Vol IXB, reproduction: behaviour and fertility control. Academic Press, New York, pp 65–116
Melamed P, Gur G, Rosenfeld H et al (2000) Reproductive development of male and female tilapia hybrids (Oreochromis niloticus x O. aureus) and changes in mRNA levels of gonadotropin (GtH) Ibeta and IIbeta subunits. J Exp Zool 286:64–75
Miura T, Miura C (2001) Japanese eel: a model for analysis of spermatogenesis. Zool Sci 18:1055–1063
Miura T, Yamauchi K, Nagahama Y, Takahashi H (1991a) Induction of spermatogenesis in male japanese eel, Anguilla japonica, by a single injection of human chorionic gonadotropin. Zool Sci 8:63–73
Miura T, Yamauchi K, Takahashi H, Nagahama Y (1991b) Human chorionic gonadotropin induces of all stages of spermatogenesis in vitro in the male Japanese eel (Anguilla japonica). Dev Biol 146:258–262
Miura T, Yamauchi K, Takahashi H, Nagahama Y (1991c) Hormonal induction of all stages of spermatogenesis in vitro in the male Japanese eel (Anguilla japonica). Proc Natl Acad Sci USA 88:5774–5778
Miura T, Miura C, Ohta T et al (1999) Estradiol-17beta stimulates the renewal of spermatogonial stem cells in males. Biochem Biophys Res Commun 264:230–234
Molur S, Walker S (1998) Report of the workshop “Conservation assessment and management plan for freshwater fishes of India”, Zoo Outreach Organisation, conservation breeding specialist group, India, Coimbatore, India
Nash J (1998) Seasonal reproduction in fish. In: Knobil E, Niell J (eds) Encyclopedia of reproduction, vol 4. Academic Press, New York, pp 329–340
Pottinger TG, Carrick TR (2000) Contrasting seasonal modulation of the stress response in male and female rainbow trout. J Fish Biol 56:667–675
Prat F, Zanuy S, Carrillo M et al (1990) Seasonal changes in plasma levels of gonadal steroids of sea bass, Dicentrarchus labrax L. Gen Comp Endocrinol 78:361–373
Reddy P (1979) Maturity and spawning in the murrel, Channa punctata (Bloch, 1973) (Pisces, Teleostei, Channidae) from Guntur, Andhra Pradesh. Proc Indian Natl Sci Acad B 45:543–553
Rodríguez L, Carrillo M, Sorbera L et al (2000) Pituitary levels of three forms of GnRH in the male European sea bass (Dicentrarchus labrax, L.) during sex differentiation and first spawning season. Gen Comp Endocrinol 120:67–74
Saikia A, Abujam S, Biswas S (2013) Reproductive biology of Channa punctatus (Bloch) from paddy field of Sivasagar, Assam. Int J Curr Res 5:542–546
Schulz RW, de França LR, Lareyre JJ et al (2010) Spermatogenesis in fish. Gen Comp Endocrinol 165:390–411
Scott D, Fuller J (1976) The reproductive biology of Scleropages formosus (Müller & Schlegel) (Osteoglossomorpha, Osteoglossidae) in Malaya, and the morphology of its pituitary gland. J Fish Biol 8:45–53
Servili A, Herrera-Pérez P, Rendón MDC, Muñoz-Cueto JA (2013) Melatonin inhibits GnRH-1, GnRH-3 and GnRH receptor expression in the brain of the European sea bass, Dicentrarchus labrax. Int J Mol Sci 14:7603–7616
Shimizu A (2003) Effect of photoperiod and temperature on gonadal activity and plasma steroid levels in a reared strain of the mummichog (Fundulus heteroclitus) during different phases of its annual reproductive cycle. Gen Comp Endocrinol 131:310–324
Singh N, Gupta PK (2014) Reproductive biology of eastern mosquito fish Gambusia holbrooki (Girard) (Poeciliiadae) in a sub-tropical Lake, Lake Nainital (India). Int J Curr Microbiol Appl Sci 3:19–31
Singh MS, Joy KP (1998) Precocious recrudescence of seminal vesicle and testis in catfish, Clarias batrachus (Linn.), subjected to a long photoperiod regime. Indian J Exp Biol 36:1264–1268
Singh R, Chaturvedi SK, Abhinav (2010) Effect of photoperiod and temperature on testicular regression in Channa punctatus. J Environ Biol 31:307–310
Sisneros J, Forlano PM, Knapp R, Bass AH (2004) Seasonal variation of steroid hormone levels in an intertidal-nesting fish, the vocal plainfin midshipman. Gen Comp Endocrinol 136:101–116
Soivio A, Pesonen S, Teravainen T et al (1982) Seasonal variations in oestrogen and testosterone levels in the plasma of brown trout (Salmo trutta lacustris) and in the metabolism of testosterone in its skin. Ann Zool Fenn 19:53–59
Song M, Gutzeit HO (2003) Effect of 17-alpha-ethynylestradiol on germ cell proliferation in organ and primary culture of medaka (Oryzias latipes) testis. Dev Growth Differ 45:327–337
Srivastav SK, Srivastav AK (1998) Annual changes in serum calcium and inorganic phosphate levels and correlation with gonadal status of a freshwater murrel, Channa punctatus (Bloch). Braz J Med Biol Res 31:1069–1073
Srivastava S, Singh R (1993) Effects of constant photoperiod-temperature regimes on testes and pituitary gonadotropic cells of the murrel, Channa punctatus (Bloch) during the annual reproductive cycle. Ann Endocrinol (Paris) 54:203–206
Suchiang P, Gupta B (2011) Variations in the plasma levels of thyroid hormones and testicular activity in the male air-breathing catfish (Clarias gariepinus) over the annual cycle. Int J Biol 3:144–155
Sulistyo I, Rinchard J, Fontaine P et al (1998) Reproductive cycle and plasma levels of steroids in male Eurasian perch Perca fluviatilis. Aquat Living Resour 11:101–110
Wiebe J (1968) The effects of temperature and daylength on the reproductive physiology of the viviparous seaperch, Cymatogaster aggregata Gibbons. Can J Zool 46:1207–1219
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The first and second author are indebted to Department of Science and Technology, India (Inspire Fellowship), and University of Delhi, India (UGC–non-NET fellowship and University teaching assistantship), respectively, for financial assistance. We are thankful to Prof. Atanu Kumar Pati, School of life sciences, Pt. Ravishankar Shukla University, Raipur, India, for his guidance in analyzing the data. Regional Meteorological Department, New Delhi, India, is duly acknowledged for providing data of environmental variables.
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Basak, R., Roy, A. & Rai, U. Seasonality of reproduction in male spotted murrel Channa punctatus: correlation of environmental variables and plasma sex steroids with histological changes in testis. Fish Physiol Biochem 42, 1249–1258 (2016). https://doi.org/10.1007/s10695-016-0214-6
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DOI: https://doi.org/10.1007/s10695-016-0214-6