Seasonal changes in channel catfish thyroid hormones reflect increased magnitude of daily thyroid hormone cycles

Abstract

Channel catfish ( Ictalurus punctatus) in pond culture, sampled once per day, have been reported to exhibit significant seasonal cycles in the thyroid hormones thyroxine (T 4) and 3,5,3′-triiodothyronine (T 3), rising from levels generally below 2 ng/ml in January to above 8 ng/ml in July. To determine if daily thyroid hormone cycles underlie these seasonal changes, we blood sampled groups of 20 catfish (10 males and 10 females) in the morning (approx. 1 h after sunrise), midday, and evening (approx. 1.5 h before sunset) on January 9, April 4, and July 29. From January to July, pond temperatures rose from 7 ° to 32 °, associated with significant ( p < 0.05) increases in mean fish weight (from 477 to 1052 g) and in monthly mean food consumption (from 34 to 474.7 g/kg fish). On all three dates, significantly ( p < 0.05) greater levels of both hormones (except T 3 in April) were found in midday and evening compared to morning samples. In January, the daily change was small (from morning to midday, mean T 3 rose from 2.2 to 3.6 ng/ml and mean T 4 from 2.3 to 4.8 ng/ml), whereas in July it was considerably greater (from morning to evening, mean T 3 rose from 7.2 to 17.8 ng/ml, and T 4 from 9.0 to 22.4 ng/ml). No significant differences were found between midday and evening levels, or between males and females. Additionally, no seasonal phase-shifting of cycles was apparent. A subset of animals was examined to evaluate the potential contribution of peripheral mechanisms in generating these seasonal and daily cycles. Whereas we observed only minor changes in thyroid hormone binding to plasma proteins during any single day, a significant seasonal increase in the ratio of free T 4:free T 3 indices (from a mean of 1.3–1.5 in January to 2.0–2.1 in July) indicated enhanced T 3 binding by plasma proteins in July. Furthermore, in vitro hepatic T 4 and T 3 deiodination activities showed across dates no significant change in T 4 outer-ring deiodination to produce T 3 (ranging from a mean of 53.1 to 70.1 pmol T 4 deiodinated/h/mg microsomal protein), but a significant ( p < 0.05) decrease in T 4 inner-ring deiodination to degrade T 4 to 3,3′5′-triiodothyronine (from a mean in January of 2.4 to 0.65 pmol T 4 deiodinated /h/mg protein in April) and a significant ( p < 0.05) decrease in T 3 inner-ring deiodination to degrade T 3 to 3,3′-diiodothyronine (from a mean in January of 115.5 to 3.1 pmol T 4 deiodinated/h/mg protein in July). These results demonstrate that channel catfish under conditions of natural temperature and photoperiod exhibit robust daily cycles in total plasma T 4 and T 3 similar in magnitude to those reported for other fish species held under controlled laboratory conditions. These cycles maintain a similar phase throughout the year, indicating that apparent seasonal increases in thyroid hormones are not due to phase-shifting of daily cycles. However, seasonal studies sampling fish only in the morning would underestimate the magnitude of the annual changes in blood thyroid hormones. Thyroidal status, as judged from total plasma T 4 and T 3 levels in the afternoon, is greatest in July, coinciding with the postspawning peak in food consumption and growth. Enhanced T 3 plasma protein binding and a shift from predominantly hepatic inner-ring deiodination in winter to outer-ring deiodination in summer suggest that peripheral mechanisms contribute to the generation of these seasonal changes.