Water temperature explains part of the variation in basal plasma cortisol level within and between fish species
Camille Houdelet
MARBEC, Universite Montpellier, CNRS, Ifremer, IRD, Montpellier, France
Search for more papers by this authorEduardo Bessa
Graduate Program in Ecology, Life and Earth Sciences, University of Brasília, Brasília, Brazil
Search for more papers by this authorCorresponding Author
Benjamin Geffroy
MARBEC, Universite Montpellier, CNRS, Ifremer, IRD, Montpellier, France
Correspondence
Benjamin Geffroy, MARBEC, Universite Montpellier, CNRS, Ifremer, IRD, 34250 Palavas-Les-Flots, France.
Email: [email protected]
Search for more papers by this authorBastien Sadoul
DECOD, Ecosystem Dynamics and Sustainability, Institut Agro, Ifremer, INRAE, Rennes, France
Search for more papers by this authorCamille Houdelet
MARBEC, Universite Montpellier, CNRS, Ifremer, IRD, Montpellier, France
Search for more papers by this authorEduardo Bessa
Graduate Program in Ecology, Life and Earth Sciences, University of Brasília, Brasília, Brazil
Search for more papers by this authorCorresponding Author
Benjamin Geffroy
MARBEC, Universite Montpellier, CNRS, Ifremer, IRD, Montpellier, France
Correspondence
Benjamin Geffroy, MARBEC, Universite Montpellier, CNRS, Ifremer, IRD, 34250 Palavas-Les-Flots, France.
Email: [email protected]
Search for more papers by this authorBastien Sadoul
DECOD, Ecosystem Dynamics and Sustainability, Institut Agro, Ifremer, INRAE, Rennes, France
Search for more papers by this authorBenjamin Geffroy, Bastien Sadoul Co-last Authors.
Abstract
Within the thermal tolerance range of fish, metabolism is known to escalate with warming. Rapid thermic changes also trigger a series of physiological responses, including activation of the stress axis, producing cortisol. Fish have adapted to their environment by producing a low level of plasmatic cortisol when unstressed (basal), so that thriving in their natural temperature should not impact their basal cortisol levels. Yet, surprisingly, little is known on how temperature affects cortisol within and between fish species. Here, we conducted a phylogenetic meta-analysis to (1) test whether temperature can explain the differences in basal cortisol between species and (2) evaluate the role of temperature on differences in cortisol levels between individuals of a same species. To do this, we retrieved basal plasma cortisol data from 126 studies, investigating 33 marine and freshwater fish species, and correlated it to water temperature. Intra-species variability in basal plasma cortisol levels was further investigated in two species: the European sea bass Dicentrarchus labrax and the Nile tilapia Oreochromis niloticus. Factors such as life stage, sex and weight were also considered in the analyses. Overall, our phylogenetic analysis revealed a clear positive correlation between basal cortisol level and the temperature at which the fish live. The role of temperature has also been confirmed within D. labrax, while it failed to be significant in O. niloticus. In this paper, the influence of habitat, life stage, sex and weight on basal plasma cortisol levels is also discussed. Since some abiotic parameters were not included in the analysis, our study is a call to encourage scientists to systematically report other key factors such as dissolved oxygen or salinity to fully depict the temperature-cortisol relationship in fishes.
CONFLICT OF INTEREST STATEMENT
The authors have no conflicts of interest to declare.
Open Research
DATA AVAILABILITY STATEMENT
All the data that support the findings are available in the supplementary material.
Supporting Information
Filename | Description |
---|---|
jfb15342-sup-0001-Figure S1.tiffTIFF image, 14.8 MB | SUPPORTING INFORMATION FIGURE S1. Phylogenetic tree of the 33 fish species used in the phylogenetic meta-analysis computed using the R package rotl. All data and R code supporting the figure are available in Supporting Information Data S1 |
jfb15342-sup-0002-Data S1.RARapplication/RAR, 28.1 MB | SUPPORTING INFORMATION DATA S1. All data for the meta-analysis as well as the R code to run the different models (ZIP) |
jfb15342-sup-0003-supinfo.pptxPowerPoint 2007 presentation , 42.3 KB | SUPPORTING INFORMATION APPENDIX S1. PRISMA flow diagram describing literature search, selection and analyses. The orange rectangles narrow the numbers of studies per dataset prior to the analysis steps (purple rectangles) performed on the basal cortisol level within each study. Numbers are provided per dataset: red for ‘all fishes’, blue for ‘only sea bass’ and green for ‘only Nile tilapia’. PRISMA, Preferred Reporting Items for Systematic Reviews and Meta-Analyses (TIF) |
jfb15342-sup-0004-Table S1.xlsxExcel 2007 spreadsheet , 11.5 KB | SUPPORTING INFORMATION TABLE S1. Comparison of the models including final fixed factors selected (temperature, habitat, life stage and sex for ‘all fishes’, and temperature and weight for both ‘only sea bass’ and ‘only Nile tilapia’). These models were compared based on their DIC using the MuMIn package (Barton, 2019), which also provides the weight of each model. DIC, deviance information criterion (XLSX) |
jfb15342-sup-0005-Table S2.xlsxExcel 2007 spreadsheet , 14.5 KB | SUPPORTING INFORMATION TABLE S2. Number of values (n), basal cortisol level (ng/ml, mean ± s.e.) and temperature (°C, mean ± s.e.) of the 33 species investigated in the meta-analyses (XLSX) |
jfb15342-sup-0006-Table S3.xlsxExcel 2007 spreadsheet , 11.7 KB | SUPPORTING INFORMATION Table S3. Estimates of heterogeneity I2 (%) from the normalized-mean meta-analysis and the CV meta-analysis for the best model with all random factors for the three different datasets ‘All fishes’, ‘European sea bass’ and ‘Nile tilapia’. The MLPMA allowed partitioning I2 among varying levels. Posterior mean and upper and lower 95% CIs for each estimate of I2 are provided. H2 is phylogenetic heritability, the proportion of variability in the data attributable to the phylogenetic component of MLPMA calculated following Nakagawa and Santos (2012). CI, credible interval; CV, coefficient of variation; MLPMA, multilevel phylogenetic meta-analysis (XLSX) |
jfb15342-sup-0007-Text S1.docxWord 2007 document , 15.6 KB | SUPPORTING INFORMATION TEXT S1. List of the 161 species used in the study |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
REFERENCES
- Alfonso, S., Sadoul, B., Cousin, X., & Bégout, M.-L. (2020a). Spatial distribution and activity patterns as welfare indicators in response to water quality changes in European Sea bass, Dicentrarchus Labrax. Applied Animal Behaviour Science, 226, 104974.
- Alfonso, S., Zupa, W., Manfrin, A., Fiocchi, E., Spedicato, M. T., Lembo, G., & Carbonara, P. (2020b). Stress coping styles: Is the basal level of stress physiological indicators linked to behaviour of sea bream? Applied Animal Behaviour Science, 231, 105085.
- Alfonso, S., Gesto, M., & Sadoul, B. (2021). Temperature increase and its effects on fish stress physiology in the context of global warming. Journal of Fish Biology, 98, 1496–1508.
- Auperin, B., & Geslin, M. (2008). Plasma cortisol response to stress in juvenile rainbow trout is influenced by their life history during early development and by egg cortisol content. General and Comparative Endocrinology, 158, 234–239.
- Baker, M. R., & Vynne, C. H. (2014). Cortisol profiles in sockeye Salmon: Sample bias and baseline values at migration, maturation, spawning, and senescence. Fisheries Research, 154, 38–43.
- Baker, M. R., Gobush, K. S., & Vynne, C. H. (2013). Review of factors influencing stress hormones in fish and wildlife. Journal for Nature Conservation, 21, 309–318.
- Barcellos, L. J. G., Kreutz, L. C., Koakoski, G., Oliveira, T. A., da Rosa, J. G. S., & Fagundes, M. (2012). Fish age, instead of weight and size, as a determining factor for time course differences in cortisol response to stress. Physiology and Behavior, 107, 397–400.
- Barton, B. A. (2002). Stress in fishes: A diversity of responses with particular reference to changes in circulating corticosteroids. Integrative and Comparative Biology, 42, 517–525.
- Barton, B., Schreck, C., & Barton, L. (1986). Effects of chronic cortisol administration and daily acute stress on growth, physiological conditions, and stress responses in juvenile rainbow trout. Diseases of Aquatic Organisms, 2, 173–185.
- Barton, K. (2019). Package ‘MuMIn’. R cran.
- Bessa, E., Sadoul, B., Mckenzie, D. J., & Geffroy, B. (2021). Group size, temperature and body size modulate the effects of social hierarchy on basal cortisol levels in fishes. Hormones and Behavior, 136, 105077.
- Björnsson, B. T., Stefansson, S. O., & McCormick, S. D. (2011). Environmental endocrinology of Salmon Smoltification. General and Comparative Endocrinology, 170, 290–298.
- Biro, P. A., Beckmann, C., & Stamps, J. A. (2010). Small within-day increases in temperature affects boldness and alters personality in coral reef fish. Proceedings of the Royal Society B: Biological Sciences, 277, 71–77.
- Bordin, D., & Freire, C. A. (2021). Remarkable variability in stress responses among subtropical coastal marine Teleosts. Marine Biology, 168, 1–17.
- Castanheira, M. F., Conceição, L. E. C., Millot, S., Rey, S., Bégout, M. L., Damsgård, B., … Martins, C. I. M. (2017). Coping styles in farmed fish: Consequences for aquaculture. Reviews in Aquaculture, 2017, 23–41. https://doi.org/10.1111/raq.12100.
- Chadwick, J. G., & McCormick, S. D. (2017). Upper thermal limits of growth in brook trout and their relationship to stress physiology. Journal of Experimental Biology, 220, 3976–3987.
- Chadwick, J. G., Nislow, K. H., & McCormick, S. D. (2015). Thermal onset of cellular and endocrine stress responses correspond to ecological limits in brook trout, an iconic cold-water fish. Conservation Physiology, 3, 1–12.
- Charapata, P., Oxman, D., McNeel, K., Keith, A., Mansouri, F., & Trumble, S. (2022). Lifetime hormone profiles for a long-lived teleost: Opercula reveal novel estimates of age-specific reproductive parameters and stress trends in yelloweye rockfish (Sebastes ruberrimus). Canadian Journal of Fisheries and Aquatic Sciences, 1728, 1712–1728.
10.1139/cjfas-2022-0048 Google Scholar
- Chatziplis, D., Oikonomlou, S., Loukovitis, D., Tsiokos, D., Samaras, A., Dimitroglou, A., … Pavlidis, M. (2020). QTL for stress and disease resistance in European Sea bass, Dicentrarhus labrax L. Animals, 10, 1668.
- Claireaux, G., & Lagardère, J. P. (1999). Influence of temperature, oxygen and salinity on the metabolism of the European sea bass. Journal of Sea Research, 42, 157–168.
- Clarke, A., & Johnston, N. M. (1999). Scaling of metabolic rate with body mass and temperature in teleost fish. Journal of Animal Ecology, 68, 893–905.
- Dahlke, F. T., Wohlrab, S., Butzin, M., & Pörtner, H. O. (2020). Thermal bottlenecks in the life cycle define climate vulnerability of fish. Science, 369, 65–70.
- Fanouraki, E., Mylonas, C. C., Papandroulakis, N., & Pavlidis, M. (2011). Species specificity in the magnitude and duration of the acute stress response in Mediterranean marine fish in culture. General and Comparative Endocrinology, 173, 313–322.
- Fatira, E., Papandroulakis, N., & Pavlidis, M. (2014). Diel changes in plasma cortisol and effects of size and stress duration on the cortisol response in European Sea bass (Dicentrarchus labrax). Fish Physiology and Biochemistry, 40, 911–919.
- Fevolden, S. E., Røed, K. H., Fjalestad, K. T., & Stien, J. (1999). Poststress levels of lysozyme and cortisol in adult rainbow trout: Heritabilities and genetic correlations. Journal of Fish Biology, 54, 900–910.
- Gesto, M., Zupa, W., Alfonso, S., Spedicato, M. T., Lembo, G., & Carbonara, P. (2020). Using acoustic telemetry to assess behavioral responses to acute hypoxia and ammonia exposure in farmed rainbow trout of different competitive ability. Applied Animal Behaviour Science, 230, 105084.
- Goikoetxea, A., Servili, A., Houdelet, C., Mouchel, O., Hermet, S., Clota, F., … Benjamin, B. (2022). Natural cortisol production is not linked to the sexual fate of European Sea bass. Fish Physiology and Biochemistry, 48, 1117–1135.
- Goikoetxea, A., Sadoul, B., Blondeau-Bidet, E., Aerts, J., Blanc, M. O., Parrinello, H., … Geffroy, B. (2021). Genetic pathways underpinning hormonal stress responses in fish exposed to short- and long-term warm ocean temperatures. Ecological Indicators, 120, 106937.
- Hadfield, J. D. (2010). MCMC methods for multi-response generalized linear mixed models: The MCMCglmm R package. Journal of Statistical Software, 33, 1–22.
- Hemre, G. I., & Krogdahl, Å. (1996). Effect of handling and fish size on secondary changes in carbohydrate metabolism in Atlantic Salmon, Salmo Salar L. Aquaculture Nutrition, 2, 249–252.
- Hinchliff, C. E., Smith, S. A., Allman, J. F., Burleigh, J. G., Chaudhary, R., Coghill, L. M., … Cranston, K. A. (2015). Synthesis of phylogeny and taxonomy into a comprehensive tree of life. Proceedings of the National Academy of Sciences of The United States of America, 112, 12764–12769.
- Houslay, T. M., Earley, R. L., Young, A. J., & Wilson, A. J. (2019). Habituation and individual variation in the endocrine stress response in the Trinidadian guppy (Poecilia reticulata). General and Comparative Endocrinology, 270, 113–122.
- Hudson, H. A., Brauer, P. R., Scofield, M. A., & Petzel, D. H. (2008). Effects of warm acclimation on serum osmolality, cortisol and hematocrit levels in the Antarctic fish, Trematomus bernacchii. Polar Biology, 31, 991–997.
- Jentoft, S., Held, J. A., Malison, J. A., & Barry, T. P. (2002). Ontogeny of the cortisol stress response in yellow perch (Perca flavescens). Fish Physiology and Biochemistry, 26, 371–378.
- Kembel, S. W., Cowan, P. D., Helmus, M. R., Cornwell, W. K., Morlon, H., Ackerly, D. D., … Webb, C. O. (2010). Picante: R tools for integrating phylogenies and ecology. Bioinformatics, 26, 1463–1464.
- Kenter, L. W., Breton, T. S., & Berlinsky, D. L. (2021). Comparing stress responses of F1 and domesticated striped bass (Morone saxatilis) following a repeated acute stressor. Aquaculture Research, 52, 4786–4798.
- Khan, U. W., Øverli, Ø., Hinkle, P. M., Pasha, F. A., Johansen, I. B., Berget, I., … Vage, D. I. (2016). A novel role for pigment genes in the stress response in rainbow trout (Oncorhynchus mykiss). Scientific Reports, 6, 28969.
- Koakoski, G., Oliveira, T. A., da Rosa, J. G. S., Fagundes, M., Kreutz, L. C., & Barcellos, L. J. G. (2012). Divergent time course of cortisol response to stress in fish of different ages. Physiology and Behavior, 106, 129–132.
- Kubokawa, K., Yoshioka, M., & Iwata, M. (2001). Sex-specific cortisol and sex steroids responses in stressed sockeye Salmon during spawning period. Zoological Science, 18, 947–954.
- Kwong, R. W. M., Kumai, Y., & Perry, S. F. (2014). The physiology of fish at low PH: The zebrafish as a model system. Journal of Experimental Biology, 217, 651–662.
- McKenzie, D. J., Geffroy, B., & Farrell, A. P. (2021). Effects of global warming on fishes and fisheries. Journal of Fish Biology, 98, 1489–1492.
- Michonneau, F., Brown, J. W., & Winter, D. J. (2016). Rotl: An R package to interact with the open tree of life data. Methods in Ecology and Evolution, 7, 1476–1481.
- Mommsen, T., Vijayan, M., & Moon, T. (1999). Cortisol in Teleosts: Dynamics, mechanism of action, and metabolic regulation. Reviews in Fish Biology and Fisheries, 9, 211–268.
- Nakagawa, S., & Santos, E. S. A. (2012). Methodological issues and advances in biological meta-analysis. Evolutionary Ecology, 26, 1253–1274.
- Pagel, M. (1999). Inferring the historical patterns of biological evolution. Nature, 401, 877–884.
- Pickering, A. D., & Christie, P. (1981). Changes in the concentrations of plasma cortisol and thyroxine during sexual maturation of the hatchery-reared brown trout, Salmo trutta L. General and Comparative Endocrinology, 44, 487–496.
- Pickering, A. D., & Pottinger, T. G. (1983). Seasonal and diel changes in plasma cortisol levels of the brown trout, Salmo trutta L. General and Comparative Endocrinology, 49, 232–239.
- Pickering, A. D., & Pottinger, T. G. (1987). Poor water quality suppresses the cortisol response of salmonid fish to handling and confinement. Journal of Fish Biology, 30, 363–374.
- Planas, J., Gutierrez, J., Fernandez, J., Carrillo, M., & Canals, P. (1990). Annual and daily variations of plasma cortisol in sea bass, Dicentrarchus LabraxL. Aquaculture, 91, 171–178.
- Pottinger, T. G., & Carrick, T. R. (1999). Modification of the plasma cortisol response to stress in rainbow trout by selective breeding. General and Comparative Endocrinology, 116, 122–132.
- Rambo, C. L., Mocelin, R., Marcon, M., Villanova, D., Koakoski, G., de Abreu, M. S., … Bonan, C. D. (2017). Gender differences in aggression and cortisol levels in zebrafish subjected to unpredictable chronic stress. Physiology and Behavior, 171, 50–54.
- Robinson, N. A., Johnsen, H., Moghadam, H., Andersen, Ø., & Tveiten, H. (2019). Early developmental stress affects subsequent gene expression response to an acute stress in Atlantic Salmon: An approach for creating robust fish for aquaculture? G3: Genes, Genomes, Genetics, 9, 1597–1611.
- Sadoul, B., Alfonso, S., Bessa, E., Bouchareb, A., Blondeau-Bidet, E., Clair, P., … Geffroy, B. (2018). Enhanced brain expression of genes related to cell proliferation and neural differentiation is associated with cortisol receptor expression in fishes. General and Comparative Endocrinology, 267, 76–81.
- Sadoul, B., Friggens, N. C., Valotaire, C., Labbé, L., Colson, V., Prunet, P., & Leguen, I. (2017). Physiological and behavioral flexibility to an acute CO 2 challenge, within and between genotypes in rainbow trout. Comparative Biochemistry and Physiology -Part A: Molecular and Integrative Physiology, 209, 25–33.
- Sadoul, B., & Vijayan, M. M. (2016). Stress and growth. In Fish physiology (pp. 167–205). London: Elsevier Inc.
- Samaras, A., Santo, C. E., Papandroulakis, N., Mitrizakis, N., Pavlidis, M., Höglund, E., … Gorissen, M. (2018). Allostatic load and stress physiology in European seabass (Dicentrarchus labrax L.) and gilthead seabream (Sparus aurata L.). Frontiers in Endocrinology, 9, 1–13.
- Samaras, A., & Pavlidis, M. (2018). Regulation of divergent cortisol responsiveness in European sea bass, Dicentrarchus labrax L. PLoS One, 13, 1–13.
- Samaras, A., Papandroulakis, N., Costari, M., & Pavlidis, M. (2016). Stress and metabolic indicators in a relatively high (European sea bass, Dicentrarchus labrax) and a low (meagre, Argyrosomus regius) cortisol responsive species, in different water temperatures. Aquaculture Research, 47, 3501–3515.
- Schreck, C. B., & Tort, L. (2016). The concept of stress in fish. In Fish Physiology (pp. 1–34). London: Elsevier.
- Schulte, P. M., Healy, T. M., & Fangue, N. A. (2011). Thermal performance curves, phenotypic plasticity, and the time scales of temperature exposure. Integrative and Comparative Biology, 51, 691–702.
- Seebacher, F., Davison, W., Lowe, C. J., & Franklin, C. E. (2005). A falsification of the thermal specialization paradigm: Compensation for elevated temperatures in Antarctic fishes. Biology Letters, 1, 151–154.
- Somero, G. N. (2004). Adaptation of enzymes to temperature: Searching for basic ‘strategies’. Comparative Biochemistry and Physiology – B Biochemistry and Molecular Biology, 139, 321–333.
- Sumpter, J. P. (1997). The endocrinology of stress. Fish Stress and Health in Aquaculture, 819, 95–118.
- Tort, L. (2011). Stress and immune modulation in fish. Developmental and Comparative Immunology, 35, 1366–1375.
- Tudorache, C., Slabbekoorn, H., Robbers, Y., Hin, E., Meijer, J. H., Spaink, H. P., & Schaaf, M. J. M. (2018). Biological clock function is linked to proactive and reactive personality types. BMC Biology, 16, 1–13.
- Vandeputte, M., Porte, J. D., Auperin, B., Dupont-Nivet, M., Vergnet, A., Valotaire, C., … Chatain, B. (2016). Quantitative genetic variation for post-stress cortisol and swimming performance in growth-selected and control populations of European sea bass (Dicentrarchus labrax). Aquaculture, 455, 1–7.
- Vargas-Chacoff, L., Arjona, F. J., Ruiz-Jarabo, I., García-Lopez, A., Flik, G., & Mancera, J. M. (2020). Water temperature affects osmoregulatory responses in gilthead sea bream (Sparus aurata L.). Journal of Thermal Biology, 88, 102526.
- Vargas-Chacoff, L., Regish, A. M., Weinstock, A., & McCormick, S. D. (2018). Effects of elevated temperature on osmoregulation and stress responses in Atlantic salmon Salmo salar smolts in fresh water and seawater. Journal of Fish Biology, 93, 550–559.
- Varsamos, S., Flik, G., Pepin, J. F., Bonga, S. E. W., & Breuil, G. (2006). Husbandry stress during early life stages affects the stress response and health status of juvenile sea bass, Dicentrarchus labrax. Fish & Shellfish Immunology, 20, 83–96.
- Wickham, H., Chang, W., Henry, L., Pedersen, T. L., Takahashi, K., Wilke, C., … Dunnington, D. (2022). Package ‘Ggplot2’ create elegant data Visualisations using the grammar of graphics.