Abstract
In fish models, seasonal change in feeding is under the influence of water temperature. However, the effects of temperature on appetite control can vary among fish species and the mechanisms involved have not been fully characterized. Using goldfish (Carassius auratus) as a model, seasonal changes in feeding behavior and food intake were examined in cyprinid species. In our study, foraging activity and food consumption in goldfish were found to be reduced with positive correlation to the gradual drop in water temperature occurring during the transition from summer (28.4 ± 2.2°C) to winter (15.1 ± 2.6°C). In goldfish with a 4-week acclimation at 28°C, their foraging activity and food consumption were notably higher than their counterparts with similar acclimation at 15°C. When compared to the group at 28°C during summer, the attenuation in feeding responses at 15°C during the winter also occurred with parallel rises of leptin I and II mRNA levels in the liver. Meanwhile, a drop in orexin mRNA along with concurrent elevations of CCK, MCH, POMC, CART, and leptin receptor (LepR) transcript expression could be noted in brain areas involved in feeding control. In short-term study, goldfish acclimated at 28°C were exposed to 15°C for 24 h and the treatment was effective in reducing foraging activity and food intake. The opposite was true in reciprocal experiment with a rise in water temperature to 28°C for goldfish acclimated at 15°C. In parallel time-course study with lowering of water temperature from 28 to 15°C, short-term exposure (6–12 h) of goldfish to 15°C could also increase leptin I and II mRNA levels in the liver. Similar to our seasonality study, transcript level of orexin was reduced along with up-regulation of CCK, MCH, POMC, CART, and LepR gene expression in different brain areas. Our results, as a whole, suggest that temperature-driven regulation of leptin output from the liver in conjunction with parallel modulations of orexigenic/anorexigenic signals and leptin responsiveness in the brain may contribute to the seasonal changes of feeding behavior and food intake observed in goldfish.
Highlights
Temperature change in the environment is a key factor known to affect energy metabolism [1] and body growth in animals [2], and these modulatory effects are partly mediated via regulation of food intake [3]
The results of our study have provided new information on the mechanisms for feeding control by temperature change in the environment which may contribute to the seasonal cycle of food intake observed in goldfish
In goldfish subjected to seasonal change in temperature during the transition from summer to winter, except for a lack in response for incomplete feeding/food spitting activity, the cumulative counts for feeding behaviors, including complete feeding/surface foraging and bottom feeding/ bottom foraging, were found to be reduced gradually from the summer (Jul–Aug, 2016), autumn (Sept–Oct, 2016), early-mid phase of the winter (Nov–Dec, 2016) to the peak phase of winter (Jan–Feb, 2017) (Figure 2A)
Summary
Temperature change in the environment is a key factor known to affect energy metabolism [1] and body growth in animals [2], and these modulatory effects are partly mediated via regulation of food intake [3]. Central expression of orexigenic/anorexigenic signals modified by temperature change has been documented in fish models, e.g., up-regulation of ghrelin in the brain of Chinese perch (Siniperca chuatsi) by temperature rise [12] and elevation of CART expression in the hypothalamus of Atlantic cod (Gadus morhua) by low temperature [6], a recent study in Arctic charr (Salvelinus alpinus) has revealed that the seasonal changes of NPY, AgRP, POMC, CART, and leptin expressed in brain areas involved in feeding control did not correlate with the annual cycle of feeding reported in the species [13]. No consensus has been reached regarding the functional role of orexigenic/anorexigenic signals within the central nervous system (CNS) in the circannual rhythm of feeding observed in fish species
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