Abstract

Simple SummaryBrown trout is a freshwater fish with economic importance and with a great potential to be used as an environmental biosensor species. Despite being selected as a model species in distinct scientific contexts, in cultured specimens, there is a surprising lack of works investigating the morpho-physiological changes associated with the reproductive cycle; particularly concerning the gonads. In this study, a multi-parameter portfolio of biometric, biochemical, hormonal, and morphological analysis was established, which allowed a seasonal and sex characterization of the gonad status of adult brown trout males and females. Sampling included four reproductive phases: spawning capable (December), regressing (March), regenerating (July), and developing (November). Sex- and season-specific changes were described. The discriminative parameters characterized here stand now as normal baseline values against which abnormal patterns can be compared with. These parameters have the potential to be used as tools for the environmental monitoring of the reproductive status of wild populations and for the control of breeding stocks in aquaculture.Brown trout is an environmental freshwater sentinel species and is economically important for recreational fishing and aquaculture. Despite that, there is limited knowledge regarding morpho-physiological variations in adults throughout the reproductive cycle. Thus, this study aimed to analyze the fitness and gonadal maturation of cultured adult brown trout in four reproductive phases (spawning capable—December, regressing—March, regenerating—July, and developing—November). The systematic evaluation of males and females was based on biometric, biochemical, and hormonal parameters, along with a histomorphological grading of gonads and the immunophenotype location of key steroidogenic enzymes. The total weight and lengths reached the lowest levels in December. Gonad weights were higher in December and November, while the opposite pattern was found for liver weights. The lowest levels of cholesterol and total protein were also noted during those stages. The 11-ketotestosterone (11-KT) and testosterone (T) for males, and estradiol (E2) and T for females, mostly explained the hormonal variations. The immunohistochemistry of cytochrome P450c17 (CYP17-I), aromatase (CYP19), and 17β-hydroxysteroid dehydrogenase (17β-HSD) showed sex and site-specific patterns in the distinct reproductive phases. The sex- and season-specific changes generated discriminative multi-parameter profiles, serving as a tool for environmental and aquaculture surveys.

Highlights

  • Fish have high adaptability to cope with seasonal cycle changes, those related to gonad development and maturation, which are highly correlated to prevailing climatic conditions, including temperature and photoperiod [1]

  • T is a male-specific androgen that functions as a precursor for E2 synthesis [5], which subsequently induces the synthesis of hepatic vitellogenin (Vtg) during the process of vitellogenesis that occurs physiologically in females [6]

  • Seasonal changes along the reproductive cycle of salmonids have been described for pituitary gonadotropins, which induce the production of steroid hormones in the gonads

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Summary

Introduction

Fish have high adaptability to cope with seasonal cycle changes, those related to gonad development and maturation, which are highly correlated to prevailing climatic conditions, including temperature and photoperiod [1]. Seasonal monitoring studies have shown that blood levels of a few hormones, such as the sex-steroids testosterone (T), estradiol (E2), and 11-ketotestosterone (11-KT), are high before spermiation and ovulation, and so may indicate that the maturation stage is reached [2,3,4]. As for 11-KT, it is mainly associated with spermatogenesis, but there is evidence of seasonal fluctuations in females [3,4]. Seasonal changes along the reproductive cycle of salmonids have been described for pituitary gonadotropins, which induce the production of steroid hormones in the gonads. In female rainbow trout (Oncorhynchus mykiss Walbaum, 1792), the follicle-stimulating hormone (FSH) increases progressively through oocyte growth and at ovulation [7], and the luteinizing hormone (LH) peaks during maturation [8]

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