Growth, osmoregulation and endocrine changes in wild Atlantic salmon smolts and post-smolts during marine migration
Introduction
Following parr–smolt transformation and downstream migration, many stocks of Atlantic salmon (Salmo salar L.), including most Norwegian stocks, begin their oceanic migration in large fjord systems and archipelagos before reaching the open ocean. Although our knowledge about the ecology of wild Atlantic salmon post-smolts is limited, previous studies from Norwegian and British waters have suggested that these life stages spend less than a month in the fjords and coastal waters (Dutil and Coutu, 1988, Holm et al., 1982, Hvidsten and Lund, 1988, Thorpe, 1994) before continuing their migration towards the richer feeding grounds in the ocean. During their marine migration, the diet of Atlantic salmon post-smolts changes, and feeding conditions and early marine growth have been postulated to be critical to the overall marine survival and year-class strength of Atlantic salmon (Andreassen et al., 2001, Friedland et al., 2000, Friedland et al., 2009, Haugland et al., 2006, McCarthy et al., 2008, Peyronnet et al., 2007, Rikardsen et al., 2004). In the northeast Atlantic, post-smolts are generally found in close relation with the North Atlantic Current (Holm et al., 2000, Holm et al., 2004, Holst et al., 2000, Shelton et al., 1997). In autumn and winter, salmon are present north of the Faroe Islands, feeding mainly on small mesopelagic fish and crustaceans, (Jacobsen and Hansen, 2001) in areas where Atlantic and Arctic water masses meet (Jákupsstovu, 1988).
The completion of parr–smolt transformation and downstream migration represents the culmination of a series of physiological and behavioral changes which are pre-adaptive for seawater entry (Hoar, 1988), with further adaptations taking place in response to seawater (see e.g. Björnsson, 1997, Björnsson et al., 1998, Handeland et al., 1996, Handeland et al., 1998, Handeland et al., 2000, McCormick, 1995, McCormick, 2009, McCormick et al., 1989, Nilsen et al., 2003, Nilsen et al., 2007, Nilsen et al., 2008, Stefansson et al., 2003, Stefansson et al., 2008). These physiological responses represent a critical part of the adaptive process to ocean conditions and studies have suggested that they confer substantial selective advantages during the critical early marine phase of anadromous salmonids (Andreassen et al., 2001, Levings et al., 1994, Stefansson et al., 2003). Despite the proposed critical role of rapid physiological adaptations for survival and growth, information on the physiological and endocrine changes in wild salmonids during their early marine phase is very limited.
We hypothesize that significant physiological adjustments are made during this period, concurrent with changes in behavior and feeding. Specifically, our hypothesis is that muscle growth (protein synthesis and deposition) is prioritized from the beginning of the oceanic migration in Atlantic salmon post-smolts, concurrent with significant osmoregulatory adjustments, in terms of adaptive changes in the Na+,K+-ATPase (NKA) system, the Na+,K+,2Cl÷ co-transporter (NKCC) and the cystic fibrosis transmembrane conductance regulator (CFTR) in the gills. Further, we propose that these changes are regulated by the key components of the endocrine system; hence we describe changes in the GH–IGF-I system and the thyroid hormones. The objective of this study was, therefore, to examine several important physiological parameters associated with seawater adaptability, growth and energetics, as well as major endocrine regulators of these processes in wild Atlantic salmon smolts and post-smolts during their migration from the river through the fjord, coastal areas and into the open ocean.
Section snippets
Study area and fish material
The fish used in this study were sampled in 2002 at the following locations; the Vosso River in western Norway, the Trondheimsfjord in central Norway, two offshore banks (the Halten bank and the Sklinna bank off the Norwegian coast) and the major summer feeding area (the Norwegian Sea, Fig. 1, Jákupsstovu, 1988). Smolts from the Vosso River were captured in fresh water (FW) by use of a fish wheel (smolt screw, Meehan, 1961) located near the estuary at Bolstad. The fish wheel rotates with the
Growth, energetics and size relations
The fork length of the fish in the present study ranged from 11.7 to 12.4 cm for smolts caught in the river and fjord, 13.6 cm offshore and 20.9 cm for fish caught in the Norwegian Sea (Table 1). Condition factor ranged from 0.95 for fish caught in the river and fjord to 1.26 for post-smolts caught in the Norwegian Sea. The hepatosomatic index increased significantly from 0.55% in the Vosso River, through the fjords and offshore waters to a maximum of 1.73% in the Norwegian Sea (Table 1).
Muscle
Growth and size relations
The post-smolts caught in the Norwegian Sea had approximately doubled their length since they left the river as smolts (Table 1). Based on smolt age and recaptures of tagged fish we know that these fish are a mixture of European fish (Holm et al., 2003) and when caught in June, the majority has spent two–three months in the sea. While it is possible to view the present data as a simple developmental series of changes during smolt migration from the river, through the fjord, out to the open sea
Acknowledgments
We thank Bjørn Sveinsbø and Valentina Tronci at the University of Bergen, and Barbro Egnér at the University of Gothenburg, for excellent help in the lab. This study was funded in part by the Research Council of Norway and partly by the Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning (FORMAS).
References (88)
- et al.
Response of the somatotropic axis of juvenile coho salmon to alterations in plane of nutrition with an analysis of the relationships among growth rate and circulating IGF-I and 41 kDa IGFBP
Gen. Comp. Endocrinol.
(2004) - et al.
The interrelation between photoperiod, growth hormone and sexual maturation of adult Atlantic salmon (Salmo salar)
Gen. Comp. Endocrinol.
(1994) - et al.
Circulating growth hormone levels in Atlantic salmon following seawater transfer: Effects of photoperiod regime, salinity, duration of exposure and season
Aquaculture
(1998) A simplified microassay of DNA and RNA using ethidium bromide
Anal. Biochem.
(1975)- et al.
Thyroid-hormones and gill ATPase during smoltification of Atlantic salmon (Salmo salar)
Aquaculture
(1985) - et al.
Daily endocrine profiles in parr and smolt Atlantic salmon
Comp. Biochem. Physiol.
(2008) - et al.
Effects of temperature and salinity on osmoregulation and growth of Atlantic salmon (Salmo salar L.) smolts in seawater
Aquaculture
(1998) - et al.
Seawater adaptation by out-of-season Atlantic salmon (Salmo salar L.) smolts at different temperatures
Aquaculture
(2000) The physiology of smolting salmonids
- et al.
FISH-LIFT: a device for sampling live fish with trawls
Fish. Res.
(2000)
Temperature and salinity effects on plasma insulin-like growth factor-I concentrations and growth in juvenile turbot (Scophthalmus maximus)
Aquaculture
Influence of exogenous thyroxine on plasma melatonin in juvenile Atlantic salmon (Salmo salar)
Comp. Biochem. Physiol.
The effect of low temperature and fasting during the winter on metabolic stores and endocrine physiology (Insulin, insulin-like growth factor-I and thyroxine) of coho salmon, Oncorhynchus kisutch
Gen. Comp. Endocrinol.
A new fluorometric method for RNA and DNA determination
Anal. Biochem.
Osmoregulatory actions of the GH/IGF axis in non-salmonid teleosts
Comp. Biochem. Physiol.
Cystic fibrosis transmembrane conductance regulator in teleost fish
Biochim. Biophys. Acta — Biomembranes
Hormonal control of gill Na+, K+-ATPase and chloride cell function
Hormonal control of salt and water balance in vertebrates
Gen. Comp. Endocrinol.
Influence of ration level and salinity on circulating thyroid hormones in juvenile Atlantic salmon (Salmo salar)
Gen. Comp. Endocrinol.
Differential hormonal responses of Atlantic salmon parr and smolt to increased daylength: a possible developmental basis for smolting
Aquaculture
Development of a homologous radioimmunoassay for coho salmon insulin-like growth factor-I
Gen. Comp. Endocrinol.
Smolting in anadromous and landlocked strains of Atlantic salmon (Salmo salar)
Aquaculture
Endocrine systems in juvenile anadromous and landlocked Atlantic salmon (Salmo salar): seasonal development and seawater acclimation
Gen. Comp. Endocrinol.
Growth hormone and insulin-like growth factor-I act together and independently when regulating growth in vertebral and muscle tissue of Atlantic salmon postsmolts
Gen. Comp. Endocrinol.
Growth hormone and insulin-like growth factors in fish: where we are and where to go
Gen. Comp. Endocrinol.
Records of post-smolt Atlantic salmon, Salmo salar L., in the Faroe-Shetland Channel in June 1996
Fish. Res.
Effect of low temperature on seawater tolerance in Atlantic salmon (Salmo salar) smolts
Aquaculture
Measurement of protein using bicinchoninic acid
Anal. Biochem.
Seasonal variations in osmoregulatory and respiratory responses to seawater exposure of juvenile Atlantic salmon (Salmo salar) maintained in freshwater
Aquaculture
Molecular mechanisms of continuous light inhibition of Atlantic salmon parr–smolt transformation
Aquaculture
The effect of environmental salinity on the protein expression of Na+/K+-ATPase, Na+/K+/2Cl(−) cotransporter, cystic fibrosis transmembrane conductance regulator, anion, exchanger 1, and chloride channel 3 in gills of a euryhaline teleost, Tetraodon nigroviridis
Comp. Biochem. Physiol.
Bimodality of growth and smolting in Atlantic salmon, Salmo salar L
Aquaculture
A peak in GH-receptor expression is associated with growth activation in Atlantic salmon vertebrae, while upregulation of IGF-I receptor expression is related to increased bone density
Gen. Comp. Endocrinol.
Circulating growth hormone, cortisol and thyroxine levels after 24 h seawater challenge of yearling coho salmon at different developmental stages
Aquaculture
Feeding and prey-selection of wild Atlantic salmon post-smolts
J. Fish Biol.
Evaluation of endocrine indices of growth in individual postsmolt coho salmon
Trans. Am. Fish. Soc.
The biology of salmon growth hormone: from daylight to dominance
Fish Physiol. Biochem.
Growth hormone endocrinology of salmonids: regulatory mechanisms and mode of action
Fish Physiol. Biochem.
RNA–DNA ratio — an index of larval fish growth in the sea
Mar. Biol.
RNA–DNA ratios as indicators of growth in fish: a review
A reagent for the single-step simultaneous isolation of RNA, DNA and proteins from cell and tissue samples
Biotechniques
The role of growth in endocrine regulation of salmon smoltification
Fish Physiol. Biochem.
Neuroendocrinology of fish metamorphosis and puberty: Evolutionary and ecophysiological perspectives
J. Mar. Sci. Technol. — Taiwan
Early marine life of Atlantic salmon, Salmo salar postsmolts in the Northern Gulf of St. Lawrence
Fish. Bull.
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