Food availability, more than body temperature, drives correlated shifts in ATP-generating and antioxidant enzyme capacities in a population of intertidal mussels (Mytilus califomianus)

Intertidal organisms are exposed to a suite of fluctuating environmental variables, but the relative influences of these variables on physiology have rarely been disentangled. We examined spatial and temporal variation in the enzymatic capacities for ATP generation (malate dehydrogenase [MDH] and citrate synthase [CS]) and for detoxification of reactive oxygen species (superoxide dismutase [SOD] and catalase [CAT]) at four microsites within a single population of the California ribbed mussel Mytilus californianus (Conrad 1837) over a 5-day period. At both a wave-exposed, cooler location and a protected, warmer location, mussels lower in the intertidal zone had higher rates of CS, MDH, and SOD activity than individuals situated higher on the shore. Activities of CS, CAT, and SOD also tended to be lower at the protected than at the exposed location. We simultaneously monitored two environmental variables that might influence mussels' biochemical status. Body temperature was recorded in mussel mimics, and food availability was derived from in situ measurements of chlorophyll a concentration and wave heights, to estimate feeding periods at each microsite. Recent food availability dominates over thermal history (the amount of recent heating) in determining the biochemical capacities of these mussels over the time windows we examined (up to the past 64 h in 8 h increments). Activities of CS, MDH, and CAT were positively correlated with recent food availability at nearly all time windows. In contrast, only infrequently was thermal history negatively correlated with activities of CS (past 8 h and 64 h), CAT (past 16―24 h), and SOD (past 48―64 h). Opportunistic field sampling in the subsequent summer also showed that enzymatic activities align better with recent food availability than with recent thermal history. A controlled laboratory study confirmed that elevation of body temperature has no impact on the enzymes measured. In both laboratory and field experiments, there were strong positive correlations between enzymes that perform a related function (e.g., r = 0.667 between MDH and CS) as well as between the potential for ATP generation and the capacity to combat oxidative stress (e.g., 0.593 < r< 0.769 between CS and CAT). Activities of MDH, CS and SOD decreased with increasing body size (metabolic scaling effect). The finding that food availability supersedes body temperature in determining metabolic status highlights the importance of considering small-scale spatial and temporal variation in multiple environmental variables that might impinge upon physiological rates, particularly when conducting large-scale surveys.