research topics in fish biology

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Fisheries articles from across Nature Portfolio

Fisheries are social, biological and geographical objects involved in producing fish for human consumption. They are usually united by a common geographical area, catch technique and/or target species, and fisheries science is the study of factors affecting catch and stock sustainability.

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Ultrastructural examination of cryodamage in Paracentrotus lividus eggs during cryopreservation

• J. Troncoso

Anchovy boom and bust linked to trophic shifts in larval diet

A characteristic of costal-pelagic fishes is their large population size fluctuations, yet the drivers remain elusive. Here, the authors analyze a 45-year timeseries of nitrogen stable isotopes measured in larvae of Northern Anchovy and find that high energy transfer efficiency from the base of the food web up to young larvae confers high survival and recruitment to the adult population.

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Nursery origin of yellowfin tuna in the western Atlantic Ocean: significance of Caribbean Sea and trans-Atlantic migrants

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• R. J. David Wells

Shark teeth zinc isotope values document intrapopulation foraging differences related to ontogeny and sex

Sex- and ontogeny-related differences in diet and habitat use of endangered sand tiger sharks from Delaware Bay revealed by analysis of shark teeth zinc isotope values.

• Jeremy McCormack
• Molly Karnes
• Sora L. Kim

Artificial reefs reduce the adverse effects of mud and transport stress on behaviors of the sea cucumber Apostichopus japonicus

• Fangyuan Hu
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Inferring the ecology of north-Pacific albacore tuna from catch-and-effort data

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Seafood access in Kiribati

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Climate policy must integrate blue energy with food security

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Forecast warns when sea life will get tangled in nets — one year in advance

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With the arrival of El Niño, prepare for stronger marine heatwaves

Record-high ocean temperatures, combined with a confluence of extreme climate and weather patterns, are pushing the world into uncharted waters. Researchers must help communities to plan how best to reduce the risks.

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Rethinking the effect of marine heatwaves on fish

Marine heatwaves are on the rise. A surprising result from the analysis of data for fish populations in Europe and North America could change ways of thinking about the ecological consequences of such events.

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Shark culling at a World Heritage site

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Ichthyological Research

• The official journal of the Ichthyological Society of Japan.
• Covers all aspects of fish biology, including taxonomy, systematics, evolution, biogeography, ecology, ethology, genetics, morphology, and physiology.
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Use of stable isotopes to document lake to stream movements of brook charr salvelinus fontinalis : a case study from southern lake superior.

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The hammerhead shark's cephalofoil reduces fluid moments during turning motion

• Yunosuke Obayashi
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The upper limit of redd abundance compared to the numbers of anadromous adult masu salmon in Horokashubuto Stream, Hokkaido, northern Japan

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The Journal of Fish Biology

The Journal of Fish Biology  is the Society's official journal, and is a leading international, peer-reviewed journal publishing high-quality papers focusing on the biology of finfish in all aquatic ecosystems: marine, estuarine and fresh water. In 2008, The Journal of Fish Biology was ranked amongst the 100 most influential journals of Biology & Medicine over the last 100 years. 

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The Journal of Fish Biology brings together, under one cover, an overall picture of current research and provides a means of international communication among researchers across many disciplines with a common interest in the biology of fish. Topics covered include: Aquaculture, Behaviour, Biochemistry, Diseases, Distribution, Ecology, Genetics, Growth, Immunology, Migration, Molecular and cell science, Morphology, Parasitology, Physiology, Pollution impacts, Population studies, Reproduction, Taxonomy, and Toxicology.

Each volume of the  Journal of Fish Biology  consists of six issues. Generally a volume comprises five regular issues and one Special Issue (the proceedings of the annual FSBI Symposium and one other special topic). Occasionally a regular issue may be replaced by a Special Issue. There are two volumes per year.

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The effects of climate change on the ecology of fishes

Roles Conceptualization, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Writing – original draft, Writing – review & editing

* E-mail: [email protected]

Affiliation Southern Seas Ecology Laboratories, School of Biological Sciences, The University of Adelaide, Adelaide, Australia

Roles Writing – original draft, Writing – review & editing

Affiliation Department of Marine Science, University of Otāgo, Dunedin, New Zealand

Affiliation Fish Ecology Lab, School of Life Sciences, University of Technology Sydney, Sydney, Australia

Affiliations ARC Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, Australia, College of Science and Engineering, James Cook University, Townsville, Australia

Affiliation Institute for Marine and Antarctic Studies, University of Tasmania, Hobart, Australia

Affiliations ARC Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, Australia, Marine Climate Change Unit, Okinawa Institute of Science and Technology Graduate University (OIST), Tancha, Onna-son, Okinawa, Japan

Affiliation Evolution & Ecology Research Centre, Centre for Marine Science and Innovation, School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney, Australia

Roles Formal analysis, Investigation, Visualization, Writing – original draft, Writing – review & editing

• Ivan Nagelkerken, 
• Bridie J. M. Allan, 
• David J. Booth, 
• Jennifer M. Donelson, 
• Graham J. Edgar, 
• Timothy Ravasi, 
• Jodie L. Rummer, 
• Adriana Vergés, 
• Camille Mellin

Published: August 7, 2023

• https://doi.org/10.1371/journal.pclm.0000258
• Reader Comments

Ocean warming and acidification are set to reshuffle life on Earth and alter ecological processes that underpin the biodiversity, health, productivity, and resilience of ecosystems. Fishes contribute significantly to marine, estuarine, and freshwater species diversity and the functioning of marine ecosystems, and are not immune to climate change impacts. Whilst considerable effort has been placed on studying the effects of climate change on fishes, much emphasis has been placed on their (eco)physiology and at the organismal level. Fishes are affected by climate change through impacts at various levels of biological organisation and through a large variety of traits, making it difficult to make generalisations regarding fish responses to climate change. Here, we briefly review the current state of knowledge of climate change effects on fishes across a wide range of subfields of fish ecology and evaluate these effects at various scales of biological organisation (from genes to ecosystems). We argue that a more holistic synthesis of the various interconnected subfields of fish ecology and integration of responses at different levels of biological organisation are needed for a better understanding of how fishes and their populations and communities might respond or adapt to the multi-stressor effects of climate change. We postulate that studies using natural analogues of climate change, meta-analyses, advanced integrative modelling approaches, and lessons learned from past extreme climate events could help reveal some general patterns of climate change impacts on fishes that are valuable for management and conservation approaches. Whilst these might not reveal many of the underlying mechanisms responsible for observed biodiversity and community change, their insights are useful to help create better climate adaptation strategies for their preservation in a rapidly changing ocean.

Citation: Nagelkerken I, Allan BJM, Booth DJ, Donelson JM, Edgar GJ, Ravasi T, et al. (2023) The effects of climate change on the ecology of fishes. PLOS Clim 2(8): e0000258. https://doi.org/10.1371/journal.pclm.0000258

Editor: Wei Yu, Shanghai Ocean University, CHINA

Copyright: © 2023 Nagelkerken et al. This is an open access article distributed under the terms of the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Funding: IN, DJB, and TR were supported by an ARC Discovery grant (DP230101932), TR and IN were supported by an OIST KICKS Grant Scheme. CM and JMD were supported by ARC Future Fellowships (FT200100870 and FT190100015). JLR was supported by the ARC Centre of Excellence for Coral Reef Studies. AV was supported by an ARC Discovery grant (DP190102030). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Competing interests: The authors have declared that no competing interests exist.

Introduction

Anthropogenic climate change is affecting a wide range of species and ecosystems across the globe [ 1 ]. Yet, our ability to accurately predict the structure and functioning of near-future biological communities and ecosystems in the Anthropocene remains limited. This is partly due to the diversity of individual species’ responses linked to their different life histories, environmental tolerances, phenotypic plasticity, and scope for genetic adaptation. Furthermore, upscaling species-specific responses to climate stressors across higher levels of biological organisation (such as populations, communities, and ecosystems) has proven challenging [ 2 ]. This is partly due to the inherently complex intra- and interspecies ecological interactions that vary in space and time and are often difficult to quantify or forecast [ 3 ]. Interactive effects of multiple environmental stressors further complicate accurate predictions of future impacts, as they can have synergistic as well as antagonistic effects [ 4 ]. We urgently need to better understand and predict how global change will affect fish species at higher levels of biological organisation such as communities and ecosystems.

Bony and cartilaginous fish species span a total of > 35,000 species globally [ 5 ], make up over half of all vertebrates on the planet, and perform key ecosystem functions, such as food production, maintenance of biodiversity, recycling and transport of nutrients, and sustaining ecosystem resilience [ 6 ]. They have a global distribution spanning from the equator to the poles, occur in the ocean as well as estuaries and freshwater systems, and can be found from intertidal habitats to the abyss. Fishes not only show strong responses to changes in their abiotic environment (e.g., salinity, pH, temperature, oxygen) [ 7 ], but also to their biotic environment [ 8 ]. The latter includes strong interactions with their habitat (especially for demersal species) and a wide range of positive and negative species interactions, such as competition, predation, grazing, parasitism, symbiosis, and disease. Their trophic interactions mediate energy flow within food webs and regulate biodiversity, productivity, and ecosystem stability [ 9 ]. Climate-driven alterations in fish communities and populations can thus have wide-reaching effects on the health and biodiversity of the ocean, on marine ecosystem functioning, as well as on humans through altered ecosystem services [ 10 , 11 ].

Predicting fish population and community responses to climate change requires a holistic consideration of the many processes and levels of biological organisation that regulate ecological interactions, behaviours, physiological performance, adaptive capacity, and fitness of fishes. Despite the breadth of the field of fish ecology, to date, we have predominantly gained insights into specific subfields of fish ecology, in particular warming effects on the physiology of individual fish species (Figs 1 and 2 , S1 Table ). Ocean acidification effects have also received considerable attention, although the empirical evidence for this stressor appears lower than that for warming effects ( Fig 1A ), even though this stressors is often considered in literature reviews ( Fig 2A ). The potential effects of hypoxia as a climate stressor on fishes remain severely understudied. Studies of climate impacts on fishes that link multiple climate stressors (e.g. warming, acidification, hypoxia and/or others), or that link multiple subfields of fish ecology (e.g. linking genetics, behaviour, physiology, community dynamics, and spatial ecology) are crucially lacking. These are important because fishes can acclimatise to changing abiotic conditions such as increased water temperature [ 12 ], compensate for biotic changes (e.g., ecological trade-offs) [ 13 ], move to escape unsuitable climates [ 14 ], alter gene expression associated with critical processes within generations [ 15 ], or genetically adapt across generations [ 16 ]. Moreover, most climate impact assessments on fishes have been performed at the organismal level, with still very little knowledge of climate effects on populations and communities (Figs 1B and 2B ).

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(A) Results from a quantitative literature review on published meta-analyses on the effects of climate change stressors on fishes. (A) Cumulative number of meta-analyses published over time, split for the various climate stressors. (B) Diagrams showing distribution of studies across different levels of biological organisation (left) and for the various subfields of fish ecology (right). See S1 Table for full details of the studies included.

https://doi.org/10.1371/journal.pclm.0000258.g001

(A) Cumulative number of reviews published over time, split for the various climate stressors. (B) Diagrams showing distribution of studies across different levels of biological organisation (left) and for the various subfields of fish ecology (right). See S1 Table for full details of the studies included.

https://doi.org/10.1371/journal.pclm.0000258.g002

Here, we first briefly review the state of knowledge in terms of fish responses to key global climate change stressors (i.e., ocean warming, acidification, and to a lesser degree also hypoxia) and some of the key underlying mechanisms. We note that the majority of fish responses to climate change stressors have been tested under the worst-case climate scenario forecasts, that is, in the absence of significant greenhouse gas emission reductions (average temperature increases of ~ 2–4 °C above ambient, and average pH decreases of ~ 0.25–0.5 units below ambient [ 10 , 17 , 18 ]). Studies are urgently needed to test responses to less extreme climate change scenarios (i.e. reflective of greenhouse gas reduction scenarios; e.g. [ 19 ]). We still know relatively little about the levels of temperature or CO 2 increase at which various fish species start showing noticeable differences in their behaviour, physiology, ecology, etc. Negative effects on fishes can already be observed at p CO 2 increases of 100–150 μ atm [ 20 , 21 ]. For temperature, many fish species show elevated upper thermal tolerances (but not preferred temperatures) when slowly acclimated to increases of up to >25 °C [ 12 ], but exposure time and intensity of increase are important determinants and can inform us about responses to gradual climate warming vs extreme heatwave events [ 22 ]. However, fishes have a wide range of life history strategies that will result in considerable inter-species differences in responses to temperature and p CO 2 increases, which also depend on their life stage, if they live in the open ocean or coastal areas, and whether they are tropical/arctic (more sensitive) or temperature species.

We further assess climate change impacts at various levels of biological organisation ( Fig 3 ) within the broader fields of molecular, organismal, population, community, landscape, ecosystem, macro-, fisheries, and conservation ecology of fishes, respectively. More extensive and detailed climate-related reviews and meta-analyses for specific subfields of fish ecology exist ( S1 Table ) but are not the focus of this review. Following the brief reviews of the various subdisciplines of ecology, we then focus on the conceptual links across the different subfields of fish ecology and levels of biological organisation, because their synthesis is important for better understanding and predicting fish species responses to climate change from genes to ecosystems. As such, we discuss the relevance of natural analogues of climate change, meta-analyses, quantitative modelling, and paleobiology to help guide climate change research on upscaling fish responses to community- and ecosystem-levels, which could provide future projections that are relevant for fish management and conservation practices.

The graph highlights how the different levels and processes are potentially interconnected (arrows).

https://doi.org/10.1371/journal.pclm.0000258.g003

Molecular ecology

Molecular plasticity and (epi)genetic adaptation.

This represents the lowest level of biological organisation at which fish responses to climate change stressors have been evaluated. It relates to changes at molecular levels, including alternation to the genome and altered expression of particular genes. Some ecophysiological responses also operate at cellular levels (e.g. neuro-endocrine functioning and changes to various types of cellular biomarkers), but these are discussed under ‘Ecophysiology’ below, where they are combined with ecophysiological alterations at the organismal level.

Recent advances in genomic and epigenomic techniques have started to reveal the genetic mechanisms underlying phenotypic plasticity and genetic adaptation of fishes in response to climate change [ 23 ]. Plasticity is often divided into responses that occur within an individual’s lifetime (developmental and reversible) and across generations (parental effects and transgenerational plasticity) [ 24 ]. Aquarium-based manipulations have shown that some coral reef fish species such as such as damselfishes and clownfishes (Pomacentridae) are able to acclimate to higher ocean temperatures (1.5 and 3 °C warmer than current-day) within just one or a few generations [ 25 , 26 ]. At the molecular level, this is driven by the increased expression of the metabolic pathway in the liver, which compensates for the impaired oxygen metabolism caused by higher temperatures [ 15 , 27 – 29 ]. Genome-wide epigenetic measurements have shown that impacts of thermal stress are passed from one generation to the next via loci-specific methylation changes, which can influence the expression of those metabolic pathways necessary to adjust aerobic scope under higher temperatures, such as is the case in the spiny chromis damselfish Acanthochromis polyacanthus [ 30 , 31 ]. Similar epigenetic responses have been documented in wild-caught fish species (Pomacentridae and Apogonidae) during marine heatwaves [ 32 ]. These studies provide support that some fish species might be able to adapt to ocean warming within just a few generations via epigenetic remodelling of their genomes. On the other hand, Wang et al. [ 33 ] showed that exposure of parent Oryzias melastigma to hypoxia resulted in negative impacts on reproduction in the next generations due to transgenerational and epigenetic effects.

Phenotypic plasticity and epigenetic adaptation might not be the only mechanisms that can help fish to cope with climate change. In coral reef fishes, natural populations have a standing genetic variation that can be advantageous when natural selection occurs under stressful conditions [ 16 , 34 ]. Furthermore, varying sensitivity in fish behaviour, for example, under ocean acidification conditions, might be due to changes in the brain transcriptome [ 16 ]. Likewise, at natural CO 2 vents, changes in brain transcriptomes were observed across different species of Pomacentridae along with an accelerated evolution of genes involved in differentially expressed pathways, such as the circadian clock, acid-base regulation, and ion transport [ 35 , 36 ]. More work is needed to understand whether a species’ adaptation potential will also benefit population and ecosystem levels and whether selection of specific traits under changing environmental conditions will alter the ecology and population structure of fish assemblages.

Organismal ecology

Studies on the impact of climate change stressors at the organismal levels typically assess how individual traits altered. These include changes to their growth, mortality, reproduction, morphology, movement, and various behaviours. They also cover the degree of plasticity of such traits in response to changing environmental conditions either within or across generations.

Phenotypic plasticity

There is now strong evidence that fishes can show some degree of physiological, morphological, or behavioural plasticity in response to ocean acidification and warming, and most predominantly within a generation (reviewed in [ 37 , 38 ]). Such developmental plasticity is perhaps unsurprising in fish considering the prevalence of their bipartite life cycles, since this form of plasticity is theoretically favoured when offspring are likely to experience conditions distinct from their parents [ 24 ]. There is also growing evidence that in cases where full compensation is not possible within a generation, parental effects and transgenerational plasticity can restore or improve phenotypes (beneficial plasticity) beyond what is possible within a generation [ 39 ]. For example, in the spiny chromis damselfish only partial compensation of aerobic metabolism was possible with developmental thermal plasticity [ 25 ] and full restoration back to control levels was possible with transgenerational warming [ 40 ]. However, beneficial plasticity to environmental change does not always occur, with limited plasticity of behaviour and reproductive capacity in response to both ocean warming and acidification within a few generations [ 37 , 39 ]. Even with parental exposure to elevated CO 2 , negative impacts to antipredator behaviours remained [ 41 ], suggesting that adaptation via inheritance of CO 2 tolerance may be critical [ 16 ] (Schunter et al. 2016).

(Eco)physiology

Ecophysiological responses to stress resulting from climate-driven changes to an organism’s environment can be expressed at primary, secondary, and tertiary levels within individuals, which include the physiological mechanisms and behavioural changes that an organism uses to re-establish and maintain homeostasis under stress [ 42 ]. At the primary physiological level, stress responses are largely neuro-endocrine and involve the release of catecholamines and corticosteroids (glucocorticoids) [ 43 ].

At the secondary physiological level, heat shock proteins (HSPs) and haematological responses are initiated that activate metabolic, cardio-respiratory, immune, and ion-balance changes [ 44 ]. For example, tissue biomarker responses to a simulated heatwave, such as changes in red muscle citrate synthase and lactate dehydrogenase activities, blood glucose and haemoglobin concentrations, spleen somatic index, and gill lamellar perimeter and width, occurred within the first week of exposure in the more active, mobile fish species ( Caesio cuning ), but were reduced and delayed in the more sessile, territorial species Cheilodipterus quinquelineatus [ 45 ].

Tertiary physiological responses are often at the whole-organism level and can affect growth, movement, reproduction, and resistance to disease [ 46 ]. Stress responses can be immediately beneficial (e.g., fight or flight), adaptive over the longer term [ 47 ], or maladaptive to alter growth, feeding, digestion, immune function, and/or reproduction [ 48 ]. For example, Nagelkerken et al. [ 13 ] (2021) observed higher survival, reproduction, and feeding, but no noticeable changes in growth rates, energy storage, antioxidants, oxidative damage, or protein content in some species of temperate triplefins (Tripterygiidae) at natural CO 2 vents compared to areas with present-day levels of p CO 2 . Hypoxia shows stronger negative responses, on average, compared to warming and acidification, on the metabolism, growth and survival in fishes, whilst warming mostly increases metabolic rates [ 49 ].

Physiological responses to climate change will vary by species, life histories, life cycle, activity, or tolerance levels [ 12 ], and bioregions [ 27 ], but also temporally. Changes in gene expression patterns can be modulated by metabolism, immune function, and HSP production [ 32 ]. Hence, while primary, secondary, and tertiary stress responses to individual climate change stressors are becoming clearer, little is still known about how the vast diversity of fish species will physiologically respond to concurrent climate change stressors and their scope for physiological acclimatisation and adaptation [ 50 ].

Behavioural ecology

Besides changes to physiology, behavioural modification is also considered one of the first key responses by fishes to environmental change [ 51 ]. Ocean acidification, warming and hypoxia can all interfere with the way fishes process sensory information through olfaction, audition, and vision [ 52 – 54 ]. For elevated CO 2 , this has been attributed to malfunctioning neurosensory systems in damselfishes [ 55 ] and coho salmon ( Oncorhynchus kisutch ) [ 56 ], leading to impairment of a suite of fitness-enhancing behaviours (e.g., shoaling, foraging, predator evasion, habitat selection, and defence), which in turn depends on species-specific sensitivities to stressors [ 17 , 57 ]. Shoaling is a particularly important aspect of fish behavioural ecology given most fish species shoal during at least part of their life cycle [ 58 ]. However, exposure to climate change stressors can negatively affect behavioural and sensory traits that underpin shoaling behaviours [ 59 , 60 ]. This can lead to reduced shoal mate familiarity [ 61 ], reduced lateralisation [ 62 ], and slower swimming speeds [ 63 ], resulting in disrupted group formation [ 64 ], all of which can lead to decreased fitness [ 58 ].

To date, most studies investigating the effects of climate change on fish behaviour have been reductionist in nature, using a single stressor under static conditions. Recent advances have allowed for experimental conditions to better mimic those of natural environments [ 65 ], including the use of complex mesocosms [ 66 ] or natural analogues of climate change [ 67 , 68 ]. Most behavioural studies have also focussed on single species, limiting our understanding of how behavioural changes of multiple interacting species can affect communities and food webs [ 69 ]. Upscaling species- to community-level behavioural responses to multiple stressors is required for a more comprehensive and realistic picture of the effects of climate change on aquatic communities [ 2 ].

Movement ecology

Behavioural responses to climate stress can also induce fish movement and migrations. Site-attached or small-range species that cannot escape their direct environment will need to rely on physiological acclimatization to climate-change stress. However, species with greater mobility may be able to avoid stressful environmental conditions by relocating [ 70 ]. For example, lake trout ( Salvelinus namaycush ) can seek out cooler groundwater refugia during late summer when the lake more generally exceeds preferred temperatures [ 71 ]. Consequently, physiological sensitivity, as determined from aquarium-based manipulations, might overestimate the impact of climate change as observed in nature [ 72 ]. Likewise, some species can avoid rapid environmental change by extending their ranges to higher latitudes, deeper waters, or occupy climate refugia (see Landscape ecology ). However, diadromous species that move between the ocean and freshwater might experience reduced movement due to hypoxic zones in estuaries functioning as a chemical barrier [ 7 ]. In comparison to terrestrial ectotherms, we know very little about how small-scale movement may allow aquatic species to buffer the negative impacts of environmental change through processes such as behavioural thermoregulation.

It is also crucial to consider climate impacts on spawning migration and behaviours, as reproduction has evolved to generally occur within a species-specific, narrow environmental window and via environmental cues that determine breeding timing and synchronisation. Environmental change can reduce the length of the spawning season [ 73 ], alter the quality and quantity of progeny, and instigate ecological trade-offs [ 13 , 74 ]. Many species use thermal cues, often combined with other environmental cues (e.g., lunar, rainfall), to determine timing of migration and spawning [ 75 ]. Phenological shifts could allow reproduction to still occur with suitable physiological windows; however, this may result in a mismatch with the timing of lower trophic levels that are essential for early life stages [ 76 ]. For example, effects of ocean warming from the late 1970s has led to decreased population recruitment of glass eels ( Anguilla spp.) due to reduced primary production and food for larvae [ 77 ]. Much of the knowledge on reproductive movement is focused on fisheries species, which are well monitored for stock assessment and management; yet, potential impacts to non-fisheries species remain largely unknown.

Population ecology

Climate stress impacts on individuals will have flow-on effects on their populations. The degree and type of phenotypic plasticity and genotypic diversity across individuals belonging to a population will play a key role in the natural selection of more climate-resilient individuals. If their climate-resilient traits are hereditary, they can be passed on the next generation and create more climate-resilient populations of a particular species.

Population growth and demography

Due to the rapid rate of climate change, the demography and life histories of fishes can play a substantial role in their ability to persist under environmental change. Attributes including long generation time, delayed maturity, low fecundity, and poor offspring provisioning could all reduce the adaptive capacity of fish to climate change and alter population abundances and size structures [ 78 , 79 ]. As predicted by the temperature-body size theory, ocean warming is likely to reduce maximum body sizes and increase somatic growth rates in general, but not always [ 80 ], with significant consequences for the demography of fish populations [ 81 ]. Likewise, altered recruitment rates due to increased larval mortality under climate change stress or phenological mismatches with required prey will modify fish population dynamics [ 82 ]. Furthermore, as waters warm, food requirements increase with fish metabolism, thus exacerbating resource limitations on population growth of some species [ 10 ]. For example, Koenigstein et al. [ 83 ] used an integrative model that included physiological life history responses, and forecast recruitment failure for Atlantic cod ( Gadus morhua ) under ocean acidification and warming, although some of the negative effects might be mitigated via increased food abundance. Severe hypoxia is often associated with mass fish kills, whilst reduced dissolved oxygen concentrations can also alter prey abundances leading to modified predator-prey interactions [ 84 ].

Community ecology

Responses at the population level will affect the demography of fishes and the size of their populations, but does not include the effects of other species (e.g. predators, competitors, parasites) on their abundances. At the community level, these species interactions are key drivers on species abundances, diversity and community compositions.

Competition and species interactions

As the environment changes, so do the complex processes and species interactions that shape communities [ 2 , 85 ]. Based on the premise that natural selection drives organisms toward optimising reproductive success, mathematical game theory has increasingly been applied to analyse the evolution of phenotypes as the environment changes [ 86 ]. At its simplest, game theory can be applied to pairwise competition between individuals based on differences in behaviour, size, age, and sex status, with game theory predicting whether a behavioural strategy is evolutionarily stable [ 87 ]. However, exposure to climate stressors (warming, acidification as well as hypoxia) can disrupt these processes owing to changes in food availability [ 88 ], predator-prey interactions [ 89 , 90 ], competition for habitat [ 91 , 92 ], and habitat selection [ 93 ], leading to food web and community destabilization [ 94 , 95 ].

Environmental warming due to climate change can alter intra- and interspecific competition [ 96 ], whilst in damselfishes elevated CO 2 can reverse competitive dominance, particularly in degraded coral habitat [ 91 ]. Likewise, for estuarine fishes with different growth-temperature relationships, even slight warming can switch the ranking in growth rates [ 97 ]. Kingsbury et al. [ 98 ] showed that range-extending coral reef fishes modified their niches in the presence of temperate species, presumably avoiding competition. Similarly, density-dependence of key fitness characteristics of fishes may alter as oceans warm. For example, Watson et al. [ 99 ] showed that the positive effect of temperature on growth rates was lower at high fish population densities compared to lower fish density of freshwater Galaxias maculatus populations. Climate change can simultaneously exert both negative and positive changes to community structures, suggesting that indirect effects of climate change may alter the interactions between strongly linked species [ 8 , 10 ] (Ockendon et al. 2014, Nagelkerken and Connell 2015).

Niche specialisation

Niche specialisation constrains the capacity of species to persist in places with altered environmental conditions. For example, habitat and diet specialisation are expected to put species at risk when resource requirements are not available in the altered environment [ 100 ]. This results in the expectation that generalist species will often fare better with climate change [ 101 ]. Much of the research on fish supports this; for example, the narrow ecological niche of range-restricted and endemic freshwater species put them at greater risk of future extinction [ 102 ]. Freshwater fishes also have reduced potential to disperse to more favourable habitats when compared to marine fishes, which is often exacerbated by human development (e.g., weirs, dams). Tropical coral reef fishes are well studied in relation to their specialization on coral habitat, with clear impacts of coral loss both for highly specialised and more generalist fish species [ 103 ]. Some of the observed impacts to more generalist species are likely due to indirect effects, for example, through relief from predators and boosted prey resources that benefit generalist benthic fish species more than specialists on temperate rocky reefs [ 67 ].

Symbiosis, parasitism, and disease

The myriad types of symbiotic relationships among fishes and range of taxa represented preclude generalisations to be made as to the impacts of ongoing climate change. Yet, what is likely is that the effects to hosts and symbionts will be altered but not uniformly [ 104 , 105 ]. Of these relationships, parasitism–due to the often-cryptic nature of parasites–has remained understudied amongst fishes, especially when it comes to interactions with climate change stressors. Nevertheless, habitat loss, reductions in water quality, and top-level predator removal that are co-occurring with climate change are predicted to increase the risk of parasitism, exacerbate interactions between fish and parasites, and ultimately impact fish survival [ 105 , 106 ]. Some of these effects may be due to both dopaminergic and seratoninergic neurological impairment that for example can decrease the interactions between tropical cleaner wrasses ( Labroides dimidiatus ) and their client fishes ( Naso elegans ) in response to ocean warming and acidification conditions, thereby increasing the risk of parasites due to degradation of the cleaner-client mutualism [ 107 ]. Moreover, under acidification conditions, fish incur a significant metabolic cost when they do not have access to cleaning stations [ 108 ], which could increase vulnerability to parasites and disease. These responses become even more complex when the survival of some parasites (e.g., gnathids) is unaffected by ocean acidification conditions [ 109 ], thereby emphasizing the non-uniformity in responses within these relationships. Hypoxia can negatively affect the immune response and physiological functioning of fishes making them more susceptible to disease [ 110 ].

Similar trends also exist in mutualistic relationships and could lead to increased disease prevalence. For example, under ocean acidification juvenile fishes may spend less time in their protective symbiotic relationships with jellyfish [ 111 ], and anemonefishes incur significant metabolic costs (~8%) when their symbiotic anemones are bleached due to ocean warming and marine heatwaves, which could explain decreases in their spawning and fecundity [ 112 ]. These altered symbiotic relationships as well as the role that climate change stressors, habitat degradation, and poor water quality directly play on fish health explain, in part, the dramatic rise in diseases in the marine environment due to global climate change [ 113 ].

Landscape ecology

Fish responses at landscape level include alterations to the landscape, including widely observed changes to habitat structural complexity and habitat composition under warming and acidification. In addition, spatial processes that operate at landscape levels can have strong influences on fishes and their communities, e.g. through altered larval dispersal and species range extensions or range contractions under warming.

Larval dispersal

Most marine fishes disperse through larval transport via ocean currents, and hence strengthened poleward boundary currents due to climate change could increase physical dispersal of larvae on these currents and enhance range extensions and gene flow [ 114 ]. On the other hand, increasing sea temperatures often shorten pelagic larval duration (and can also increase survivorship) which could lead to decreased larval dispersal kernels, and reduced population connectivity due to a higher degree of self-recruitment [ 115 ]. Irrespectively, warming oceans are increasing tropical larval settlement and survival in temperate ecosystems, with successful species characterised by life history traits such as smaller maximum length and reduced age and length at maturity [ 116 ].

Tropicalisation and borealisation of cold water communities

As many species shift their distribution poleward in response to climate change, the proportion of ‘warm affinity’ species within fish communities has markedly increased in many regions of the world, a process known as ‘tropicalisation’ [ 117 ]. This tropicalisation can strongly impact the trophic structure of fish assemblages. In warm temperate reefs, tropicalisation has led to striking increases in the proportion of herbivorous as well as omnivorous fish biomass [ 118 , 119 ]. Interestingly, these changes in trophic structure observed on tropicalising reefs mirror patterns observed along latitudinal gradients, where warmer tropical latitudes are typically also characterised by a greater proportion of herbivores [ 120 , 121 ]. Species that are most successful in extending their range are often also either habitat [ 101 ], behavioural [ 122 ], or dietary [ 123 ] generalists.

In the Arctic, warming has led to the expansion of boreal fish communities toward the poles, a process coined ‘borealisation’ [ 124 ]. In the northern Barents Sea, large migratory fish predators and small planktivores are increasing in abundance, and small benthivores are declining, which is increasing their relative importance in the pelagic food web [ 124 , 125 ].

Range-extending fishes as ecosystem engineers

Climate change impacts the role of fish as ecosystem engineers by altering the intensity or direction of trophic interactions. For example, greater herbivory–driven by the range expansion of warm-affinity fishes such as species of parrotfishes (Scaridae), surgeonfishes (Acanthuridae), rabbitfishes (Siganidae) and drummers (Kyphosidae)–has led to the overgrazing of canopy-forming seaweeds or seagrasses [ 126 ]. Marine macrophytes are the foundation vegetated habitat of temperate systems. As such, their decline can have major cascading impacts on benthic communities and fish assemblages. For instance, in the eastern Mediterranean the loss of habitat-forming seaweeds caused by the range expansion of two Siganus species has been linked to a decrease in both fish species richness and abundance [ 127 ]. In Australia, increases in fish herbivory have also been linked to the decline of dominant kelp forests and the maintenance of turf-dominated reefs [ 128 , 129 ]. Coni et al. [ 68 ] observed that overgrazing of kelp by sea urchins ( Centrostephanus rodgersii ) created barrens that are favoured by range extending fishes (in particular Acanthurus spp. and Abudefduf spp.) compared to native kelp habitat. However, many of these changes may represent a transitional state, and recent evidence shows the apparent tropicalisation of fish and benthic communities in regions like Japan can somewhat be reversed by elevated CO 2 [ 130 ] and by extreme cold events which are also predicted to increase under climate change [ 131 ].

Ecosystem ecology

At the level of ecosystems, altered food web structures, productivity, consumption rates, and energy flows across trophic levels have been observed. These can alter individual growth, reproduction and survival rates, as well as create altered species interactions (e.g. competition for food or altered predator-prey dynamics) with ensueing effects on species community composition, diversity and ecosystem productivity.

Trophodynamics and energy flow

Increasing herbivory in tropicalised reefs can increase the flow of energy to higher trophic levels, potentially leading to increases in benthic fish productivity [ 119 , 132 ]. In the Mediterranean Sea, however, increases in the proportion of herbivorous fish have been linked to a reduction in total fish biomass [ 127 ]. Tropicalisation and increased herbivory are also associated with enhanced production of detritus via increased defecation [ 133 ], thus impacting nutrient cycling and benthic microbial communities [ 134 ]. The physiological mechanisms underpinning these patterns are unclear, as there is little evidence that low temperatures disadvantage the digestion of algal or plant materials [ 135 ]. In the Arctic, food web properties are increasingly resembling those of boreal food webs, with a greater relative importance of pelagic species [ 125 ]. Novel feeding interactions between range-expanding and resident Arctic species are predicted to amplify the impact of species redistributions [ 136 ]. Ocean acidification can modify food web structures and energy flow, with elevated CO 2 generally acting as a nutrient for algae, boosting food webs through bottom-up effects [ 137 ]. However, ocean acidification and warming combined can constrict food webs at mid-levels, eventually leading to the collapse of top levels, fewer trophic levels, and a bottom-heavy food web [ 94 ]. Hypoxia can alter the community and size structures of zooplankton, resulting in altered food wen interactions with potential impacts on foraging, consumption and growth in fishes [ 138 ].

Macro-ecology

Large-scale patterns in biodiversity.

Biogeographic patterns that have persisted for millions of years are likely to change through the next century in response to global change and overexploitation [ 139 , 140 ]. Climate impacts are even affecting the most notable biogeographic property known for fishes–the ‘latitudinal gradient in biodiversity’, with greater fish species richness in the tropics at both regional (gamma diversity) and site (alpha diversity) scales [ 141 ]. Nevertheless, marine richness dips at the equator, with maximal species richness evident at ~15° latitude North and South [ 142 ]. Through the past half century, richness has apparently declined on the equator and risen in mid-latitudes [ 70 ], with outcomes attributable to species emigrating poleward due to climate change [ 143 ].

The trophic composition of fish communities is changing in parallel with broad-scale changes in species richness. The proportion of species with particular traits shows predictable variation with species richness, including a higher proportion of planktivorous, small-bodied and pelagic fishes in locations with high species richness [ 144 , 145 ]. Identifying and understanding variation in trait composition represents a challenging but important field of fish ecology, given the prominent influence of traits on metapopulation and food web dynamics. However, field observations are needed across large spatial scales, which might be achieved through citizen science [ 146 ] and by capitalising on rapid advances in metagenomic sample collection and processing [ 147 ].

Functional diversity and ecosystem stability

Fish functional diversity tends to decrease with climate change, leading to functional convergence toward traits that are more adapted to novel environments [ 148 ]. Such patterns have emerged in marine [ 148 ], estuarine [ 149 ], and freshwater [ 150 ] fish communities, with long-lived species with late maturation and/or large body sizes being disproportionately impacted [ 139 , 151 ]. However, different proxies of functional richness can sometimes show opposing effects to climate change stressors, highlighting the importance of testing complimentary measures of diversity [ 152 ]. Higher functional redundancy (i.e., higher number of species with similar ecological functions) can initially buffer communities against the detrimental impacts of climate disturbance [ 153 ], yet the general trend over time is a decrease of functional redundancy with, for example, a disproportionate loss of piscivores and fish species with pelagic eggs in the North Sea [ 148 ]. Reduced functional diversity can, in turn, impact ecosystem stability and increase the risk of losing important ecosystem functions through biotic homogenization and the loss of ecological specialists such as some species of gobies (Gobiidae) [ 101 ].

Furthermore, reduced oxygen carrying capacity at higher temperatures coupled with increased nutrient runoff from catchments can lead to establishment of anoxic ‘dead zones’. These are now a global phenomenon, with an exponentially increasing footprint, and affecting a total ocean area estimated to be > 245,000 km 2 in 2008 [ 154 ].

Fisheries ecology

Alterations to individual fitness and population sizes of targeted fisheries species can have flow-on effects on seafood production. Moreover, with species shifting their biogeographic ranges under ocean warming, populations of fishes species are relocating to other areas, which can have socio-economic effects on local fishermen as well as commercial fisheries.

Fisheries production

Mounting evidence suggests complex impacts of climate change on fisheries production, resulting from the adverse effects of single climate stressors (e.g., global warming, ocean acidification, extreme weather events), as well as their cumulative impacts and interactions with other human pressures (e.g., overexploitation, pollution) [ 155 ]. Globally, changes in ocean conditions have been linked to a reduction of body size in commercially important marine fishes (e.g., Atlantic cod Gadus morhua ), potentially impacting global fisheries catches [ 156 ]. Weather extremes, such as floods and droughts, are also increasingly impacting estuarine ecosystems on which many freshwater and marine species rely for at least part of their life cycle [ 7 , 149 ]. Furthermore, climate-driven species range shifts progressively redistribute fish stocks, leading to both species extinctions and invasions that are projected to increase in the future [ 157 ]. Therefore, many species will likely shift across national and other political boundaries in coming decades, creating potential for conflict over newly shared resources, as previously observed with Pacific salmon ( Oncorhynchus spp.) stocks [ 158 ]. Although potential adaptive strategies arise for fisheries under climate change, future research is urgently needed to identify barriers, constraints, and limits for climate adaptation [ 155 ]. Furthermore, most research has so far considered climate change as a single macro-stressor [ 155 ], and the direct effects of other stressors (e.g., ocean acidification, hypoxia) have mostly remained inconclusive and require further research [ 159 ].

Fish nutritional quality

Fish are a rich source of essential nutrients, such as iron, zinc, Omega-3 fatty acids, and vitamins, that support human health and provide an important pathway for tackling micronutrient deficiencies in many countries [ 160 , 161 ]. Yet, ocean warming and acidification have the potential to alter fish nutrient concentration through both direct (metabolism, nutrient assimilation efficiency) and indirect (nutritional quality and composition of basal food sources) effects [ 162 ]. However, divergent nutritional responses to climate change among species and functional groups suggest the emergence of ‘winners’ and ‘losers’ of climate change among species targeted by fisheries [ 163 ]. For example, herbivorous rabbitfishes (Siganidae) caught on regime-shifted macroalgal habitats after mass coral bleaching were enriched in iron and zinc [ 163 ]. This contrasted with experimental research on a euryhaline fish, the yellowfin bream ( Acanthopagrus australis) , that showed no effects of future ocean conditions on fish nutritional content, possibly linked to its broad habitat distribution and greater physiological tolerance [ 164 ]. Therefore, an important mechanism for future fisheries adaptation will be to identify the species that are most likely to sustain food and nutrition into the future and reorientate fisheries management accordingly [ 165 ].

Conservation ecology

Conservation of most species is best achieved through spatial mechanisms that protect many species within whole ecosystems–that is through ‘marine protected areas’ (MPAs) where adverse pressures are reduced as much as practical [ 166 ]. All of the many potential benefits of MPAs, including biodiversity conservation, insurance against fisheries collapse, recreation, aesthetic enjoyment, and educational opportunities [ 167 ], are potentially compromised by climate change, including interactions with other stressors [ 168 ]. Ocean warming leads to loss of fish populations from MPAs as species track preferred sea temperatures toward the poles, while extreme heatwaves can cause loss of essential fish habitats including coral, kelp, mangrove, and seagrass habitat structure. Furthermore, ocean acidification potentially affects organisms with calcareous structures, and rising sea level affects intertidal fish species, particularly when the shore is bounded by urban development that prevents landward progression [ 169 ].

A global analysis by [ 170 ] identified a widespread mismatch between climate vulnerability of recreational fishes and conservation effort, with most effort focussed on marine fishes of high socio-economic value and little effort on freshwater and diadromous species. A first step toward minimising species loss is the amelioration of local compounding stressors [ 171 ]. Another partial solution involves consolidating MPAs into networks, where individual parks operate as stepping stones that assist species in translocating poleward [ 172 ]. Restoring degraded coral reefs, kelp forests, seagrass beds, shellfish reefs, and mangroves will also be necessary for the long-term recovery of habitat-dependent species [ 173 ]. However, excessive cost has restricted restoration efforts to local scales [ 174 ]. Identifying and protecting potentially resilient areas, and integrating climate change into MPA planning and evaluation, are also fundamental if healthy ecosystems are to be maintained [ 175 ].

Scaling up from genes to ecosystems

Scaling up from organismal-level impacts of climate change on fishes to those at the population- and community-levels is challenging and requires incorporating the mediating effects of species traits and natural ecological processes across biological levels from genes to ecosystems ( Fig 3 ). All levels of biological organisation are interconnected, either directly, or via other pathways. For example, genomic responses may allow species to adjust their physiology to cope with climate stress, and as such maintain their physiological performance and homeostasis, which would reduce climate-driven alterations to their fitness and consequently community structuring and food web dynamics. Yet, because of the many interconnected direct and indirect pathways, it is more likely than not that some degree of change ensues from one or more climate stressors. Such changes may facilitate novel ecological interactions, novel community structures, and rewired food webs. In-depth studies at several natural analogues have already shown modifications to occur at more than one level of biological organisation under the effects of ocean warming (e.g., [ 68 ]–community and landscape ecology), ocean acidification (e.g., [ 13 , 67 ]–behaviour, physiology, demography, competition, niche specialisation, trophodynamics, biodiversity, and habitat change), or hypoxia (e.g., [ 176 ]). However, these studies have also identified the inherent complexity in accurately predicting fish responses to climate change.

Because species all have their unique ecological niches, environmental tolerances, behavioural repertoires, and adaptive capacities, different species or populations will respond to climate change in very different ways. Yet, effective management and conservation to address the effects of climate change requires insights that can be generalised and consistent across multiple taxa and biogeographies (e.g. Table 1 ). Such broader insights into somewhat predictable or consistent responses are necessary to inform climate adaptation strategies before further effects of climate change emerge, and may be acquired through some of the approaches as discussed below.

https://doi.org/10.1371/journal.pclm.0000258.t001

Natural analogues that incorporate ecological complexity

Integrating responses at multiple levels of biological organisation is inherently difficult to study in laboratory settings, but natural laboratories that mimic future climate conditions (e.g., volcanic CO 2 vents, ocean warming hotspots, natural environmental gradients such as upwelling areas) can incorporate (part of) such ecological complexity. This is important because ecological complexity can buffer negative impacts of climate stressors such as those observed in more simplified laboratory systems [ 66 ]. Moreover, natural variability (e.g., daily, seasonally) of climate stressors–which is mimicked at natural analogues–is known to alter species responses to climate stress (e.g., diminished fish gene expression in Embiotoca jacksoni compared to stable stressor conditions [ 177 ]). Especially for species with restricted home ranges, these analogues allow insights into the integrated ecological responses of fishes to climate change stressors, responses like epigenetic adaptation, behavioural modifications, physiological acclimatization, phenological responses, demographic changes, range shifts, species interactions, habitat regime shifts, and natural selection, all of which combine to explain how communities, ecosystems, and biodiversity might be reshaped directly and indirectly by environmental change [ 178 ]. They also have their drawbacks, such as single stressor effects, small spatial scales, and species influx from adjacent systems that reflect present-day conditions. However, studies have attempted to address some of these issues for fishes, for example, by working on site-attached species [ 67 ], performing meta-analyses of natural analogues [ 18 ], or by combining analogues that reflect different climate stressors (e.g. [ 68 ]).

Generalisable trends from meta-analyses

Meta-analyses represent a powerful tool to predict species responses to climate stress and their consistency across functional groups, biogeographies, and ecosystems. However, they are still heavily restricted to specific subfields of fish ecology, such as ecophysiology, and at the level of individual organisms ( S1 Table , Fig 1 ). Some authors have used quantitative meta-analyses to test the degree to which species responses are in accordance with previous (modelled) climate change forecasts (e.g., [ 1 , 14 , 179 ]). Meta-analyses can suffer from publication bias (i.e., toward reporting only detectable effects), but with the uprise of open access journals that publish studies based on methodological and analytical rigour rather than novelty or significant effects, this effect is likely to diminish. However, meta-analyses are insufficient to forecast fish responses to climate change across multiple levels of biological organisation and across time. Advanced ecological modelling approaches could be used for this purpose.

Holistic ecological models for more accurate future predictions

The various ecological models forecasting fish responses to climate change–species distribution models (SDMs), food web models, whole-ecosystem models, bioenergetic models, and dynamic bioclimate envelope models, to name a few–vary along a gradient of model complexity, each with specific objectives, strengths, and weaknesses. At the simplest end of the spectrum, SDMs only require species occurrences matched with associated environmental conditions to determine a species’ habitat suitability over time and space. The relative simplicity of SDMs has led to many applications for fish communities across ecosystems and bioregions [ 180 ]. However, the ability of SDMs to forecast species distributions under future conditions remains controversial [ 181 ] because they assume stable species-environment relationships, which can be violated by adaptive mechanisms such as plasticity (but see [ 182 ]). In their original implementation, SDMs also do not account for species interactions, which can instead be achieved by food web models [ 183 , 184 ]. Food web models quantify the flow of energy and biomass through ecosystems, yet their parametrisation for complex ecosystems remains difficult and is rarely spatially explicit (but see [ 185 , 186 ]). Integration of SDMs and food web models thus represents a promising avenue and has previously been used to forecast changes to fish species richness and their trophic linkages (e.g., in the Mediterranean under warming [ 187 ]). Whole-ecosystem models such as Atlantis can incorporate biophysics, socioeconomics, management, and human impacts to forecast changes in fish biomass of functional groups (e.g., [ 188 ]). Bioenergetic models (e.g., Dynamic Energy Budgets) are suitable to predict how different physiological processes interact at the organismal level [ 189 ]. However, due to the large amount of data used to parametrize these models, most applications remain restricted to a few well-studied and commercially exploited species. To date, dynamic bioclimate envelope models likely represent the most integrative models, e.g., combining spatially explicit population dynamics with a bioclimate envelope model for >1,000 exploited invertebrate and fish species at a global scale [ 157 ].

Next-generation models need to be developed that integrate adaptive responses of fish to climate change across multiple levels of biological organisations as well as changing species interactions and behaviours (e.g., [ 190 ]). Although no model can integrate fish responses to climate change across all biological levels simultaneously, a better identification and parametrisation of important responses at relevant spatiotemporal scales, particularly through meta-analyses, will be necessary to construct future ecological models in support of fisheries management and biodiversity conservation. Improved compatibility between models and collaboration between research teams should also allow to combine models predicting responses at various biological levels and, importantly, validate model predictions and quantify the uncertainty stemming from every model component.

Using past extreme climate events to predict the future

Past climate perturbations such as the Paleocene Eocene Thermal Maximum may provide clues about the impacts of climate change in the Anthropocene, although such events typically occurred across longer timescales than present climate change. Nevertheless, responses of modern-day marine taxa to ocean warming, acidification, and hypoxia align to those observed for fossils extinctions during the Phanerozoic eon [ 191 ]. Likewise, Avaria-Llautureo et al. [ 192 ] observed smaller-sized anchovies and herrings with lower dispersal ability during historical periods (during the past 150 Myrs) of warmers waters, as predicted by theory, whilst Salvatteci et al. [ 193 ] observed an ecological replacement of the present-day migratory anchovies with smaller-bodied fishes during the last interglacial period in a warmer, oxygen-poor ocean. A critical, yet often overlooked step in ecological modelling is model validation. Past extreme climatic events or periods of gradual climate change can be used retrospectively for this purpose, to inform about the potential responses of fishes to future climate.

Conclusions

Predicting what future fish populations and communities might look like will not be an easy task due to the various dimensions of change (time, space, traits, etc.) and the levels of biological organisation (and the interactions amongst these levels) affected for a highly diverse group of ocean fauna. Yet, the increasing meta-data on fish responses to climate change, advances in modelling and computing power, discovery of new natural analogues of climate change, and insights into the consequences of past extreme climatic events, will allow us to integrate these insights for more realistic predations of climate change effects on fishes. Elucidating generalisable species responses to climate change will be important to develop climate adaption management and conservation strategies. Fish communities of the future will be different from how we know them, but we need to make sure that under rapid environmental change we acquire the relevant knowledge for the management of species and their communities to sustain global biodiversity, fisheries productivity, and the critical ecosystem services that fishes perform.

Supporting information

S1 table. results of a literature search for meta-analyses on the effects of climate change on fishes in web of science on 19 october 2022..

Search terms were: all fields ‘meta analysis’ and all fields ‘climate change or warming or temperature or ocean acidification or carbon dioxide or elevated CO2 or reduced ph or hypox* or anox*’ and all fields ‘fish*’. Hypox* included hypoxia and hypoxic, whilst anox* included anoxia and anoxic. A few additional meta-analyses from our own paper collections were added that were missed in the literature search. Results needed to include an effect size, or a mean/median with error bars; papers with just regression graphs were excluded. OA = ocean acidification, OW = ocean warming, MR = marine, FW = freshwater. For the systematic reviews the same terms as for meta-analyses were used in Web of Science, except that ’meta analysis’ was replaced with ’systematic review’ as a search term. The semi-quantitative analysis of non-systematic review papers was based on a personal library (IN) accumulated during the past 11 years.

https://doi.org/10.1371/journal.pclm.0000258.s001

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Impact of climate change on marine life shown to be much bigger than previously known

by Royal Netherlands Institute for Sea Research

Fish and invertebrate animals are far more affected by warmer and more acidic seawater than was previously known. This is the conclusion of a study co-led by NIOZ marine biologist Katharina Alter, based on a new analysis method published in Nature Communications .

Lead author Katharina Alter of the Royal Netherlands Institute for Sea Research (NIOZ) explains why it is essential to summarize and analyze the results of published studies addressing the effects of climate change . "To gain a better understanding of the overall worldwide impact of climate change, marine biologists calculate its effects on all fish or all invertebrate species lumped together."

"Yet, effects determined in different individual studies can cancel each other out: for example, if invertebrate animals such as snails profit from a certain environmental change and other invertebrates, such as sea urchins, suffer from it, the overall effect for invertebrates is concluded to be zero, although both animal groups are affected."

In fact, snails eat more due to climate change, and sea urchins eat less. Alter says, "Both effects matter and even have cascading effects: turf algae, the food for sea urchins , grow more while the growth of kelp, the food for gastropods, decreases. The difference in feeding in the two invertebrates causes a shift in the ecosystem from a kelp-dominated ecosystem to a turf algae-dominated ecosystem, consequently changing the living environment for all other animals living in this ecosystem."

Important for understanding ecological shifts

Together with colleagues from Wageningen University and 12 other research institutions from the US, France, Argentina, Italy, and Chile, dr. Alter developed a new research method that no longer cancels out seemingly contradictory results but uses both to determine the consequences of climate change on animals' fitness.

Before the use of this method, ocean warming and more acidic seawater were known to affect fish and invertebrate animals in three general ways negatively: their chance of survival is reduced, their metabolism is increased, and the skeletons of invertebrates are weakened.

Using the new method, the international group of marine researchers discovered that climate change has negative effects on additional important biological responses of fish and invertebrates: physiology, reproduction, behavior, and physical development. Alter says, "Because this may result in ecological shifts impacting marine ecosystem structures, our results suggest that climate change will likely have stronger impacts than previously thought."

Up to 100% of biological processes affected

Increasing levels of carbon dioxide in the air have been causing warmer and more acidic seawater for decades, a trend that is expected to continue in the future. However, it is unknown at which speed and to what extent.

Alter and her colleagues calculated the consequences of three projected scenarios of carbon dioxide increase, and thus of ocean warming and ocean acidification : extreme increase, moderate increase at the current speed and—due to possible measures—mitigated increase.

Alter says, "Our new approach suggests that if ocean warming and acidification continue on the current trajectory, up to 100% of the biological processes in fish and invertebrate species will be affected, while previous research methods found changes in only about 20 and 25% of all processes, respectively."

Furthermore, the research shows that measures to mitigate atmospheric carbon dioxide levels will help reduce changes in biological processes: in the low carbon dioxide scenario, 50% of responses in invertebrates and 30% in fish will be affected.

The big gain of the new method, according to Alter, is that more details become known about the effects of climate change on species. "The new calculation method weighs the significant deviation from the current state irrespective of its direction—be it beneficial or detrimental—and counts it as the impact of warming and acidifying seawater. With our new approach, you can include the broadest range of measured responses and detect impacts that were hidden in the traditional approach."

Journal information: Nature Communications

Provided by Royal Netherlands Institute for Sea Research

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“But It’s Just a Fish”: Understanding the Challenges of Applying the 3Rs in Laboratory Aquariums in the UK

Simple summary.

Fish are widely used in research and some species have become important model organisms in the biosciences. Despite their importance, their welfare has usually been less of a focus of public interest or regulatory attention than the welfare of more familiar terrestrial and mammalian laboratory animals; indeed, the use of fish in experiments has often been viewed as ethically preferable or even neutral. Adopting a social science perspective and qualitative methodology to address stakeholder understandings of the problem of laboratory fish welfare, this paper examines the underlying social factors and drivers that influence thinking, priorities and implementation of fish welfare initiatives and the 3Rs (Replacement, Reduction and Refinement) for fish. Illustrating the case with original stakeholder interviews and experience of participant observation in zebrafish facilities, this paper explores some key social factors influencing the take up of the 3Rs in this context. Our findings suggest the relevance of factors including ambient cultural perceptions of fish, disagreements about the evidence on fish pain and suffering, the language of regulators, and the experiences of scientists and technologists who develop and put the 3Rs into practice. The discussion is focused on the UK context, although the main themes will be pertinent around the world.

Adopting a social science perspective and qualitative methodology on the problem of laboratory fish welfare, this paper examines some underlying social factors and drivers that influence thinking, priorities and implementation of fish welfare initiatives and the 3Rs (Replacement, Reduction and Refinement) for fish. Drawing on original qualitative interviews with stakeholders, animal technologists and scientists who work with fish—especially zebrafish—to illustrate the case, this paper explores some key social factors influencing the take up of the 3Rs in this context. Our findings suggest the relevance of factors including ambient cultural perceptions of fish, disagreements about the evidence on fish pain and suffering, the discourse of regulators, and the experiences of scientists and animal technologists who develop and put the 3Rs into practice. The discussion is focused on the UK context, although the main themes will be pertinent around the world.

1. Introduction

The relevance of human-animal interactions, relationships and bonds to laboratory animal welfare, robust animal-dependent science and ethics is widely acknowledged by practitioners, e.g., [ 1 , 2 , 3 , 4 , 5 , 6 , 7 , 8 ]. How these are embedded in and reflective of wider social processes, relations and structures is also increasingly a matter of interest to social scientists, historians and ethicists, many of whom are also concerned to better understand how such broader societal issues shape the implementation and development of public policy and associated ethical frameworks, e.g., [ 9 , 10 , 11 ], including the 3Rs [ 12 , 13 ]. There is also thriving literature on the role of public opinion concerning the use of laboratory animals, much of which illustrates an interest in how species differences can mediate social attitudes and potentially structure policy priorities, e.g., [ 14 , 15 , 16 , 17 ]. The case of the use of fish in regulated scientific research is a good example of this, but has seldom before been addressed for some partial exceptions, see [ 18 , 19 , 20 , 21 ]. Using the 3Rs as a point of entry, this paper adopts a qualitative social scientific perspective, highlighting social drivers that could be influencing thinking on, prioritization of and implementation of laboratory fish welfare.

In the United Kingdom and many other countries, fish have not historically qualified for sympathy because they were deemed too dissimilar to humans [ 22 ] (p. 177). Times have changed: following rising concerns about food fish sustainability, oceanic health, and the industrialization of both wild-capture fisheries and aquaculture, the ethics of human-fish relations in their different forms and locations have slowly become topics of both popular (e.g., [ 23 , 24 , 25 , 26 ]) and academic (e.g., [ 27 , 28 , 29 , 30 , 31 , 32 ]) criticism. Additionally, there has been an explosion of scientific interest in the cognitive abilities of fish and their capacity for emotional experiences, topics which tend to have a close association with debates about welfare, ethics and the controversy about fish pain, e.g., [ 33 , 34 , 35 , 36 ]. Fish welfare has also risen slowly up the agenda of animal welfare charities and campaign groups. Following the steep rise of finfish aquaculture in the global North, the websites of most of the large, multi-campaign issue organizations now feature dedicated pages to fish farming and humane slaughter. There are also a growing number of online campaign groups dedicated specifically to raising awareness about suffering in fisheries and advocating for fish sentience—Fish Feel, Let Fish Live, and fishcount.org are prominent examples see [ 37 , 38 , 39 ]. Via the European Union in particular, regulators have made attempts at entrenching the legal recognition of fish as sentient beings in practice, and have been active in areas including humane slaughter regulations and the harmonizing of husbandry standards for farmed fish, e.g., [ 40 , 41 , 42 ]. These and other developments (notably welfare-motivated restrictions on recreational angling in Switzerland and Germany) have recently led some fisheries biologists to wonder what the developing welfare agenda means for the future of aquaculture, angling, commercial fishing and research? [ 43 ].

However, the (re)emergence of discussions around contested moralities of recreational angling [ 44 , 45 , 46 , 47 , 48 , 49 ], welfare in the context of wild-capture fisheries [ 50 , 51 , 52 , 53 ], the ethics of dietary trends (pescetarianism) [ 54 , 55 ], and the putative demands amongst consumers in some countries for higher welfare farmed fish [ 56 , 57 , 58 , 59 , 60 , 61 ], all suggest that there remain stubborn, sometimes intractable, challenges in all of these areas. Growth in the number of commentators does not necessarily reflect serious changes in policy and practice. It is also not yet clear whether recent interest by the news media in scientific work exploring the mental and emotional capacities of some fish species—including for example their capacity to feel pain [ 62 ], pass the mirror test of putative self-awareness [ 63 ], or “pine” for their mates and get depressed [ 64 , 65 ]—either reflect or have provoked substantial changes in public attitude. What people make of such information is open to debate. The film Finding Nemo, with its positive and engaging portrayal of one the ocean’s most charismatic fish species and its famous line “fish are friends—not food”, was predicted to have caused a ripple effect in public sentiment towards fish and the aquatic world. However, ironically, when the geographer Driessen [ 66 ] investigated this, he discovered that the film had, in fact, become a popular name for cafés specializing in fish and chips. With one café already adopting it as a name, the same appears set to be true of Blue Planet II, David Attenborough’s hugely popular documentary, which has been credited with kick-starting debate about the state of the planet’s oceans, and showed the world footage of sophisticated and surprising fish behaviors, including tool use [ 67 , 68 ].

This wider social and cultural context is important when approaching the welfare situation of laboratory fish and the 3Rs. The intensification of fish use in laboratory research generally—and the rise to prominence of zebrafish models in particular—have likewise provoked higher levels of interest in the issue of fish welfare in the sector in the UK and internationally. This includes an emergence of reflections on different ethical issues associated with the use of fish in research specifically [ 21 , 69 , 70 ]. There has also been a growing willingness to consider, develop and implement 3Rs initiatives focused on fish amongst animal technologists, scientists, veterinarians and policy makers, and both the UK and pan-European laboratory animal welfare and veterinary organizations have all played different roles in highlighting fish welfare amongst their constituencies, e.g., [ 71 , 72 , 73 ]. Furthermore, there are direct links between developments in laboratory fish welfare and other sectors. In the UK, intensive aquaculture and the laboratory aquarium are connected via personnel, technology and knowledge transfer. For example, via links between forums such as the Fish Veterinary Society and the Laboratory Animal Veterinary Society (both subsections of the British Veterinary Society), or notable colloquiums organized by organizations like the National Centre for the Replacement, Refinement and Reduction of Animals in Research (NC3Rs) and the Centre for Environment, Fisheries and Aquaculture Science (CEFAS).

Yet, again, there remains a widespread sense amongst those who work with fish or who regulate fish-based science that the degree of attention that fish of any species receive is not yet commensurate with the quantities in which they are used, their importance to science, nor—if much recent behavioral and neuroscientific evidence is accepted—their possible levels of suffering. As the authors’ have often heard in the course of their research, this sense is quite widely shared amongst scientists, technologists and others who work with fish (including zebrafish) in the UK. This can filter through and be reflected in efforts to prioritize 3Rs and other welfare-relevant interventions that benefit fish. By discussing challenges to the 3Rs with reference to wider context, this paper sets out to stimulate discussion and reflection by proposing that developments (or lack thereof) in this field are connected to a variety of interlinked social drivers, and scientific, institutional and regulatory viewpoints.

2. Materials and Methods

Within the social sciences, qualitative methods offer an effective and insightful means of understanding the intersection of the broader (largely utilitarian) ethical frameworks which shape animal research, and the more individualized moral convictions, beliefs and practices of those who work closely with laboratory animals and who are often tasked with implementing policy. Interviews and participant observation, alongside the analysis of key literatures, policy documents and archival materials, have formed the basis of several landmark studies in the field, e.g., [ 9 , 74 ], and have proved highly effective in developing understandings of how ethics and the 3Rs are “put into practice” in the field of animal research [ 75 ]. Adopting a similar approach, this paper seeks to energise debate on fish and the 3Rs by drawing on the authors’ experiences of participant observation in UK zebrafish facilities, participation in professional events and conferences, as well as interviews with stakeholders. It is not intended to be a technical review of 3Rs initiatives and related welfare issues for zebrafish (of these there are a growing number, see e.g., [ 21 , 69 , 76 , 77 , 78 , 79 , 80 , 81 ]). The objective here is to gain insights into how people who work with laboratory fish understand and explain their practices and their relationships to the humans and animals they work with, and also to the wider field of animal research. In other words, we are offering an account of the ways in which people talk about: (i) whether or not they (and others) care about fish (attitudes towards); and (ii) how this shapes their ability to care for them (husbandry practices). By relating these to wider literatures, policy documents and other textual sources we can begin to build up a picture of the key social norms and discourses in and around laboratory zebrafish research, the possible implications of these for fish welfare, and hopefully shed light on barriers to implementing and developing the 3Rs initiatives for from a sociological, rather than technical, point of view.

The arguments presented in this paper are derived from a larger body of ongoing research into the species and spaces of contemporary animal research in the UK, performed as a part of the collaborative research project “The Animal Research Nexus” project (see www.animalresearchnexus.org ). This project seeks to understand the factors that have shaped and continue to underpin the social contract on which animal research in the UK rest, better understand emergent issues and challenges, and contribute positively to cultures of communication across the sector. This paper draws on data and insights developed in one sub-strand of this wider project. This strand of work focused on understanding the care and welfare work of animal technologists, the managers of aquarium facilities and scientists who work with fish, asking how their understandings of their work relate to wider ethical and legal frameworks. As a part of this, we also engaged with other stakeholders, including veterinary professionals and the regulators of animal research in the UK—in particular, Home Office Inspectors—as well as animal welfare organisations.

This study adopts a mixed method approach, drawing on a combination of in-depth interviews, participant observation and documentary analyses. Firstly, in order to gain an insight into how fish welfare is put into practice, the first author has taken part in two one-week-long stints as a participant-observer in two different zebrafish aquariums in the UK, conducted repeat visits to a facility to see how they introduced a new zebrafish room, and participated in a professional training course for researchers and technicians who work with zebrafish. Secondly, we have reviewed publicly available documentation and relevant professional literature. Thirdly, we conducted in-depth semi-structured qualitative interviews with 27 individuals (two interviews involved more than one participant being interviewed at a time), including scientists, animal technologists, facility managers, veterinary professionals, representatives of animal welfare charities, and regulators. Additionally, both authors have paid shorter visits to numerous fish facilities across the UK over the past seven years, as well as attended and participating in a variety of professional conferences and related forums and engaging in ongoing collaboration and dialogue with the wider animal research community and associated stakeholders, including both those supportive of and against animal research. While we have interviewed three scientists based at contract research organizations and pharmaceutical companies, and those who specialise in commercial regulatory testing, our focus has been on university-based bioscience research. This is because this is where the vast majority of fish research in the UK is conducted. This is additionally justified because there is already a disproportionate focus on toxicology research in the 3Rs literature [ 82 , 83 ]. Lasting, on average, around one and a half hours, interviews were conducted, where possible, at the place of work of the interviewee. Interviews were digitally recorded, transcribed and analyzed thematically using the qualitative data analyses tool NVivo. A number of key themes were identified ( Table 1 ). A close reading of the relevant sections of text associated with each of these codes was then used to establish which of these themes are most pertinent to understanding the social and cultural barriers to implementing the 3Rs for zebrafish welfare, the topic of this paper—other themes identified, of course, relate more to emergent elements of the wider program. This was justified with primary reference to what participants themselves said about the 3Rs, our own experience of interacting with stakeholders and working in zebrafish facilities (participant observation), reference to themes in associated literature (discourse analysis), as well as in the light of secondary social science literature on the social organisation of animal science and the 3Rs.

Summary of main themes emerging from qualitative interviews.

These themes represent the top 25 codes generated by the authors in the process of data analyses. They are reported in descending order, from most used to least frequently used. Codes and the themes they represent often overlap. The number of times a code is used can suggest the importance of the subject to both the speaker and analyst, but the frequency of use is not on its own a measure of importance or relevance to the present topic.

While a number of foci suggest themselves, some of which the authors’ explore in forthcoming work, we have thus restricted the discussion below to three key themes: “knowledge and consensus”, “attitudes and experiences”, and “institutional support and capacity”.

In keeping with the intentions of qualitative research of this kind, emphasis is placed on depth as opposed to breadth. The sample size is small, and the results selected for presented here are indicative of a wide range of themes and key issues that should be taken into account rather than thought of as being representative in any way. A logical next step may be to use some of the perceived issues and concerns raised here as a basis for a larger, quantitative study. Inevitably, we have also neglected to discuss a number of important social and scientific issues relevant to understanding the challenges to taking up 3Rs initiatives focused on zebrafish, or fish in general. These include, for example, generic concerns about the lower status of animal welfare science and 3Rs related research versus the attractions of other fields of biological research and the relative ghettoisation of 3Rs research as a distinct category [ 84 ] (p.128). It is also possible that if and when concerns about the reproducibility of much zebrafish-based science grows, so too will “neophobia” increase in prominence as a barrier to 3Rs interventions with zebrafish though is not something reflected in our data [ 85 ].

Due to the sensitive nature of the topic (animal research), a policy of anonymisation and decontextualisation has been applied to all transcripts in order to ensure the privacy of participants. All names used in this paper are pseudonyms. All interviews were conducted with the written consent of participants. This research has been granted ethical approval by the Central University Research Ethics Committee (CUREC) of the University of Oxford (Reference Number: SOGE 18A-7). By agreement with the Wellcome Trust and research participants, anonymised interview transcripts will be deposited in the UK Data Archive based at the University of Essex ( https://www.data-archive.ac.uk ) after a period of 10 years from the completion of the Animal Research Nexus Project in 2022, except in cases where participants have explicitly opted out of this arrangement.

Focusing on Zebrafish

This paper focuses on zebrafish because, over the last three decades, they have become by far the most prominent species of fish used in animal research. In 2018, zebrafish accounted for 12 percent of all procedures done on live animals (including creation and breeding of GA lines) in the UK. All other species of fish combined accounted for 2.6 percent of animals used [ 86 ]. The species’ relatively steep rise towards the apex of lab “supermodels” has often meant that those seeking to develop 3Rs and other welfare-relevant scientific and husbandry protocols have had to work hard to keep up with the pace of change whilst striving to improve [ 80 , 87 ]. At the same time, the rise of the zebrafish, in conjunction with other trends such the intensification of aquaculture production and related public anxieties about environmental externalities and food safety, have most likely served to cast light onto the issue of fish welfare more generally, e.g., [ 42 , 88 , 89 ]. To this extent, and remaining mindful of the extensive diversity of fish kinds, many of the points made in this paper will nevertheless also be relevant to other fish species.

A number of factors are regularly cited as key attractions of the zebrafish model for biologists. These include its hardiness in captivity, small size, short generation time, rapid development and large clutch size. These factors also make them relatively cheap to maintain in large numbers. In addition, the comparative simplicity of the zebrafish genome facilitated the application of various molecular technologies. In combination with the extraordinary optical accessibility of its embryos and young larvae (they are transparent and fertilized externally to the mother’s body), these features have made zebrafish a highly tractable model for other vertebrate animals, and useful in a wide range of fields. However, these very advantages of the organism for science can also contribute to the entrenchment of particular attitudes towards them, and towards fish generally. Moreover, they can raise 3Rs considerations in their own right. Ironically, their hardiness in captivity has proven a disincentive for refining their husbandry conditions [ 90 ] (p.141). Depending on local aquarium practices and pricing structures, the low costs of maintaining zebrafish in large numbers and the ease with which they can usually be bred can create an incentive to keep transgenic lines running even when they are not being used, and a disincentive to cryopreserve and regenerate on demand—strategies which would be seen as more consistent with a reduction in animal use. The fact that zebrafish models can be valuable surrogates for other vertebrates also tends to compound the view of them as “lower” on the so-called phylogenetic scale, contributing in turn to the view that the use of fish (as embryos or larvae, but also adults) represents a kind of “relative replacement” for other vertebrate animals [ 91 ] (p.274), which is to say, a means for achieving 3Rs (replacement or refinement) targets, as opposed to individuals to whom the 3Rs principles of refinement, reduction and replacement could be applied (see also [ 92 ]).

The scale at which zebrafish are maintained and the ease and rate at which they can be induced to reproduce can also all contribute to a sense of their replaceability, and underline the difficulty of forming a bond with them as individuals—even in comparison to other small, short-lived and relatively easily replaced laboratory vertebrates like mice [ 93 , 94 ]. Some people, especially animal technologists, attempt to think of fish as unique individual beings that deserve attention as such. At one facility, we know there is an informal motto that runs along the lines of: “they’re all a group of fish, but every fish is an individual” (interview with Eugenie, aquarium facility manager, 8 February 2018). However, at the same time, it is acknowledged that this requires effort to sustain, and successful and lasting individualisation is the exception, not the rule (see also [ 95 ]). For all these and other reasons—some of which will be explored in more detail below—it is common to hear the argument that the apparent lack of social or ethical concerns associated with the use of fish in experiments is in itself one of the advantages of using zebrafish-based model systems, e.g., [ 20 ] (p. 407–408). Fish in general, but zebrafish specifically, are indeed frequently viewed as the “easier ethical option”, as one participant in our study put it (interview with Helen, representative of an animal welfare organization, 9 January 2019). In sum, while similar things may be said about other fish species, there are good reasons to pay special attention to zebrafish.

3. Results and Discussion

Analyses of our interview data suggest the presence of three especially significant social norms or discourses about fish welfare in the laboratory context. For summary purposes, we have labelled these “knowledge and consensus”, “attitudes and experiences”, and “institutional support and capacity”. Each of these narratives is internally diverse in terms of the individual opinions expressed, as well as overlapping and mutually reinforcing. Key themes included in the discussions which follow include: (structural) enrichment, fish, regulatory attitudes with respect to fish and the public; views about fish, embryos and larvae from within the aquarium and the size and composition of the zebrafish community

3.1. Knowledge and Consensus

Appendix A of the European Convention for the Protection of Vertebrate Animals used for Experimental and other Scientific Purposes (ETS123) provides key guidelines for the accommodation and care of animals used in science across Europe. Speaking about the challenge of managing a number of expert working groups convened by Council of Europe during the process of revising Appendix A in the early 2000s, an ex-UK Home Office Inspector told us “ [It] was like herding cats—they would not agree on anything ” (interview with Colin, ex-Home Office Inspector, 26 June 2019). In his experience, the field of fish welfare has been characterised by a lot of disagreement, often underpinned by insufficient knowledge of fish/zebrafish welfare science and of the basic biology that informs it, at least in comparison to the knowledge of the other major laboratory animal species. Similarly, our research suggests that, amongst those involved in the worlds of zebrafish science, there is limited consensus on what best practice is in a number of important welfare and 3Rs-relevant areas. Debate rages on numerous topics, including stocking density, food and feeding regimes, methods of anesthesia, euthanasia, the need for analgesia, and the need for environmental enrichment, to name only a few. This is reflected, as Colin explained, in the relative paucity of official guidance available for fish at the EU level or the level of individual member states—even for zebrafish, which are the most studied and used species. This section therefore explores narratives about knowledge, consensus and disagreement, focusing on two different examples. Firstly, the question of environmental enrichment, and secondly variation in beliefs about the ability of fish to feel pain and suffer, both of which are clearly relevant to welfare generally and the 3Rs specifically.

3.1.1. “Putting Things in Tanks”

There exists a division in the zebrafish community in the UK between those who are in favor of environmental enrichment, and those who raise concerns about it (see also [ 96 ] p.586). To be specific, some facility managers and technologists—experienced husbandry professionals, some with backgrounds in relevant scientific disciplines—express doubts about the benefits of structural enrichment: the addition of plastic plants, substrates and so forth so as to provide cover and stimulation for fish who otherwise live in barren, clear plastic tanks. Some suggested that structural enrichment can encourage abnormal behavior, but the most common issue raised was that the welfare benefits of structural enrichment were not very clear. Felix, an experienced facility manager with a background in research, suggested there was a fashion for “putting things in tanks” (interview with Felix, aquarium facility manager, 1 November 2018). Felix, and others whom we have spoken to who share his point of view, are far from dismissive of enrichment for fish in general but worry that a focus on structural enrichments is a distraction from the factors they think are really more important for fish welfare and should be the focus of attention. Felix terms these more important factors the “subtle enrichments, your lighting, your temperatures, your feeding, your flows, those are a much more valuable asset than a plastic plant within a tank”.

People like Felix worry that the evidence base about the value of such structural enrichments for zebrafish is weak. An ex-Home Office inspector comments:

I think probably the biggest constraint is just actually the lack of good data and scientific knowledge about what an appropriate environment for the zebrafish might be. I think again there is quite a lot of anthropomorphic views on what a zebrafish actually requires. You put them into an empty tank and that must be bad for them so they then put in lots of substrate and weeds and various other things in as well, you know, but we don’t really know, I don’t know… [interview with Craig, ex-Home Office Inspector, 25 June 2019]

Another facility manager concurs, arguing the welfare benefits of this kind of enrichment are in her estimation “fairly unproven”:

[W]e can’t make that much more progress I personally don’t feel unless we can really say this is what is good for them in terms of like environmental enrichment, do we want divers in there with bubbles, and why would we want that, where do they ever see that, or plastic plants, would they see that in the wild? Is it appropriate? [interview with Fae, aquarium facility manager, 27 February 2018]

No one, of course, is suggesting the use of plastic divers and shipwrecks in academic research aquariums. The point being made is that the desire for objects in tanks is largely a human one: it satisfies our humane and aesthetic demands, rather than (so the suggestion goes) the real needs of the animals (as far as we know). Hence it has been pursued in the absence of evidence about its benefits. Fae and others in her position do not disagree that it is possible to observe certain behavioral changes on the introduction of an object like a plastic plant or simulated substrate, for example, which suggest a preference for occupying enriched parts of the tank. It is the interpretation of what these observed behavioral changes might actually mean for fish welfare that is questioned.

These kinds of concerns were echoed by animal technologists who work closely with fish. For example, Frank noted:

We can look at cortisone levels or whatever but you don’t really know if you’re actually helping them. Like with a plant, I mean on one hand you’re creating cover for them to hide in if they’re getting bullied or fighting, on the other hand, you’re creating something for someone to get territorial about and stressed about. [interview with Frank, senior animal technologist, 18 January 2018]

A Home Office inspector also noted that

[I]n terms of enrichment, for instance, we don’t actually know largely what fish want. […] And I think that--, that’s a significant challenge to get over some of the hurdles and show people how it can happen. [interview with Gail, Home Office Inspector, 15 May 2019]

While Gail sees this lack of knowledge as a barrier to acceptance, this does not feature in her discourse as a reason for being cautious about advocating their uptake in aquariums. Evidently, people operate with different ideas about what a sufficient evidential bar is. This reflects divisions in the field of laboratory animal welfare more generally as to whether the intuitions and experiences of the practices and protocols developed by technologists in individual facilities offer a strong enough evidence base for novel enrichment practices [ 75 ]. In this context, it is, of course, possible to cleave too bio-physiological measures of “health” only, in which the psychological and emotional factors usually comprehended within the wider term “welfare” are excluded. [ 44 ]. However, the latter, more encompassing and holistic outlook certainly seems to motivate managers and technologists who go out of their way to provide structural enrichments when they can. Sometimes this can be a real labor of love. One establishment found it could not afford to buy plastic plants from a hobby shop, so developed a way of making “plants” by fashioning them from plastic bags and weighing these down with marbles. This took six months of soaking the bags in a light bleach solution to stop the plastic leaching substances that may interfere with scientific results, and careful and time-consuming handwork by staff members to shape the fronds and attach the weights [RM, Field Notes,11 January 2018].

Advocates of structural enrichment do cite published evidence in favor of their opinions. A paper suggesting that zebrafish express a preference for substrates by positioning themselves over photographs of gravel is particularly often cited in the UK (see [ 97 ]). Those already inclined to enrichment tend to find such evidence a better reason to act than others who are not. An animal welfare policy expert felt that these results clearly “show that they [zebrafish] benefit from environmental enrichment”, but implied that this evidence was ignored (interview with Helen, representative of animal welfare organization, 9 January 2019). Others object to this interpretation of the meaning of fish preference behaviors or report having been told of (the referecne to hearsay is deliberate here) statistical or methodological weaknesses in papers about enrichment, and explain that people they know—others in the field—have taken these as a basis for inaction.

We would suggest that these differences cannot be understood by looking at the published scientific literature only. Technologists and facility managers are moreover also at pains to point out the practical and economic downsides of structural environmental enrichments. For example, they can obscure technologists’ view of the fish whilst performing mandatory health checks, slowing them down and potentially leaving them less time for other important husbandry and welfare issues. They may also gather dirt and become unhygienic, and of course, they cost money to purchase in the first place which may have previously been allocated elsewhere.

Another factor shaping orientations on this topic seems to be an identification with and long-term exposure to the world of mammalian husbandry, and especially previous experience working with rodents. Amongst our participants, those who most clearly expressed skepticism towards structural enrichment (plants, houses, substrate or even images of substrate), tended to identify strongly as “fish people” first and foremost. They may, for example, have backgrounds in marine biology, aquaculture, or hobby aquaria, or simply have no or limited professional interaction with the world of rodent husbandry. In some cases, the facilities which we visited who do not enrich as a matter of course are geographically, socially and administratively separate from the biological service facilities which run mammalian animal units. They tend to see the need to put “things in tanks” as something imported from the world of “fluffies” (as the technologists at one facility called them), and often pushed by people with more knowledge of mice specifically than of fish. Fae again expresses the point: “we look to mammals”, she told us “and go oh yeah environmental enrichment, that’s structural things in tanks” (interview with Fae, aquarium facility manager, 27 February 2018).

On the other hand, Fae herself recalled how 20 or 30 years ago, it was common to see mice and rat cages that were entirely devoid of structural enrichments, like many zebrafish tanks today. Thus, the experience with rodents gets overlaid onto fish, as though fish must, or should be, on the same trajectory. In this case, “things in tanks” follow from being used to seeing “things in cages”. Evelyn, who is has extensive experience in all manner of mammalian husbandry, including running rat and mouse houses, and who takes pride in the compliment that her aquarium is run “like a mouse unit”, told us that

if the mice were in the same situation 20 years ago [as the fish are today] they were just mice, but now like we have to provide enrichment, we have to provide certain bedding and nesting materials, we have to do this, we have to do that, and at some point or other, maybe not in my time, but the fish will have the same rights [laughs] somewhere along the line. [interview with Evelyn, aquarium facility manager, 18 January 2018]

Thus, knowledge of the welfare trajectory of mice is actually an explicit motivation for pursuing innovations, including enrichment, for fish in some cases. To be clear, the point is not that some of our research participants objected to better or more complex enrichments. Rather, they expressed skepticism about whether structural enrichments specifically have positive welfare effects that outweigh their downsides in different circumstances. Notably, it seems that this doubt is likely to be spiced with concerns about the source of advocacy for structural forms of environmental enrichment, including the belief that this is an ideology that is imported, without due consideration to context and species differences, from the world of rodent husbandry. Such views are connected to identity as well as to evaluations of evidence .

The matter became more acute for some participants when they perceived pressure to adopt structural enrichments to be coming from regulatory authorities, the most visible face of which are the UK Home Office Inspectors (HOI). Felix, for example, stated that, in his view, it was the Home Office who starting pressing for enrichment for fish “because that’s what they did for rodents”. Cynically, he concluded that “[I] could have solved the majority of my problems [related to facility inspections] if I had just had a plastic plant in the tank” (interview with Felix, animal facility manager, 1 November 2018). Another facility manager we spoke to, a keen proponent of enrichment for all kinds of animal, lamented the fact that, in his opinion some researchers do actually choose to enrich as a kind of virtue signaling to outsiders, especially the Home Office, not because they actually care much about what it might mean for animal welfare (RM, Field Notes, 16 August 2018).

The objection to “putting things in tanks” is thus sociological as well as scientific: those making the argument draw not only on scientific evidence but on their understandings of the views of outsiders to the fish world and their relationship to authority figures, as well as more pragmatic material and economic factors. We would suggest that similar combinations of factors are present in the instances of a variety of other disagreements associated with fish welfare in the aquarium. It is also important to note that everyone would welcome more research into the use of enrichments specifically and the biology of fish welfare generally. However, it would appear—and this is an issue demanding more research—it is equally important to achieving a sense of agreement on the underlying framework for deciding on what good welfare is and how it should be assessed. Furthermore, as we’ve suggested, where welfare recommendations are produced or come from (by scientists, by technologists or by particular groups or individuals, for example) and who they are promoted by (aquarists, “mouse people” or an HOI and so forth) can be very important, over and above the recommendations themselves, in determining their reception by the laboratory animal community.

3.1.2. Pain and Analgesia

Although the view is not universal, for many people who work with fish, fish welfare generally and the 3Rs specifically only have meaning on the assumption that these animals are sentient beings, feel pain and suffer as a consequence [ 88 , 98 ]. This intuition is reinforced by the fact that the law in the UK and the European Union effectively assumes that they are sentient and certainly that they feel pain. As such, the ongoing and high-profile debate about whether or not fish have, as a matter of scientific fact, the capacity to feel pain and suffer [ 35 , 99 , 100 ] has limited direct influence on the implementation and development of 3Rs-orientated welfare initiatives targeted at fish. In the day-to-day running of laboratory animal facilities, good animal welfare is a matter of complying with regulation, not challenging the epistemic or ethical assumptions of the law with respect to the possibility of emotional and subjective experience in fish.

Nevertheless, the fact that there is a continuing controversy about fish pain might have a variety of more-or-less indirect effects that are relevant to understanding barriers to implementing the 3Rs with fish. Almost everyone we spoke to about this issue expressed varying degrees of uncertainty about whether fish actually feel pain, what this means to them, and whether humans will ever be in a position to know much about this. Given the oft-remarked phenomenon of “sentientism” (not to mention “speciesism”), this is unsurprising [ 101 ]. In some cases, though, opinions on the subject were connected directly to the scholarly debate. For example, one researcher who takes a negative view of the issue argued:

“What I want to say is, erm, I think it is a difficult subject because until you really know, you can’t estimate what an animal perceives or what it doesn’t perceive. But what all the research shows at the moment is that you [the fish] do not have the higher brain structures required to perceive pain. [interview with Hanna, researcher, 27 November 2018]

In other cases, it was based more on personal intuition and belief. Referring to the behavior of post-operative fish, Evelyn said:

They [the fish] act like everything is fine, but there is always a nagging doubt in the back of my head, there always will be. My dad was a fisherman, you know, and you can’t tell me that having a hook through your lip is not going to be painful. Can they [the fish] feel it? I don’t know. [interview with Evelyn, animal facility manager, 18 January 2018]

It is hard of course in any case to attribute the causes of particular actions or lack thereof specifically to beliefs about fish pain. However, there are a number of specific areas where such beliefs are more likely to shape action and influence debate in the field.

The foremost example of this is probably the use (or lack thereof) of analgesia. Some of our participants pointed out that it is a default legal requirement to administer pain relief for all protected animals when appropriate, yet in the case of fish there was no standard analgesic authorized for use, nor indeed is analgesia use as widely practiced as it could be. There are many reasons that the use of analgesia following procedures on small fish like zebrafish may be problematic. Many of these refer to basic problems of a lack of evidence and/or consensus. Problems include a need to better understand the trade-offs between analgesia and other welfare concerns. For example, does the benefit of analgesia for a social species like a zebrafish outweigh the benefits of remaining in group housing, since isolation is usually necessary to administer it, and in what circumstances? They also include limited knowledge of the potential confounding variables that analgesic agents can introduce into experimental outcomes, a lack of knowledge of the pharmacological effects of different analgesic agents on different species, as well as problems connected with how to recognise and assess the effectiveness of these agents in these animals [ 102 , 103 ].

Nevertheless, more than one veterinarian has proposed that the existence of controversy on the subject of fish pain could be an underlying factor explaining the unwillingness amongst those responsible to implement analgesia protocols [ 104 ]. In the opinion of Schroeder and Mocho [ 105 ] (p.36), moreover, there is a danger that prospective applicants for licenses downplay evidence suggesting that fish do feel pain in favor of emphasising that it has not been conclusively shown that they do, and interpret the latter “as ‘carte blanche’ to avoid the use of analgesics altogether”. While much more fine-grained evidence needs to be gathered in order to understand resistance to, or at least slowness of spread, of analgesic protocols at the facility level, there are reasonable grounds for considering the fish pain controversy to be a contributory factor. While pain itself could be seen as introducing confounding effects, in one case we are aware of, permission not to administer analgesia following invasive surgery was granted for a combination of reasons, both scientific (related to the introduction of confounding effects) and welfare based, including the production of published arguments suggesting that fish are unlikely to experience the emotional effects of pain of the sort associated with higher and forebrain structures in mammals (interview with Hanna, researcher; RM Field Notes, 11 January 2018). So, plausibly, it is at least something which could tip the balance against analgesia in tie-breaker situations. Again here it is not only the scientific evidence which is shaping decisions about fish welfare, but how that evidence (or the lack thereof) is selectively deployed in decision making processes, with individuals most drawn to the evidence they believe supports their case, as has long been observed by science studies scholars in a range of fields of research, e.g., [ 106 ].

While the debates over analgesia use offer an example of the fish-pain controversy potentially shaping welfare practice, the most important effects of the ongoing debate on fish pain are likely to be more diffuse, influencing attitudes and priorities in subtle ways. In particular, there is the possibility that uncertainty about the nature of fish sentience gets shifted into plausible but unsubstantiated beliefs about fish’s relative lack of sentience in comparison to other vertebrates in some kind of a putative scale of sentience for which there is little or no objective basis. While regulations sensitive to the recognition of degrees of sentience may one day be possible and desirable [ 107 ], as it is such views about differences amongst vertebrates are likely to be informed by outdated ideas about the phylogenetic scale [ 91 ], as well as more arbitrary and sentimental ideas about what people believe is acceptable to do to different categories of animal [ 6 , 9 , 108 ]. A Home Office Inspector we interviewed tried to pick her way through this complex terrain:

So there’s been huge arguments over those 20 years about are fish sentient at all? […] And I’ve always taken the presumption, well it’s in our law, that they wouldn’t be protected if they weren’t sentient--, if we didn’t believe they were sentient [they wouldn’t be there] and therefore we should be doing the best that we can for them. But equally they are a fantastic model as a replacement because, as far as we know, they are less sentient than other species, but we don’t know. So we would still suggest that it is better to move into zebrafish than to use mice, and I say that with some hesitancy […] most people in society I think would be more comfortable with fish being a replacement for mice. [interview with Gail, Home Office Inspector, 15 May 2019]

In this passage, it is very clear how beliefs about what the public feel about the use of different animals fills the gap opened up by the admission of fundamental uncertainty about the nature of fish sentience and experience. This movement is common in our experience. The concept of “societal sentience” has been proposed to understand such situations [ 109 ]. This refers to how people, especially policy makers, imagine what the public feels about animals—i.e., it is the feelings (sentience) of people that are in focus here, more than animals. In this context, relationships and attitudes to animals like fish, as well as beliefs about the extent to which those attitudes are shared with a wider ‘socially sentient’ public, can become extremely important in mediating decisions about their use and, by extension the urgency and relevance of 3Rs initiatives. This is the subject of the following section.

3.2. Attitudes and Experiences

When there is an acknowledged lack of scientific consensus on issues that are of community and policy relevance, the values and perspectives held by collective and individual stakeholders can play a key role in shaping policy decisions and practices [ 110 ]. This section explores attitudes towards fish and the 3Rs held by those working in research settings and the factors shaping them. It focuses on the influence of those involved in regulation, including policy documents and legislation, as well as those with first-hand experiences working with zebrafish.

3.2.1. Regulators and the Public

The legal framework that regulates animal research in the UK is remarkably un-speciesist. Fish are formally afforded the same protections as most other vertebrate animals. For example, the two most commonly used laboratory animals—fish and mice—have exactly the same status in legislation. The importance of this should not be underestimated—not only in legal terms, but in terms of the broader agenda it helps set and the message it sends to all who work in the field. However, this picture changes somewhat with a closer look at the legislation and especially its modes of implementation. What emerges is a sense of hierarchy. In the UK, some animals do have some additional protections consequent on their special status in human society (primates, cats, dogs and horses). This suggests a subtle gradient of “social acceptability” in terms of what is expected to be tolerated by the public [ 109 ] (p.683) and, consequently, a prioritisation of the interests of certain species above that others emerges.

In the UK, the Animals in Science Regulation Unit (ASRU), based in the Home Office, is responsible for regulating the operation of the Animals (Scientific Procedures) Act 1986 (ASPA). ASRU’s Inspectorate division plays a key role in interpreting and applying the law and developing policy. A central element of this is reviewing and approving project license applications (a license is required to perform regulated experimental procedures on regulated animals in the UK). As a part of applying for a license, prospective licensees are required by law to demonstrate they have considered the 3Rs in the development of their research program. To assist applicants in completing the necessary documentation, the Inspectorate produce an annotated license form. This guidance document suggests applicants justify that their chosen animal model is the most refined possible, asking as prompt: “Why can’t you use animals with a lower capacity to experience pain, suffering, distress or lasting harm, e.g., fish instead of mice?” [ 111 ] (p.22). (The document is called “ASPeL Project License Application Template—General License Under the Animals (Scientific Procedures) Act 1986”, version V 2.0 21/12/17 and is (at the time of writing) still available via the Home Office website. Previous versions contained similar advice.) It is hard to assess the specific effects of this kind of “official” advice, but it is likely to have proven important in the past in promulgating the idea that the use of fish versus mice (or other mammals) is a kind of refinement or “relative replacement” in itself. For example, one grant awarded by the UK’s main 3Rs funding body, the NC3Rs, explicitly described the use of zebrafish as “a great opportunity for reduction of the use of higher order vertebrate species thereby reducing animal suffering” as its central 3Rs justification see [ 112 ]. This suggests embedded social and cultural assumptions about the sentience of fish and mice that are hard to justify purely in scientific terms. Implicitly or explicitly viewing the use of fish versus mice in this way sits awkwardly with the formal equality articulated in the definition of protected animal in legislation. It actually undermines what has been years of effort by Inspectors and others in the UK to elevate the status of fish and promote their welfare—and indeed recent advice has clearly moved away from this.

The management of risk is a related important way in which representations of the public’s putative attitude towards fish may be made relevant to regulators. In our interviews, HOIs themselves talk a lot about risk assessment and risk management, particularly in terms of the allocation of Inspector resources and site inspections. A risk-based approach has become increasingly central and formalised in the wake of tightening budgets in the last decade. Risk in this context refers to a number of things, especially risk of non-compliance with the law and the presence of new species and use of novel procedures at a facility [ 113 ] (pp.22–23). But what could be described as “societal concerns” also emerged in our research, informing these sources of risk and adding their own dimension (see also [ 114 ] p.16). This includes concerns about the possibility of overt public outcries over the use or mistreatment of animals in research, and we suggest that in practice this is often interpreted as political or reputational risk to the Minister. For example, Craig, reflecting on the acceleration of a risk-based management approach at the Home Office, told us that in his opinion “the whole thing that actually drives ASPA [legislation] I think is essentially public perception” (interview with Craig, ex-Home Office Inspector, 25 June 2019). Thus, work involving specially protected species for which the public has great sympathy, such as with nonhuman primates, is typically viewed as especially high risk. Heather also noted how “public perception and risk” are a part of the calculation which informs how Inspectors allocate their attention:

You know, so obviously, the feeling is that the public would prefer, if you like, primates to be inspected more frequently and are maybe less concerned about mice being [inspected]. [interview with Heather, ex-Home Office Inspector, 17 January 2019]

This is clearly connected to ideas about species hierarchies, albeit in contextually specific ways.

Craig and Gail also referred to conservation work involving badgers as an example of an especially high-risk research program because badgers are believed to command a great deal of public attention and have been widely politicised in the UK (see [ 115 ]). In contrast, Gail says, “there are people who are doing conservation work on species that perhaps are not so high in the public consciousness and so the relative risk for the Minister then is lower” (interview with Gail, Home Office Inspector, 15 May 2019). Things which are likely to scandalise the Secretary of State are, of course, breaches in legal compliance in terms of animal welfare law, and harms being caused which are indefensible in the face of limited benefits. Thus, animal welfare and the management of (political) risk are not incompatible goals, but they are not necessary always perfectly aligned either. Zebrafish per se cannot be said to rank as a low priority in all circumstances—this would be too much of a generalisation and a lot of effort has gone into trying to raise the profile of zebrafish welfare at the Home Office and beyond. However, given what has been said about the perception of fish, their representation in the regulatory discourse, and widespread assumptions about what the public feel about fish, it is perhaps not unreasonable to suggest that they might occasionally fall between the cracks created when the different prerogatives of risk assessment are misaligned. This could contribute in turn to the effective, though unintentional, marginalisation of fish and a reduced likelihood of their being prioritised as candidates for investment in welfare interventions.

The relative marginalisation of fish is also evident in the materials of organised campaign groups, who are capable of aggregating and directing diffuse and ill-formed public sentiment, and who are an important intermediary in shaping the perspectives of those who make and enforce and policy [ 116 ]. A review of the homepages of relevant organisations in Britain suggests that they do not consider fish an important focus for their campaigns. The websites of the main groups campaigning for the abolition of animal research in the UK (Cruelty Free International, National Anti-Vivisection Society, Animal Free Research UK) feature a total of zero images of fish on their homepages, though primates, dogs and rabbits are well represented. The RSPCA’s Laboratory Animal’s webpage, despite the organisation’s important role in disseminating husbandry and welfare standards [ 71 ] and raising awareness of fish welfare in UK labs, likewise featured no images of fish at the time of writing. Turning to the homepages of UK-based organisations specifically focused on funding 3Rs initiatives and/or the development of alternatives to the use of animals in science (FRAME, NC3Rs, Lord Dowding Fund), we find a total of one fish-related image out of a total of 17 representations of animals displayed at any one time. Indeed, fish are not the “poster critters” of animal research generally: homepages of the major “industry bodies” (Institute of Animal Technology, Laboratory Animal Science Association, Laboratory Animal Veterinary Association) feature zero images of fish out of total of 15 representations of animals. (This analyses was performed on 20/08/2019. All identifiable representations of animals were counted, including organizational logos. Addresses for the relevant websites are as follows: National Anti-Vivisection Society: http://www.navs.org.uk/home/ ; Animal Free Research UK: https://www.animalfreeresearchuk.org/ ; Cruelty Free International (previously BUAV): https://www.crueltyfreeinternational.org/ ; RSPCA Laboratory animals: https://www.rspca.org.uk/adviceandwelfare/laboratory ; FRAME: https://frame.org.uk/ ; Lord Dowding Fund: http://www.ldf.org.uk/research/ ; NC3Rs: https://www.nc3rs.org.uk/ ; LASA: http://www.lasa.co.uk/ ; LAVA: https://www.lava.uk.net/index.php?sid=2dc936c14ca15e85e7d76b7d6b23092a ; IAT: https://www.iat.org.uk/ . The National Anti-Vivisection Society and Lord Dowding Fund websites feature a new stock image in their banners each time their pages are refreshed. Out of a total of at least 18 unique images registered, none feature fish.) Thus, if the unofficial status of fish is at least partially a function of the perception of the Inspectorate with respect to societal concerns and political risk, it is arguably a reasonably well-grounded one.

3.2.2. Relating to Fish in the Aquarium

The views of the “general public” are thus important (see, e.g., [ 18 ]), but what is perhaps most critical in the light of our discussion is appreciation of how the public is imagined by policy makers [ 109 ]. This imaginary in turn shapes the priorities of regulators with implications for the scrutiny and prioritization of 3Rs efforts. This could be viewed as a “top-down” influence on the implementation of the 3Rs for fish. Complementing this insight, we turn attention in this section to look in more detail at some of the views about fish held by technologists, aquarium managers and veterinarians, because these are also central to the development and application of the 3Rs in situ [ 75 ], or from the “bottom-up”.

In our experience, it is very common for people who work with fish on a daily basis to object to what they see as the semi-official neglect of fish and the tendency to view the use of fish as in itself a kind of refinement or even replacement. These attitudes are often accompanied by a desire to advocate for fish and see them treated equally with other animal denizens of the lab:

So, I think this idea that fish are some sort of replacement, I don’t think it’s right because we’ve decided to protect these animals so they should all be treated equally. [interview with Fiona, Named Veterinary Surgeon, 8 February 2018]

They should have the same rights as everything else, and it might be just a fish, but going back a very long time someone told me that it was just a monkey… So you know, there should be no difference in my--, I know a monkey is a monkey and intelligent, but they’re in this building looking at us to be their eyes, ears and voice and protect them, there should be no difference whether it’s a fruit fly or a fish or a monkey or a pig or a mouse, whatever. [interview with Evelyn, aquarium facility manager, 18 January 2018]

At one animal facility, we observed how a poster on a corridor wall advertising aspects of the European Directive (2010/63) on the use of animals in research was decorated with images of small furry mammals. Irritated by the absence of a representation of fish, aquarium staff had stuck pictures of fish over them [RM Field Notes, 11 January 2018, Figure 1 ].

An image of zebrafish is pasted over an image of mouse on an education and training poster at a UK zebrafish aquarium facility (detail from poster). 29 October 2019. Photo credit: Reuben Message.

It is also common for people who work regularly with fish to say that they see fish and other animals as equals, but that they are aware of people who do not:

[For me a fish is] still a living being so I don’t see it as being different myself. But I think a lot of people feel differently. [interview with Francis, researcher, 20 April 2018]

At the same time, however, people who work with fish will also often admit that they themselves do not feel the same way about fish as they do about other animals, especially mammals. Asked whether she empathised with her fish, Erica demurred with some difficulty:

I think that [the word empathy] might be too strong. But definitely in that direction. Yeah, it’s because their faces are different [laughs], so you can’t really empathise with something that looks different from you, I think. Not that I’m saying that’s the right thing, but--, [interview with Erica, senior animal technologist, 23 April 2018]

Despite being, as we have seen, a very enthusiastic champion of the “equal rights” of fish and advocate of laboratory animal equality, Evelyn admits that she finds working with fish emotionally less engaging. Fish are more difficult to attach to than animals like primates, pigs, sheep, rabbits and rats [interview with Evelyn, aquarium facility manager, 18 January 2018]. Grant, an experienced fish researcher and keen aquarium hobbyist, noted:

[…] from a personal point of view you can fairly well guess I care about my fish, and that lights me up. […Yet] I still feel more comfortable that we would use a fish rather than a mouse any day of the week. Even the smartest fish. That step into mammals--, […] is a difficult thing to deal with. [interview with Grant, researcher, 6 February 2018]

Gideon, another zebrafish user, declaimed the “double standard”, as he sees it, that gets applied to fish, but then noted that he also understands why the double standard exists because he feels it himself, and speculates on the causes:

Yeah, less emotional attachment. It’s undeniable, it’s not the same. […] I don’t know, maybe because it’s sushi. [interview with Gideon, researcher, 9 October 2018]

Frank, reflecting a very common theme amongst aquarists, noted that if he “had to cull a pig or a dog or a cat, I wouldn’t be in the job”, and explained that:

I’d rather work with fish because you don’t get the attachment that you would with mice. Maybe I’m the other way. I try not to be, but I am quite sort of, I can be anthropomorphic. I know that you can’t reflect your emotions onto them but it’s hard not to do so. In that sense I don’t have that relationship with the fish. I take them seriously and I care seriously and I want them to be healthy, but it wouldn’t keep me up at night, if I had to cull some fish at the end of the day it wouldn’t keep me up at night. [interview with Frank, senior animal technologist, 18 January 2018]

There are of course many reasons why fish generally and zebrafish specifically engender this kind of ambivalence, even amongst people who know them best and attend to them often on a daily basis. As discussed above, these include their small size, their relatively short lives and high reproductive rates, and the often very large numbers in which they are kept. All of these factors militate against humans forming lasting bonds with them as individuals. Then there are other specific biological and ecological characteristics of fish: their lack of “face” and “voice” with familiar interactional and emotional cues [ 66 ]. They lack what has been termed “nonhuman charisma” [ 117 ], an ascribed property of some animals that has been credited, in the context of animal conservation, with generating social interest and species–specific knowledge bases which in turn forms the basis for decisions on policy and funding priorities. In this sense, nonhuman charisma leads to what could be thought of as differing degrees of “political” influence for different animal taxa.

In the case of aquarium fish, the water adds a further element of detachment; while wild fish are even more remote, it’s still the case that even when in the same room as us, captive fish live visibly separate lives from our own, behind glass and in a different element.

Because they’re in glass tanks and they’re very separate you don’t kind of get that interaction quite the same as you would with a smaller mammal. [Consequently], it’s easier to kind of detach yourself a little bit emotionally from that fish. [interview with Gemma, senior animal technologist, 8 February 2018]

Such themes of perceived psychic distance are very common in discussions with technologists and others who work with zebrafish. For Fae, though, this results in a regrettable state of affairs. She argued that people’s ability to relate or attach to animals plays too big a role in driving priorities, to the detriment of fish welfare:

And I think this is what it is, I mean this is what I find annoying at times, it’s not really about the fish it’s what people can relate to and what people believe, and you know this is why we have these massive variations in welfare with fish because people just don’t get it and like they’re not thinking--, you know, if they can’t relate to it themselves I think it’s much harder. [Interview with Fae, aquarium facility manager, 27 February 2018]

It is difficult to connect these kinds of attitudes directly to the situation of the 3Rs. Harboring the kinds of conflicted emotions that we have been discussing of course does not preclude one from being active in pursuing 3Rs initiatives because people can be inconsistent and motivated by many different and competing prerogatives at once. But areas where these kinds of feelings amongst scientists and technicians towards fish do seem particularly likely to influence their actions or priorities, however, include the assessment of welfare and especially severity. Feeling emotionally and thus morally distant from fish in their alien habitats could conceivably compound the practitioners struggle to recognise, evaluate or correctly rank relevant signs of ill welfare or suffering.

3.3. Institutional Support and Capacity

The challenges of a contested evidence base, combined with general sense amongst both general “public” and those working with laboratory animals who find it “hard to care” about fish are compounded by (and arguably compound) the challenges that are experienced in mobilising institutional support for 3Rs initiatives. It is obvious that the kind and degree of institutional and economic support for fish-focused 3Rs initiatives are crucial to their success. A great deal could be said on this point, though much of this would apply to barriers to the development of the 3Rs for all species, not just fish or zebrafish. We focus here on only one main point with the claim that, as important as zebrafish are as a model organism, the size of the scientific and technical community it supports are still significantly smaller than the mouse community, and this means that it often does not possess the diversity of functions necessary to identify problems and credibly take forward solutions to them. In his observations, however, ex-HOI Colin, who has a lot of experience across the European Union as well as the UK, made this point most perspicuously. While gesturing towards the issue of funding, he explained that the problem is not simply that there was not enough of it, but that, in comparison to rodents, there was not yet within in the zebrafish world sufficient capacity to compete for it on even terms. Thus, Colin described a relative absence of what he called a “welfare support group” comprised of “vets, technicians [technologists], and welfare scientists” analogous to that which exists for what he called “the furries”. As he explained:

[fish-directed 3Rs research] is not sexy enough I don’t think and there’s not enough people involved to actually--, you know, because it’s difficult for technicians [technologists] to go to Wellcome [funders of biomedical science] and say, “Could I have a pot of money?” or even NC3Rs [National Centre for the 3Rs], whereas there’s a lot of people out there who’ve done animal welfare degrees or whatever and are interested in furries or whatever, and they know they’ll get funding. [interview with Colin, ex-Home Office Inspector, 26 June 2019]

And, he continued by pointing out that

[…] the other issue with fish people, the fish scientists are--, zebrafish scientists tend to be totally focused on zebrafish and the science, they’re not all that interested in welfare, they’re not behavioural type people, whereas in the furry world you’ve got behavioural type scientists who are interested in [welfare and the 3Rs]. [interview with Colin, ex-Home Office Inspector, 26 June 2019]

This is, of course, just the impression of one experienced observer, but it suggests an important point. Namely, that the diversity of available skills, interests and concomitant credibility is a function to some extent of the size of the extended community of practice. If this community is small, this represents an important sociological constraint on the development of new 3Rs interventions.

In our experience, many 3Rs-relevant welfare and husbandry initiatives are, in fact, driven “from the bottom up” by technologists and aquarium facility managers, not only academic research scientists. In the UK, centers of excellence have emerged around some, usually sizable aquariums managed by motivated individuals, though there is no particular pattern to this: in some cases, these individuals have backgrounds in general animal management or the management of rodents in particular but have become over time become leaders in the field of fish husbandry; in other cases, managers have backgrounds in aquatic biology, fish behavior or indeed biomedical research, and have moved into management. Many such initiatives are very local and small scale. The development of “DIY” environmental enrichment (see above) falls in this category, as does the move by one facility to introduce spirulina as an additive to fish diet (this has the effect of enhancing the lateral pink streak often expressed by male zebrafish. As a consequence, lab users are able to easily and reliably identify the sexes visually, instead of needing to anaesthetize them for closer examination as had been done routinely previously by some lab members). Other initiatives may begin life on the aquarium floor, but expand outwards: for example, the first Body Condition Scoring System for zebrafish was developed by staff at University College London’s zebrafish aquarium [ 118 ]. Initiatives such as the Zebrafish Health and Welfare Glossary, which promotes a standardised approached to welfare evaluation and nomenclature, have also been developed and primarily promoted by technical staff [ 119 ].

Local, technologist-led 3Rs initiatives are likely to vary considerably in the degree to which they are supported—in all senses of the word—by academic scientists and the wider bureaucratic, professional and institutional structures in which they emerge and to which they relate. While those who initiate and become involved in such efforts may have different or mixed motivations—from personal desire to change the lives of animals for the better, to a sense of professional responsibility or career ambition—it should be noted that in doing so they are liable sometimes to go beyond the proverbial “call of duty”, and there are consequently limits as to what can expected in terms of uptake and scale.

Academic researchers, of course, are not absent from this picture. Many 3Rs-geared ambitions for zebrafish would be impossible without specialist scientific expertise. In the UK, for example, Lynne Sneddon and colleagues have published influential data from numerous experiments focused explicitly on the possibility of deriving 3Rs interventions from them, for example, in areas such as analgesia research [ 81 , 120 , 121 , 122 , 123 ], enrichment [ 97 ] and automated welfare monitoring [ 124 ]. Academic researchers have also led in the development of protocols with direct 3Rs implications, for instance, concerning the genotyping of zebrafish by means of fin clips on very young larvae (3dpf) [ 125 ]. Indeed, looking at the database of funded research from the premier source of 3Rs funding in the UK—the NC3Rs—we find as of 2 December 2019 that with one exception, all funded zebrafish-based projects have established research scientists listed as their principal investigators. (See NC3Rs “Our Science” search results for the keyword “zebrafish”. The search was restricted to all kinds of grant and excluded training see shorturl.at/qL489. The exception is a veterinarian fronting a project investigating behavioral and physiological responses to fin clipping). This reflects the nature of applications received, and it is of course correct that awards for projects requiring detailed knowledge of scientific design are headed by those competent in this area, and is a reflection of active involvement by academics—notably, though, a large proportion of these awards focused on developing <5dpf embryos models, not on the benefits to fish as ends in themselves. It is of course possible that in some cases, technologists may be actively involved behind the scenes in some cases. Nevertheless, this should be set against Colin’s contention that those often most motivated to get involved with 3Rs work that benefits zebrafish do not have the means or credibility (including knowledge of research design, for example) to get the most desirable kinds of support for their work. Indeed, some may find themselves unable to apply for certain funding streams because of the non-academic classification of their roles and career trajectory, whatever their competence as scientists.

There seems certainly to be a niche or gap to be bridged between the local and less “science-heavy” 3Rs initiatives and those requiring special expertise in research design and data analyses, as well as specialist and expensive technologies. Developing and validating replacement models, for example, tends to be very “science-heavy”. Speaking of the importance of collaboration and capacity building in this area, one of our informants also described the need for what he called the “dovetailing” of interests, in particular, finding ways of bringing the scientific nous and technologies of academic researchers to bear on husbandry related problems in ways which could benefit everyone; scientists, technologists and fish. For example, the use of fluorescent markers of neuronal activity, as routinely done in many labs, could help to answer basic issues related to husbandry and welfare, such as the identification of appropriate endpoints (interview with Farol, aquarium facility manager, 21 March 2018). Efforts in this direction, however, face at least two general problems. Firstly, there is the problem of a lack of incentives for academics on a conventional scientific career path, given the lower status of such questions in the hierarchies embedded in the scientific reward system, and the relative ghettoisation of 3Rs and animal welfare science work generally. Secondly, the social stigma we have discussed that apparently continues to position fish as a means of achieving reductions or refinements, rather than as a focus for receiving 3Rs benefits. For Colin, at least, it is worth noting that an underlying reason for 3Rs/fish welfare research not being considered “sexy enough” (see above), is the attitude that “they’re only fish”, and thus do not warrant the attention (interview with Colin, ex-Home Office Inspector, 26 June 2019). These kinds of attitudes probably compound the basic problems of size and capacity suggested here.

4. Conclusions

While fish are rarely the “poster critters” of animal welfare campaigns, the welfare of aquatic species, in general, is increasingly becoming an object of social interest and concern, as well as scientific relevance. Moreover, given that ASPA makes no distinction between fish and other forms of vertebrate life in its definition of a protected animal, and that scientific opinion about the capacity of fish to suffer seriously is mounting, there is an ethical, regulatory and scientific remit for focusing on barriers to implementing and developing the 3Rs for fish. In this paper, we have shown how qualitative social science offers useful insights into the social drivers that could be influencing thinking, prioritisation and implementation of the 3Rs with respect to laboratory fish welfare.

Firstly, we highlighted the importance of narratives about knowledge, consensus and disagreement. In our examples, limited knowledge of what constitutes appropriate environmental enrichment for zebrafish and disagreements over the ability of fish to feel pain and suffer, can hamper the implementation of refinements, despite regulatory encouragement. Furthermore, an awareness of where knowledge about what constitutes “good welfare” is produced and who it is promoted by can be as important as the knowledge itself in shaping its reception and the consequent implementation (or not) of refinements. This is seen, for example, in the division between those with a lot of experience with mammals who are inclined towards “putting things in tanks” as they are used to seeing “things in cages”, and those who have worked mainly with fish and suspect other who suggest more subtle enrichments such as lighting regimes and water chemistry are more important. We also described how the existence of controversy on the subject of fish pain could be an underlying factor explaining the unwillingness amongst those responsible for implementing analgesia protocols, for example. We also proposed that there is a kind of scale of sentience, which ranks fish below other vertebrates and which shapes attitudes to fish welfare despite having little or no objective basis.

Secondly, we discussed how relationships and attitudes to fish, as well as beliefs about the extent to which those attitudes are shared with a wider ‘socially sentient’ public, may be important to mediating decisions about their use, their deployment as an alternative for other animals with the same legal status (such as mice) and, by extension, the urgency and relevance of 3Rs initiatives. For example, we noted how the apparently relatively low priority given to fish welfare amongst animal welfare and rights organisations is often linked to a perceived lack of broader public concern. Regulators may also follow suit, despite their best intentions and efforts. In this context, those who work with fish in laboratory settings often act as advocates for fish to be treated equally with other animal denizens of the lab. However, even within laboratory settings technologists, researchers and vets can struggle to relate to fish and find themselves questioning the extent to which they have internalized an image of fish as somehow less sentient and capable of suffering than mammals. This highlights the importance of a degree of self-awareness and reflexivity amongst those responsible for assessing fish welfare and implementing the 3Rs (already evident in the words of many of the those we spoke to) about how practices are shaped by social beliefs, experiences and values as well as scientific expertise.

Finally, we noted how more general trends towards a lack of investment and research interests in the 3Rs, recognised across the animal research community, are compounded by specific issues associated with the overall capacity of zebrafish community to engage successfully in 3Rs initiatives. In this context, we also presented the claim that zebrafish have not hitherto been perceived as “sexy enough” to attract the attention of enough credible experts in animal welfare science and animal behavior who are interested in pursuing 3Rs-related work. In our experience, moreover, many 3Rs-relevant welfare and husbandry initiatives are also driven “from the bottom up” by technologists and aquarium facility managers, not only by academic research scientists. This led to our informants highlighting the need for further collaboration and capacity building in this area, bringing the scientific knowledge and approaches of academic researchers to bear on husbandry related problems in particular, in partnership with motivated technical staff.

Acknowledgments

Penny Hawkins, Hibba Mazhary and colleagues, collaborators and advisors on the Animal Research Nexus project, including Alexandra Palmer who helped conduct some of the interviews cited in this research. We would also especially like to thank everyone who gave their time to participate in our research, who shared their knowledge, and who often hosted us at their places of work.

Author Contributions

Conceptualization, R.M. and B.G.; methodology, R.M. and B.G.; investigation, R.M. and B.G.; writing—original draft preparation, R.M. and B.G.; writing—review and editing, R.M. and B.G.; project administration, B.G.; funding acquisition, B.G. and the Animal Research Nexus team.

This research was funded by the Wellcome Trust, grant number 205393/A/16/Z as a part of the Animal Research Nexus project. The APC was funded by a Wellcome Trust Block Grant to the University of Oxford.

Conflicts of Interest

The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results.

A.3 Ocean Biology and Biogeochemistry Inclusion Plan Correction

A.3 Ocean Biology and Biogeochemistry (OBB) focuses on better understanding the ocean’s role in the Earth System, and predicting future causes and impacts of change driven by Earth’s climate, the environment, and event-scale phenomena on ocean biology, biogeochemistry, and ecology. A.3 OBB requests the following subelements of research investigations in no priority order:

• Tipping points and episodic events, and their impacts to aquatic ecosystems.
• Advancing the remote detection of floating debris.
• Refining our predictive understanding of the ocean biological pump.
• Successor studies

A.3 OBB has been corrected. The summary table of requirements for anonymized proposals lacked a row for the inclusion plan. The anonymized inclusion plan is to be placed in a special section of up to two pages following the OSDMP, see Sections 3.5 and the Table in Section 5.1. New text is in bold. The due date remains unchanged: proposals are due July 3, 2024.

Questions regarding OBB may be directed to Laura Lorenzoni at [email protected] and Kelsey Bisson at [email protected] .

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Mediterranean Coastal Fish Biology and Ecology

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The Mediterranean Sea hosts a relevant number of emblematic species and habitats, which give rise to high diversity and endemism. Coastal fish cover several extremely important roles in marine ecosystem functioning, and many species are highly exploited by fisheries and support the economy of several ...

Keywords : Mediterranean Sea, Coastal Waters, Fish Ecology, Fish Biology, Habitat, Trophic Relationships, Fish Communities

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