LETTERS PUBLISHED ONLINE: 22 JULY 2012 | DOI:10.1038/NCLIMATE1628 Emerging Vibrio risk at high latitudes in response to ocean warming Craig Baker-Austin 1 * , Joaquin A. Trinanes 2,3 , Nick G. H. Taylor 1 , Rachel Hartnell 1 , Anja Siitonen 4 and Jaime Martinez-Urtaza 5 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 unprece- dented 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 un- equalled 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. Recent evidence suggests that global average temperatures have risen by nearly 0.8 C since the late nineteenth century and have risen by approximately 0.2 C per decade over the past 25 years 3 . In addition to increasing temperatures, altering patterns of precipitation and runoff are expected that may drive a consequent reduction in the salinity of estuaries and coastal wetlands 4 . Many marine bacterial pathogens of relevance to human health, such as vibrios, grow preferentially in warm (>15 C), low-salinity (<25 ppt NaCl) sea water 5 . The anticipated warming and reduced salinity of coastal regions located at high latitudes will provide new areas for the natural occurrence of pathogenic strains. Warming patterns have been related to the emergence of Vibrio outbreaks in temperate and cold regions, such as in Chile 6 , Peru 7 , Israel 8 , the US Pacific northwest 9 and northwest Spain 5 . Despite the increasing number of reports showing the poleward spreading of Vibrio diseases, conclusive evidence linking the emergence of infections with climate change remains contentious. This situation is in part owing to the effects of warming being more pronounced at higher latitudes 3 and often in areas that lack detailed historical epidemiological data sets 5 , meaning the emergence of cases is often 1 Centre for Environment Fisheries and Aquaculture Science, Barrack Road, Weymouth, Dorset DT4 8UB, UK, 2 Laboratory of Systems, Technological Research Institute, Universidad de Santiago de Compostela, Campus Universitario Sur, Santiago de Compostela, 15782, Spain, 3 National Oceanic and Atmospheric Administration, National Environmental Satellite Data and Information Service, CoastWatch, 5200 Auth Road, Camp Springs, Maryland 20746, USA, 4 Bacteriology Unit, National Institute for Health and Welfare (THL), Helsinki, FI-00271, Finland, 5 Instituto de Acuicultura, Universidad de Santiago de Compostela, Campus Universitario Sur, Santiago de Compostela, 15782, Spain. These authors contributed equally to this work. Present address: European Centre for Disease Prevention and Control (ECDC), Tomtebodavägen 11 A, 17183 Stockholm, Sweden. *e-mail: craig.baker-austin@cefas.co.uk. interpreted as a sporadic event owing to exceptional conditions, rather than a response to long-term environmental change. The Baltic Sea area provides a particularly interesting region to study emerging Vibrio disease. During the extremely warm sum- mers of 1994, 2003 and 2006, a plethora of reports emerged docu- menting Vibrio-associated wound infections linked to recreational exposure in this area 10–14 and included numerous fatalities 12–14 . The Baltic Sea is warming rapidly 1,2 and represents one of the largest low-salinity marine ecosystems on Earth. Low sea surface salinity (<NaCl 25 ppt) is a major risk factor contributing to Vibrio prevalence and associated clinical risk in marine systems 5,15 . Furthermore, more than 30 million people live within 50 km of the Baltic Sea and this, coupled to an increasingly susceptible population in Europe, may substantially increase clinical risk 5 . All these factors suggest the population neighbouring the Baltic Sea is at particular risk from pathogenic vibrios, particularly in light of future projections regarding increasing sea surface temperature (SST) and freshening salinity conditions 3,16 . We examined associations between epidemiological data on the emergence and dynamics of Vibrio disease in the Baltic and long- term SST records and recent satellite-derived fields (see Methods). The analysis of the different SST data sets corroborated a significant warming trend evident across the Baltic Sea area, especially during the summer (Fig. 1a and Supplementary Fig. S1A,B). For the region between 54 N–60 N and 10 E–20 E, the increasing trend in an- nual SST from 1854 to 2010 was 0.51 C per century (approximately 1 C for summer months) and this rate increased for the 1900–2010 period to 0.77 C (approximately 1.5 C for summer). Significantly, the warming rate from 1980 to 2010 increased to approximately 5 C (6 C for summer months) per century, a sixfold increase from the 1854 to 2010 rate. Autoregressive integrated moving average (ARIMA) models also showed a clear warming trend in the region, higher than 1 C per century (Fig. 1a). These findings augment analysis 1 that indicated significant and unprecedented recent warming trends in the Baltic Sea region up to 2003 and demonstrate that this trend has continued recently. From recently analysed Hadley SST data sets, the post-1987 warming rate in the Baltic Sea exceeded 1.0 C per decade, more than seven times the global rate, and the Baltic area experienced the fastest net SST warming trend (1.35 C) of any large marine ecosystem between 1982 and 2007 (ref. 2). The recent warming trend identified here represents, to our knowledge, the fastest warming marine NATURE CLIMATE CHANGE | ADVANCE ONLINE PUBLICATION | www.nature.com/natureclimatechange 1 © 2012 Macmillan Publishers Limited. All rights reserved.