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The ontogeny of Na+ balance during rapid smoltification in pink salmon (Oncorhynchus gorbuscha)

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Abstract

Pink salmon hatch in fresh water, but their highly anadromous life history requires them to migrate into the ocean immediately after gravel-emergence, at a very small size. During their down-river migration these larvae undergo rapid smoltification that completely remodels their osmoregulatory physiology. At this time, the larvae reportedly have high whole-body Na+ contents and we hypothesised that the active accumulation of internal Na+ occurs in preparation for ocean entry. Using a comparative approach, the present study characterised the ontogeny of Na+ regulation in larvae of the anadromous pink salmon and the fresh-water rainbow trout. Our results indicate that larvae from both species actively accumulated Na+; however, whole-body Na+ content was higher in rainbow trout larvae compared to pink salmon. The time-course of this response was similar in the two species, with highest Na+-uptake rates (\(J^{{{\text{in}}}}_{{{\text{Na}}^{ + } }}\)) shortly after yolk sac absorption, but the mechanism of Na+ accumulation differed between the species. Rainbow trout larvae greatly increased \(J^{{{\text{in}}}}_{{{\text{Na}}^{ + } }}\) to overcompensate for a large simultaneous increase in Na+-efflux rate (\(J^{{{\text{out}}}}_{{{\text{Na}}^{ + } }}\)), whereas pink salmon mounted a smaller increase in \(J^{{{\text{in}}}}_{{{\text{Na}}^{ + } }}\) while maintaining tight control over \(J^{{{\text{out}}}}_{{{\text{Na}}^{ + } }}\), which is supported by a significantly lower paracellular permeability. Our results indicate that the transient accumulation of internal Na+ is not a unique feature of the highly anadromous life history in pink salmon and may be a common ontogenetic pattern during larval development in salmonids; and perhaps it is associated with the development of the cardiovascular system during the larvae’s transition to a more active lifestyle.

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Acknowledgements

Dedicated to the memory of Emily Gallagher who sadly passed away on June 22nd, 2015, at the young age of 27. Emily conducted all experiments, analysed and interpreted the data and wrote a first version of the manuscript as her MSc. thesis. Thanks are due to Sara Northrup and the Fraser Valley Trout Hatchery for providing the rainbow trout embryos and the Quinsam River Hatchery for the generous donation of pink salmon embryos. We thank Patrick Tamkee and Victor Chan for their assistance with fish care.

Funding

This study was supported by a Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery Grant (261924–13) and an Accelerator Supplement (446005–13) to CJB.

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EJG and CJB conceptualized the study; EJB carried out all experiments, analysed the data and wrote a first version of this manuscript as her MSc thesis under the supervision of CJB; TSH analysed data, produced the figures and wrote this manuscript with editorial input from CJB.

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Correspondence to Till S. Harter.

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Animal housing and all procedures were in strict compliance with the guidelines of the Canadian Council on Animal Care (CCAC) and were approved by The University of British Columbia (Protocol No. A11-0235).

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Communicated by Bernd Pelster.

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Gallagher, E.J., Harter, T.S. & Brauner, C.J. The ontogeny of Na+ balance during rapid smoltification in pink salmon (Oncorhynchus gorbuscha). J Comp Physiol B 191, 17–28 (2021). https://doi.org/10.1007/s00360-020-01309-x

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