KEYWORDS: first feeding, plant ingredients, alevins, tongue sensing system, feeding behavior
Introduction
Taste perception is crucial for animals to detect nutrients and provide essential dietary information for growth and survival. In rainbow trout (Oncorhynchus mykiss ) alevins , early growth performance can be influenced by food intake, particularly when fed terrestrial ingredients that exclude fish meal and fish oil. Our study aimed to investigate the role of taste receptors in nutrient detection and the associated signaling pathways leading to central nervous system activation in the regulation of feeding behavior.
Material and Methods
We conducted a nutritional experiment from the first feeding through 30 days, comparing the performance of fish fed a commercial-like diet (C diet: a blend of fish meal, fish oil, and plant ingredients) with those on a 100% plant-based diet (V diet). After 5 and 30 days of feeding, fish were fasted for 16 hours and then re-fed with either the C or V diet, with sampling conducted at two time points: 20 minutes and 6 hours post-meal. We assessed the expression of nutrient-sensing genes related to fatty acids, amino acids, and sweetness, as well as taste receptor genes for different flavors . Additionally, we examined calcium signaling pathways in the tongue, focusing on indolamine and catecholamine pathways, alongside appetite-regulating neuropeptides in the brain and gut hormones in the intestinal system of the alevins.
Results
Results revealed that fish on the V diet experienced a decrease in body weight gain starting from day 10, which continued through to day 30. Changes in feed intake were also observed between days 0–10 and 21–30 after the first meal. In tongue tissue, after 5 days of feeding, fish on the C diet showed a slight upregulation of nutrient taste receptors, but not those related to flavor , along with a clear activation of the calcium signaling pathway. By day 30, there was a general upregulation of both nutrient and flavor taste receptors, although calcium signaling appeared less distinct in regulation. A significant dysregulation of the serotonin pathway, along with its degradation, was observed in the tongues of fish fed the V diet at both 5 and 30 days. Notably, for the first time in fish, catecholamine quantification levels in the tongue were identified as a potential marker for nutrient detection. Fish on the V diet showed a high quantification of L-DOPA after 5 days, which was markedly reduced by day 30. This impaired turnover of monoamines and catecholamines in the tongue may disrupt the tongue-brain axis, potentially contributing to the reduced food intake observed. This hypothesis was further supported by poorly regulated brain neuropeptides and intestinal hormones in fish fed the V diet after 30 days.
Conclusions
Together, these findings demonstrate that a plant-based diet disrupts the feeding response at an early stage, highlighting the heightened sensitivity of rainbow trout alevins’ tongue sensory systems to novel food sources during critical stages of development. Our study underscores the importance of early dietary influences on taste perception and the central regulation of feeding behavior in fish.
Acknowledgements: This research was funded by the French National Research Agency (grant no. ANR-21-CE20-0009-01 “FEEDOMEGA”).