Acclimation temperature and parasite infection drive metabolic changes in a freshwater fish at different biological scales

Abstract

Environmental stressors such as elevated temperature and parasite infection can impact individual energy metabolism. However, organismal responses to co‐occurring stressors and their effects across biological scales remain unexplored despite the importance of integrative studies for accurately predicting the resilience of natural populations in changing environments. Using wild‐caught, naturally parasitized pumpkinseed sunfish, Lepomis gibbosus, we quantified changes in cellular and whole‐organism metabolism in response to temperature and parasite infection. We acclimated pumpkinseeds for 3 weeks at 20°C, 25°C or 30°C before measuring whole‐organism oxygen uptake (ṀO2) using intermittent flow‐respirometry to quantify maximal and standard metabolic rates (MMR and SMR, respectively) and aerobic scope (AS). We also measured the maximal activity of enzymes [citrate synthase (CS), respiratory complexes I + III and IV of the electron transport system and lactate dehydrogenase (LDH)] linked with cellular bioenergetics in fish heart, brain, spleen and gills using spectrophotometry. We found no interactions between acclimation temperatures and parasite intensity on cellular or whole‐organism metabolism. However, both stressors were independently related to fish metabolism, with differing impacts across biological scales. Whereas MMR increased with acclimation temperature, this was not mirrored by increasing SMR or decreasing AS, suggesting thermal compensation across acclimation temperatures at the whole‐organism level. On a cellular level, acclimation responses were similar across organs, with maximal activity of all enzymes decreasing with increasing acclimation temperature. However, LDH activity remained higher than aerobic enzyme activities (CS, ETS complexes I + III and IV) across acclimation temperatures and organs, especially in gills, where LDH activity drastically increased at 30°C. This may indicate a stronger reliance on anaerobic metabolism to sustain whole‐organism metabolic performance at high temperatures. Fish with greater trematode infection had lower MMR. There were no relationships between parasite intensity and SMR, AS or maximal enzyme activity. Our work shows that co‐occurring stressors have distinct impacts on fish metabolism: parasites are primarily related to whole‐organism metabolism while temperature impacts metabolism across biological scales. This highlights that interactions among co‐occurring stressors are important for ecological realism and accurate predictions regarding population resilience to environmental changes. Read the free Plain Language Summary for this article on the Journal blog.