School of BioSciences - Research Publications

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    Tag use to monitor fish behaviour in aquaculture: a review of benefits, problems and solutions
    Macaulay, G ; Warren-Myers, F ; Barrett, LT ; Oppedal, F ; Fore, M ; Dempster, T (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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    Sentinels in Salmon Aquaculture: Heart Rates Across Seasons and During Crowding Events
    Warren-Myers, F ; Hvas, M ; Vagseth, T ; Dempster, T ; Oppedal, F (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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    Sterilization of sea lice eggs with ultraviolet C light: towards a new preventative technique for aquaculture
    Barrett, LT ; Pert, CG ; Bui, S ; Oppedal, F ; Dempster, T (JOHN WILEY & SONS LTD, 2020-03)
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    Farmed salmonids drive the abundance, ecology and evolution of parasitic salmon lice in Norway
    Dempster, T ; Overton, K ; Bui, S ; Stien, LH ; Oppedal, F ; Karlsen, O ; Coates, A ; Phillips, BL ; Barrett, LT (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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    Parasite management in aquaculture exerts selection on salmon louse behaviour
    Coates, A ; Johnsen, IA ; Dempster, T ; Phillips, BL (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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    Salmon lice nauplii and copepodids display different vertical migration patterns in response to light
    Szetey, A ; Wright, DW ; Oppedal, F ; Dempster, T (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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    Acclimatisation with lice-infested salmon improves cleaner fish lice consumption
    Gentry, K ; Bui, S ; Oppedal, F ; Bjelland, R ; Nola, V ; Dempster, T (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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    Challenges and benefits of applying fish behaviour to improve production and welfare in industrial aquaculture
    Macaulay, G ; Bui, S ; Oppedal, F ; Dempster, T (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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    Prevention not cure: a review of methods to avoid sea lice infestations in salmon aquaculture
    Barrett, LT ; Oppedal, F ; Robinson, N ; Dempster, T (WILEY, 2020-11-01)
    The Atlantic salmon aquaculture industry still struggles with ectoparasitic sea lice despite decades of research and development invested into louse removal methods. In contrast, methods to prevent infestations before they occur have received relatively little research effort, yet may offer key benefits over treatment‐focused methods. Here, we summarise the range of potential and existing preventative methods, conduct a meta‐analysis of studies trialling the efficacy of existing preventative methods and discuss the rationale for a shift to the prevention‐focused louse management paradigm. Barrier technologies that minimise host–parasite encounter rates provide the greatest protection against lice, with a weighted median 76% reduction in infestation density in cages with plankton mesh ‘snorkels’ or ‘skirts’, and up to a 100% reduction for fully enclosed cages. Other methods such as geographic spatiotemporal management, manipulation of swimming depth, functional feeds, repellents and host cue masking can drive smaller reductions that may be additive when used in combination with barrier technologies. Finally, ongoing development of louse‐resistant salmon lineages may lead to long‐term improvements if genetic gain is maintained, while the development of an effective vaccine remains a key target. Preventative methods emphasise host resistance traits while simultaneously reducing host–parasite encounters. Effective implementation has the potential to dramatically reduce the need for delousing and thus improve fish welfare, productivity and sustainability in louse‐prone salmon farming regions.
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    Plio-Pleistocene sea-level changes drive speciation of freshwater fishes in north-western Australia
    Shelley, JJ ; Swearer, SE ; Dempster, T ; Adams, M ; Le Feuvre, MC ; Hammer, MP ; Unmack, PJ (WILEY, 2020-08)
    AIM: Despite the influence of sea‐level changes on biogeographic/phylogeographic patterns in freshwater ecosystems being well documented, studies that explicitly link the influence of sea‐level change with speciation are rare. We aim to test the hypothesis that sea‐level changes during the Pliocene and Pleistocene have driven speciation in north‐western Australia's (NWA’s) largest freshwater fish family, Terapontidae, building upon a body of evolutionary literature focussed on the family. LOCATION: North‐western Australian rivers including those draining the Kimberley Plateau. TAXON: Grunters (Family: Terapontidae, Genera: Hannia, Hephaestus, Leiopotherapon, Syncomistes). METHODS: A GIS was used to reconstruct palaeodrainages during lowered sea levels and to delineate regions of high connectivity during low and high (current) sea‐level conditions. For seven species, the degree of phylogenetic divergence among river basins in different regions was evaluated using a maximum likelihood phylogeny and analyses of the proportion of genetic divergence expressed with 601 base pairs of the mtDNA cytochrome b (cytb) gene. RESULTS: A low proportion of cytb haplotypes were shared among catchments not connected by the same receiving waters (e.g. estuaries) under current (high) sea levels, indicating that contemporary dispersal is limited over fine spatial scales. Deeper phylogeographic patterns were largely congruent with reconstructed low sea‐level (LSL) drainage arrangements indicating that historic among‐catchment connectivity was far more widespread under LSL conditions. MAIN CONCLUSIONS: The NWA landscape represents a geographic template that has shaped patterns of broad dispersal under low sea levels, and fine‐scale isolation under high sea levels. The weight of evidence from recent literature on species boundaries and evolutionary patterns within the terapontids suggests that most NWA species were derived rapidly and recently from a series of spatio‐temporal vicariant events caused by such sea‐level fluctuations during the late Pliocene and Pleistocene. Together, the findings provide a rare, comprehensively tested example of sea‐level change driving speciation in the tropics.