Parasites under pressure: salmon lice have the capacity to adapt to depth-based preventions in aquaculture

Coates, Andrew; Phillips, Ben L.; Oppedal, Frode; Bui, Samantha; Overton, Kathy; Dempster, Tim

doi:10.1016/j.ijpara.2020.05.009

Cited by 14 publications

(25 citation statements)

References 70 publications

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“…However, farmers may also intervene with barriers to infestation, including technologies to prevent encounters between lice and hosts in the surface layers where lice are most common, such as snorkel cages (Geitung et al 2019) and skirts (Grøntvedt et al 2018, Stien et al 2018, and behavioural manipulation of swimming depth using deep lights and feeding (Frenzl et al 2014). Swimming depth of the infectious copepodid larval stage varies among families (Coates et al 2020) and may have a genetic basis. If the vertical distribution of lice is influenced by heritable traits, then the increasing mean depth of available hosts could drive the evolution of lice larvae with deeper distributions.…”

Section: Host Availability and Host-finding Traitsmentioning

confidence: 99%

Farmed salmonids drive the abundance, ecology and evolution of parasitic salmon lice in Norway

Dempster¹,

Overton²,

Bui³

et al. 2021

Aquacult. Environ. Interact.

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Sea cage fish farming is typically open to the environment, with disease transmission possible between farmed and wild hosts. In salmonid aquaculture, salmon louse Lepeophtheirus salmonis infestations cause production losses, reduce welfare for farmed fish and increase infestation rates for wild fish populations. The high density of hosts in farms likely also shifts the coevolutionary arms race between host and parasite, with ecological and evolutionary consequences for the salmon louse. Using farm-reported salmon and louse abundances and publicly reported estimates of wild salmonid host abundances and the salmon lice they carry, we estimated (1) the relative abundance of farmed and wild salmonid hosts and (2) the relative importance of each for the abundance of salmon lice for the coastal zone of Norway from 1998 to 2017. Farmed hosts increased in importance over time with the expansion of the industry. From 2013 to 2017, farmed salmonids outnumbered wild salmonids by 267-281:1. By 2017, farmed salmonids accounted for 99.6% of available hosts and produced 99.1% of adult female salmon lice and 97.6% of mated (ovigerous) adult female salmon lice in Norwegian coastal waters. The persistent dominance of farmed hosts has clear implications: (1) management decisions that aim to limit lice abundance can be guided by lice data from farms alone, as lice on wild salmonids make a trivial contribution to the national lice population; and (2) strategies to prevent or treat lice infestations are vulnerable to the evolution of resistance, as the pool of wild hosts is inconsequential and will not act as a refuge large enough to stem the evolution of resistance. As the Norwegian salmon industry expands and salmon lice infestations continue, farmed salmon will drive the ecology and evolution of salmon lice.

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Section: Host Availability and Host-finding Traitsmentioning

confidence: 99%

Farmed salmonids drive the abundance, ecology and evolution of parasitic salmon lice in Norway

Dempster¹,

Overton²,

Bui³

et al. 2021

Aquacult. Environ. Interact.

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“…A family's tendency to either ascend or descend could mean the difference between passing around a 10 m skirt or snorkel (bypassing the cage) or passing underneath it (and infesting the cage), even when other hydrodynamic factors are involved. The strong patterns across related groups, and the absence of observed environmental or maternal effects, suggests a genetically inherited element to the vertical distribution of copepodids (Coates et al 2020). Such genetic variation has been observed in other planktonic crustaceans: Daphnia are stratified in the water according to genotype (Dumont et al 1985;De Meester 1993;King & Miracle 1995).…”

Section: Selection For Deeper Copepodid Distributionsmentioning

confidence: 99%

“…The strong patterns across related groups, and the absence of observed environmental or maternal effects, suggests a genetically inherited element to the vertical distribution of copepodids (Coates et al . 2020). Such genetic variation has been observed in other planktonic crustaceans: Daphnia are stratified in the water according to genotype (Dumont et al .…”

Section: Depth‐based Preventionsmentioning

confidence: 99%

Evolution of salmon lice in response to management strategies: a review

Coates

Phillips

Bui

et al. 2021

Reviews in Aquaculture

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Ectoparasitic salmon lice (Lepeophtheirus salmonis) present a major challenge to Atlantic salmon (Salmo salar) aquaculture. The demand for effective louse control has produced diverse management strategies. These strategies essentially impose novel selection pressures on parasite populations, driving the evolution of resistance. Here we assess the potential for salmon lice to adapt to current prevention and control methods. Lice have evolved resistance to at least four of five chemical therapeutants, and use of these chemicals has declined significantly in recent years. The industry has shifted to alternative non-chemical approaches, yet lice may adapt to these as well. Early research suggests that phenotypic variation exists in the louse population upon which non-chemical selection pressures could act and that this variation may have a genetic basis. From the existing evidence, as well as an examination of evolutionary processes in other relevant parasite and pest systems, we conclude that the evolution of non-chemical resistance is an emergent concern that must be considered by the industry. We recommend areas for focused research to better assess this risk. It is also important to determine whether phenotypic shifts in response to non-chemical selection may shift the ecological niche of the parasite, as this may have cascading effects on wild salmon populations. We also recommend further research to identify strategy combinations that have antagonistic selective effects that slow louse evolution and those with synergistic effects that should be avoided. Greater understanding of evolutionary processes can inform aquaculture policies that counteract the rise of resistant parasite populations.

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“…Differences were consistent when columns were pressurized to simulate the conditions found at a range of depths down to 10 m. Overall, higher pressures stimulated an increased frequency of upwards swimming, but the strength of this response varied strongly between families. There was no clear evidence of environmental or maternal effects accounting for this variation, pointing to at least some heritable component to vertical swimming behaviour in copepodids, although more research is needed to quantify this (Coates et al, 2020 ).…”

Section: Introductionmentioning

confidence: 99%

“…Assuming a genetic element to this behavioural variation, if depth‐based preventions select for louse copepodids that occur deeper in the water column (those that pass underneath barriers), adaptive responses are likely to ensue. To assess this possibility, it is first essential to determine whether the inter‐family variation observed in experimental columns (Coates et al, 2020 ) translates to differences in depth in the natural environment. Differences in the distribution of families might be diluted by the much larger scale of the natural water column or by environmental factors such as currents and salinity.…”

Section: Introductionmentioning

confidence: 99%

Parasite management in aquaculture exerts selection on salmon louse behaviour

Coates

Johnsen

Dempster

et al. 2021

Evolutionary Applications

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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.

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Parasites under pressure: salmon lice have the capacity to adapt to depth-based preventions in aquaculture

Cited by 14 publications

References 70 publications

Farmed salmonids drive the abundance, ecology and evolution of parasitic salmon lice in Norway

Farmed salmonids drive the abundance, ecology and evolution of parasitic salmon lice in Norway

Evolution of salmon lice in response to management strategies: a review

Parasite management in aquaculture exerts selection on salmon louse behaviour

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