Contrasting Aquaculture Systems Shape Distinct Growth and Short-Term Stress-Resistance Trait Clusters in the Red Swamp Crayfish

This study investigated whether these contrasting environments are associated with the development of coherent, organism-wide phenotypic–physiological syndromes reflecting a fundamental life-history trade-off. A controlled 60-day trial was conducted comparing crayfish from a high-input pond system (fed to satiation) and a low-input rice paddy system (primarily natural diet). Pond crayfish were fed a commercial formulated feed twice daily to satiation (approximately 3% of biomass per day). Rice paddy crayfish primarily consumed natural food webs and received a once-daily supplement of 30% of the pond feed amount (approximately 0.9% of biomass per day). Results revealed two distinct syndromes. Pond-cultured crayfish exhibited a growth-oriented syndrome: they were 33% heavier with a compact, volumetrically enhanced body shape, coupled with elevated lipid-anabolic enzyme activities (lipase and ACC), higher hemolymph protein and cholesterol concentrations, but also significantly increased levels of a stress-related endocrine factor (cortisol-like immunoreactivity) and oxidative damage (MDA). Conversely, rice paddy-cultured crayfish displayed a stress-resistance-oriented syndrome: a streamlined, deeper-abdomen morphology, fortified antioxidant (SOD, CAT, and GST) and immune (lysozyme and phenoloxidase) capacities, enhanced carbohydrate digestion (amylase), and lower systemic stress. Transcriptomic analysis showed that the hepatopancreas of paddy-cultured crayfish was enriched in pathways related to lipid metabolism, detoxification, and endocrine regulation, notably with upregulation of the SULT1E1 gene. Our findings demonstrate that the distinct environmental and nutritional conditions of each aquaculture system are linked to specific multi-level adaptation syndromes, presenting a clear trade-off between rapid biomass production and systemic stress resistance (within the 60-day trial period), providing a mechanistic basis for optimizing sustainable practices: integrated systems enhance stock robustness, while intensive systems require strategies to mitigate physiological load.