Seasonal changes in channel catfish thyroid hormones reflect increased magnitude of daily thyroid hormone cycles
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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 (T4) and 3,5,3-triiodothyronine (T3), rising from levels generally below 2ng/ml in January to above 8ng/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. 1h after sunrise), midday, and evening (approx. 1.5h 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 1052g) and in monthly mean food consumption (from 34 to 474.7g/kg fish). On all three dates, significantly (p < 0.05) greater levels of both hormones (except T3 in April) were found in midday and evening compared to morning samples. In January, the daily change was small (from morning to midday, mean T3 rose from 2.2 to 3.6ng/ml and mean T4 from 2.3 to 4.8ng/ml), whereas in July it was considerably greater (from morning to evening, mean T3 rose from 7.2 to 17.8ng/ml, and T4 from 9.0 to 22.4ng/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 T4:free T3 indices (from a mean of 1.3-1.5 in January to 2.0-2.1 in July) indicated enhanced T3 binding by plasma proteins in July. Furthermore, in vitro hepatic T4 and T3 deiodination activities showed across dates no significant change in T4 outer-ring deiodination to produce T3 (ranging from a mean of 53.1 to 70.1pmol T4 deiodinated/h/mg microsomal protein), but a significant (p < 0.05) decrease in T4 inner-ring deiodination to degrade T4 to 3,35-triiodothyronine (from a mean in January of 2.4 to 0.65pmol T4 deiodinated /h/mg protein in April) and a significant (p < 0.05) decrease in T3 inner-ring deiodination to degrade T3 to 3,3-diiodothyronine (from a mean in January of 115.5 to 3.1pmol T4 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 T4 and T3 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 T4 and T3 levels in the afternoon, is greatest in July, coinciding with the postspawning peak in food consumption and growth. Enhanced T3 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. 2006 Elsevier B.V. All rights reserved.
