Elsevier

Aquaculture

Volume 516, 1 February 2020, 734603
Aquaculture

Characterization of smoltification in the Tasmanian strain of Atlantic salmon (Salmo salar) in recirculation and flow-through systems

https://doi.org/10.1016/j.aquaculture.2019.734603Get rights and content

Highlights

  • First study to measure gill NKA activity and gene expression in the Tasmanian stock of Atlantic salmon during smoltification.

  • Smolt development and salinity tolerance happened in both rearing conditions in freshwater and after transfer to saltwater.

  • Gill NKA activity increased significantly in both rearing conditions 2 weeks after transfer to saltwater.

Abstract

This study examined morphological, physiological and molecular indicators of smoltification in Atlantic salmon (Salmo salar) juveniles in a flow-through (FT) and recirculating aquaculture system (RAS). Fish were exposed to 24-h light to initiate smoltification, for 5 (FT) and 7 (RAS) weeks prior to transfer from freshwater (FW) to seawater (SW) and were sampled weekly preceding and following SW transfer. Mass, length, condition factor, plasma chloride, gill Na+/K+-ATPase (NKA) activity and expression of salinity-specific isoforms of NKA mRNA transcripts were monitored. Fish raised in FT had significantly lower specific growth rate (SGR) in FW than in SW and showed a significant 5-6-fold increase in gill NKA activity, and high plasma chloride levels after transfer to SW. These fish also exhibited no significant reduction in relative mRNA expression of NKAα1a in FW but a sharp significant downregulation post-SW transfer. No significant increase in NKAα1b was seen until week 8 (3 weeks post-SW transfer). The log2 ratio of NKAα1b to NKAα1a showed a significant 8-fold increase throughout the study. Fish raised in the RAS had significantly higher SGR in FW than SW, and showed significantly higher plasma chloride in saltwater challenged fish compared to the freshwater control at all weeks during the FW phase. Fish had a 50% higher initial NKA activity than in FT, increasing significantly 2-3-fold and showed an immediate down-regulation of NKAα1a after exposure to 24-hr light in FW, and a further reduction after SW-transfer. There was no significant increase in NKAα1b in the RAS-raised fish for the duration of the study, and there was a significant 8-fold increase in log2 ratio of NKAα1b to NKAα1a. Whilst there were too many varying factors to statistically compare hatchery type in this study, it's evident that there are potentially system-related effects worthy of future investigation.

Introduction

Atlantic salmon (Salmo salar) is an anadromous teleost that is commonly cultured for food around the globe, with present production approximately 2.2 M tonnes (FAO, 2018). There are many challenges that face the commercial culture of anadromous species; perhaps the most crucial aspect is the process of transferring fish from their land-based freshwater (FW) hatcheries to ocean-based sea pens. Wild S. salar, along with other members of the Salmonidae family have developed several physiological mechanisms in order to facilitate their downstream migration that results in such a drastic change in environment. S. salar juveniles that are above a size/growth threshold are sensitive to a seasonal increase in photoperiod, water temperature and stream flow (McCormick, 2013; Stefansson and Björnsson, 2008). These along with several other parameters are thought to stimulate the migratory life phase and induce physiological, morphological and behavioural changes that allow for post-migration survival at sea (Hoar, 1988; McCormick et al., 2013; Stefansson and Björnsson, 2008). This developmental phenomenon is referred to as the parr-smolt transformation, or smoltification. In commercial hatcheries, these seasonal increases in photoperiod are often artificially manipulated in an attempt to induce the onset of smoltification-related changes before the fish are transferred to sea.

Perhaps the most important change during smoltification is the development of a higher tolerance to seawater (SW) (McCormick, 2001). Teleosts attempt to maintain a relatively constant osmolality (around 300–350 mOsmol L−1), no matter the salinity of their surrounding environment (McCormick, 2013). FW and SW are approximately 0 mOsmol L−1 and 1000 mOsmol L−1 respectively. Consequently, during the transitional “migration” phase, the gill must switch from active ion uptake in FW to active ion secretion in SW, essentially reversing in function (Evans et al., 2005; Handeland et al., 2013; McCormick et al., 2009).

The gill is the primary osmoregulatory organ in all teleosts. Gill Na+/K+-ATPase (NKA) are transport proteins within the chloride cells (or ionocytes) found in the gill epithelium, and are the primary drivers of branchial ionic regulation in both FW and SW. Gill NKA activity is widely used as an indicator of advanced hypo-osmoregulatory ability in salmon smolts and has been correlated with development of SW tolerance (McCormick and Saunders, 1987). NKA provides an electrochemical gradient which allows the passive exit of Na+ and Cl ions from the gill chloride cells (Hwang et al., 2011). Several isoforms of NKA proteins have been identified in Atlantic salmon and other salmonids (Blanco and Mercer, 1998; Madsen et al., 2009; Richards et al., 2003). Of particular interest are NKAα1a and NKAα1b, which are differentially regulated by salinity and have been linked with ion-uptake in FW and ion-secretion in SW respectively (Christensen et al., 2018; McCormick et al., 2009; Richards et al., 2003). NKAα1b is normally upregulated during smolt development in FW, and shows an increase in both the abundance of the protein and the number of ionocytes in which the protein is expressed (Christensen et al., 2018). The NKAα1b-expressing ionocytes are thought to be inactive in FW smolts, and become activated once fish are transferred to SW (McCormick et al., 2013). NKAα1a abundance remains relatively stable in FW, however significantly decreases post-SW transfer (Christensen et al., 2018; McCormick et al., 2013).

Globally, while the aquaculture sector continues to grow and become a more prominent contributor to human nutrition, there has been increased pressure on the industry to improve its sustainability credentials on multiple levels, including reduced carbon footprint and reduced nutrient-rich effluent from hatcheries and other operations. Recently there has been a shift from more traditional flow-through (FT) hatcheries, which use ambient water from a nearby water source (typically a river) that is crudely filtered before running through the hatchery systems and are then expelled back into the natural environment (Bergheim et al., 2009). There is often little or no treatment to reduce waste metabolites from the outflow of these systems. Developments in recirculating aquaculture system (RAS) technology means that hatcheries can reduce water requirements by 100-fold or more (Roque d’Orbcastel et al., 2009). This style of production is being promoted in the European aquaculture industry (Badiola et al., 2012), and make it possible to provide a highly controllable environment and water quality conditions that can result in year round production, as well as improved biosecurity and disease management (Summerfelt et al., 2009).

The effects of different FW rearing systems on production of S. salar smolts has not been well studied. One study by Kolarevic et al. (2014) compared growth performance, survival, physiological indicators and welfare of S. salar smolts raised in either a RAS or FT systems. They found that whilst there was no significant difference in growth performance or mortality between the two system types, there were differences at the physiological and molecular level. Fish from the FT system presented significantly higher mRNA expression of NKAα1b at the time of SW transfer compared to fish produced in the RAS, but also saw a higher prevalence of fin damage and short operculum deformity. This disparity in welfare parameters still showed significance for 4 months after SW transfer.

The Tasmanian salmon industry is following the global trend and moving the majority of its smolt production to RAS hatcheries (Tassal, pers. Comm.). It is crucial for industry to know precisely when smolts are ready to be transferred to sea in both FT and RAS hatcheries. Traditionally, morphological indicators such as silvering of scales, darkening of fin margins and body elongation were used to determine smoltification readiness. However, it has been shown that these morphological changes do not necessarily happen in conjunction with the physiological changes that are necessary for successful survival at sea (Folmar and Dickhoff, 1981). Commercial salmon hatcheries in Tasmania (Australia) currently use a 24-h SW challenge method similar to that outlined by Blackburn and Clarke (1987) to determine smolt transfer readiness, however hatcheries in the northern hemisphere commonly use a gill NKA activity assay (Christensen et al., 2018; McCormick et al., 2002; Zydlewski and Zydlewski, 2012).

Our goal was to characterise smoltification and to collect baseline information on morphometric (growth parameters) and physiological indicators of smoltification (plasma chloride, gill NKA activity, gene expression) in the Tasmanian strain of Atlantic salmon S. salar reared in two different hatchery systems; FT and RAS respectively. This will ultimately result in a better understanding of smoltification in the Tasmanian stock of S. salar, and the long-term improvement of smolt quality and farm level practices that will lead to reduced mortality of smolts upon transfer to sea-pens.

Section snippets

Fish rearing

Two studies to assess smoltification in juvenile Atlantic salmon were conducted in FW hatchery facilities (Tassal Operations, Hobart, TAS, Australia). The first study was conducted at SALTAS Hatchery (Tasmania) in which fish were kept in a flow-through system (FT), and then transferred to marine pens at Tassal's North West Bay lease. The second study was conducted at Rookwood Road Hatchery (Tasmania), where fish were maintained in RAS, before being transferred to marine pens at Tassal's Tasman

Flow-through hatchery

There was a significant effect of time on mass (p < 0.001) for the duration of the study, with significant increases between weeks 1 and 5, 6 and 8, and 9 and 10. Mean initial and final mass was 72.2 g (±2.52) and 141.1 g (±3.94) respectively (Table 1). Fork length also showed a significant effect of time (P < 0.001), with significant increases in length between weeks 1 and 5, 6 and 8, and 9 and 10 (Table 1). Initial mean fork length was 178 mm (±2.09), and final mean fork length was 236 mm

Discussion

The smoltification process in salmonids is characterised by morphological, behavioural and physiological changes that equip juvenile fish with the necessary adaptations to migrate to and survive in full strength SW (Hoar, 1988; McCormick, 2013; Stefansson and Björnsson, 2008). Increased osmoregulatory function and the development of a higher tolerance to SW is perhaps the most important change during the smoltification phase. Anadromous fish in the wild tend to migrate to seawater at their own

Declaration of competing interests

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

This research would not have been possible without the financial and technical support from Tassal Operations (Hobart, Tasmania, Australia). The authors would like to especially thank Linda Sams, Craig Selkirk, Daniel Smith, Chantelle Reid, Alistair Brown, Carlos Zarza, Andrew Copland, Mike McMann, and all other hatchery team members from Rookwood and SALTAS for their efforts in the collection of samples and data, as well the feeding of fish and maintenance of systems. A special thanks to Jared

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