Abstract
Marine heatwaves have been linked to negative ecological effects in recent decades1,2. If marine heatwaves regularly induce community reorganization and biomass collapses in fishes, the consequences could be catastrophic for ecosystems, fisheries and human communities3,4. However, the extent to which marine heatwaves have negative impacts on fish biomass or community composition, or even whether their effects can be distinguished from natural and sampling variability, remains unclear. We investigated the effects of 248 sea-bottom heatwaves from 1993 to 2019 on marine fishes by analysing 82,322 hauls (samples) from long-term scientific surveys of continental shelf ecosystems in North America and Europe spanning the subtropics to the Arctic. Here we show that the effects of marine heatwaves on fish biomass were often minimal and could not be distinguished from natural and sampling variability. Furthermore, marine heatwaves were not consistently associated with tropicalization (gain of warm-affiliated species) or deborealization (loss of cold-affiliated species) in these ecosystems. Although steep declines in biomass occasionally occurred after marine heatwaves, these were the exception, not the rule. Against the highly variable backdrop of ocean ecosystems, marine heatwaves have not driven biomass change or community turnover in fish communities that support many of the world’s largest and most productive fisheries.
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Data availability
The data used in this project are available at https://doi.org/10.17605/OSF.IO/H6UKT.
Code availability
The code for this study is publicly available on GitHub at https://github.com/afredston/marine_heatwaves_trawl and archived at https://doi.org/10.17605/OSF.IO/H6UKT.
References
Smith, K. E. et al. Biological impacts of marine heatwaves. Annu. Rev. Mar. Sci. 15, 119–145 (2023).
Smale, D. A. et al. Marine heatwaves threaten global biodiversity and the provision of ecosystem services. Nat. Clim. Change 9, 306–312 (2019).
Cheung, W. W. L. et al. Marine high temperature extremes amplify the impacts of climate change on fish and fisheries. Sci. Adv. 7, eabh0895 (2021).
Cheung, W. W. L. & Frölicher, T. L. Marine heatwaves exacerbate climate change impacts for fisheries in the northeast Pacific. Sci. Rep. 10, 6678 (2020).
Harris, R. M. B. et al. Biological responses to the press and pulse of climate trends and extreme events. Nat. Clim. Change 8, 579–587 (2018).
Hobday, A. J. et al. A hierarchical approach to defining marine heatwaves. Prog. Oceanogr. 141, 227–238 (2016).
Auth, T. D., Daly, E. A., Brodeur, R. D. & Fisher, J. L. Phenological and distributional shifts in ichthyoplankton associated with recent warming in the northeast Pacific Ocean. Glob. Change Biol. 24, 259–272 (2018).
Suryan, R. M. et al. Ecosystem response persists after a prolonged marine heatwave. Sci. Rep. 11, 6235 (2021).
Le Grix, N., Zscheischler, J., Rodgers, K. B., Yamaguchi, R. & Frölicher, T. L. Hotspots and drivers of compound marine heatwaves and low net primary production extremes. Biogeosciences 19, 5807–5835 (2022).
Tittensor, D. P. et al. Next-generation ensemble projections reveal higher climate risks for marine ecosystems. Nat. Clim. Change 11, 973–981 (2021).
Mills, K. et al. Fisheries management in a changing climate: lessons from the 2012 ocean heat wave in the northwest Atlantic. Oceanography 26, 191–195 (2013).
Barbeaux, S. J., Holsman, K. & Zador, S. Marine heatwave stress test of ecosystem-based fisheries management in the Gulf of Alaska Pacific cod fishery. Front. Mar. Sci. 7, 703 (2020).
Cavole, L. et al. Biological impacts of the 2013–2015 warm-water anomaly in the northeast Pacific: winners, losers, and the future. Oceanography 29, 273–285 (2016).
The State of World Fisheries and Aquaculture 2020 (FAO, 2020); https://doi.org/10.4060/ca9229en.
Oliver, E. C. J. et al. Marine heatwaves. Annu. Rev. Mar. Sci. 13, 313–342 (2021).
Liu, G. et al. Reef-scale thermal stress monitoring of coral ecosystems: new 5-km global products from NOAA Coral Reef Watch. Remote Sens. 6, 11579–11606 (2014).
Craig, J. K. et al. Ecosystem Status Report for the U.S. South Atlantic Region (National Oceanic and Atmospheric Administration, 2021); https://doi.org/10.25923/qmgr-pr03.
Turcotte, F., Swain, D. P., McDermid, J. L. & DeLong, R. A. Assessment of the NAFO Division 4TVn Southern Gulf of St. Lawrence Atlantic Herring (Clupea harengus) in 2018–2019 (Canadian Science Advisory Secretariat, 2021).
Halpern, B. S. et al. A global map of human impact on marine ecosystems. Science 319, 948–952 (2008).
Lotze, H. K. et al. Depletion, degradation, and recovery potential of estuaries and coastal seas. Science 312, 1806–1809 (2006).
Ives, A. R., Dennis, B., Cottingham, K. L. & Carpenter, S. R. Estimating community stability and ecological interactions from time-series data. Ecol. Monogr. 73, 301–330 (2003).
Smith, K. E. et al. Socioeconomic impacts of marine heatwaves: global issues and opportunities. Science 374, eabj3593 (2021).
Chaudhary, C., Richardson, A. J., Schoeman, D. S. & Costello, M. J. Global warming is causing a more pronounced dip in marine species richness around the Equator. Proc. Natl Acad. Sci. USA 118, e2015094118 (2021).
McLean, M. et al. Disentangling tropicalization and deborealization in marine ecosystems under climate change. Curr. Biol. 31, 4817–4823 (2021).
Burrows, M. T. et al. Ocean community warming responses explained by thermal affinities and temperature gradients. Nat. Clim. Change 9, 959–963 (2019).
Freedman, R. M., Brown, J. A., Caldow, C. & Caselle, J. E. Marine protected areas do not prevent marine heatwave-induced fish community structure changes in a temperate transition zone. Sci. Rep. 10, 21081 (2020).
Robinson, J. P. W., Wilson, S. K., Jennings, S. & Graham, N. A. J. Thermal stress induces persistently altered coral reef fish assemblages. Glob. Change Biol. 25, 2739–2750 (2019).
Magurran, A. E., Dornelas, M., Moyes, F., Gotelli, N. J. & McGill, B. Rapid biotic homogenization of marine fish assemblages. Nat. Commun. 6, 8405 (2015).
Baselga, A. Separating the two components of abundance-based dissimilarity: balanced changes in abundance vs. abundance gradients. Methods Ecol. Evol. 4, 552–557 (2013).
Alabia, I. D. et al. Marine biodiversity refugia in a climate-sensitive subarctic shelf. Glob. Change Biol. 27, 3299–3311 (2021).
Catford, J. A., Wilson, J. R. U., Pyšek, P., Hulme, P. E. & Duncan, R. P. Addressing context dependence in ecology. Trends Ecol. Evol. 37, 158–170 (2022).
Schindler, D. E., Armstrong, J. B. & Reed, T. E. The portfolio concept in ecology and evolution. Front. Ecol. Environ. 13, 257–263 (2015).
Thorson, J. T., Scheuerell, M. D., Olden, J. D. & Schindler, D. E. Spatial heterogeneity contributes more to portfolio effects than species variability in bottom-associated marine fishes. Proc. R. Soc. B 285, 20180915 (2018).
Chesson, P. L. Multispecies competition in variable environments. Theor. Popul. Biol. 45, 227–276 (1994).
Kjesbu, O. S. et al. Highly mixed impacts of near-future climate change on stock productivity proxies in the north east Atlantic. Fish Fish. 23, 601–615 (2022).
Brown, C. J., Mellin, C., Edgar, G. J., Campbell, M. D. & Stuart‐Smith, R. D. Direct and indirect effects of heatwaves on a coral reef fishery. Glob. Change Biol. 27, 1214–1225 (2021).
Jacox, M. G., Alexander, M. A., Bograd, S. J. & Scott, J. D. Thermal displacement by marine heatwaves. Nature 584, 82–86 (2020).
Frölicher, T. L., Fischer, E. M. & Gruber, N. Marine heatwaves under global warming. Nature 560, 360–364 (2018).
Maureaud, A. A. et al. Are we ready to track climate-driven shifts in marine species across international boundaries? A global survey of scientific bottom trawl data. Glob. Change Biol. 27, 220–236 (2021).
Chase, J. M. et al. Species richness change across spatial scales. Oikos 128, 1079–1091 (2019).
Husson, B. et al. Successive extreme climatic events lead to immediate, large-scale, and diverse responses from fish in the Arctic. Glob. Change Biol. 28, 3728–3744 (2022).
Leimu, R. & Koricheva, J. Cumulative meta-analysis: a new tool for detection of temporal trends and publication bias in ecology. Proc. R. Soc. Lond B 271, 1961–1966 (2004).
Olsen, A., Larson, S., Padilla-Gamiño, J. & Klinger, T. Changes in fish assemblages after marine heatwave events in West Hawai‘i Island. Mar. Ecol. Prog. Ser. 698, 95–109 (2022).
Hillebrand, H. et al. Thresholds for ecological responses to global change do not emerge from empirical data. Nat. Ecol. Evol. 4, 1502–1509 (2020).
Long, R. D., Charles, A. & Stephenson, R. L. Key principles of marine ecosystem-based management. Mar. Policy 57, 53–60 (2015).
Oliver, E. C. J. et al. Projected marine heatwaves in the 21st century and the potential for ecological impact. Front. Mar. Sci. 6, 734 (2019).
Pinsky, M. L., Eikeset, A. M., McCauley, D. J., Payne, J. L. & Sunday, J. M. Greater vulnerability to warming of marine versus terrestrial ectotherms. Nature 569, 108–111 (2019).
Hoegh-Guldberg, O. et al. in Special Report on Global Warming of 1.5 °C (eds Masson-Delmotte, V. et al.) 175–311 (IPCC, WMO, 2018).
Meinshausen, M. et al. Realization of Paris Agreement pledges may limit warming just below 2 °C. Nature 604, 304–309 (2022).
R Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2021); https://www.R-project.org/.
Sherman, K. The large marine ecosystem concept: research and management strategy for living marine resources. Ecol. Appl. 1, 349–360 (1991).
Maureaud, A. A. et al. FishGlob_data: an integrated database of fish biodiversity sampled with scientific bottom-trawl surveys. Preprint at https://doi.org/10.31219/osf.io/2bcjw (2023).
World Register of Marine Species (WoRMS Editorial Board, 2022); https://www.marinespecies.org (2022).
Barnes, R. & Sahr, K. dggridR: Discrete Global Grids. R package version 3.0.0 https://CRAN.R-project.org/package=dggridR (2023).
Ricard, D., Branton, R. M., Clark, D. W. & Hurley, P. Extracting groundfish survey indices from the Ocean Biogeographic Information System (OBIS): an example from Fisheries and Oceans Canada. ICES J. Mar. Sci. 67, 638–645 (2010).
Day, P. B., Stuart-Smith, R. D., Edgar, G. J. & Bates, A. E. Species’ thermal ranges predict changes in reef fish community structure during 8 years of extreme temperature variation. Divers. Distrib. 24, 1036–1046 (2018).
Hutchins, L. W. The bases for temperature zonation in geographical distribution. Ecol. Monogr. 17, 325–335 (1947).
Black, B. A., Schroeder, I. D., Sydeman, W. J., Bograd, S. J. & Lawson, P. W. Wintertime ocean conditions synchronize rockfish growth and seabird reproduction in the central California Current ecosystem. Can. J. Fish. Aquat. Sci. 67, 1149–1158 (2010).
Tran, L. L. & Johansen, J. L. Seasonal variability in resilience of a coral reef fish to marine heatwaves and hypoxia. Glob. Change Biol. 29, 2522–2535 (2023).
Dahlke, F. T., Wohlrab, S., Butzin, M. & Pörtner, H.-O. Thermal bottlenecks in the life cycle define climate vulnerability of fish. Science 369, 65–70 (2020).
Jean-Michel, L. et al. The Copernicus global 1/12° oceanic and sea ice GLORYS12 reanalysis. Front. Earth Sci. 9, 698876 (2021).
Amaya, D. J., Alexander, M. A., Scott, J. D. & Jacox, M. G. An evaluation of high-resolution ocean reanalyses in the California Current system. Prog. Oceanogr. 210, 102951 (2023).
Amaya, D. J. et al. Bottom marine heatwaves along the continental shelves of North America. Nat. Commun. 14, 1038 (2023).
Banzon, V., Smith, T. M., Chin, T. M., Liu, C. & Hankins, W. A long-term record of blended satellite and in situ sea-surface temperature for climate monitoring, modeling and environmental studies. Earth Syst. Sci. Data 8, 165–176 (2016).
Reynolds, R. W. et al. Daily high-resolution-blended analyses for sea surface temperature. J. Clim. 20, 5473–5496 (2007).
Jacox, M. G. Marine heatwaves in a changing climate. Nature 571, 485–487 (2019).
Vogt, L., Burger, F. A., Griffies, S. M. & Frölicher, T. L. Local drivers of marine heatwaves: a global analysis with an Earth system model. Front. Clim. 4, 847995 (2022).
Gruber, N., Boyd, P. W., Frölicher, T. L. & Vogt, M. Biogeochemical extremes and compound events in the ocean. Nature 600, 395–407 (2021).
Devictor, V., Julliard, R., Couvet, D. & Jiguet, F. Birds are tracking climate warming, but not fast enough. Proc. R. Soc. B 275, 2743–2748 (2008).
Baselga, A. et al. betapart: Partitioning Beta Diversity into Turnover and Nestedness Components. R package version 1.5.6 https://CRAN.Rproject.org/package=betapart (2022).
Chaikin, S., Dubiner, S. & Belmaker, J. Cold-water species deepen to escape warm water temperatures. Glob. Ecol. Biogeogr. 31, 75–88 (2022).
Dulvy, N. K. et al. Climate change and deepening of the North Sea fish assemblage: a biotic indicator of warming seas. J. Appl. Ecol. 45, 1029–1039 (2008).
Hastings, R. A. et al. Climate change drives poleward increases and equatorward declines in marine species. Curr. Biol. 30, 1572–1577 (2020).
English, P. A. et al. Contrasting climate velocity impacts in warm and cool locations show that effects of marine warming are worse in already warmer temperate waters. Fish Fish. 23, 239–255 (2022).
Beukhof, E. et al. Marine fish traits follow fast-slow continuum across oceans. Sci. Rep. 9, 17878 (2019).
Flanagan, P. H., Jensen, O. P., Morley, J. W. & Pinsky, M. L. Response of marine communities to local temperature changes. Ecography 42, 214–224 (2019).
Babcock, R. C. et al. Decadal trends in marine reserves reveal differential rates of change in direct and indirect effects. Proc. Natl Acad. Sci. USA 107, 18256–18261 (2010).
Spalding, M. D. et al. Marine ecoregions of the world: a bioregionalization of coastal and shelf areas. BioScience 57, 573–583 (2007).
Palomares, M. L. D. et al. Fishery biomass trends of exploited fish populations in marine ecoregions, climatic zones and ocean basins. Estuar. Coast. Shelf Sci. 243, 106896 (2020).
Brooks, M. E. et al. glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. R J. 9, 378–400 (2017).
Wood, S. N. Generalized Additive Models: An Introduction with R (Chapman and Hall/CRC, 2006).
Fagerland, M. W. t-tests, non-parametric tests, and large studies – a paradox of statistical practice? BMC Med. Res. Methodol. 12, 78 (2012).
Acknowledgements
This research was performed as part of the FISHGLOB working group, ‘Fish biodiversity under global change: a worldwide assessment from scientific trawl surveys’, co-funded by the Centre for the Synthesis and Analysis of Biodiversity (CESAB) of the French Foundation for Research on Biodiversity (FRB), the Canadian Institute of Ecology and Evolution (CIEE) and the French embassy in Canada. We also acknowledge funding by the Lenfest Ocean Program grant no. 00032755 (A.L.F. and M.L.P.) and by US National Science Foundation grant nos. DEB-1616821 and CBET-2137701 (M.L.P.). T.L.F. acknowledges funding from the Swiss National Science Foundation (grant no. PP00P2_198897) and the European Union’s Horizon 2020 research and innovation programme under grant no. 820989 (project COMFORT, Our common future ocean in the Earth system—quantifying coupled cycles of carbon, oxygen and nutrients for determining and achieving safe operating spaces with respect to tipping points). W.W.L.C. and J.P.-A. acknowledge funding support from a NSERC discovery grant (RGPIN-2018-03864) and a SSHRC partnership grant (Solving-FCB). The work reflects only the authors’ views; the European Commission and its executive agency are not responsible for any use that may be made of the information the work contains.
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All authors contributed to writing and revising the manuscript. A.L.F., L.P., W.W.L.C., M.L.P., A.A.M., Z.J.K., M.L.D.P., J.T.T., A.A., B.M., J.P.-A. and N.L.S. contributed to the study conception and design. A.L.F., L.P., M.L.P., A.A.M., Z.J.K., T.L.F., M.L.D.P., J.T.T., B.M. and J.P.-A. contributed to data acquisition and analysis. All authors approved the submitted manuscript and subsequent revisions.
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Extended data figures and tables
Extended Data Fig. 1 Alternate version of Fig. 2 from the main text, showing results by region.
MHWs were calculated from the detrended GLORYS sea bottom temperature data with a five-day minimum duration threshold for MHWs, as used in the main text. Points represent log ratios of mean biomass in a survey from one year to the next. The fitted lines are linear regressions. The shaded areas are 95% confidence intervals. Survey names and sample sizes per survey are listed in Supp. Tab. 1.
Extended Data Fig. 2 Results did not change when alternative methods were used to quantify marine heatwaves.
Results were robust to (a) removing the five-day threshold for MHWs, (b) using SST from OISST instead of SBT from GLORYS (detrended), (c) using non-detrended data, (d) using a MHW metric of duration (days), (e) using a MHW metric of intensity (°C), (f) calculating degree heating days instead of MHW anomalies, and (g) using only summer MHWs (see Methods). The fitted lines are linear regressions. The shaded areas are 95% confidence intervals. For all panels n = 369 except in (b) n = 441.
Extended Data Fig. 3 Marine heatwave cumulative intensity (total anomaly in °C-days) in each survey region with and without detrending the temperature data to remove the signal of secular warming.
The main text results are detrended. Here, we plot MHW cumulative intensity based on all SBT anomalies from GLORYS, rather than applying the five-day threshold that was used the main text, to more clearly show the differences between the two methods.
Extended Data Fig. 4 Daily 95th percentile anomalies in the two marine heatwave data sources: sea surface temperature from OISST and sea bottom temperature from GLORYS (both detrended).
To simplify comparison we plot all anomalies, not just those MHWs that exceeded a five-day threshold. Note that the OISST time-series began in 1982 and GLORYS began in 1993. Region names are listed in Supp. Tab. 1.
Extended Data Fig. 5 Results are consistent across different metrics of the fish community.
We calculated mean abundance (a), mean biomass (b, used in the main text), median abundance (c), and median biomass (d). MHWs were calculated from the detrended GLORYS sea bottom temperature data with a five-day minimum duration threshold for MHWs, as used in the main text. Points represent log ratios of each metric in a survey from one year to the next (n = 343). The fitted lines are linear regressions. The shaded areas are 95% confidence intervals. The Northeast US survey was omitted because it did not have abundance data recorded.
Extended Data Fig. 6 Depth changes in the fish assemblage in response to marine heatwaves.
Fish assemblage depth change (log ratio) was not predicted by (a) the presence or absence of a MHW or (b) MHW cumulative intensity (total anomaly in °C-days; n = 369). MHWs were calculated from the detrended GLORYS sea bottom temperature data with a five-day minimum duration threshold for MHWs, as used in the main text. The fitted line in (b) is a linear regression and the shaded area is its 95% confidence interval.
Extended Data Fig. 7 Marine heatwave effect on taxon-specific biomass log ratios grouped by traits.
Biomass log ratio and MHW cumulative intensity (total anomaly in °C-days) grouped by (a) feeding mode (n = 29,628), (b) trophic level (n = 29,909), and (c) habitat preference (n = 29,681) of each taxon. Trait data were extracted from Beukhof et al75. (see Methods). MHWs were calculated from the detrended GLORYS sea bottom temperature data with a five-day minimum duration threshold for MHWs, as used in the main text. Fitted lines are linear regressions. Shaded areas are 95% confidence intervals.
Extended Data Fig. 8 The presence or absence of a MHW did not affect temporal community dissimilarity.
We measured community dissimilarity as partitioned occurrence-based beta diversity metrics of substitution and subset (Jaccard turnover (a) and nestedness (b)) and partitioned biomass-based beta diversity metrics of substitution and subset (Bray-Curtis balanced variation (c) and biomass gradient (d)). Community dissimilarity metrics were calculated within each region from one year to the next (n = 369). MHWs were calculated from the detrended GLORYS sea bottom temperature data with a five-day minimum duration threshold for MHWs, as used in the main text.
Extended Data Fig. 9 Results from a power analysis simulating how much data would be required to detect a range of MHW-induced biomass losses.
Approximately 600 survey-years in total (summed across all regions) would be required to find a significant effect if MHWs reduced biomass by 6% using either the GLORYS (a) or OISST (b) datasets; the dashed vertical line shows the sample size of our actual datasets. Given the true size of our datasets (n = 369 survey-years for GLORYS and 441 for OISST), our analysis had the power to detect a MHW-induced biomass decline of ~9% with GLORYS (c) and ~8% with OISST (d). The dashed horizontal line denotes one conventionally accepted threshold for power (0.8).
Extended Data Fig. 10 Biomass trends over time in each survey.
The top five taxa by biomass are highlighted. Shaded grey rectangles denote when any MHWs occurred in the preceding survey-year. MHWs were calculated from the detrended GLORYS sea bottom temperature data with a five-day minimum duration threshold for MHWs, as used in the main text. Note that x- and y-axes vary depending on time-series length and overall survey catch.
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Fredston, A.L., Cheung, W.W.L., Frölicher, T.L. et al. Marine heatwaves are not a dominant driver of change in demersal fishes. Nature 621, 324–329 (2023). https://doi.org/10.1038/s41586-023-06449-y
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DOI: https://doi.org/10.1038/s41586-023-06449-y