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Port Jackson Shark, Heterodontus Portusjacksoni, in Response to Lowered Salinity

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Port Jackson Shark, Heterodontus Portusjacksoni, in Response to Lowered Salinity J Comp Physiol B (2004) 174: 211–222 DOI 10.1007/s00360-003-0404-2 ORIGINAL PAPER A. R. Cooper Æ S. Morris Osmotic, sodium, carbon dioxide and acid-base state of the Port Jackson shark, Heterodontus portusjacksoni, in response to lowered salinity Accepted: 20 October 2003 / Published online: 19 December 2003 Ó Springer-Verlag 2003 Abstract In marine elasmobranch fish the consequences content exhibited by the sharks, which caused a large for CO2 and acid–base state of moving into low salinity reduction in intracellular buffer. In water as dilute as water are not well described. Sub-adult Port Jackson 50% SW there was no evidence of specific effects on + sharks, Heterodontus portusjacksoni, occasionally enter the mechanisms of management of CO2 or H excretion brackish water and survive in 50% seawater (SW). The but rather significant and indirect effects of the severe unidirectional Na efflux and content, plasma volume, haemodilution. glomerular filtration rate (GFR), body mass, as well as CO2 and acid-base state in H. portusjacksoni were Keywords Acid-base Æ Na efflux Æ Shark Æ Hyposaline Æ investigated following transfer from 100% SW to 75% Heterodontus SW and then to 50% SW. A rapid water influx resulted in a doubling of the plasma volume within 24 h in sharks Abbreviations a–v arterial–venous Æ CA carbonic in 75% SW and an 11% increase in body weight. Os- anhydrase Æ CaCO2 content of CO2 in arterial 51 51 motic water influx was only partially offset by a dou- blood Æ CCO2 CO2 content Æ Cr-EDTA chromium- bling of the GFR. There was a 40% decrease in plasma ethylenediaminetetraactic acid Æ CvCO2 content of CO2 [Na] through a transiently elevated Na clearance and in venous blood Æ FW freshwater Æ GFR glomerular haemodilution. The result was a decrease in the inward filtration rate Æ Hct haematocrit Æ Jout Na flux gradient for Na+ together with reductions of nearly rate Æ MCHC mean cell haemoglobin 50% in CO2 and buffer capacity. The sharks remained concentration Æ OP osmotic pressure Æ PaCO2 partial hypo-natric to 50% SW by partially conforming to the pressure of CO2in arterial blood Æ PCO2 partial pressure decrease in external osmotic pressure and avoided the of CO2 Æ pHa arterial blood pH Æ pHer intra-erythrocyte + + need for active Na uptake. The gradient for Na efflux fluid Æ pHpl whole blood pH Æ pHv venous blood would by extrapolation approach zero at 27% SW pH Æ PvCO2 partial pressure of CO2in venous which may of itself prove a lethal internal dilution. In blood Æ SID strong ion difference Æ SW sharks transferred to 75% SW, a small transient seawater Æ TMAO trimethylamine-N-oxide Æ UFR hypercapnia and a later temporary metabolic alkalosis urinary flow rate were all largely explained through anaemia promoting loss of CO2 and buffer capacity. In sharks transferred to 50% SW the metabolic alkalosis persisted until the end Introduction of the 1-week trial. Within the erythrocytes, increased pH was consequent on the large decrease in haemoglobin Some elasmobranchs are able to move between seawater (SW) and freshwater (FW) (Thorson et al. 1973; Pier- marini and Evans 1998) but others, such as the Port Communicated by G. Heldmaier Jackson shark Heterodontus portusjacksoni, have a more A. R. Cooper limited tolerance of reduced salinity (Cooper and Morris School of Biological Sciences, University of Sydney, 1998a). Environmental salinity is an important factor in 2006 Sydney, NSW, Australia determining the distribution of a range of elasmo- S. Morris (&) branchs (e.g. Hopkins and Cech 2003). Morlab, School of Biological Sciences, University of Bristol, The movement of marine elasmobranchs into diluted Woodland Road, Bristol, BS8 1UG, UK E-mail: [email protected] SW or in a few cases into FW results in osmotic water Tel.: +44-117-9289181 influx facilitated by high branchial permeability (for Fax: +44-117-9288520 review see: Pang et al. 1977; Shuttleworth 1988; Evans 212 1993). In the most completely euryhaline species this anhydrase (Tufts and Perry 1998; Perry and Gilmour gain is managed so there is no resulting dilution anaemia 2002). The accompanying acidosis can be compensated (Piermarini and Evans 1998). In less euryhaline species for by a net increase in extracellular base (Maetz et al. net water gain occurs despite increases in glomerular 1976; Claiborne and Heisler 1984; Wood et al. 1984; filtration rates (GFRs) and urinary flow rates (UFRs) Claiborne et al. 2002; Choe and Evans 2003). Hyper- (Smith 1931a, 1931b; Goldstein and Forster 1971; capnic acidosis in fishes is compensated more slowly in ) Henderson et al. 1978) and the blood becomes diluted low salinity or in [HCO3 ]-deplete waters (Janssen and (for review see: Hickman and Trump 1969; Holmes and Randall 1975; Eddy et al. 1977; Heisler 1982, 1988; Donaldson 1969; Thorson et al. 1983; Shuttleworth Toews et al. 1983; Iwama and Heisler 1991; Choe and 1988; Evans 1993). The result can be lowered blood Evans 2003). Anaemia also reduces the non-bicarbonate haematocrit (Hct) and [Hb] of sharks (Goldstein and buffering capacity of the blood (Wood et al. 1979a, Forster 1971; Chan and Wong 1977b) including in H. 1979b) thus haemodilution and consequently lowered portusjacksoni (Cooper and Morris 1998a). Such anae- buffer capacity may have direct consequences for CO2 mia perturbs the acid–base and respiratory state of te- excretion. leosts (Wood et al. 1979b, 1982; Perry and Gilmour The acid–base response on transfer to a different 1993) but the acid–base responses of elasmobranchs are salinity is inextricably linked to both ion regulation, and not so well documented (e.g. Wood et al. 1994). ion regulation mechanisms (especially Na+ linked to There are almost no studies of the effect of salinity on H+ extrusion), and to maintenance of plasma volume. the blood acid–base status of marine elasmobranchs and Thus, the osmotic water influx and Na+ regulatory yet potentially this is an important aspect of their ability capacity are potentially major determinants of acid–base to penetrate into dilute water (e.g. Choe and Evans state. 2003). Teleosts moved from FW to higher salinity show Sub-adult Port Jackson sharks H. portusjacksoni are a relative metabolic acidosis (e.g. Maxime et al. 1990; distributed throughout the bays and lower estuaries of Claiborne et al. 1994), whereas those treated to the re- temperate coastal Australia (McLaughlin and OÕGower verse transfer to lower salinity show a relative metabolic 1970, 1971; Last and Stevens 1994), and are occasionally alkalosis (e.g. Madsen et al. 1996). A similar metabolic found in brackish waters up to 30 km from the sea. alkalosis correlated with living in FW has been described These sharks are not good regulators but nonetheless for the stingray Dasyatis sabina (Choe and Evans 2003). penetrate into estuaries. The osmotic and ionic status of The reasons for acid–base changes with salinity are H. portusjacksoni transferred to 50% SW appears to complex and unresolved but seem associated with come to a new equilibrium within 7 days (Cooper and changes in strong ion difference and differential ion Morris 1998a). H. portusjacksoni showed large declines uptake (Choe and Evans 2003). Marine elasmobranchs in plasma [Na+] and [Cl)], as well as [urea] and trim- are hypo-ionic with respect to SW and thus there is a ethylamine-N-oxide concentration ([TMAO]) and Hct, tendency for passive influx of ions. In contrast, elas- upon transfer to diluted SW (Cooper and Morris 1998a). mobranchs in FW must conserve and take up inorganic It seems possible that salinity-induced perturbations of ions from the water. Avoiding active ion uptake requires respiratory and acid–base state may contribute to lim- the fish to remain hypo-ionic to the water—effectively a iting the distribution of this shark into dilute SW. The strategy of conformation and with a lower limit that current study quantifies the changes in unidirectional does not allow penetration into FW. The strategy em- Na+ efflux and body Na+-status, together with changes ployed has implications for acid–base and respiratory in plasma fluid volume and volume management, and state. Of central importance is the management of Na+. examines these together with published data (Cooper There is debate as to the relative importance in elas- and Morris 1998a) as they may relate to maintenance of + + mobranchs of an apical Na /H exchanger (Piermarini CO2 transport and acid–base state in H. portusjacksoni and Evans 2001; Choe and Evans 2003) compared to an moving into 75% and 50% SW. apical V-ATPase-driven H+ excretion typical of teleosts in FW (Lin and Randall 1995; Wilson et al. 2000). + However, net H excretion promoting an internal Materials and methods alkalosis becomes more likely when the fish switch to + active Na uptake. Experimental design, blood sampling and acid–base measurements Lowered Hct of elasmobranch (Wood et al. 1994) and teleost fishes (Perry and Gilmour 1993; Gilmour and The acute ( £ 24 h) and chronic (up to 168 h) acid–base and CO2 Perry 1996) can reduce the rate of CO excretion (review: status of H. portusjacksoni transferred to diluted SW was deter- 2 mined using the experimental protocol described in Cooper and Tufts and Perry 1998). The mechanisms by which the Morris (1998a). Male and female Port Jackson sharks (0.7–2.0 kg) hypercapnia is compensated remain unclear. Elasmo- were caught by long-line off Bermagui, NSW and transported to branchs are unable to enhance CO2 excretion by in- Sydney Aquarium, Darling Harbour. Experimental sharks were transferred to the recirculating aquaria at the University of Sydney creased Hb-oxygenation since they lack a Haldane )1 effect but may be able to increase cardiac output without and acclimated in full-strength SW (33–35 g l ) maintained at 19.0±0.5 °C for 1 week prior to experimentation.
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