Effects of size, age and photoperiod on hypoosmoregulation in brook trout, Salvelinus fontinalis

Abstract

Brook trout (Salvelinus fontinalis) raised from eggs under two photoperiod and two feeding regimes were tested for physiological changes preparatory for transition from freshwater to seawater. Size, age, growth rate, photoperiod, and diel rhythms were examined for possible influences on plasma osmolarity, [Na+], [Cl-], [K+], [Mg2+], thyroxine concentration, hematocrit, and gill Na+,K+-ATPase activity of brook trout in freshwater. Significant diel cycles were found in plasma osmolarity, (Na+] and thyroxine concentration. Significant size and/or age related changes occurred for plasma osmolarity, [Na+], [K+] and hematocrit, but could explain little of their total variation (0.02 < r2 <0.18). A sexually dimorphic response to photoperiod was observed in hematocrit for both mature and immature fish, with hematocrit of mature females declining in autumn and hematocrit of immature males increasing in autumn. Gill Na+,K+-ATPase activity did not respond to photoperiod or feeding treatment and showed no change with size or age. Plasma thyroxine levels responded to feeding and photoperiod treatment. There was a significant correlation between the percent mean difference in plasma thyroxine and the mean difference in growth rate between high and low feed fish (r2 = 0.51), suggesting a relationship between thyroxine and growth. In 11 experiments over 1.5 yrs, brook trout were gradually exposed to 32 ppt seawater for 20 d to investigate the ontogeny of salinity tolerance. A single experiment examined daily changes in plasma osmolarity, [Na+], [Cl-], [K+], [Mg2+], thyroxine, hematocrit and gill Na+,K+-ATPase during adaptation to 10 ppt, 20 ppt and 32 ppt. Size was the primary determinant of seawater survival (r2 = 0.77); the effect of size on seawater survival slowed after fish reached a fork length of 14 cm. The effect of age on seawater. survival (r2 = 0.65) was through its covariance with size. Photoperiod affected seawater survival only through its influence on the timing of male maturation, which decreased salinity tolerance. Hypoosmoregulation of plasma osmolarity, [Na+], [Cl-], [K+], [Mg2+] and hematocrit increased linearly with size over the entire range of sizes (6-32 cm). Gill Na+,K+-ATPase activity after 20 d in seawater decreased with increasing size of brook trout, possibly reflecting decreased demand for active ion transport in larger fish. Plasma thyroxine concentrations generally declined in seawater, but no definitive role of this hormone in seawater adaptation was found. Size dependent survival and osmoregulatory ability of brook trout is compared to other salmonids and a conceptual model is developed. Decreased salinity tolerance and hypoosmoregulatory ability was found in mature male brook trout and was not found in females or immature males. Lowered salinity tolerance of adult males becomes acute during autumn photoperiod when normal spawning occurs. Plasma [Cl-], [Mg2+], osmolarity and hematocrit are significantly higher in mature males after transfer to seawater, relative to mature females. It is postulated that reduced adult male hypoosmoregulatory ability explains skewed sex ratios in anadromous populations, limits the extent of anadromy, and was a significant phase in the evolution of extended salmonid migration. Anadromous brook trout of Riviere a la Truite, Quebec, were examined for physiological changes associated with salmonid smoltification, and compared to non-anadromous brook trout of the Matamek River. There were no significant differences in plasma thyroxine concentration, gill Na+,K+-ATPase activity, hematocrit or osmoregulatory ability of anadromous and non-anadromous brook trout. Moisture content was significantly different between fish from the two river systems, but had the same pattern of declining moisture content as summer progressed. Silver coloration of brook trout in Riviere a la Truite was significantly associated with larger fish and higher gill Na+,K+-ATPase activity, but not with changes in plasma thyroxine, moisture content, hematocrit or condition factor. Silver coloration was absent in Matamek River brook trout. Brook trout at high salinity estuarine sites had significantly greater gill Na+,K+-ATPase activity and hypoosmoregulatory ability than brook trout at low salinity sites. Atlantic salmon (Salmo salar) in high salinity estuarine sites had significantly higher plasma thyroxine and gill Na+,K+-ATPase activity than brook trout. The results indicate that smoltification is relatively undeveloped in brook trout and that estuarine residence is important in salinity adaptation and eventual seaward migration.