Growth phenotype and environmental stress drive performance in field-cultured mussels (Mytilus galloprovincialis)

Understanding the physiological mechanisms driving growth variation in commercially important mussels (Mytilus galloprovincialis) under realistic field conditions is critical for optimising aquaculture production. While laboratory studies have identified differences in energy acquisition efficiency and metabolic rates as key factors influencing growth phenotypes, little is known about how these phenotypes develop under natural, variable trophic environments typical of intertidal aquaculture systems. In this study, two groups of 300 juvenile mussels (12.39 ± 0.87 mm) were transplanted to cages at low (L, < 1 m) and high (H, 2.5 m) intertidal zones on a breakwater. After six months, fast (F), intermediate (I) and slow (S) growing phenotypes were identified and subjected to feeding trials and measurements of energy balance, gill surface area and structure, and shell dry weight. At both tidal heights, slow growers exhibited lower gill cilia density and developed denser shells compared to fast growers. In the low intertidal zone, slow growers nearly matched fast growers in food acquisition and absorption but allocated more energy to somatic maintenance, including shell thickening, gonadal development, and antioxidant defences instead of growth. In contrast, at the high intertidal zone, growth differences were primarily driven by variation in energy acquisition rather than gill surface area. These findings challenge laboratory-derived models suggesting fast growers benefit from reduced metabolic rates and highlight the importance of environmental heterogeneity in shaping physiological strategies. The results have important implications for improving growth performance and sustainability in regional intertidal mussel aquaculture by accounting for context-dependent energy allocation and acquisition strategies. • Growth phenotypes emerge consistently under field aquaculture conditions. • High intertidal mussels show elevated metabolic costs and reduced growth. • Slow growers invest more energy in shell, gonads, and stress defences. • Fast growth in harsh conditions is linked to greater energy acquisition. • Gill surface area–growth link is context-dependent, not universal.