Annual dietary shifts of lumpfish (Cyclopterus lumpus) in salmonid sea cages detected by joint morphological and DNA metabarcoding stomach content analyses

Lumpfish ( Cyclopterus lumpus ) are commonly used as a cleaner fish in industrial salmonid sea cages as a biological control for the parasitic salmon louse ( Lepeophtheirus salmonis ) that infests Atlantic salmon ( Salmo salar ). Interannual differences in sea lice consumption by lumpfish may reflect changes in the availability of alternative wild prey, which can be influenced by sea water temperature and salinity. We used traditional morphological identification of diet contents and DNA metabarcoding on 187 ethanol preserved lumpfish stomachs that had been collected from industrial salmonid sea cages in southern Newfoundland, Canada, between August and November in 2018, 2020, and 2023. Both morphological and DNA metabarcoding revealed significant differences in lumpfish diet composition across sampling years. Morphological analysis showed that 2018 was high for caprellid amphipods, krill, and “other”; 2020 was high for formulated salmon pellets and for ctenophore/cnidarians; and 2023 was high for caprellid amphipods and salmon pellets. DNA metabarcoding confirmed morphologically-identified species and enabled identification of soft-bodied and quickly-digested prey items, such as the salmon louse, to the genus and species levels. PERMANOVAs analyses of DNA metabarcoding showed that year explained 15.7% of variance at the genus level and 10.4% variance at the species level. Generalized Additive Models (GAMs) explained 64–84% of the deviance in temperature and 37.4% of the deviance in salinity, indicating that consistent seasonal environmental trends differed significantly among the 3 years. Changes in temperature and salinity were associated with variation in lumpfish diets across the three years, but additional annual surveys are needed to understand the mechanism. The highest summer seawater temperatures at 5 m occurred in 2023, the year when company SCUBA divers reported unusually low lumpfish survival in late October, and when the diets of those that remained alive contained no wild Norwegian krill. We suggest that rising sea temperatures may reduce the suitability of lumpfish as cold-water cleaner fish in southern Newfoundland. The continued deployment of lumpfish may require sea cage designs that provide access to deeper, and cooler water refuges.