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Energetic Aspects of Osmoregulation in Fish

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Energetic Aspects of Osmoregulation in Fish ENERGETIC ASPECTS OF OSMOREGULATION IN FISH by JOHN DAVID MORGAN B.Sc, The University of British Columbia, 1979 M.Sc, The University of British Columbia, 1991 A THESIS SUBMITTED IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY in THE FACULTY OF GRADUATE STUDIES (Department of Animal Science) We accept this thesis as conforming to the required standard THE UNIVERSITY OF BRITISH COLUMBIA September 1997 © John David Morgan In presenting this thesis in partial fulfilment of the requirements for an advanced degree at the University of British Columbia, I agree that the Library shall make it freely available for reference and study. I further agree that permission for extensive copying of this thesis for scholarly purposes may be granted by the head of my department or by his or her representatives. It is understood that copying or publication of this thesis for financial gain shall not be allowed without my written permission. v , Department of f\ ^v. »v^A. Se,ve^cg_, The University of British Columbia Vancouver, Canada Date Se-pA^W KVI DE-6 (2/88) 11 ABSTRACT The energetic aspects of osmoregulation in several species of fish were examined, using an experimental approach on both a whole-animal and tissue level. The first series of experiments examined the metabolic response of temperate and tropical fish species to acute and gradual salinity change, using whole-animal oxygen consumption rates and gill Na+,K+-ATPase activity as indicators of osmoregulatory energetics. Juvenile dolphin fish (Coryphaena hippurus) were exposed for 24 h to a reduced water salinity (34 to 20 ppt). They responded by decreasing oxygen consumption and gill Na+,K+-ATPase activity, suggesting a decrease in osmoregulatory costs. Mozambique tilapia (Oreochromis mossambicus) transferred from fresh water (FW) to seawater (SW), showed an elevation in plasma growth hormone levels, gill Na+,K+-ATPase activity, and a 20% increase in oxygen uptake after 4 d. No increases in these variables were seen in tilapia transferred from FW to isosmotic salinity (ISO). These results indicated that the physiological changes associated with SW entry represent a significant short-term cost, whereas ISO did not impose (or reduce) an energy demand in tilapia during the acclimation process. In a long-term study (6 wk), coho salmon (Oncorhynchus kisutch) smolts did not show any differences in metabolic rate between FW, ISO and SW, whereas gill Na+,K+-ATPase activity was lowest in ISO, higher in FW and highest in SW. In this case, there was no correlation between whole-animal oxygen consumption rates and the relative activity of ion transport enzymes in the gills. An acute (24 h) transfer of cutthroat trout (O. clarki clarki) from FW to SW resulted in a significant elevation of both oxygen uptake and plasma Cortisol levels. To further examine the influence of Cortisol on oxygen consumption and osmoregulatory variables, cutthroat trout parr were given Cortisol implants that elevated plasma Cortisol titres to a iii level similar to that found in fish following SW exposure. Cortisol significantly increased oxygen consumption rates and plasma glucose levels of trout in FW, consistent with its glucocorticoid role. This study suggests that some of the increases in oxygen consumption that occurred during the intitial stages of SW exposure may have been related to the metabolic effects of Cortisol, rather than the direct costs usually associated with osmoregulation. To separate the energy costs of NaCl transport from other whole-animal metabolic responses to salinity change, experiments were conducted using isolated preparations of osmoregulatory tissues. Oxygen consumption and Na+,K+-ATPase activity were measured in excised rectal gland and gill tissue of the spiny dogfish (Squalus acanthias), using ouabain to estimate the portion of tissue respiration required by the Na+/K+-pump. Ouabain-sensitive oxygen consumption of the rectal gland accounted for 55% of tissue respiration, compared to 22% for the gill. On a whole- mass basis, the cost of NaCl secretion in the rectal gland was estimated to be 0.5% of whole- animal oxygen uptake. A similar approach was used on excised gill tissue from FW-adapted cutthroat trout, to assess the oxygen cost of NaCl uptake in the FW trout gill. In that study, bafilomycin was also used to inhibit H+-pump activity in the gill tissue. A similar portion of gill tissue respiration was required by the Na+/K+-pump (18%) and H+-pump (19%), and the cost of NaCl uptake in the FW trout gill was estimated at 1.8% of resting metabolic rate. Finally, an isolated, perfused gill arch preparation was used to compare gill energetics in FW- and SW- adapted cutthroat trout. The total gill oxygen consumption of FW gills was significantly (33%) higher than SW gills, and accounted for 3.9% and 2.4% of resting metabolic rate, respectively. The results of those experiments indicate that the energy demands of ion transport in osmoregulatory organs, such as the rectal gland and gill, represent a relatively small portion of the total energy budget in fish. IV TABLE OF CONTENTS Page Abstract ii Table of Contents iv List of Tables vi List of Figures vii List of Abbreviations ix Acknowledgements x General Introduction 1 Section I. Whole-animal metabolic responses to salinity change 12 Chapter 1 Physiological responses to hyposaline exposure, handling and confinement stress in juvenile dolphin fish 13 Introduction 13 Materials and Methods 14 Results 17 Discussion 21 Chapter 2 Physiological and respiratory responses of the Mozambique tilapia to salinity acclimation 25 Introduction 25 Materials and Methods 27 Results 31 Discussion 35 Chapter 3 Salinity effects on oxygen consumption, gill Na+,K+-ATPase and ion regulation in juvenile coho salmon smolts 43 Introduction 43 Materials and Methods 44 Results 50 Discussion 55 Chapter 4 Metabolic response of cutthroat trout to acute salinity change 58 Introduction 58 Materials and Methods 59 Results 61 Discussion 61 V Page Section II. Hormonal effects associated with whole-animal responses to salinity change 66 Chapter 5 Cortisol-induced changes in oxygen consumption and ionic regulation in coastal cutthroat trout parr 67 Introduction 67 Materials and Methods 68 Results 74 Discussion 78 Section III. Detailed components of ion transport-related costs in osmoregulatory tissues 84 Chapter 6 Oxygen consumption and Na+,K+-ATPase activity of rectal gland and gill tissue in the spiny dogfish 85 Introduction 85 Materials and Methods 87 Results 92 Discussion 96 Chapter 7 Energy cost of NaCl uptake in freshwater cutthroat trout gill tissue 101 Introduction 101 Materials and Methods 102 Results and Discussion 108 Chapter 8 Oxygen consumption in isolated, perfused gills of freshwater- and seawater-adapted cutthroat trout 116 Introduction 116 Materials and Methods 118 Results 124 Discussion 128 General Discussion 135 References 139 vi LIST OF TABLES Page Table 1 Body mass, liver glycogen content, plasma glucose, protein and ion concentrations, blood hemoglobin concentration, hematocrit values, and erythrocyte counts in juvenile dolphin fish, before and after a 24 h exposure to 34 ppt and 20 ppt salinity. 20 Table 2 Chemical composition of water samples collected from the tilapia salinity treatment tanks. 28 Table 3 Chemical composition of water samples collected from the coho salmon salinity treatment tanks. 46 Table 4 Body mass, and plasma Cortisol, glucose and ion levels in cutthroat trout in FW and 24 h after transfer to SW. 62 Table 5 Length, mass, and plasma Cortisol and ion concentrations of cutthroat trout parr following a 24 h seawater challenge test. 70 Table 6 Plasma Cortisol, glucose and ion concentrations, and gill Na+,K+-ATPase activity in non-implanted and cortisol-implanted cutthroat trout parr, before and after a 24 h seawater challenge test. 77 Table 7 Size characteristics and concentrations of constituents in dogfish plasma and seawater at the Bamfield Marine Station. 93 Table 8 Ouabain-sensitive oxygen consumption and Na+,K+-ATPase activity in rectal gland and gill tissue of the spiny dogfish. 95 Table 9 Body and gill mass, oxygen consumption rate, gill Na+,K+-ATPase and H+- ATPase activities, and plasma glucose and ion concentrations in cutthroat trout reared in fresh water. 109 Table 10 Cost of NaCl uptake in the freshwater cutthroat trout gill. 114 Table 11 Oxygen consumption rates, gill Na+,K+-ATPase and H+-ATPase activities, and plasma Cortisol, glucose and ion concentrations in cutthroat trout acclimated for 2 wk to FW and SW. 125 Table 12 Body and gill mass of cutthroat trout used in the isolated, perfused gill preparations. 127 Vll LIST OF FIGURES Page Figure 1 Salt and water exchange in (A) hagfish, (B) elasmobranchs, (C) marine teleosts, and (D) freshwater teleosts. 2 Figure 2 Model for the movement of NaCl by chloride cells of seawater teleosts. 4 Figure 3 Model of ion transfer across the gill epithelium of a freshwater teleost. 6 Figure 4 Metabolic rates of juvenile dolphin fish after a 24 h exposure to 34 ppt and 20 ppt salinity. 18 Figure 5 Plasma Cortisol concentrations in juvenile dolphin fish, before and after a 24 h exposure to 34 ppt and 20 ppt salinity. 19 Figure 6 Gill Na+,K+-ATPase activity in juvenile dolphin fish, before and after a 24 h exposure to 34 ppt and 20 ppt salinity. 22 Figure 7 Plasma Cortisol and glucose levels in tilapia after transfer from FW to FW, ISO and 75% SW. 32 Figure 8 Plasma growth hormone (GH) and prolactin (PRL177 and PRLlg8) levels in tilapia after transfer from FW to FW, ISO and 75% SW. 33 Figure 9 Plasma [Na+], [K+] and [CI'] of tilapia after transfer from FW to FW, ISO and 75% SW. 34 Figure 10 Gill Na+,K+-ATPase activity of tilapia after transfer from FW to FW, ISO and 75% SW.
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