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Emerging Vibrio risk at high latitudes in response to ocean warming

A Corrigendum to this article was published on 27 July 2016

This article has been updated

Abstract

There is increasing concern regarding the role of climate change in driving bacterial waterborne infectious diseases. Here we illustrate associations between environmental changes observed in the Baltic area and the recent emergence of Vibrio infections and also forecast future scenarios of the risk of infections in correspondence with predicted warming trends. Using multidecadal long-term sea surface temperature data sets we found that the Baltic Sea is warming at an unprecedented rate. Sea surface temperature trends (1982–2010) indicate a warming pattern of 0.063–0.078 °C yr−1 (6.3–7.8 °C per century; refs 1, 2), with recent peak temperatures unequalled in the history of instrumented measurements for this region. These warming patterns have coincided with the unexpected emergence of Vibrio infections in northern Europe, many clustered around the Baltic Sea area. The number and distribution of cases correspond closely with the temporal and spatial peaks in sea surface temperatures. This is among the first empirical evidence that anthropogenic climate change is driving the emergence of Vibrio disease in temperate regions through its impact on resident bacterial communities, implying that this process is reshaping the distribution of infectious diseases across global scales.

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Figure 1: Warming trends in the region limited by 54° N–60° N, 10° E–20° E in the Baltic Sea.
Figure 2: Vibrio cases and SST.
Figure 3: SST temperature and salinity for the summer of 2006 and estimation of the risk of infection.

Change history

  • 27 June 2016

    In the version of this Letter originally published, an outdated version of Figure panel 3d was displayed in Fig. 3, and so the population density and risk data shown was incorrect. Figure panel 3d has been replaced in the online version of this Letter.

References

  1. Mackenzie, B. R. & Schiedek, D. Daily ocean monitoring since the 1860s shows record warming of northern European seas. Glob. Change Biol. 13, 1335–1347 (2007).

    Article  Google Scholar 

  2. Belkin, I. M. Rapid warming of large marine ecosystems. Prog. Oceanogr. 81, 207–213 (2009).

    Article  Google Scholar 

  3. IPCC Climate Change 2007: Synthesis Report (Cambridge Univ. Press, 2007).

  4. Hakkinen, S. Surface salinity variability in the northern North Atlantic during recent decades. J. Geophys. Res. 107, 8003 (2002).

    Article  Google Scholar 

  5. Baker-Austin, C., Stockley, L., Rangdale, R. & Martinez-Urtaza, J. Environmental occurrence and clinical impact of Vibrio vulnificus and Vibrio parahaemolyticus: A European perspective. Environ. Micro. Rep. 2, 7–18 (2010).

    Article  Google Scholar 

  6. Gonzalez-Escalona, N.,V. et al. Vibrio parahaemolyticus diarrhea, Chile, 1998 and 2004. Emerg. Infect. Dis. 11, 129–131 (2005).

    Article  Google Scholar 

  7. Martinez-Urtaza, J. et al. Emergence of Asiatic vibrio diseases in South America in phase with El Niño. Epidemiology 19, 829–837 (2008).

    Article  Google Scholar 

  8. Paz, S. et al. Climate change and the emergence of Vibrio vulnificus disease in Israel. Environ. Res. 103, 390–396 (2007).

    Article  CAS  Google Scholar 

  9. CDC 2008. Centers for Disease Control and Prevention (CDC), Outbreak of Vibrio parahaemolyticus infections associated with eating raw oysters–Pacific Northwest, 1997, Morb. Mort. Week. Rep. 47, 457–462 (2008).

  10. Dalsgaard, A. et al. Clinical manifestations and molecular epidemiology of Vibrio vulnificus infections in Denmark. Eur. J. Clin. Microbiol. Infect. Dis. 15, 227–232 (1996).

    Article  CAS  Google Scholar 

  11. Ruppert, J. et al. Two cases of severe sepsis due to Vibrio vulnificus wound infection acquired in the Baltic Sea. Eur. J. Clin. Microbiol. Infect. Dis. 23, 912–915 (2004).

    CAS  Google Scholar 

  12. Lukinmaa, S. et al. Territorial waters of the Baltic Sea as a source of infections caused by Vibrio cholerae non-O1, non-O139: Report of 3 hospitalized cases. Diagn. Microbiol. Infect. Dis. 54, 1–6 (2006).

    Article  Google Scholar 

  13. Andersson, Y. & Ekdahl, K. Wound infections due to Vibrio cholerae in Sweden after swimming in the Baltic Sea, summer 2006. Euro Surveill. 11, E060803.2 (2006).

    CAS  Google Scholar 

  14. Frank, C., Littman, M., Alpers., K. & Hallauer, J. Vibrio vulnificus wound infections after contact with the Baltic Sea, Germany. Euro Surveill. 11, E060817.1 (2006).

    CAS  Google Scholar 

  15. Motes, M. L. et al. Influence of water temperature and salinity on Vibrio vulnificus in northern Gulf and Atlantic coast oysters (Crassostrea virginica). Appl. Environ. Microbiol. 64, 1459–1465 (1998).

    CAS  Google Scholar 

  16. Meier, H. E. M., Kjellström, E. & Graham, L. P. Estimating uncertainties of projected Baltic Sea salinity in the late 21st century. Geophys. Res. Lett. 33, L15705 (2006).

    Article  Google Scholar 

  17. Høi, L. et al. Occurrence of Vibrio vulnificus Biotypes in Danish Marine Environments. Appl. Environ. Microbiol. 64, 7–13 (1998).

    Google Scholar 

  18. Gotoh, K. T. et al. Bile acid-induced virulence gene expression of Vibrio parahaemolyticus reveals a novel therapeutic potential for bile acid sequestrants. PLoS One 5, e13365 (2010).

    Article  Google Scholar 

  19. Mahoney, J. C. et al. Comparison of the pathogenic potentials of environmental and clinical Vibrio parahaemolyticus strains indicates a role for temperature regulation in virulence.. Appl. Environ. Microbiol. 76, 7459–7465 (2010).

    Article  CAS  Google Scholar 

  20. Randa, M. A., Polz, M. F. & Lim, E. Effects of temperature and salinity on Vibrio vulnificus population dynamics as assessed by quantitative PCR. Appl. Environ. Microbiol. 70, 5469–5476 (2004).

    Article  CAS  Google Scholar 

  21. Vezzulli, L. et al. Long-term effects of ocean warming on the prokaryotic community: evidence from the vibrios. ISME J. 6, 21–30 (2012).

    Article  Google Scholar 

  22. Oberbeckmann, S. et al. Seasonal dynamics and modeling of a Vibrio community in coastal waters of the North Sea. Microb. Ecol. 63, 543–551 (2012).

    Article  Google Scholar 

  23. Collin, B. & Rehnstam-Holm, A. S. Occurance and potential pathogensis of Vibrio cholerae, Vibrio parahaemolyticus and Vibrio vulnificus on the south coast of Sweden. FEMS Microb. Ecol. 1–8 (2011).

  24. Meier, H. E. M. Baltic Sea climate in the late twenty-first century: A dynamical downscaling approach using two global models and two emission scenarios. Clim. Dynam. 27, 39–68 (2006).

    Article  Google Scholar 

  25. Lindegren, M. et al. Ecological forecasting under climate change: The case of Baltic cod. Proc. R. Soc. Lond. B 277, 2121–2130 (2010).

    Article  Google Scholar 

  26. Lima, F. P. & Wethey, D. S. Three decades of high-resolution coastal sea surface temperature reveal more than warming. Nature Commun. 3, 704. (2012).

    Article  Google Scholar 

  27. Lobitz, B. M. et al. Climate and infectious disease: Use of remote sensing for detection of Vibrio Cholerae by indirect measurement. Proc. Natl Acad. Sci. USA 97, 1438–1443 (2000).

    Article  CAS  Google Scholar 

  28. Durbin, J. & Koopman, S. J. Time Series Analysis by State Space Methods (Oxford Univ. Press, 2001).

    Google Scholar 

  29. R Development Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2011) Available at: http://www.R-project.org/.

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Acknowledgements

C.B-A. was supported by the Cefas Seedcorn programme. J.A.T. was partially financially supported by NOAA/CoastWatch and by project 09MDS009CT from X. de Galicia. We thank members of the VibrioNet consortium and C. Schets for informal discussion on the epidemiological data sets and J. V. McArthur and R. Cary Tuckfield for comments on earlier versions of the manuscript.

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C.B-A., J.A.T. and J.M-U. conceived the project. J.A.T. and J.M-U. designed experiments and C.B-A., J.A.T., J.M-U. and N.G.H.T. analysed the data. R.H. and A.S. provided valuable interpretations. C.B.A, J.A.T., N.G.H.T. and J.M-U. wrote the paper.

Corresponding author

Correspondence to Craig Baker-Austin.

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The authors declare no competing financial interests.

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Baker-Austin, C., Trinanes, J., Taylor, N. et al. Emerging Vibrio risk at high latitudes in response to ocean warming. Nature Clim Change 3, 73–77 (2013). https://doi.org/10.1038/nclimate1628

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