Abstract
Changes in behaviour and physiology are the primary responses of fishes to anthropogenic impacts such as climate change and over-fishing. Behavioural changes (such as a shift in distribution or changes in phenology) can ensure that a species remains in an environment suited for its optimal physiological performance. However, if fishes are unable to shift their distribution, they are reliant on physiological acclimatization (either by broadening their metabolic curves to tolerate a range of stressors, or by shifting their metabolic curves to maximize their performance at extreme stressors). However, since there are links between fish physiology and behaviour, changes to either of these trait groups may have reciprocal interactions. This paper reviews the current knowledge of the links between the behaviour and aerobic metabolic physiology of fishes, discusses these in the context of exploitation and climate change and makes recommendations for future research needs. The review revealed that our understanding of the links between fish behaviour and metabolic physiology is rudimentary. However, both are hypothesized to be linked to stress responses along the hypothalamic pituitary axis. The link between metabolic physiological capacity and behaviour is particularly important as both determine the response of an individual to a changing climate and are under selection by fisheries. While, it appears that all types of capture fisheries are likely to reduce the adaptive potential of fished populations to climate stressors, angling, which is primarily associated with recreational fishing, may induce the separation of natural populations by removing individuals with bold behavioural traits and potentially the physiological traits required to facilitate behavioural change. Future research should focus on assessing how the links between metabolic physiological capacity and behaviour influence catchability, the response to climate change drivers and post-release recovery. The plasticity of phenotypic traits should be examined under a range of stressors of differing intensity, in several species and life history stages. Future studies should also assess plasticity (fission or fusion) in the phenotypic structuring of social hierarchy and how this influences habitat selection. Ultimately, to fully understand how physiology is influenced by the selective processes driven by fisheries, long-term monitoring of the physiological and behavioural structure of fished populations, their fitness and catch rates are required. This will provide information that can be used by managers to retain behavioural and physiological trait diversity, which will be necessary to improve the resilience of fished populations to the impacts of climate change and safeguard the provision of resources for future generations.
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References
Abeliovich A, Paylor R, Chen C, Kim JJ, Wehner JM, Tonegawa S (1993) PKCγ mutant mice exhibit mild deficits in spatial and contextual learning. Cell 75:1263–1271
Almeida JA, Barreto RE, Novelli EL, Castro FJ, Moron SE (2009) Oxidative stress biomarkers and aggressive behavior in fish exposed to aquatic cadmium contamination. Neotrop Ichthyol 7:103–108
Alós J, Palmer M, Arlinghaus R (2012) Consistent selection towards low activity phenotypes when catchability depends on encounters among human predators and fish. PloS one 7:e48030
Alton LA, Portugal SJ, White CR (2013) Balancing the competing requirements of air-breathing and display behaviour during male–male interactions in Siamese fighting fish Betta splendens. Comp Biochem Physiol a Mol Integr Physiol 164:363–367
Andersen KH, Beyer JE (2015) Size structure, not metabolic scaling rules, determines fisheries reference points. Fish Fish 16:1–22
Archard GA, Earley RL, Hanninen AF, Braithwaite VA (2012) Correlated behaviour and stress physiology in fish exposed to different levels of predation pressure. Funct Ecol 26:637–645
Arlinghaus R, Mehner T, Cowx IG (2002) Reconciling traditional inland fisheries management and sustainability in industrialized countries, with emphasis on Europe. Fish Fish 3:261–316
Arlinghaus R, Klefoth T, Cooke SJ, Gingerich A, Suski C (2009) Physiological and behavioural consequences of catch-and-release angling on northern pike (Esox lucius L.). Fish Res 97:223–233
Arlinghaus R, Cooke SJ, Potts W (2013) Towards resilient recreational fisheries on a global scale through improved understanding of fish and fisher behaviour. Fish Manag Ecol 20:91–98
Arlinghaus R, Laskowski KL, Alós J, Klefoth T, Monk CT, Nakayama S, Schröder A (2017) Passive gear-induced timidity syndrome in wild fish populations and its potential ecological and managerial implications. Fish Fish 18:360–373
Aubin-Horth N, Deschênes M, Cloutier S (2012) Natural variation in the molecular stress network correlates with a behavioural syndrome. Horm Behav 61:140–146
Auer SK, Salin K, Metcalfe NB (2015) Aerobic scope explains individual variation in feeding capacity. Biol Let 11:20150793
Balduzzi S, Rücker G, Schwarzer G (2019) How to perform a meta-analysis with R: a practical tutorial. Evid Based Mental Health 22:153–160
Baran NM, Streelman TJ (2020) Ecotype differences in aggression, neural activity, and behaviorally relevant gene expression in cichlid fish. Genes Brain Behav 19:e12657
Barrett L, Blumstein DT, Clutton-Brock TH, Kappeler PM (2013) Taking note of Tinbergen, or: the promise of a biology of behaviour. Philos Trans R Soc b Biol Sci 368:20120352
Beever EA, Hall LE, Varner J, Loosen AE, Dunham JB, Gahl MK, Smith FA, Lawler JJ (2017) Behavioral flexibility as a mechanism for coping with climate change. Front Ecol Environ 15:299–308
Behrens JW, von Friesen LW, Brodin T, Ericsson P, Hirsch PE, Persson A, Sundelin A, van Deurs M, Nilsson PA (2020) Personality-and size-related metabolic performance in invasive round goby (Neogobius melanostomus). Physiol Behav 215:112777
Bell AM (2007) Evolutionary biology: animal personalities. Nature 447:539–540
Bell AM, Sih A (2007) Exposure to predation generates personality in threespined sticklebacks (Gasterosteus aculeatus). Ecol Lett 10:828–834
Binder TR, Wilson AD, Wilson SM, Suski CD, Godin JGJ, Cooke SJ (2016) Is there a pace-of-life syndrome linking boldness and metabolic capacity for locomotion in bluegill sunfish? Anim Behav 121:175–183
Biro PA, Post JR (2008) Rapid depletion of genotypes with fast growth and bold personality traits from harvested fish populations. Proc Natl Acad Sci 105:2919–2922
Biro PA, Stamps JA (2010) Do consistent individual differences in metabolic rate promote consistent individual differences in behavior? Trends Ecol Evol 25:653–659
Biro PA, Beckmann C, Stamps JA (2010) Small within-day increases in temperature affects boldness and alters personality in coral reef fish. Proc R Soc b Biol Sci 277:71–77
Biro PA, Garland T Jr, Beckmann C, Ujvari B, Thomas F, Post JR (2018) Metabolic scope as a proximate constraint on individual behavioral variation: effects on personality, plasticity, and predictability. Am Nat 192:142–154
Brander K (2010) Impacts of climate change on fisheries. J Mar Syst 79:389–402
Careau V, Thomas D, Humphries MM, Réale D (2008) Energy metabolism and animal personality. Oikos 117:641–653
Careau V, Mariette MM, Crino O, Buttemer WA, Buchanan KL (2020) Repeatability of behavior and physiology: no impact of reproductive investment. Gen Compar Endocrinol 290:113403
Cattano C, Claudet J, Domenici P, Milazzo M (2018) Living in a high CO2 world: a global Meta-analysis shows multiple trait-mediated fish responses to ocean acidification. Ecol Monogr 88:320–335
Chabot D, McKenzie DJ, Craig JF (2016) Metabolic rate in fishes: definitions, methods and significance for conservation physiology. J Fish Biol 88:1–9
Chappell MA, Garland T, Rezende EL, Gomes FR (2004) Voluntary running in deer mice: speed, distance, energy costs and temperature effects. J Exp Biol 207:3839–3854
Chen C, Rainnie DG, Greene RW, Tonegawa S (1994) Abnormal fear response and aggressive behavior in mutant mice deficient for alpha-calcium-calmodulin kinase II. Science 266:291–294
Childs AR, Cowley PD, Næsje TF, Booth AJ, Potts WM, Thorstad EB, Økland F (2008) Do environmental factors influence the movement of estuarine fish? A case study using acoustic telemetry. Estuar Coast Shelf Sci 78:227–236
Chown SL, Hoffmann AA, Kristensen TN, Angilletta MJ Jr, Stenseth NC, Pertoldi C (2010) Adapting to climate change: a perspective from evolutionary physiology. Clim Res 43:3–15
Claireaux G, Webber D, Kerr S, Boutilier R (1995) Physiology and behaviour of free-swimming Atlantic cod (Gadus morhua) facing fluctuating temperature conditions. J Exp Biol 198:49–60
Clark TD, Sandblom E, Jutfelt F (2013) Aerobic scope measurements of fishes in an era of climate change: respirometry, relevance and recommendations. J Exp Biol 216:2771–2782
Clark TD, Messmer V, Tobin AJ, Hoey AS, Pratchett MS (2017) Rising temperatures may drive fishing-induced selection of low-performance phenotypes. Sci Rep 7:1–1
Clarke RD (1992) Effects of microhabitat and metabolic, rate on food intake, growth and fecundity of two competing coral reef fishes. Coral Reefs 11:199–205
Clarke A, Johnston NM (2002) Scaling of metabolic rate with body mass and temperature in teleost fish. J Anim Ecol 68:893–905
Cockrem J (2007) Stress, corticosterone responses and avian personalities. J Ornithol 148:169–178
Coleman K, Wilson DS (1998) Shyness and boldness in pumpkinseed sunfish: individual differences are context-specific. Anim Behav 56:927–936
Collins M, Knutti R, Arblaster J, Dufresne JL (2013) Long-term climate change: projections, commitments and irreversibility. In: Stocker TF, Qin D, Plattner GK (eds) Climate change 2013: the physical science basis. Cambridge University Press Cambridge, United Kingdom
Cooke SJ, Suski CD (2005) Do we need species specific guidelines for catch-and-release recreational angling to effectively conserve diverse fishery resources? Biodivers Conserv 14:1195–1209
Cooke SJ, Suski CD, Ostrand KG, Wahl DH, Philipp DP (2007) Physiological and behavioral consequences of long-term artificial selection for vulnerability to recreational angling in a teleost fish. Physiol Biochem Zool 80:480–490
Cooke SJ, Brownscombe JW, Raby GD, Broell F, Hinch SG, Clark TD, Semmens JM (2016) Remote bioenergetics measurements in wildfish: opportunities and challenges. Compar Biochem Physiol Part A Mol Integr Physiol. https://doi.org/10.1016/j.cbpa.2016.03.022
Cooke SJ, Twardek WM, Reid AJ, Lennox RJ, Danylchuk SC, Brownscombe JW, Danylchuk AJ (2019) Searching for responsible and sustainable recreational fisheries in the Anthropocene. J Fish Biol. https://doi.org/10.1111/jfb.13935
Crocker CE, Cech JJ Jr (1997) Effects of environmental hypoxia on oxygen consumption rate and swimming activity in juvenile white sturgeon, Acipenser transmontanus, in relation to temperature and life intervals. Environ Biol Fishes 50:383–389
Croft DP, Krause J, James R (2004) Social networks in the guppy (Poecilia reticulata). Proc R Soc B 271:516-S519
Cutts CJ, Metcalfe NB, Taylor AC (1998) Aggression and growth depression in juvenile salmon – the consequences of variation in metabolic rate. J Fish Biol 52:1026–1037
Cutts CJ, Metcalfe NB, Taylor AC (1999) Competitive asymmetries in territorial juvenile Atlantic salmon, Salmo salar. Oikos 86:479–486
Cutts CJ, Adams CE, Campbell A (2001) Stability of physiological and behavioural determinants of performance in Arctic char (Salvelinus alpinus). Can J Fish Aquat Sci 58:961–968
Danylchuk SE, Danylchuk AJ, Cooke SJ, Goldberg TL, Koppelman J, Philipp DP (2007) Effects of recreational angling on the post-release behavior and predation of bonefish (Albula vulpes): the role of equilibrium status at the time of release. J Exp Mar Biol Ecol 346:127–133
Dijkstra PD, Seehausen O, Metcalfe NB (2013) Metabolic differentiation in an incipient species pair of cichlid fish. J Fish Biol 82:1975–1989
Dijkstra PD, Pierotti ME, Seehausen O, Metcalfe NB (2016) Metabolism, oxidative stress and territorial behaviour in a female colour polymorphic cichlid fish. Behav Ecol Sociobiol 70:99–109
Donelson JM, Munday PL, McCormick MI, Pitcher CR (2012) Rapid transgenerational acclimation of a tropical reef fish to climate change. Nat Clim Chang 2:30
Donelson JM, Sunday JM, Figueira WF, Gaitán-Espitia JD, Hobday AJ, Johnson CR, Leis JM, Ling SD, Marshall D, Pandolfi JM, Pecl G (2019) Understanding interactions between plasticity, adaptation and range shifts in response to marine environmental change. Philos Trans R Soc B 374:20180186
Dorfman D (2005) Aggression and oxygen uptake in Siamese fighting fish. Bull New Jersey Acad Sci 50:11–14
Duncan MI, Bates AE, James NC, Potts WM (2019) Exploitation may influence the climate resilience of fish populations through removing high performance metabolic phenotypes. Sci Rep 9:1–10
Dwyer GK, Stoffels RJ, Pridmore PA (2014) Morphology, metabolism, and behavior: responses of three fishes with different lifestyles to acute hypoxia. Freshw Biol 59:819–831
Eliason EJ, Farrell AP (2016) Oxygen uptake in Pacific salmon Oncorhynchus spp.: when ecology and physiology meet. J Fish Biol 88:359–388
FAO (Food and Agricultural Organization of the United Nations) (2012) Technical guidelines for responsible fisheries: recreational fisheries. Food and Agriculture Organization of the United Nations, Rome, p 176
Finstad AG, Forseth T, Ugedal O, Naesje TF (2007) Metabolic rate, behaviour and winter performance in juvenile Atlantic salmon. Funct Ecol 21:905–912
Fischer P (2000) An experimental test of metabolic and behavioural responses of benthic fish species to different types of substrate. Can J Fish Aquat Sci 57:2336–2344
Forstner H, Wieser W (1990) Patterns of routine swimming and metabolic rate in juvenile cyprinids at three temperatures: analysis with a respirometer-activity-monitoring system. J Comp Physiol B 160:71–76
Fox RJ, Donelson JM, Schunter C, Ravasi T, Gaitán-Espitia JD (2019) Beyond buying time: the role of plasticity in phenotypic adaptation to rapid environmental change. Philos Trans R Soc B Biol Sci. https://doi.org/10.1098/rstb.2018.0174
Freitas C, Olsen EM, Moland E, Ciannelli L, Knutsen H (2015) Behavioral responses of Atlantic cod to sea temperature changes. Ecol Evol 5:2070–2083
Gale MK, Hinch SG, Donaldson MR (2013) The role of temperature in the capture and release of fish. Fish Fish 14:1–33
Gingerich AJ, Cooke SJ, Hanson KC, Donaldson MR, Hasler CT, Suski CD, Arlinghaus R (2007) Evaluation of the interactive effects of air exposure duration and water temperature on the condition and survival of angled and released fish. Fish Res 86:169–178
Grantner A, Taborsky M (1998) The metabolic rates associated with resting, and with the performance of agonistic, submissive and digging behaviours in the cichlid fish Neolamprologus pulcher (Pisces: Cichlidae). J Comp Physiol B 168:427–433
Griffiths MH (2000) Long-term trends in catch and effort of commercial linefish off South Africa’s Cape Province: snapshots of the 20th century. S Afr J Mar Sci 22:81–110
Haddaway NR, Woodcock P, Macura B, Collins A (2015) Making literature reviews more reliable through application of lessons from systematic reviews. Conserv Biol 29:1596–1605
Halsey LG, Killen SS, Clark TD (2018) Exploring key issues of aerobic scope interpretation in ectotherms: absolute versus factorial. Rev Fish Biol Fish Sci 28:405–415
Hansen MJ, Ligocki IY, Zillig KE, Steel AE, Todgham AE, Fangue NA (2020) Risk-taking and locomotion in foraging threespine sticklebacks (Gasterosteus aculeatus): the effect of nutritional stress is dependent on social context. Behav Ecol Sociobiol 74:1–12
Harley CDG, Hughes AR, Hultgren KM, Miner BG, Sorte CJB, Thornber CS, Rodriguez LF, Tormanek L, Williams SL (2006) The impacts of climate change in coastal marine systems. Ecol Lett 9:228–241
Harrison PM, Gutowsky LF, Martins EG, Patterson DA, Cooke SJ, Power M (2015) Personality-dependent spatial ecology occurs independently from dispersal in wild burbot (Lota lota). Behav Ecol 26:483–492
Hassenstein B, Reichardt W (1956) Systemtheoretische analyse der zeit, reihenfolgen und vorzeichenauswertung bei der bewegungsperzeption des Rfisselk~ifers Chlorophanus. Naturforsch 11b:513–524
Heinrich B, Bartholomew GA (1979) Roles of endothenny and size in inter- and intraspecific competition for elephant dung in an African dung beetle, Scarabaeus laevistriatus. Physiol Zool 52:484–496
Herrera M, Castanheira MF, Conceição LE, Martins CI (2014) Linking risk taking and the behavioral and metabolic responses to confinement stress in gilthead seabream Sparus aurata. Appl Anim Behav Sci 155:101–108
Hessenauer JM, Vokoun JC, Suski CD, Davis J, Jacobs R, O’Donnell E (2015) Differences in the metabolic rates of exploited and unexploited fish populations: a signature of recreational fisheries induced evolution? PLoS One 10:e0128336
Hoegh-Guldberg O, Cai R, Poloczanska ES, Brewer PG, Sundby S, Hilmi K, Fabry VJ, Jung S (2014) The ocean. In: Barros VR, Field CB, Dokken DJ (eds) Climate change 2014: impacts, adaptation and vulnerability: Part B regional aspects—contribution of working group II to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge, pp 1655–1731
Hollins JPW, Thambithurai D, Van Leeuwen TE, Allan B, Koeck B, Bailey D, Killen SS (2019) Shoal familiarity modulates effects of individual metabolism on vulnerability to capture by trawling. Conserv Physiol 7:coz043
Hollins JPW, Koeck B, Crespel A, Bailey DM, Killen SS (2020) Does thermal plasticity affect susceptibility to capture in fish? Insights from a simulated trap and trawl fishery. Can J Fish Aquat Sci. https://doi.org/10.1139/cjfas-2020-0125
Holt RE, Jørgensen C (2015) Climate change in fish: effects of respiratory constraints on optimal life history and behaviour. Biol Let 11:20141032
Hsieh CH, Reiss CS, Hewitt RP, Sugihara G (2008) Spatial analysis shows that fishing enhances the climatic sensitivity of marine fishes. Can J Fish Aquat Sci 65:947–961
Huey RB, Stevenson RD (1979) Integrating thermal physiology and ecology of ectotherms: a discussion of approaches. Am Zool 19:357–366
Hunter E, Metcalfe JD, O’Brien CM, Arnold GP, Reynolds JD (2004) Vertical activity patterns of free-swimming adult plaice in the southern North Sea. Mar Ecol Prog Ser 279:261–273
Huntingford FA, Andrew G, Mackenzie S, Morera D, Coyle SM, Pilarczyk M, Kadri S (2010) Coping strategies in a strongly schooling fish, the common carp Cyprinus carpio. J Fish Biol 76:1576–1591
James NC, Whitfield AK, Cowley PD (2008) Preliminary indications of climate-induced change in a warm-temperate South African estuarine fish community. J Fish Biol 72:1855–1863
Jonas I, Schubert KA, Reijne AC, Scholte J, Garland T Jr, Gerkema MP, Scheurink AJW, Nyakas C, van Dijk G (2010) Behavioral traits are affected by selective breeding for increased wheelrunning behavior in mice. Behav Genet 40:542–550
Keyser FM, Broome JE, Bradford RG, Sanderson B, Redden AM (2016) Winter presence and temperature-related diel vertical migration of striped bass (Morone saxatilis) in an extreme high-flow passage in the inner Bay of Fundy. Can J Fish Aquat Sci 1786:1777–1786
Killen SS, Marras S, McKenzie DJ (2011) Fuel, fasting, fear: routine metabolic rate and food deprivation exert synergistic effects on risk-taking in individual juvenile European sea bass. J Anim Ecol 80:1024–1033
Killen SS, Marras S, Ryan MR, Domenici P, McKenzie DJ (2012) A relationship between metabolic rate and risk-taking behaviour is revealed during hypoxia in juvenile European sea bass. Funct Ecol 26:134–143
Killen SS, Marras S, Metcalfe NB, McKenzie DJ, Domenici P (2013) Environmental stressors alter relationships between physiology and behaviour. Trends Ecol Evol 28:651–658
Killen SS, Mitchell MD, Rummer JL, Chivers DP, Ferrari MCO, Meekan MG, McCormick MI (2014) Aerobic scope predicts dominance during early life in a tropical damselfish. Funct Ecol 28:1367–1376
Killen SS, Glazier DS, Rezende EL, Clark TD, Atkinson D, Willener AS, Halsey LG (2016) Ecological influences and morphological correlates of resting and maximal metabolic rates across teleost fish species. Am Nat 187:592–606
Killen SS, Marras S, Nadler L, Domenici P (2017) The role of physiological traits in assortment among and within fish shoals. Philos Trans R Soc b Biol Sci 372:20160233
Killen SS, Esbaugh AJ, Martins N, Tadeu Rantin F, McKenzie DJ (2018) Aggression supersedes individual oxygen demand to drive group air-breathing in a social catfish. J Anim Ecol 87:223–234
Koeck B, Závorka L, Aldvén D, Näslund J, Arlinghaus R, Thörnqvist PO, Winberg S, Björnsson BT, Johnsson JI (2019) Angling selects against active and stress-resilient phenotypes in rainbow trout. Can J Fish Aquat Sci 76:320–333
Kolok AS, Hartman MM, Sershan J (2002) The physiology of copper tolerance in fathead minnows: insight from an intraspecific, correlative analysis. Environ Toxicol Chem 21:1730–1735
Krause J, Ruxton G, Cheng D, Kirkman E (2000) Species-specific patterns of refuge use in fish: the role of metabolic expenditure and body length. Behaviour 137:1113–1127
Lahti K, Huuskonen H, Laurila A, Piironen J (2002) Metabolic rate and aggressiveness between brown trout populations. Funct Ecol 16:167–174
Laubenstein TD, Rummer JL, Nicol S, Parsons DM, Pether SM, Pope S, Smith N, Munday PL (2018) Correlated effects of ocean acidification and warming on behavioral and metabolic traits of a large pelagic fish. Diversity 10:35
Laubenstein TD, Rummer JL, McCormick MI, Munday PL (2019) A negative correlation between behavioural and physiological performance under ocean acidification and warming. Sci Rep 9:1–10
Lennox R, Cooke SJ (2014) State of the interface between conservation and physiology: a bibliometric analysis. Conserv Physiol 2:1–9
Lewin WC, Arlinghaus R, Mehner T (2006) Documented and potential biological impacts of recreational fishing: insights for management and conservation. Rev Fish Sci 14:305–367
Li CY, Tseng YC, Chen YJ, Yang Y, Hsu Y (2020) Personality and physiological traits predict contest interactions in Kryptolebias marmoratus. Behav Process 173:104079
Long T, Yuan M, Yuan H (2021) Heritability of animal individuality in fish: distribution, behavior, metabolism and stress response. Aquaculture. https://doi.org/10.1016/j.aquaculture.2021.736415
Louison MJ, Stein JA, Suski CD (2019) The role of social network behavior, swimming performance, and fish size in the determination of angling vulnerability in bluegill. Behav Ecol Sociobiol 73:139
Lovegrove BG (2003) The influence of climate on the basal metabolic rate of small mammals: a slow-fast metabolic continuum. J Comp Physiol 173:87–112
Martins CI, Silva PI, Conceição LE, Costas B, Höglund E, Øverli Ø, Schrama JW (2011) Linking fearfulness and coping styles in fish. PLoS One 6:e28084
Marty L, Dieckmann U, Ernande B (2015) Fisheries-induced neutral and adaptive evolution in exploited fish populations and consequences for their adaptive potential. Evol Appl 8:47–63
Mathias ML, Nunes AC, Marques CC, Auffray JC, Britton-Davidian J, Ganem G, Gündüz I, Ramalhinho MG, Searle JB, Speakman JR (2006) Effects of climate on oxygen consumption and energy intake of chromosomally divergent populations of the house mouse (Mus musculus domesticus) from the island of Madeira (North Atlantic, Portugal). Funct Ecol 20:330–339
Mathot KJ, Martin K, Kempenaers B, Forstmeier W (2013) Basal metabolic rate can evolve independently of morphological and behavioural traits. Heredity 111:175–181
McCarthy ID (2001) Competitive ability is related to metabolic asymmetry in juvenile rainbow trout. J Fish Biol 59:1002–1014
McKenzie DJ, Axelsson M, Chabot D, Claireaux G, Cooke SJ, Corner RA, De Boeck G, Domenici P, Guerreiro PM, Hamer B, Jørgensen C (2016) Conservation physiology of marine fishes: state of the art and prospects for policy. Conserv Physiol 4:cow046
McLean S, Persson A, Norin T, Killen SS (2018) Metabolic costs of feeding predictively alter the spatial distribution of individuals in fish schools. Curr Biol 28:1144–1149
McLean MF, Litvak MK, Stoddard EM, Cooke SJ, Patterson DA, Hinch SG, Welch DW, Crossin GT (2020) Linking environmental factors with reflex action mortality predictors, physiological stress, and post-release movement behaviour to evaluate the response of white sturgeon (Acipenser transmontanus Richardson, 1836) to catch-and-release angling. Comp Biochem Physiol Part A Mol Integr Physiol 240:110618
McNab BK (2002) The physiological ecology of vertebrates: a view from energetics. Cornell University Press
Metcalfe JD, Arnold G (1997) Tracking fish with electronic tags. Nature 387:665–666
Metcalfe NB, Thomson BC (1995) Fish recognize and prefer to shoal with poor competitors. Proc R Soc London Seri B Biol Sci 259:207–210
Metcalfe NB, Taylor AC, Thorpe JE (1995) Metabolic rate, social status and life-history strategies in Atlantic salmon. Anim Behav 49:431–436
Metcalfe JD, Le Quesne WJF, Cheung WWL, Righton DA (2012) Conservation physiology for applied management of marine fish: an overview with perspectives on the role and value of telemetry. Philos Trans R Soc b Biol Sci 367:1746–1756
Metcalfe NB, Van Leeuwen TE, Killen SS (2016) Does individual variation in metabolic phenotype predict fish behaviour and performance? J Fish Biol 88:298–321
Miyoshi K, Hayashida K, Sakashita T, Fujii M, Nii H, Nakao K, Ueda H (2014) Comparison of the swimming ability and upstream-migration behavior between chum salmon and masu salmon. Can J Fish Aquat Sci 71:217–225
Morrongiello J, Thresher R (2015) A statistical framework to explore ontogenetic growth variation among individuals and populations: a marine fish example. Ecol Monogr 85:93–115
Neat FC, Taylor AC, Huntingford FA (1998) Proximate costs of fighting in male cichlid fish: the role of injuries and energy metabolism. Anim Behav 55:875–882
Neubauer P, Andersen KH (2019) Thermal performance of fish is explained by an interplay between physiology, behaviour and ecology. Conserv Physiol 7:coz025
Norin T, Malte H (2012) Intraspecific variation in aerobic metabolic rate of fish: relations with organ size and enzyme activity in brown trout. Physiol Biochem Zool 85:645–656
Norin T, Malte H, Clark TD (2015) Differential plasticity of metabolic rate phenotypes in a tropical fish facing environmental change. Funct Ecol. https://doi.org/10.1111/1365-2435.12503
Pankhurst NW, Munday PL (2011) Effects of climate change on fish reproduction and early life history stages. Mar Freshw Res 62:1015–1026
Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evolut Syst 37:637–669
Pauly D, Cheung WW (2018) Sound physiological knowledge and principles in modelling shrinking of fishes under climate change. Glob Change Biol 24:15–26
Petersen JK, Petersen GI (1990) Tolerance, behaviour and oxygen consumption in the sand goby, Pomatoschistus minutus (Pallas), exposed to hypoxia. J Fish Biol 37:921–933
Pimentel MS, Faleiro F, Marques T, Bispo R, Dionísio G, Faria AM, Machado J, Peck MA, Pörtner H, Pousão-Ferreira P, Gonçalves EJ, Rosa R (2016) Foraging behaviour, swimming performance and malformations of early stages of commercially important fishes under ocean acidification and warming. Clim Change 137:495–509
Pörtner HO (2008) Ecosystem effects of ocean acidification in times of ocean warming: a physiologist’s view. Marine Ecol Prog Ser 373:203–217
Pörtner HO, Knust R (2007) Climate change affects marine fishes through the oxygen limitation of thermal tolerance. Science 315:95–97
Pörtner HO, Peck MA (2010) Climate change effects on fishes and fisheries: towards a cause-and-effect understanding. J Fish Biol 77:1745–1779
Pörtner HO, Bock C, Mark FC (2018) Connecting to ecology: a challenge for comparative physiologists? Response to ‘Oxygen-and capacity-limited thermal tolerance: blurring ecology and physiology.’ J Exp Biol 221:jeb174185
Puckett KJ, Dill LM (1985) The energetics of feeding territoriality in juvenile Coho salmon (Oncorhynchus kisutch). Behaviour 92:97–111
Reale D, Reader SM, Sol D, McDougall PT, Dingemanse NJ (2007) Integrating animal temperament within ecology and evolution. Biol Rev 82:291–318
Redpath TD, Cooke SJ, Suski CD, Arlinghaus R, Couture P, Wahl DH, Philipp DP (2010) The metabolic and biochemical basis of vulnerability to recreational angling after three generations of angling-induced selection in a teleost fish. Can J Fish Aquat Sci 67:1983–1992
Reid D, Armstrong JD, Metcalfe NB (2012) The performance advantage of a high resting metabolic rate in juvenile salmon is habitat dependent. J Anim Ecol 81:868–875
Rhein M, Rintoul SR, Aoki S (2013) Climate change 2013: the physical science basis: contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change. In: Stocker TF, Qin D, Plattner GK, Tignor M, Allen SK, Boschung J, Nauels A, Xia VY, Midgley B (eds) Climate change. Cambridge University Press, USA, pp 255–316
Rijnsdorp AD, Peck MA, Engelhard GH, Mollmann C, Pinnegar JK (2009) Resolving the effect of climate change on fish populations. ICES J Mar Sci 66:1570–1583
Romero LM, Dickens MJ, Cyr NE (2009) The reactive scope model: a new model integrating homeostasis, allostasis, and stress. Hormones Behav 55:375–389
Ros AFH, Becker K, Oliveira RF (2006) Aggressive behaviour and energy metabolism in a cichlid fish, Oreochromis mossambicus. Physiol Behav 89:164–170
Rouault M, Pohl B, Penven P (2010) Coastal oceanic climate change and variability from 1982 to 2009 around South Africa. Afr J Mar Sci 32:237–246
Rupia EJ, Binning SA, Roche DG, Lu W (2016) Fight-flight or freeze-hide? Personality and metabolic phenotype mediate physiological defence responses in flatfish. J Anim Ecol 85:927–937
Sandblom E, Clark TD, Gräns A, Ekström A, Brijs J, Sundström LF, Odelström A, Adill A, Aho T, Jutfelt F (2016) Physiological constraints to climate warming in fish follow principles of plastic floors and concrete ceilings. Nat Commun 7:1–8
Satterfield D, Johnson DW (2020) Local adaptation of antipredator behaviors in populations of a temperate reef fish. Oecologia 194:571
Scantlebury M, Waterman JM, Hillegass M, Speakman JR, Bennett NC (2007) Energetic costs of parasitism in the Cape ground squirrel Xerus inauris. Proc R Soc Lond 274:2169–2177
Schindler DE, Hilborn R (2015) Prediction, precaution, and policy under global change. Science 347:953–954
Schjolden J, Stoskhus A, Winberg S (2005) Does individual variation in stress responses and agonistic behavior reflect divergent stress coping strategies in juvenile rainbow trout? Physiol Biochem Zool 78:715–723
Scott GR, Sloman KA (2004) The effects of environmental pollutants on complex fish behaviour: integrating behavioural and physiological indicators of toxicity. Aquat Toxicol 68:369–392
Seebacher F, Krause J (2017) Physiological mechanisms underlying animal social behaviour. Philos Trans R Soc Biol Sci 372:20160231
Seebacher F, Ward AJW, Wilson RS (2013) Increased aggression during pregnancy comes at a higher metabolic cost. J Exp Biol 216:771–776
Seppänen E, Tiira K, Huuskonen H, Piironen J (2009) Metabolic rate, growth and aggressiveness in three Atlantic salmon Salmo salar populations. J Fish Biol 74:562–575
Shultz AD, Murchie KJ, Griffith C, Cooke SJ, Danylchuk AJ, Goldberg TL, Suski CD (2011) Impacts of dissolved oxygen on the behavior and physiology of bonefish: implications for live-release angling tournaments. J Exp Mar Biol Ecol 402:19–26
Sih A, Bell AM, Johnson JC, Ziemba RE (2004) Behavioral syndromes: an integrative overview. Q R Biol 79:241–277
Sims DW, Mouth VJW, Genner MJ, Southward AJ, Hawkins SJ (2004) Low-temperature-driven early spawning migration of a temperate marine fish. J Anim Ecol 73:333–341
Skeeles MR, Winkler AC, Duncan MI, James NC, van der Walt KA, Potts WM (2020) The use of internal heart rate loggers in determining cardiac breakpoints of fish. J Therm Biol. https://doi.org/10.1016/j.jtherbio.2020.102524
Sloat MR, Reeves GH (2014) Individual condition, standard metabolic rate, and rearing temperature influence steelhead and rainbow trout (Oncorhynchus mykiss) life histories. Can J Fish Aquat Sci 71:491–501
Somero GN (2010) The physiology of climate change: how potentials for acclimatization and genetic adaptation will determine ‘winners’ and ‘losers.’ J Exp Biol 213:912–920
Sousa LL, Queiroz N, Mucientes G, Humphries NE, Sims DW (2016) Environmental influence on the seasonal movements of satellite-tracked ocean sunfish Mola mola in the north-east Atlantic Environmental influence on the seasonal movements of satellite-tracked ocean sunfish Mola mola in the north-east Atlantic. Anim Biotelemetry. https://doi.org/10.1186/s40317-016-0099-2
Suski CD, Philipp DP (2004) Factors affecting the vulnerability to angling of nesting male largemouth bass and smallmouth bass. Trans Am Fish Soc 133:1100–1106
Sutter DAH, Suski CD, Philipp DP, Klefoth T, Wahl DH, Kersten P, Cooke SJ, Arlinghaus R (2012) Recreational fishing selectively captures individuals with the highest fitness potential. Proc Natl Acad Sci 109:20960–20965
Tan H, Polverino G, Martin JM, Bertram MG, Wiles SC, Palacios MM, Bywater CL, White CR, Wong BB (2020) Chronic exposure to a pervasive pharmaceutical pollutant erodes among-individual phenotypic variation in a fish. Environ Pollut 263:114450
Thomas DW, Morand-Ferron J, Careau V (2001) Physiological ecology of Mediterranean blue tits (Parus caeruleus) 1. A test for inter-population differences in resting metabolic rate and thermal conductance as a response to hot climates. Zoology 104:33–40
Tinbergen N (1963) On aims and methods of ethology. Z Tierpsychol 20:410–433. https://doi.org/10.1111/j.1439-0310.1963.tb01161.x
Tudorache C, Schaaf MJ, Slabbekoorn H (2013) Covariation between behaviour and physiology indicators of coping style in zebrafish (Danio rerio). J Endocrinol 219:251–258
Urbina MA, Forster ME, Glover CN (2011) Leap of faith: voluntary emersion behaviour and physiological adaptations to aerial exposure in a non-aestivating freshwater fish in response to aquatic hypoxia. Physiol Behav 103:240–247
Uusi-Heikkila S, Wolter C, Klefoth T, Arlinghaus R (2008) A behavioural perspective on fishing-induced evolution. Trends Ecol Evol 23:419–421
Vaz-Serrano J, Ruiz-Gomez MDL, Gjøen HM, Skov PV, Huntingford FA, Øverli Ø, Höglund E (2011) Consistent boldness behaviour in early emerging fry of domesticated Atlantic salmon (Salmo salar): decoupling of behavioural and physiological traits of the proactive stress coping style. Physiol Behav 103:359–364
Vedor M, Queiroz N, Mucientes G, Couto A, da Costa I, Dos Santos A, Vandeperre F, Fontes J, Afonso P, Rosa R, Humphries NE (2021) Climate-driven deoxygenation elevates fishing vulnerability for the ocean’s widest ranging shark. Elife 10:e62508
Von Holst E (1936) Vom dualismus der motorischen und der automatisc-rhythmischen funktion im ruckenmark und vom wesen des automatischen rhythmus. Pfliigers Archiv Fur Die Gesamte Physiologie 237:356–378
Von Holst E, Mittelstaedt H (1950) The principle of reafference: Interactions between the central nervous system and the peripheral organs. Die Naturwissenschften 37:464–476
Ward TD, Algera DA, Gallagher AJ, Hawkins E, Horodysky A, Jørgensen C, Killen SS, McKenzie DJ, Metcalfe JD, Peck MA, Vu M (2016) Understanding the individual to implement the ecosystem approach to fisheries management. Conserv Physiol 4:cow005
Warnock WG, Rasmussen JB (2014) Comparing competitive ability and associated metabolic traits between a resident and migratory population of bull trout against a non-native species. Environ Biol Fishes 97:415–423
Warren DT, McCormick MI (2019) Intrageneric differences in the effects of acute temperature exposure on competitive behaviour of damselfishes. PeerJ 7:e7320
Warren DT, Donelson JM, McCormick MI, Ferrari MCO, Munday PL (2016) Duration of exposure to elevated temperature affects competitive interactions in juvenile reef fishes. PLOS ONE 11:e0164505
Whitlock RE, Hazen EL, Walli A, Farwell C, Bograd SJ, Foley DG, Castleton M, Block BA (2015) Direct quantification of energy intakein an apex marine predator suggests physiology is a key driver of migrations. Sci Adv 1:e1400270
Wilson ADM, Brownscombe JW, Sullivan B, Jain-Schlaepfer S, Cooke SJ (2015) Does angling technique selectively target fishes based on their behavioural type? PLoS One 10:e0135848
Wong B, Candolin U (2015) Behavioral responses to changing environments. Behav Ecol 26:665–673
Yamamoto T, Ueda H, Higashi S (1998) Correlation among dominance status, metabolic rate and otolith size in masu salmon. J Fish Biol 52:281–290
Zou H, Shi M, Li R, Zhang X, Lu W (2021) Comparative transcriptomic analysis of in the hindbrain of olive flounder (Paralichthys olivaceus) considering individual behavior-type and oxygen metabolism. Comp Bioche Physiol Part D Genom Proteom 38:100799
Zub K, Piertney S, Szafranska PA, Konarzewski M (2012) Environmental and genetic influences on body mass and resting metabolic rates (RMR) in a natural population of weasel Mustela nivalis. Mol Ecol 21:1283–2129
Acknowledgements
We thank the reviewers of this manuscript for their valuable comments, which greatly improved the manuscript. We thank graphic artist, Carys Bailey, for her collaboration on Fig. 4, “The fission or fusion of social groups is expected in the Anthropocene as climate change and angling have coupled effects on the selection for metabolic and behavioural traits.”
Funding
This work was supported by the African Coelacanth Ecosystem Programme [Grant Number 110762 (WMP)] and the National Research Foundation [Grant Number 12093 (ARC)].
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Bailey, L.A., Childs, A.R., James, N.C. et al. Links between behaviour and metabolic physiology in fishes in the Anthropocene. Rev Fish Biol Fisheries 32, 555–579 (2022). https://doi.org/10.1007/s11160-022-09701-2
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DOI: https://doi.org/10.1007/s11160-022-09701-2