Parasite management in aquaculture exerts selection on salmon louse behaviour

Abstract

The evolution of pest resistance to management strategies is a major challenge for farmed systems. Mitigating the effects of pest adaptation requires identifying the selective pressures imposed by these strategies. In Atlantic salmon (Salmo salar) aquaculture, barriers are used to prevent salmon louse (Lepeophtheirus salmonis) larvae (copepodids) from entering salmon cages. These barriers are effective against shallow‐swimming copepodids, but those swimming deeper can pass underneath and infest salmon. Laboratory experiments suggest that depth regulation in copepodids is a variable behavioural trait with a genetic basis. We used biological–hydrodynamic dispersal models to assess how this trait variation alters the dispersion of lice through the ocean environment and into farms. The dispersal of copepodids with 3 behavioural phenotypes (deep, mean or shallow) was modelled over winter–spring and spring–summer periods in a Norwegian fjord system with intensive aquaculture. The infestation pressure of each phenotype on barrier cages was estimated from their modelled depth distributions: copepodids deeper than 10 m were predicted to successfully pass underneath barriers. The deep phenotype was the most abundant below 10 m and reached infestation pressures 3 times higher than that of the mean phenotype. In contrast, the shallow phenotype infestation pressure reached less than half that of the mean phenotype. These differences in relative fitness indicate that barriers can impose strong directional selection on the swimming behaviour of copepodids. The strength of this selection varied seasonally and geographically, with selection for the deep phenotype stronger in winter–spring and at coastal locations than in spring–summer and within fjords. These findings can be applied across farms to slow louse adaptation, by limiting barriers during situations of strong selection, although this must be balanced against trade‐offs to short‐term efficacy. More broadly, our study highlights new ways in which dispersal models can address evolutionary questions crucial for sustainable parasite management in aquaculture.

Evolutionary predictions for a parasite metapopulation: Modelling salmon louse resistance to pest controls in aquaculture

“…Using a limited number of treatments focused on key farm sites (Samsing et al., 2019) may be the most cost‐effective approach for suppressing lice across the entire region. The efficacy of some louse management strategies is affected by environmental conditions such as temperature and salinity (Coates, Johnsen, et al., 2021; Oldham, 2023). The success of a strategy at controlling lice across a farm network may therefore depend on the location and the season at which it is applied (Barrett, Overton, et al., 2020).…”

Research pre-empting parasite adaptation is key to sustainable disease management in aquaculture

“…With an open mind and a grasp of evolutionary principles, useful parallels can be drawn from surprising sources: e.g. the potential for lice to adapt to depth-based barriers through a phenotypic shift in swimming depth (Coates et al 2021b) bears a striking resemblance to the adaptation of non-parasitic crustaceans in response to predation (Gliwicz 1986, De Meester 1996, Cousyn et al 2001.…”

Innovation in the Norwegian aquaculture industry

“…50 As is too often the case when treatment is the attempted solution to a regularly occurring health issue, resistance start to develop. 34,51,52 As such, the industry is currently using a host of approaches including chemical treatments, feed additives and cleaner fish. While feed additives and cleaner fish may have some prevention effect, effective prevention remains elusive.…”

“…A number of approaches have also been developed to treat against salmon lice 50 . As is too often the case when treatment is the attempted solution to a regularly occurring health issue, resistance start to develop 34,51,52 . As such, the industry is currently using a host of approaches including chemical treatments, feed additives and cleaner fish.…”