Register      Login
Australian Journal of Zoology Australian Journal of Zoology Society
Evolutionary, molecular and comparative zoology
RESEARCH ARTICLE

Seasonal variation in the profile of sex steroids and histological testicular development of brook trout (Salvelinus fontinalis Mitchill) during the annual reproductive cycle in Tasmania

Shafaq Fatima A B , Mark Adams A and Ryan Wilkinson A
+ Author Affiliations
- Author Affiliations

A Institute for Marine and Antarctic Studies (IMAS), University of Tasmania, Locked Bag 1370, Launceston, Tas. 7250, Australia.

B Corresponding author. Email: shafaq.fatima2013@gmail.com

Australian Journal of Zoology 65(5) 313-318 https://doi.org/10.1071/ZO17030
Submitted: 31 May 2016  Accepted: 3 April 2018   Published: 4 May 2018

Abstract

Early maturation in brook trout males has been a constraint for commercial production of this species in Tasmania. However, control of maturation in males can be achieved by manipulating photoperiod (duration of light phase). To design an appropriate light treatment regime, an assessment of the annual reproductive cycle was initially required under ambient photoperiod as the annual reproductive cycle of male brook trout under ambient Tasmanian conditions of light and temperature was unknown. Here we describe the seasonal variations in testicular development and plasma profiles of testosterone (T), 11-ketotestosterone (11-KT) and oestradiol-17β (E2) during the second year in a male brook trout cohort held under ambient light conditions. Brook trout males were recruited for maturation in December when a reduction in daylength presumably stimulated testicular development. Increases in levels of T, 11-KT and gonadosomatic index (GSI) values were observed soon after the summer solstice, corresponding with maturation. The highest GSI mean value (3.44 ± 0.11%) was observed in April when mature males could be manually stripped of milt and such males were present until July. Profiles of sex steroids and histological development observed in this study were finely synchronised with variations in seasonal photoperiod changes. Photoperiod before recruitment during December should be controlled to manipulate maturation in brook trout males during their second year.

Additional keywords: maturation, photoperiod.


References

Almeida, F. F. L., Kristoffersen, C., Taranger, G. L., and Schulz, R. W. (2008). Spermatogenesis in Atlantic cod (Gadus morhua): a novel model of cystic germ cell development. Biology of Reproduction 78, 27–34.
Spermatogenesis in Atlantic cod (Gadus morhua): a novel model of cystic germ cell development.Crossref | GoogleScholarGoogle Scholar |

Amer, M. A., Miura, T., Miura, C., and Yamauchi, K. (2001). Involvement of sex steroid hormones in the early stages of spermatogenesis in Japanese huchen (Hucho perryi). Biology of Reproduction 65, 1057–1066.
Involvement of sex steroid hormones in the early stages of spermatogenesis in Japanese huchen (Hucho perryi).Crossref | GoogleScholarGoogle Scholar |

Andersson, E., Kumar, S. R., Ackers, J., Taranger, G. L., Stefansson, S. O., and Trant, J. M. (2003). Photoperiod and temperature affects seasonal ovarian gene expression of p450 aromatase and gonadotropin receptors in Atlantic salmon (Salmo salar L.) broodstock. Fish Physiology and Biochemistry 28, 411.
Photoperiod and temperature affects seasonal ovarian gene expression of p450 aromatase and gonadotropin receptors in Atlantic salmon (Salmo salar L.) broodstock.Crossref | GoogleScholarGoogle Scholar |

Baynes, S. M., and Scott, A. P. (1985). Seasonal variations in parameters of milt production and in plasma concentration of sex steroids of male rainbow trout (Salmo gairdneri). General and Comparative Endocrinology 57, 150–160.
Seasonal variations in parameters of milt production and in plasma concentration of sex steroids of male rainbow trout (Salmo gairdneri).Crossref | GoogleScholarGoogle Scholar |

Billard, R. (1992). Reproduction in rainbow trout: sex differentiation, dynamics of gametogenesis, biology and preservation of gametes. Aquaculture 100, 263–298.
Reproduction in rainbow trout: sex differentiation, dynamics of gametogenesis, biology and preservation of gametes.Crossref | GoogleScholarGoogle Scholar |

Bromage, N., Porter, M., and Randall, C. (2001). The environmental regulation of maturation in farmed finfish with special reference to the role of photoperiod and melatonin. Aquaculture 197, 63–98.
The environmental regulation of maturation in farmed finfish with special reference to the role of photoperiod and melatonin.Crossref | GoogleScholarGoogle Scholar |

Choi, S., Lee, C. H., Park, W., Kim, D. J., and Sohn, Y. C. (2010). Effects of shortened photoperiod on gonadotropin-releasing hormone, gonadotropin, and vitellogenin gene expression associated with ovarian maturation in rainbow trout. Zoological Science 27, 24–32.
Effects of shortened photoperiod on gonadotropin-releasing hormone, gonadotropin, and vitellogenin gene expression associated with ovarian maturation in rainbow trout.Crossref | GoogleScholarGoogle Scholar |

Cuesta, A., Vargas-Chacoff, L., Garcia-Lopez, A., Arjona, F. J., Martinez-Rodriguez, G., Meseguer, J., Mancera, J. M., and Esteban, M. A. (2007). Effect of sex-steroid hormones, testosterone and estradiol, on humoral immune parameters of gilthead seabream. Fish & Shellfish Immunology 23, 693–700.
Effect of sex-steroid hormones, testosterone and estradiol, on humoral immune parameters of gilthead seabream.Crossref | GoogleScholarGoogle Scholar |

Dziewulska, K., and Domagala, J. (2004). Testicular development in the sea trout (Salmo trutta morpha trutta L.) after sex differentiation, with a reference to precocious maturation. Journal of Applied Ichthyology 20, 282–289.
Testicular development in the sea trout (Salmo trutta morpha trutta L.) after sex differentiation, with a reference to precocious maturation.Crossref | GoogleScholarGoogle Scholar |

Fatima, S, Adams, M, and Wilkinson, R (2014). Monthly variations in the profile of sex steroids and gonadal development of brook trout (Salvelinus fontinalis, Mitchill) during puberty under Tasmanian climate conditions. Australian Journal of Zoology 62, 200–205.
Monthly variations in the profile of sex steroids and gonadal development of brook trout (Salvelinus fontinalis, Mitchill) during puberty under Tasmanian climate conditions.Crossref | GoogleScholarGoogle Scholar |

Fatima, S., Adams, M., and Wilkinson, R. (2015). Annual variations in the profile of sex steroids and ovarian development of brook trout (Salvelinus fontinalis, Mitchill) during the annual reproductive cycle in Tasmania. Australian Journal of Zoology 63, 220–223.
Annual variations in the profile of sex steroids and ovarian development of brook trout (Salvelinus fontinalis, Mitchill) during the annual reproductive cycle in Tasmania.Crossref | GoogleScholarGoogle Scholar |

Gielen, J. T., and Goos, H. J. T. (1984). The brain–pituitary–gonadal axis in the rainbow trout, Salmo gairdneri. III. Absence of an inhibiting action of testosterone on gonadotropin release in juveniles. General and Comparative Endocrinology 56, 457–465.
The brain–pituitary–gonadal axis in the rainbow trout, Salmo gairdneri. III. Absence of an inhibiting action of testosterone on gonadotropin release in juveniles.Crossref | GoogleScholarGoogle Scholar |

Grier, H. J., and Taylor, R. G. (1998). Testicular maturation and regression in the common snook. Journal of Fish Biology 53, 521–542.
Testicular maturation and regression in the common snook.Crossref | GoogleScholarGoogle Scholar |

Hunt, S. M. V., Simpson, T. H., and Wright, R. S. (1982). Seasonal changes in the levels of 11-oxotestosterone and testosterone in the serum of male salmon, Salmo salar L, and their relationship to growth and maturation cycle. Journal of Fish Biology 20, 105–119.
Seasonal changes in the levels of 11-oxotestosterone and testosterone in the serum of male salmon, Salmo salar L, and their relationship to growth and maturation cycle.Crossref | GoogleScholarGoogle Scholar |

Kime, D. E., and Manning, N. J. (1982). Seasonal patterns of free and conjugated androgens in the brown trout Salmo trutta. General and Comparative Endocrinology 48, 222–231.
Seasonal patterns of free and conjugated androgens in the brown trout Salmo trutta.Crossref | GoogleScholarGoogle Scholar |

King, H. R., Lee, P. S., and Pankhurst, N. W. (2003). Photoperiod-induced precocious male sexual maturation in Atlantic salmon (Salmo salar). Fish Physiology and Biochemistry 28, 427–428.
Photoperiod-induced precocious male sexual maturation in Atlantic salmon (Salmo salar).Crossref | GoogleScholarGoogle Scholar |

Kobayashi, M., Aida, K., and Stacey, N. E. (1991). Induction of testis development by implantation of 11-ketotestosterone in female goldfish. Zoological Science 8, 389–393.

Leclercq, E., Taylor, J. F., Sprague, M., and Migaud, H. (2011). The potential of alternative lighting systems to suppress pre-harvest sexual maturation of 1+Atlantic salmon (Salmo salar) post-smolts reared in commercial sea cages. Aquacultural Engineering 44, 35–47.
The potential of alternative lighting systems to suppress pre-harvest sexual maturation of 1+Atlantic salmon (Salmo salar) post-smolts reared in commercial sea cages.Crossref | GoogleScholarGoogle Scholar |

Mayer, I., Schmitz, M., Borg, B., and Schulz, R. (1992). Seasonal endocrine changes in male and female arctic charr (Salvelinus alpinus). 1. Plasma levels of 3 androgens, 17α-hydroxy-20β-dihydroprogesterone, and 17β-estradiol. Canadian Journal of Zoology 70, 37–42.
Seasonal endocrine changes in male and female arctic charr (Salvelinus alpinus). 1. Plasma levels of 3 androgens, 17α-hydroxy-20β-dihydroprogesterone, and 17β-estradiol.Crossref | GoogleScholarGoogle Scholar |

Migaud, H., Davie, A., and Taylor, J. F. (2010). Current knowledge on the photoneuroendocrine regulation of reproduction in temperate fish species. Journal of Fish Biology 76, 27–68.
Current knowledge on the photoneuroendocrine regulation of reproduction in temperate fish species.Crossref | GoogleScholarGoogle Scholar |

Milla, S., Terrien, X., Sturm, A., Ibrahim, F., Giton, F., Fiet, J., Prunet, P., and Le Gac, F. (2008). Plasma 11-deoxycorticosterone (DOC) and mineralocorticoid receptor testicular expression during rainbow trout (Oncorhynchus mykiss) spermiation: implication with 17alpha, 20beta-dihydroxyprogesterone on the milt fluidity? Reproductive Biology and Endocrinology 6, 19.
Plasma 11-deoxycorticosterone (DOC) and mineralocorticoid receptor testicular expression during rainbow trout (Oncorhynchus mykiss) spermiation: implication with 17alpha, 20beta-dihydroxyprogesterone on the milt fluidity?Crossref | GoogleScholarGoogle Scholar |

Miura, T., Yamauchi, K., Takahashi, H., and Nagahama, Y. (1991). Hormonal induction of all stages of spermatogenesis in vitro in the male Japanese eel (Anguilla japonica). Proceedings of the National Academy of Sciences of the United States of America 88, 5774–5778.
Hormonal induction of all stages of spermatogenesis in vitro in the male Japanese eel (Anguilla japonica).Crossref | GoogleScholarGoogle Scholar |

Oppedal, F., Taranger, G. L., Juell, J. E., Fosseidengen, E., and Hansen, T. (1997). Light intensity affects growth and sexual maturation of Atlantic salmon (Salmo salar) postsmolts in sea cages. Aquatic Living Resources 10, 351–357.
Light intensity affects growth and sexual maturation of Atlantic salmon (Salmo salar) postsmolts in sea cages.Crossref | GoogleScholarGoogle Scholar |

Pankhurst, N. W., and Carragher, J. F. (1992). Oocyte maturation and changes in plasma steroid levels in snapper Pagrus auratus (=Chrysophrys) (Sparidae) following treatment with human chorionic gonadotropin. Aquaculture 101, 337–347.
Oocyte maturation and changes in plasma steroid levels in snapper Pagrus auratus (=Chrysophrys) (Sparidae) following treatment with human chorionic gonadotropin.Crossref | GoogleScholarGoogle Scholar |

Piferrer, F. (2001). Endocrine sex control strategies for the feminization of teleost fish. Aquaculture 197, 229–281.
Endocrine sex control strategies for the feminization of teleost fish.Crossref | GoogleScholarGoogle Scholar |

Porter, M. J. R., Duncan, N. J., Roed, A. J., Oppedal, F., Taranger, G. L., and Bromage, N. R. (2000). Differential effects of light intensity on growth, maturation and plasma melatonin in Atlantic salmon and its importance in Aquaculture. In ‘Proceedings of the 6th International Symposium on the Reproductive Physiology of Fish, Bergen, Norway, July 4–9, 1999’. (Eds B. Norberg, O. S. Kjesbu, G. L. Taranger, E. Andersson, and S. O. Stefansson.) pp. 321–324.

Pottinger, T. G. (1988). Seasonal variation in specific plasma tissue and target tissue binding of androgens, relative to plasma steroid levels, in the brown trout, Salmo trutta L. General and Comparative Endocrinology 70, 334–344.
Seasonal variation in specific plasma tissue and target tissue binding of androgens, relative to plasma steroid levels, in the brown trout, Salmo trutta L.Crossref | GoogleScholarGoogle Scholar |

Roth, B., Jenssen, M. D., Jonassen, T., and Imsland, A. (2007). Change in flesh quality associated with early maturation of Atlantic halibut (Hippoglossus hippoglossus). Aquaculture Research 38, 757–763.
Change in flesh quality associated with early maturation of Atlantic halibut (Hippoglossus hippoglossus).Crossref | GoogleScholarGoogle Scholar |

Schulz, R. W., and Miura, T. (2002). Spermatogenesis and its endocrine regulation. Fish Physiology and Biochemistry 26, 43–56.
Spermatogenesis and its endocrine regulation.Crossref | GoogleScholarGoogle Scholar |

Scott, A. P., and Sumpter, J. P. (1983). A comparison of the female reproductive cycles of autumn spawning and winter spawning strains of rainbow trout (Salmo gairdneri Richardson). General and Comparative Endocrinology 52, 79–85.
A comparison of the female reproductive cycles of autumn spawning and winter spawning strains of rainbow trout (Salmo gairdneri Richardson).Crossref | GoogleScholarGoogle Scholar |

Scott, A. P., and Sumpter, J. P. (1989). Seasonal variations in testicular germ cell stages and in plasma concentrations of sex steroids in male rainbow trout (Salmo gairdneri) maturing at 2 years old. General and Comparative Endocrinology 73, 46–58.
Seasonal variations in testicular germ cell stages and in plasma concentrations of sex steroids in male rainbow trout (Salmo gairdneri) maturing at 2 years old.Crossref | GoogleScholarGoogle Scholar |

Shearer, K. D., and Swanson, P. (2000). The effect of whole body lipid on early sexual maturation of 1+ age male chinook salmon (Oncorhynchus tshawytscha). Aquaculture 190, 343–367.
The effect of whole body lipid on early sexual maturation of 1+ age male chinook salmon (Oncorhynchus tshawytscha).Crossref | GoogleScholarGoogle Scholar |

Skilbrei, O. T., and Heino, M. (2011). Reduced daylength stimulates size-dependent precocious maturity in 0+ male Atlantic salmon parr. Aquaculture 311, 168–174.
Reduced daylength stimulates size-dependent precocious maturity in 0+ male Atlantic salmon parr.Crossref | GoogleScholarGoogle Scholar |

Taranger, G. L., Vikingstad, E., Klenke, U., Mayers, I., Stefansson, S. O., Norberg, B., Hansen, T., Zohar, Y., and Andersson, E. (2003). Effects of photoperiod, temperature and GnRHa treatment on the reproductive physiology of Atlantic salmon (Salmo salar L.) broodstock. Fish Physiology and Biochemistry 28, 403–406.
Effects of photoperiod, temperature and GnRHa treatment on the reproductive physiology of Atlantic salmon (Salmo salar L.) broodstock.Crossref | GoogleScholarGoogle Scholar |

Taylor, J. F., Porter, M. J. R., Bromage, N. R., and Migaud, H. (2008). Relationships between environmental changes, maturity, growth rate and plasma insulin-like growth factor-I (IGF-I) in female rainbow trout. General and Comparative Endocrinology 155, 257–270.
Relationships between environmental changes, maturity, growth rate and plasma insulin-like growth factor-I (IGF-I) in female rainbow trout.Crossref | GoogleScholarGoogle Scholar |

Tveiten, H., Mayer, I., Johnsen, H. K., and Jobling, M. (1998). Sex steroids, growth and condition of Arctic charr broodstock during an annual cycle. Journal of Fish Biology 53, 714–727.
Sex steroids, growth and condition of Arctic charr broodstock during an annual cycle.Crossref | GoogleScholarGoogle Scholar |

Unwin, M. J., Rowe, D. K., Poortenaar, C. W., and Boustead, N. C. (2005). Suppression of maturation in 2-year-old Chinook salmon (Oncorhynchus tshawytscha) reared under continuous photoperiod. Aquaculture 246, 239–250.
Suppression of maturation in 2-year-old Chinook salmon (Oncorhynchus tshawytscha) reared under continuous photoperiod.Crossref | GoogleScholarGoogle Scholar |

Wilkinson, R. J., Longland, R., Woolcott, H., and Porter, M. J. R. (2010). Effect of elevated winter–spring water temperature on sexual maturation in photoperiod manipulated stocks of rainbow trout (Oncorhynchus mykiss). Aquaculture 309, 236–244.
Effect of elevated winter–spring water temperature on sexual maturation in photoperiod manipulated stocks of rainbow trout (Oncorhynchus mykiss).Crossref | GoogleScholarGoogle Scholar |