Abstract
A critical assumption underlying projections of biodiversity change associated with global warming is that ecological communities comprise balanced mixes of warm-affinity and cool-affinity species which, on average, approximate local environmental temperatures. Nevertheless, here we find that most shallow water marine species occupy broad thermal distributions that are aggregated in either temperate or tropical realms. These distributional trends result in ocean-scale spatial thermal biases, where communities are dominated by species with warmer or cooler affinity than local environmental temperatures. We use community-level thermal deviations from local temperatures as a form of sensitivity to warming, and combine these with projected ocean warming data to predict warming-related loss of species from present-day communities over the next century. Large changes in local species composition appear likely, and proximity to thermal limits, as inferred from present-day species’ distributional ranges, outweighs spatial variation in warming rates in contributing to predicted rates of local species loss.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Rent or buy this article
Prices vary by article type
from$1.95
to$39.95
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Williams, S. E., Shoo, L. P., Isaac, J. L., Hoffmann, A. A. & Langham, G. Towards an integrated framework for assessing the vulnerability of species to climate change. PLoS Biol. 6, e325 (2008)
Dawson, T. P., Jackson, S. T., House, J. I., Prentice, I. C. & Mace, G. M. Beyond predictions: biodiversity conservation in a changing climate. Science 332, 53–58 (2011)
Watson, J. E. M., Iwamura, T. & Butt, N. Mapping vulnerability and conservation adaptation strategies under climate change. Nature Clim. Change 3, 989–994 (2013)
Burrows, M. T. et al. Geographical limits to species-range shifts are suggested by climate velocity. Nature 507, 492–495 (2014)
Burrows, M. T. et al. The pace of shifting climate in marine and terrestrial ecosystems. Science 334, 652–655 (2011)
García Molinos, J . et al. Climate velocity and the future global redistribution of marine biodiversity. Nature Clim. Change http://dx.doi.org/10.1038/nclimate2769 (2015)
Beaugrand, G., Edwards, M., Raybaud, V., Goberville, E. & Kirby, R. R. Future vulnerability of marine biodiversity compared with contemporary and past changes. Nature Clim. Change 5, 695–701 (2015)
Lima, F. P. & Wethey, D. S. Three decades of high-resolution coastal sea surface temperatures reveal more than warming. Nature Commun. 3, 704 (2012)
Foden, W. B. et al. Identifying the world’s most climate change vulnerable species: a systematic trait-based assessment of all birds, amphibians and corals. PLoS ONE 8, e65427 (2013)
Pacifici, M. et al. Assessing species vulnerability to climate change. Nature Clim. Change 5, 215–224 (2015)
Sunday, J. M., Bates, A. E. & Dulvy, N. K. Global analysis of thermal tolerance and latitude in ectotherms. Proc. R. Soc. Lond. B 278, 1823–1830 (2011)
Sunday, J. M. et al. Species traits and climate velocity explain geographic range shifts in an ocean-warming hotspot. Ecol. Lett. 18, 944–953 (2015)
Kordas, R. L., Harley, C. D. G. & O’Connor, M. I. Community ecology in a warming world: the influence of temperature on interspecific interactions in marine systems. J. Exp. Mar. Biol. Ecol. 400, 218–226 (2011)
Okey, T. A., Agbayani, S. & Alidina, H. M. Mapping ecological vulnerability to recent climate change in Canada’s Pacific marine ecosystems. Ocean Coast. Manage. 106, 35–48 (2015)
Devictor, V., Julliard, R., Couvet, D. & Jiguet, F. Birds are tracking climate warming, but not fast enough. Proc. R. Soc. Lond. B 275, 2743–2748 (2008)
Devictor, V. et al. Differences in the climatic debts of birds and butterflies at a continental scale. Nature Clim. Change 2, 121–124 (2012)
Zografou, K. et al. Signals of climate change in butterfly communities in a Mediterranean protected area. PLoS ONE 9, e87245 (2014)
Bates, A. E. et al. Resilience and signatures of tropicalization in protected reef fish communities. Nature Climate Change 4, 62–67 (2013)
Cheung, W. W. L., Watson, R. & Pauly, D. Signature of ocean warming in global fisheries catch. Nature 497, 365–368 (2013)
Edgar, G. J. & Stuart-Smith, R. D. Systematic global assessment of reef fish communities by the Reef Life Survey program. Scientific Data 1, 140007 (2014)
Edgar, G. J. & Stuart-Smith, R. D. Ecological effects of marine protected areas on rocky reef communities: a continental-scale analysis. Mar. Ecol. Prog. Ser. 388, 51–62 (2009)
Tyberghein, L. et al. Bio-ORACLE: a global environmental dataset for marine species distribution modelling. Glob. Ecol. Biogeogr. 21, 272–281 (2012)
Tittensor, D. P. et al. Global patterns and predictors of marine biodiversity across taxa. Nature 466, 1098–1101 (2010)
Stuart-Smith, R. D. et al. Integrating abundance and functional traits reveals new global hotspots of fish diversity. Nature 501, 539–542 (2013)
Magnuson, J. J., Crowder, L. B. & Medvick, P. A. Temperature as an ecological resource. Am. Zool. 19, 331–343 (1979)
Jablonski, D. et al. Out of the tropics, but how? Fossils, bridge species, and thermal ranges in the dynamics of the marine latitudinal diversity gradient. Proc. Natl Acad. Sci. USA 110, 10487–10494 (2013)
Kellermann, V. et al. Upper thermal limits of Drosophila are linked to species distributions and strongly constrained phylogenetically. Proc. Natl Acad. Sci. USA 109, 16228–16233 (2012)
Thomas, C. D. et al. Extinction risk from climate change. Nature 427, 145–148 (2004)
Mumby, P. J., Chollett, I., Bozec, Y.-M. & Wolff, N. H. Ecological resilience, robustness and vulnerability: how do these concepts benefit ecosystem management? Current Opinion in Environmental Sustainability 7, 22–27 (2014)
Reynolds, R. W., Rayner, N. A., Smith, T. M., Stokes, D. C. & Wang, W. An improved in situ and satellite SST analysis for climate. J. Clim. 15, 1609–1625 (2002)
Hiddink, J. G. & Ter Hofstede, R. Climate induced increases in species richness of marine fishes. Glob. Change Biol. 14, 453–460 (2008)
Nguyen, K. D. T. et al. Upper temperature limits of tropical marine ectotherms: global warming implications. PLoS ONE 6, e29340 (2011)
Pörtner, H. O. Climate change and temperature-dependent biogeography: oxygen limitation of thermal tolerance in animals. Naturwissenschaften 88, 137–146 (2001)
Pörtner, H. O. & Knust, R. Climate change affects marine fishes through the oxygen limitation of thermal tolerance. Science 315, 95–97 (2007)
Figueira, W. F., Biro, P., Booth, D. J. & Valenzuela, V. C. Performance of tropical fish recruiting to temperate habitats: role of ambient temperature and implications of climate change. Mar. Ecol. Prog. Ser. 384, 231–239 (2009)
Brown, J. H., Stevens, G. C. & Kaufman, D. M. The geographic range: size, shape, boundaries, and internal structure. Annu. Rev. Ecol. Syst. 27, 597–623 (1996)
Sunday, J. M., Bates, A. E. & Dulvy, N. K. Thermal tolerance and the global redistribution of animals. Nature Clim. Change 2, 686–690 (2012)
Deutsch, C., Ferrel, A., Seibel, B., Pörtner, H. O. & Huey, R. B. Climate change tightens a metabolic constraint on marine habitats. Science 348, 1132–1135 (2015)
Graham, N. A. J. et al. Dynamic fragility of oceanic coral reef ecosystems. Proc. Natl Acad. Sci. USA 103, 8425–8429 (2006)
Araújo, M. B. et al. Heat freezes niche evolution. Ecol. Lett. 16, 1206–1219 (2013)
Tilman, D. Community invasibility, recruitment limitation, and grassland biodiversity. Ecology 78, 81–92 (1997)
Victor, D. G. & Kennel, C. F. Climate policy: ditch the 2°C warming goal. Nature 514, 30–31 (2014)
Spalding, M. D. et al. Marine ecoregions of the world: a bioregionalization of coastal and shelf areas. Bioscience 57, 573–583 (2007)
Bates, A. E. et al. Distinguishing geographical range shifts from artefacts of detectability and sampling effort. Divers. Distrib. 21, 13–22 (2015)
Acknowledgements
We thank the many Reef Life Survey (RLS) divers who participated in data collection and provide ongoing expertise and commitment to the program, University of Tasmania staff including J. Berkhout, A. Cooper, M. Davey, J. Hulls, E. Oh, J. Stuart-Smith and R. Thomson. Development of RLS was supported by the former Commonwealth Environment Research Facilities Program, and analyses were supported by the Australian Research Council, Institute for Marine and Antarctic Studies, and the Marine Biodiversity Hub, a collaborative partnership supported through the Australian Government’s National Environmental Science Programme. Additional funding and support for field surveys was provided by grants from the Ian Potter Foundation, CoastWest, National Geographic Society, Conservation International, Wildlife Conservation Society Indonesia, The Winston Churchill Memorial Trust, Australian-American Fulbright Commission, and ASSEMBLE Marine.
Author information
Authors and Affiliations
Contributions
R.D.S.-S., A.E.B. and G.J.E. conceived the idea, G.J.E., R.D.S.-S. and many others collected the data. R.D.S.-S. drafted the paper, with substantial input from A.E.B., G.J.E., N.S.B. and S.J.K. S.J.K. prepared the maps, A.E.B. and R.D.S.-S. analysed the data and prepared figures.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Additional information
A ‘live’ (periodically updated) database containing the Reef Life Survey ecological data used in this study is accessible online through http://www.reeflifesurvey.com.
Extended data figures and tables
Extended Data Figure 1 Sites used in analyses at which fish and invertebrate communities were surveyed by the Reef Life Survey program.
Numerous points are overlapping and hidden (n = 2,447). Ecoregion boundaries are shown in grey lines.
Extended Data Figure 2 Community temperature index values for reef fishes and invertebrates against mean annual sea surface temperature.
a–d, CTI calculated using abundance-weighted fish (a) and invertebrate (b) data, and including sites at which mean CTI confidence scores were less than 2.5 (n = 2,447 and 2,383 for fishes and invertebrates, respectively). Sites are colour-coded by ecoregion to help distinguish spatial patterns, but as a result of numerous ecoregions (n = 81), many ecoregion colours are similar. CTI calculated using presence-only fish (c) and invertebrate (d) data, and excluding sites with confidence scores <2.5 (n = 2,188 and 1,812 for fishes and invertebrates, respectively). Dotted lines have a slope of one, plotted for comparison with data.
Extended Data Figure 3 Global distribution of reef fish and invertebrate community thermal bias.
a, b, Community thermal bias (°C) is the difference in abundance-weighted CTI from local long-term mean annual sea surface temperature. Positive regions (warm colours) encompass ecological communities with a predominance of individuals with warmer thermal affinity than mean local sea temperatures. Colours are scaled to the mean thermal bias of sites surveyed within each ecoregion (see Extended Data Table 1 for sample sizes). Only ecoregions with sites that were surveyed are included.
Extended Data Figure 4 Frequency distribution of fish and invertebrate species’ latitudinal range midpoints.
a, b, Species for which confidence in thermal distribution midpoints (and therefore geographical distribution midpoints) was low are excluded (see Methods).
Extended Data Figure 5 Frequency distribution of fish (left) and invertebrate (right) species’ thermal distribution midpoints in 10° latitudinal bands from Papua New Guinea and down eastern Australia (rows).
a–j, Note y axes are on different scales and only species with confidence scores of two and three are included (see Methods).
Extended Data Figure 6 Frequency distribution of thermal distribution midpoints of species in major fish families spanning temperate and tropical zones.
Note y axes are on different scales and only species with confidence scores of two and three are included.
Extended Data Figure 7 Global distribution of TBiasmax of reef faunal communities.
TBiasmax is calculated as the difference between CTImax (using the 95th percentiles of species’ thermal distributions and presence data) and mean summer SST. Colours are scaled to the mean TBiasmax of sites surveyed within each ecoregion (see Extended Data Table 1 for sample sizes). Only ecoregions in which quantitative surveys were undertaken are included.
Extended Data Figure 8 The CTImax (mean 95th percentile of species thermal distributions) for reef faunal communities across temperate (blue), tropical (red) and subtropical (grey) sites.
SST data are means of the warmest 8 weeks of the year over the survey period (2008–2014). Points represent the surveyed community of fishes and invertebrates at each site (n = 2,091, only confidence scores >2.5). Regression lines are fitted to the maximum values within each ecoregion, with separate regressions fitted for sites categorised from Fig. 1 as temperate, tropical and subtropical.
Supplementary information
Supplementary Information
This file contains Supplementary Text and References. (PDF 97 kb)
Rights and permissions
About this article
Cite this article
Stuart-Smith, R., Edgar, G., Barrett, N. et al. Thermal biases and vulnerability to warming in the world’s marine fauna. Nature 528, 88–92 (2015). https://doi.org/10.1038/nature16144
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/nature16144
This article is cited by
-
A marine heatwave drives significant shifts in pelagic microbiology
Communications Biology (2024)
-
Climate change-related warming reduces thermal sensitivity and modifies metabolic activity of coastal benthic bacterial communities
The ISME Journal (2023)
-
Temperate functional niche availability not resident-invader competition shapes tropicalisation in reef fishes
Nature Communications (2023)
-
Tipping points of marine phytoplankton to multiple environmental stressors
Nature Climate Change (2022)
-
Climate change impacts the vertical structure of marine ecosystem thermal ranges
Nature Climate Change (2022)
Comments
By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.