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Mechanisms and energetic implications of osmoregulation in embryos and larvae of Chum and Coho salmon Groot, Erick P.

Abstract

Mechanisms and the energetic implications of osmoregulation were investigated in the early life stages of chum (Oncorhynchus keta) and coho salmon (O. kisutch) at three different developmental stages: eyed embryo, prehatch embryo, and yolk sac larva. Embryos and larvae were acclimated (>7 d) to selected ranges of saltwater (SW) concentrations (0 to 30 %oS) in order to examine whole-animal (Chapter 1), cellular (Chapter 2), and biochemical (Chapter 3) aspects of early life osmoregulation Chum embryos and larvae survived exposure to SW at higher salinities than coho embryos and larvae. Saltwater-challenged chum fry were able to successfully hypo-osmoregulate in 35 %oS for 24 h (plasma osmolality ~ 350 mOsm) whereas coho fry were only able to tolerate 24 %oS and were less capable at effective hypo-osmoregulation (plasma osmolality ~ 440 mOsm). Measurements of whole-animal metabolism and saltwater tolerance showed that chum salmon were markedly more tolerant to SW than coho salmon and that SW acclimation had markedly different effects at each of the three developmental stages tested. Saltwater acclimation had the most marked effect on chum salmon larvae with increased oxygen consumption rates (MO₂) of up to 53% in 30 %oS. This increased energy expenditure did not appear to be the result of increased swimming activity or changes in energy allocation to growth processes. It was postulated that evidence for increased energy expenditure might be revealed by examining cellular (Chapter 2) and biochemical (Chapter 3) aspects of early life osmoregulation. Examination of cutaneous and branchial epithelia using fluorescent microscopy (DASPEI) showed an extensive distribution of cutaneous chloride cells (CCs) with relatively high densities (-500 to -1350 CC-mrn⁻²) on all major embryonic and larval cutaneous surfaces. Examination of CCs in prehatch chum and coho embryos, using transmission electron microscopy, showed cellular fine structure that was typical of CCs in adult fish acclimated to similar conditions. However, SW-acclimated coho embryos appeared to have fewer CCs with typical SWacclimated fine structure than chum embryos. These data along with estimated and modelled changes in total whole-body numbers of cutaneous and branchial CCs, support the theory that cutaneous epithelia are the site of early life osmoregulatory processes until the gills are fully developed in the fry stage. Some preliminary data and speculation are provided that support a recent suggestion in the literature that the larval gill may function as an ion regulatory organ before it assumes its primary role as a respiratory structure in juvenile and adult fish. This study is the first to examine Na⁺,K⁺-ATPase and H⁺-ATPase activity in embryos and larvae and shows that these enzymes function at activity levels that are similar to adult fish. Ontogenic changes in Na⁺,K⁺-ATPase and H⁺-ATPase activity in chum salmon incubated in FW increased by 16 times progressively throughout development, from the eyed embryo stage to the fry stage. Acclimation to SW appeared to increase Na⁺,K⁺-ATPase activity in the branchial epithelia of chum larvae but not coho. No obvious trends related to SW acclimation were observed in the cutaneous tissues at any of the three developmental stages. H⁺-ATPase activity was highest in the branchial epithelium of yolk sac larvae in FW, specifically coho salmon. Based on H⁺-ATPase activity changes in SW, it is suggested that this enzyme also functions as part of the ion uptake mechanism in FW CCs of embryos and larvae. Yolk sac epithelium is proposed for use as a model FW ion regulatory epithelium that is flat and contains CCs. Chloride cell density and Na⁺,K⁺-ATPase and H⁺-ATPase activity in general did not correlate strongly with changes in osmotic concentration and thus did not provide any additional explanation for the observed changes in MO₂ reported in Chapter 1. Collectively the evidence supports the theory that cutaneous osmoregulation is significant during the early life stages of salmonid development but that the energy consumed by ion transport processes is not high in relation to whole-animal metabolism.

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