School of BioSciences - Research Publications
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ItemTag use to monitor fish behaviour in aquaculture: a review of benefits, problems and solutions(WILEY, 2021-06)Abstract A variety of tagging techniques are now available to monitor fish behaviour, physiology and their environmental experience. Tagging is frequently used in aquaculture research to monitor free‐swimming individuals within farmed populations. However, for information gathered from tagged fish to be representative of farmed populations, tagging must not fundamentally affect fish behaviour, physiology or survival. Here, we systematically review studies that used tags to monitor farmed fish behaviour and test factors that affect tag retrieval and tag‐related mortality. Most studies using tags assessed movement and swimming behaviour in salmonids, predominantly in Europe and North America. Mortality of tagged fish was 10 times higher in sea‐cages (mean = 25%, range = 0–61.5%, n = 22 studies) than in tanks (mean = 2.5%, range = 0–17%, n = 23 studies), while mortality of tagged fish in sea‐cages was markedly higher in longer trials (from 4% in single day trials to 36% after 100 days). Higher‐than‐usual mortality rates among tagged fish, together with largely unknown sublethal effects on behaviour, should caution against using tagging studies to make decisions related to farm management. Moreover, key metrics such as mortality rates of tagged and untagged fish or evidence of sublethal effects are often unreported. We make several recommendations to improve future tagging studies and increase transparency in reporting. A greater insight into the causes of tagged fish mortality in sea‐cages is required to secure animal welfare and data validity in studies that use tags to assess fish behaviour in aquaculture.
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ItemSentinels in Salmon Aquaculture: Heart Rates Across Seasons and During Crowding Events(FRONTIERS MEDIA SA, 2021-11-26)Advances in tag technology now make it possible to monitor the behavior of small groups of individual fish as bioindicators of population wellbeing in commercial aquaculture settings. For example, tags may detect unusual patterns in fish heart rate, which could serve as an early indicator of whether fish health or welfare is becoming compromised. Here, we investigated the use of commercially available heart rate biologgers implanted into 24 Atlantic salmon weighing 3.6 ± 0.8 kg (mean ± SD) to monitor fish over 5 months in a standard 12 m × 12 m square sea cage containing ∼6,000 conspecifics. Post tagging, fish established a diurnal heart rate rhythm within 24 h, which stabilized after 4 days. Whilst the registered tagged fish mortality over the trial period was 0%, only 75% of tagged fish were recaptured at harvest, resulting in an unexplained tag loss rate of 25%. After 5 months, tagged fish were approximately 20% lighter and 8% shorter, but of the similar condition when compared to untagged fish. Distinct diurnal heart rate patterns were observed and changed with seasonal day length of natural illumination. Fish exhibited lower heart rates at night [winter 39 ± 0.2 beats per min (bpm), spring 37 ± 0.2 bpm, summer 43 ± 0.3 bpm, mean ± SE] than during the day (winter 50 ± 0.3 bpm, spring 48 ± 0.2 bpm, summer 49 ± 0.2 bpm) with the difference between night and day heart rates near half during the summer (6 bpm) compared to winter and spring (both 11 bpm). When fish experienced moderate and severe crowding events in early summer, the highest hourly heart rates reached 60 ± 2.5 bpm and 72 ± 2.4 bpm, respectively, on the day of crowding. Here, if the negative sublethal effects on fish that carry tags (e.g., growth rate) can be substantially reduced, the ability to monitor diurnal heart rate patterns across seasons and detect changes during crowding events, and using heart rate biologgers could be a useful warning mechanism for detecting sudden changes in fish behavior in sea cages.
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ItemFarmed salmonids drive the abundance, ecology and evolution of parasitic salmon lice in Norway(INTER-RESEARCH, 2021)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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ItemParasite management in aquaculture exerts selection on salmon louse behaviour(WILEY, 2021-08)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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ItemSalmon lice nauplii and copepodids display different vertical migration patterns in response to light(INTER-RESEARCH, 2021)Light is a fundamental environmental cue which influences the migration of many marine organisms. For the salmon louse Lepeophtheirus salmonis, light is believed to drive the diel vertical migration behaviour of their planktonic larvae. Salmon lice are of critical importance to the salmonid industry due to the damage they cause to wild and farmed hosts. Salmon lice larvae have an eyespot and are positively phototactic, yet how light intensity alters their vertical distribution remains unclear. Here, we tested how light intensity (0, 0.5, 10 and 80 µmol m-2 s-1), dispersal duration (1, 4 and 12 h) and release point (surface or bottom) influenced the vertical migration of salmon lice nauplii and copepodids under controlled conditions in experimental columns. Overall, higher light intensity increased the proportion of nauplii that aggregated at the surface. Copepodid behaviour differed from that of nauplii, as they swam upwards in both light and fully dark conditions, and surface aggregations increased with dispersal duration. Results from the experiments did not support the existing view that light strongly influences the vertical position of copepodids in the water column. Combined with previous work, our results reveal that salmon lice larval stages display different vertical responses to light, temperature and salinity, which may be explained by the different strategies of nauplii (maximise survival and dispersal) and copepodids (maximise host-finding success). Our results have implications for salmon lice dispersal models, where responses of copepodids and nauplii to light are currently parametrised by the same equations. Implementing stage-specific behaviours towards light may improve the outputs of dispersal models.
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ItemAcclimatisation with lice-infested salmon improves cleaner fish lice consumption(INTER-RESEARCH, 2021)Securing the welfare and maximising the lice removal efficacy of ~60 million cleaner fish used each year on salmonid farms is essential to develop a productive and ethical industry with low salmon lice Lepeophtheirus salmonis levels. We tested whether ballan wrasse Labrus bergylta welfare and lice consumption differed depending upon whether they were acclimatised in cages with either no Atlantic salmon Salmo salar, salmon without lice, or lice-infested salmon, prior to deployment in sea cages. After 1 wk, commercial densities of lice-infested salmon were stocked with the acclimatised wrasse in cages and kept for a further 3 wk. Each week, the number of lice on salmon was counted and a subset of wrasse was sampled for gut contents and physical welfare. Lice occurred less frequently in wrasse guts (6% of all dietary items) compared to caprellid amphipods (76%). Ballan wrasse consumed more lice if they were pre-exposed to lice-infested salmon (mean ± SE = 0.79 ± 0.4 lice) compared to wrasse not pre-exposed to salmon (0.15 ± 0.1 lice, p = 0.003) or wrasse pre-exposed to salmon without lice (0.01 ± 0.09 lice, p = 0.03). This did not affect overall mobile lice loads on salmon, which doubled over the study period regardless of acclimatisation strategy. Decline in condition factor (K) and the increase in specific physical damage over time were not affected by acclimatisation strategy. If welfare can be secured, acclimatisation could be tested on cleaner fish at commercial scales as a strategy to improve biological control agents.
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ItemChallenges and benefits of applying fish behaviour to improve production and welfare in industrial aquaculture(WILEY, 2021-03)Abstract An understanding of behaviour is used in zoos, laboratories and agriculture to reduce stressful aspects of the captive environment for animals. While fish are one of the most cultivated of all vertebrate groups, incorporating their behaviour into production management has proved elusive. Here, we evaluate the current evidence base relating to use of (i) innate behaviours of fish and (ii) their ability to learn new behaviours via human‐mediated training or through social learning, in fish farms. Studies that tested habituation and conditioning (training) as a tool to improve welfare demonstrate positive effects for improving fish welfare and coping capacity. However, methods solely reliant on innate behavioural responses to stimuli will always be imperfect, due to variation in individual responses which are often context dependent. To date, there has been no successful demonstration of social learning as a tool for aquaculture. While many experimental scale studies report promising results, few have translated to commercial scale, highlighting a mismatch between theoretical and practical use and cautions against extrapolation of results from small‐scale studies to commercial situations. While some promising evidence exists that fish behaviour can be integrated into farm management, logistical and scale‐related hurdles must be overcome before this can occur. We conclude that fish behaviour is an additional and currently under‐researched resource that could be integrated into farm practices to improve production and welfare in industrial aquaculture.
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ItemNo Preview AvailableEvolution of salmon lice in response to management strategies: a review(WILEY, 2021-06)Abstract 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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ItemAn overview of ecological traps in marine ecosystems(WILEY, 2021-05)Humans are altering marine ecosystems at unprecedented rates, and these changes can result in animals selecting poor‐quality habitats if the cues they use become misleading. Such “ecological traps” increase extinction risk, reduce ecosystem resilience, and are a consequence of human‐induced rapid environmental change. Although there is growing evidence for traps impacting terrestrial species, the phenomenon has so far received little attention from marine scientists. To explore why so few studies have attempted to identify traps in the ocean, we conducted a literature review of the major drivers of marine environmental change to determine how their impacts on habitat choice and species fitness are being assessed. From this we summarize the current evidence for marine traps, present case studies to show why the phenomenon is potentially common in the ocean, highlight ways to advance awareness and understanding of traps, and demonstrate how this information can help improve management of marine environments.