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
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