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      Effects of GnRHa treatment during vitellogenesis on the reproductive physiology of thermally challenged female Atlantic salmon ( Salmo salar)

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          Abstract

          Tasmanian Atlantic salmon ( S. salar) broodstock can experience temperatures above 20 °C, which impairs reproductive development and inhibits ovulation. The present study investigated the prolonged use of gonadotropin releasing hormone analogue (GnRHa) during vitellogenesis as a means of maintaining endocrine function and promoting egg quality at elevated temperature in maiden and repeat spawning S. salar. GnRHa-treatment during vitellogenesis did not compensate for the negative effects of thermal challenge on the timing of ovulation, egg size, egg fertility or embryo survival in any fish maintained at 22 °C relative to 14 °C. The lack of effectiveness was reflected by the endocrine data, as plasma follicle stimulating hormone and luteinising hormone levels were not different between treated and untreated groups at 22 °C. Furthermore, plasma testosterone and E2 levels were unchanged in GnRHa-treated fish at 22 °C, and plasma levels were generally lower in both groups maintained at 22 °C relative to 14 °C. Transcription of vitellogenin, and zona pellucida B and C was not enhanced in GnRHa-treated fish relative to untreated fish at 22 °C, presumably due to observed suppression of plasma E2. These results indicate that thermal impairment of reproduction is likely to occur on multiple levels, and is difficult to overcome via hormonal manipulation.

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          Most cited references35

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          Oogenesis in teleosts: how eggs are formed.

          One of the major objectives of the aquaculture industry is the production of a large number of viable eggs with high survival. Major achievements have been made in recent years in improving protocols for higher efficiency of egg production and viability of progeny. Main gaps remain, however, in understanding the dynamic processes associated with oogenesis, the formation of an egg, from the time that germ cells turn into oogonia, until the release of ova during spawning in teleosts. Recent studies on primordial germ-cells, yolk protein precursors and their processing within the developing oocyte, the deposition of vitamins in eggs, structure and function of egg envelopes and oocyte maturation processes, further reveal the complexity of oogenesis. Moreover, numerous circulating endocrine and locally-acting paracrine and autocrine factors regulate the various stages of oocyte development and maturation. Though it is clear that the major regulators during vitellogenesis and oocyte maturation are the pituitary gonadotropins (LH and FSH) and sex steroids, the picture emerging from recent studies is of complex hormonal cross-talk at all stages between the developing oocyte and its surrounding follicle layers to ensure coordination of the various processes that are involved in the production of a fertilizable egg. In this review we aim at highlighting recent advances on teleost fish oocyte differentiation, maturation and ovulation, including those involved in the degeneration and reabsorption of ovarian follicles (atresia). The role of blood-borne and local ovarian factors in the regulation of the key steps of development reveal new aspects associated with egg formation. Copyright 2009 Elsevier Inc. All rights reserved.
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            Temperature and salmonid reproduction: implications for aquaculture.

            Fish reproduction is likely to be affected by increasing water temperatures arising from climate change. Normal changes in environmental temperature have the capacity to affect endocrine function and either advance or retard gametogenesis and maturation, but above-normal temperatures have deleterious effects on reproductive processes. In Atlantic salmon Salmo salar, exposure to elevated temperature during gametogenesis impairs both gonadal steroid synthesis and hepatic vitellogenin production, alters hepatic oestrogen receptor dynamics and ultimately results in reduced maternal investment and gamete viability. Exposure to high temperature during the maturational phase impairs gonadal steroidogenesis, delaying or inhibiting the preovulatory shift from androgen to maturation-inducing steroid production. There are also deleterious effects on reproductive development of female broodstock of rainbow trout Oncorhynchus mykiss and Arctic charr Salvelinus alpinus when they are exposed to elevated temperature. Less is known about temperature effects on male fishes but inhibition of spermiation has been observed in S. salar and O. mykiss. Among wild stocks, the response to elevated temperature will involve behavioural thermoregulation with consequent change in geographical ranges and the possibility of local extinctions in some regions. For domesticated stocks, containment in the culture environment precludes behavioural thermoregulation and aquaculturists will be required to develop adaptive strategies in order to maintain productivity. The most direct strategy is to manage the thermal environment using one or more of a range of developing aquaculture technologies. Alternatively, there is potential to mitigate the effects of elevated temperature on reproductive processes through endocrine therapies designed to augment or restore natural endocrine function. Studies largely on S. salar have demonstrated the capacity for synthetic luteinizing hormone-releasing hormone to offset the inhibitory effects of elevated temperature on maturational events in both sexes, but the potential for hormone therapy to provide protection during gametogenesis is still largely unexplored.
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              Endocrine manipulations of spawning in cultured fish: from hormones to genes

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                Author and article information

                Contributors
                Journal
                PeerJ
                PeerJ
                peerj
                peerj
                PeerJ
                PeerJ Inc. (San Francisco, USA )
                2167-8359
                20 October 2017
                2017
                : 5
                : e3898
                Affiliations
                [1 ]Genecology Research Centre, Faculty of Science, Health, Education and Engineering, University of the Sunshine Coast , Sippy Downs, Queensland, Australia
                [2 ]Australian Seafood Cooperative Research Centre , Bedford Park, South Australia, Australia
                [3 ]Australian Rivers Institute, Griffith University , Gold Coast, Queensland, Australia
                [4 ]Salmon Enterprises of Tasmania , Wayatinah, Tasmania, Australia
                Article
                3898
                10.7717/peerj.3898
                5652270
                7ef68d3f-d774-4f74-9225-40880d595a79
                ©2017 Anderson et al.

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, reproduction and adaptation in any medium and for any purpose provided that it is properly attributed. For attribution, the original author(s), title, publication source (PeerJ) and either DOI or URL of the article must be cited.

                History
                : 5 July 2017
                : 16 September 2017
                Funding
                Funded by: Australian Fisheries Research & Development Corporation
                Award ID: 2008/217
                Funded by: Australian Seafood Cooperative Research Centre
                Award ID: 2008/762
                Award ID: 2010/719
                Funded by: Salmon Enterprises of Tasmania Pty. Ltd
                This work was supported by the Australian Fisheries Research & Development Corporation (grant 2008/217), the Australian Seafood Cooperative Research Centre (grants 2008/762 and 2010/719), and Salmon Enterprises of Tasmania Pty. Ltd. through an ‘in-kind’ contribution (Saltas). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Aquaculture, Fisheries and Fish Science
                Molecular Biology

                temperature,atlantic salmon,fertility,gene expression,reproduction,gonadotropin releasing hormone

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