Vol 453 | 15 May 2008 | doi:10.1038/nature06937
ARTICLES
Attributing physical and biological impacts
to anthropogenic climate change
Cynthia Rosenzweig1, David Karoly2, Marta Vicarelli1, Peter Neofotis1, Qigang Wu3, Gino Casassa4,
Annette Menzel5, Terry L. Root6, Nicole Estrella5, Bernard Seguin7, Piotr Tryjanowski8, Chunzhen Liu9,
Samuel Rawlins10 & Anton Imeson11
Significant changes in physical and biological systems are occurring on all continents and in most oceans, with a
concentration of available data in Europe and North America. Most of these changes are in the direction expected with
warming temperature. Here we show that these changes in natural systems since at least 1970 are occurring in regions of
observed temperature increases, and that these temperature increases at continental scales cannot be explained by natural
climate variations alone. Given the conclusions from the Intergovernmental Panel on Climate Change (IPCC) Fourth
Assessment Report that most of the observed increase in global average temperatures since the mid-twentieth century is
very likely to be due to the observed increase in anthropogenic greenhouse gas concentrations, and furthermore that it is
likely that there has been significant anthropogenic warming over the past 50 years averaged over each continent except
Antarctica, we conclude that anthropogenic climate change is having a significant impact on physical and biological systems
globally and in some continents.
and productivity, including shifts from cold-adapted to warmadapted communities, phenological changes and alterations in
species interactions19–22.
Detection and attribution in natural systems
Following the definition of attribution of observed changes in the
climate system23, changes in physical and biological systems are
attributed to regional climate change based on documented
Length of data series:
Number of data series
600
20–25 yr
26–35 yr
>35 yr
500
400
300
200
100
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The IPCC Working Group II Fourth Assessment Report found, with
very high confidence, that observational evidence from all continents
and most oceans shows that many natural systems are being affected
by regional climate changes, particularly temperature increases1,2.
The Working Group II further concluded that a global assessment
of data since 1970 shows that anthropogenic warming is likely
(66–90% probability of occurrence) to have had a discernible
influence on many physical and biological systems. Here we expand
this assessment with a larger database of observed changes and
extend the attribution from the global to the continental scale using
multiple statistical tests. We also consider the part that other driving
forces, especially land-use change, might have played at the study
locations.
Observed responses to climate change are found across a wide
range of systems as well as regions. Changes related to regional
warming have been documented primarily in terrestrial biological
systems, the cryosphere and hydrologic systems; significant changes
related to warming have also been studied in coastal processes,
marine and freshwater biological systems, and agriculture and
forestry (Fig. 1). In each category, many of the data series are over
35 years in length.
Responses in physical systems include shrinking glaciers in every
continent3,4, melting permafrost5,6, shifts in the spring peak of river
discharge associated with earlier snowmelt7,8, lake and river warming
with effects on thermal stratification, chemistry and freshwater
organisms9–11, and increases in coastal erosion12–14. In biological
systems, changes include shifts in spring events (for example, leaf
unfolding, blooming date, migration and time of reproduction),
species distributions and community structure15–18. Additionally,
studies have demonstrated changes in marine-ecosystem functioning
Figure 1 | Data series of observed changes in physical and biological
systems. Length of the data series and types of observed changes in physical
and biological systems. COST725 data series of terrestrial biological changes
(.28,000 European phenological time series17) were measured over 30 years
(1971–2000; not displayed).
1
NASA/Goddard Institute for Space Studies and Columbia Center for Climate Systems Research, 2800 Broadway, New York, New York 10025, USA. 2School of Earth Sciences,
University of Melbourne, Victoria 3010, Australia. 3School of Meteorology, University of Oklahoma, 100 East Boyd Street, Norman, Oklahoma 73019, USA. 4Centro de Estudios
Cientı́ficos, Avenida Arturo Prat 514, Casilla 1469, Valdivia, Chile. 5Center of Life and Food Sciences Weihenstephan, Technical University of Munich, Am Hochanger 13, 85 354
Freising, Germany. 6Stanford University, Center for Environmental Science and Policy, Stanford, California 94305, USA. 7INRA Unité Agroclim, Site Agroparc, domaine Saint-Paul,
F-84914 Avignon Cedex 9, France. 8Department of Behavioural Ecology, Institute of Environmental Biology, Adam Mickiewicz University, Umultowska 89, PL-61–614 Poznan, Poland.
9
China Water Information Center, Lane 2 Baiguang Road, Beijing 100761, China. 10Caribbean Epidemiology Center, 16–18 Jamaica Boulevard, Federation Park, PO Box 164, Port of
Spain, Trinadad and Tobago. 113D-Environmental Change, Curtiuslaan 14, 1851 AM, Heiloo, Netherlands.
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NATURE | Vol 453 | 15 May 2008
statistical analyses confirmed by process-level understanding in
the interpretation of results. For example, a statistical association
between poleward expansion of species’ ranges and warming
temperatures is expected when temperatures exceed physiological
thresholds. The observed changes in both climate and the natural
system are demonstrated to be: unlikely to be entirely due to natural
variability; consistent with the estimated responses of either physical
or biological systems to a given regional climate change; and not
consistent with alternative, plausible explanations of the observed
change that exclude regional climate change.
Attribution of changes in natural systems to anthropogenic warming requires further analysis because the observed regional climate
changes must be attributed to anthropogenic causes. Combining these
two types of attribution, called ‘joint’ attribution2, has lower statistical
confidence than either of the individual attribution steps alone.
One approach to joint attribution, which uses what may be called
an ‘end-to-end’ method, has already been conducted in several
studies of specific physical and biological systems. This approach
involves linking climate models with process-based or statistical
models to simulate changes in natural systems caused by different
climate forcing factors, and comparing these directly with observed
changes in natural systems. When temperature data from the
HadCM3 global climate model were used to examine the likely cause
for changes in the timing of spring events of Northern Hemisphere
wild animals and plants, results show the strongest agreement
when the modelled temperatures were derived from simulations
incorporating anthropogenic forcings24. Other similar studies have
shown that the retreat of two glaciers in Switzerland and Norway
cannot be explained by natural variability of climate and glacier mass
balance25, that observed global and Arctic patterns of changes in
streamflow are consistent with the response to anthropogenic climate
change26,27, and that the observed increase in the area of forests
burned in Canada over the last four decades is consistent with the
response caused by anthropogenic climate change28.
Here we conduct a joint attribution study across multiple physical
and biological systems at both the global and the continental scale.
We demonstrate statistical consistency of observed changes (which
are very unlikely to be caused by natural internal variability of the
systems themselves or other driving forces) in natural systems with
warming and conduct spatial analyses that show that the agreement
between the patterns of observed significant changes in natural
systems and temperature changes is very unlikely to be caused by
the natural variability of the climate (Supplementary Fig. 1).
Combined with the attribution of global and continental-scale
warming to anthropogenic climate forcing demonstrated by IPCC
Working Group I Fourth Assessment Report, this analysis provides
strong support for joint attribution of observed impacts.
Consistency with warming
Based on a database of documented responses in physical and biological systems from 1970 to 2004, temperature-related changes have
been observed in all continents. Each documented response is a
‘statistically significant’ signal that is beyond the natural internal
variability of those systems. The largest numbers of entries in the
database are for Europe and North America, followed by North
Central Asia (Fig. 2). Sparse evidence of responses related to temperature changes exists in Latin America, Africa and Australia. Physical
and biological systems in regions without data series may or may not
be changing, but are not documented in peer-reviewed literature.
Most (about 90% of the .29,500 data series, P = 0.001) changes
in these systems at the global scale have been in the direction expected
as a response to warming. Ninety-five per cent of the 829 documented physical changes have been in directions consistent with warming, such as glacier wastage and an earlier spring peak of river
discharge. For biological systems, 90% of the ,28,800 documented
changes in plants and animals are responding consistently to
temperature changes (mostly by means of earlier blooming, leaf
unfolding and spring arrival). Warming in oceans, lakes and rivers
is also affecting marine and freshwater biological systems (for
example, changes in phenology, migration and community composition in algae, plankton and fish).
An evaluation of possible publication bias has been undertaken
using comprehensive phenological network data in Europe29, in
which a systematic analysis of all available records (for example,
leafing and flowering) documented the percentages of data series that
are not changing and of significant changes in both directions (for
example, in spring, in 66% there is no significant change, in 31% the
onset dates are significantly advanced, and in 3% the onset dates are
significantly delayed)29. The percentage of data series with significant
changes consistent with warming found in Europe (,90%) is close to
that found in North America and Asia, providing an indication that
the database may represent an unbiased sample of changes in both
directions in those continents.
Spatial analyses at global and continental scales
The IPCC Working Group I Fourth Assessment Report concluded
that most of the observed increase in global average temperatures
since the mid-twentieth century is very likely (. 90% probability of
occurrence) to be due to the observed increase in anthropogenic
greenhouse gas concentrations30. It is very likely that the observed
warming patterns cannot be explained by changes in natural external
forcing factors, such as changes in solar irradiance or volcanic aerosols; the latter is likely to have had a cooling influence during this
period.
At the global scale, agreement between the pattern of observed
changes in physical and biological systems and the pattern of
observed temperature change holds for two different gridded temperature data sets and two different pattern-comparison methods,
and is exceptionally unlikely (P = 0.01) to be explained by natural
internal climate variability or natural variability of the systems; the
latter is determined in the individual studies (Fig. 3). The spatial
coherence of temperature trends across the globe is taken into
account in these pattern comparisons using more than 3,000 years
of climate model simulation data. The prevalence of observed
statistically significant changes in physical and biological systems in
expected directions consistent with anthropogenic warming in every
continent and in most oceans means that anthropogenic climate
change is having a discernible effect on physical and biological systems at the global scale.
For the first time, IPCC Working Group I Fourth Assessment
Report extended its attribution of temperature trends to the continental scale, concluding that it is likely that there has been significant
anthropogenic warming over the past 50 years averaged over each
continent except Antarctica31. Similarly, a discernible anthropogenic
influence is found in changes in natural systems in some continents
where there is sufficient spatial coverage of responses in natural systems, including Asia and North America, and marginally in Europe.
In these continents, there is a much greater probability of finding
coincident significant warming and observed responses in the
expected direction. Despite the presence of strong climate variability
related to the North Atlantic Oscillation in Europe as well as its
relatively small size, which makes it harder to distinguish signal from
noise31, the plethora of evidence allows a signal to be detected, primarily in biological systems. The statistical agreement between the
locations and directions of observed significant changes in natural
systems and observed significant warming across Asia and North
America (P,0.05) and across Europe (P,0.1) is very unlikely to
be due to natural variability alone (Fig. 3). Responses not consistent
with warming observed in 5u 3 5u grid cells with warming temperature may be due to those systems responding to seasonal rather
than recorded annual changes or to local cooling not represented in
average cell temperatures; biological variation across species may also
have a role (for example, late flowering species tend to be less affected
by warming than earlier flowering ones). For the other continents,
354
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NATURE | Vol 453 | 15 May 2008
the sparse coverage of observed response studies makes it difficult to
separate the observed responses related to anthropogenic temperature rise from those possibly caused by large-scale natural climate
variations.
Discussion and conclusions
The wide variety of observed responses to regional climate trends in
expected directions combined with the attribution of climate trends
to anthropogenic causes at both global and continental scales30
demonstrates that anthropogenic climate change is already having
a significant impact on multiple systems globally and in some continents. Most observed system changes are found in the cryosphere
and in terrestrial biological systems and are consistent with the functional understanding and modelled predictions of climate change
impacts. The far fewer data series in Africa, Australia and Latin
America are closely co-located with warming, but these cannot yet
be attributed to anthropogenic climate forcing.
The issues of other climate and non-climate driving forces are
important. In considering other drivers of change for phenology,
much of the evidence in plants comes from changes observed in
the spring. Even though day length can have a modulating effect
on spring phenology depending on the plant species, it is not a factor
in these studies because species remain in situ for the length of
the time series, during which day length has not changed. There
is also the possibility that increasing CO2 is directly influencing
plant phenology; however, experimental results show no consistent
direction of response (that is, an advance or delay)32. Concerning
trees, older trees tend to unfold leaves in spring later than younger
28,117
119
94% 90%
405
579
94% 88%
53
11
98% 100%
5
9
100% 100%
8
98
22
100% 91%
16
96% 88%
Cryosphere
Hydrology
Coastal processes
Temperature change (°C)
1970–2004
Number of terrestrial biology data series in Europe
1–100
101–1,000
Physical
systems
Marine
Freshwater
Terrestrial biology
Agriculture
1,001–7,500
–2.4 –2.0 –1.0 –0.2 0.2
Figure 2 | Location and consistency of observed changes with warming.
Locations of significant changes in physical systems (snow, ice and frozen
ground as well as hydrology and coastal processes) and biological systems
(terrestrial, marine and freshwater biological systems), and linear trends of
1.0
2.0
3.5
Biological
systems
Number of
significant
observed
changes
Number of
significant
observed
changes
Percentage of
significant
changes
consistent
with warming
Percentage of
significant
changes
consistent
with warming
surface air temperature (HadCRUT3; ref. 35) between 1970 and 2004.
Regions are based on data in refs 36 and 37. White areas do not contain
sufficient climate data to estimate a trend. Note that there are overlapping
symbols in some locations; Africa includes parts of the Middle East.
355
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ones, so with longer time series on one specific object, the onset
dates should become later with time owing to ageing, not earlier as
observed owing to warming. Finally, some of the plant data, especially in Europe, come from phenological gardens that have been
protected from the direct effects of land-use change for decades.
Land-use change, management practices, pollution and human
demography shifts are all—along with climate—drivers of environmental change. Explicit consideration of these factors in observedchange studies strengthens the robustness of the conclusions. To
determine the role of other driving forces in the data series used in
this analysis, we assessed the likelihood of their having a direct effect
on the observed system (see Supplementary Table 1). Out of the
,29,500 data series documented in ,80 studies included in the
database, effects documented in only 3 studies (9 data series in 4
cells) were likely to have been caused by a driving force other than
climate change (for example, habitat destruction, pollution or fishery
by-catch disposal). Removing these data series from the statistical
analyses does not change the results significantly.
Land-use change can affect physical and biological systems
indirectly through its effects on climate. Yet, for recent climate trends
on a global scale, the effect of land-use change is small31. In addition,
40
20
Significant
warming
Warming
NAM
Cooling
Significant
cooling
n = 52
Cz = 0.52 (P < 0.05)
80
60
40
20
100
Significant
warming
Warming
LA
Cooling
60
40
20
0
Significant
warming
100
Warming
AS
Cooling
60
40
20
0
Significant
warming
Warming
Cooling
Significant
cooling
Figure 3 | Distribution of cells with temperature changes and significant
observed changes. Expected and observed distributions of cells with
significant responses consistent with warming and distributions of cells with
significant responses not consistent with warming for 5u 3 5u grid cells of
temperature change between 1970 and 2004 (HadCRUT3). The global total
includes polar regions and marine systems. Shown is the number of cells (n)
EUR
n = 33
Cz = 0.58 (P ~ 0.1)
80
60
40
20
100
Significant
warming
Warming
AFR
Cooling
Significant
cooling
n=3
Cz = 0.94 (P ~ 0.1)
80
60
40
20
0
Significant
warming
Significant
cooling
n = 42
Cz = 0.70 (P < 0.05)
80
100
0
Significant
cooling
n=5
Cz = 0.86 (P = NS)
80
Percentage of cells
0
Percentage of cells
Percentage of cells
Cells with significant changes consistent
with warming
Cells with significant changes not consistent
with warming
Expected values of distributions of cells with
temperature changes and significant changes
60
0
Percentage of cells
n = 183
Cz = 0.62 (P << 0.01)
80
100
Percentage of cells
Global
100
Percentage of cells
Percentage of cells
100
because these effects may result in warming in some regions and
cooling in others (for example, agricultural expansion tends to warm
the Amazon and cool the mid-latitudes)33,34, they are very unlikely to
explain the coherent responses that have been found across the
diverse range of systems and across the continental and global scales
considered (Supplementary Table 2). Cooling in temperate regions
occurs because the clearing of forests for agriculture may increase
albedo during periods of snow cover, although recent afforestation
may be dampening this effect.
Documentation of observed changes in physical and biological
systems in tropical and subtropical regions is still sparse. These areas
include Africa, South America, Australia, Southeast Asia, the Indian
Ocean and some regions of the Pacific. One reason for this lack of
documentation might be that some of these areas do not have pronounced temperature seasons, making events such as the advance of
spring phenology less relevant. Other possible reasons for this imbalance are a lack of data and published studies, lag effects in responses,
and resilience in systems. Improved observation networks are
urgently needed to enhance data sets and to document sensitivity
of physical and biological systems to warming in tropical and subtropical regions, where many developing countries are located.
Warming
ANZ
Cooling
Significant
cooling
n=4
Cz = 0.93 (P < 0.05)
80
60
40
20
0
Significant
warming
Warming
Cooling
Significant
cooling
with observed impacts and temperature data, the pattern congruence
between locations of significant responses and standardized temperature
trends (Cz), and the probability (P) that pattern agreement could be
explained by natural internal variability of temperature fields.
Abbreviations: AFR, Africa; ANZ, Australia and New Zealand; AS, Asia;
EUR, Europe; LA, Latin America; NAM, North America; NS, not significant.
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METHODS SUMMARY
We developed a database of observed changes in natural systems from peerreviewed papers, demonstrating a statistically significant trend in change in
either direction related to temperature and containing data for at least 20 years
between 1970 and 2004. Observations in the studies were characterized as a
‘change consistent with warming’ or a ‘change not consistent with warming’.
The databases of the observed significant changes in the natural systems were
overlaid with two gridded observed temperature data sets and the spatial patterns of the observed system changes were compared with the observed temperature trends using two different pattern-comparison measures.
Full Methods and any associated references are available in the online version of
the paper at www.nature.com/nature.
Received 28 January; accepted 19 March 2008.
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Supplementary Information is linked to the online version of the paper at
www.nature.com/nature.
Acknowledgements We thank J. Palutikof, D. Rind and A. Watkinson for their
feedback, and J. Mendoza for work on the graphics. The Goddard Institute for
Space Studies authors acknowledge the support of the Earth Science Division,
NASA Science Mission Directorate. D.K. is supported by the Australian Research
Council as a Federation Fellow. Q.W. is supported by a Gary Comer Science and
Education Foundation Postdoctoral Fellowship and by the National Science
Foundation grant ATM-0555326. We acknowledge the Program for Climate
Model Diagnosis and Intercomparison (PCMDI) and the WCRP’s Working Group
on Coupled Modelling (WGCM) for their roles in making available the multi-model
data set. Support of this data set is provided by the Office of Science, US
Department of Energy.
Author Contributions C.R., D.K., G.C., A.M., T.L.R., B.S., P.N. and M.V. conceived
the analytical framework; P.N., M.V., A.M. and N.E. constructed the database;
M.V., D.K. and Q.W. performed the statistical analyses; G.C., A.M., T.L.R., P.T., B.S.,
C.L. and S.R. provided expertise in observed changes in physical and biological
systems; and P.N., A.M., C.R. and A.I. analysed other driving forces.
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www.nature.com/reprints. Correspondence and requests for materials should be
addressed to C.R. (crosenzweig@giss.nasa.gov).
357
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doi:10.1038/nature06937
METHODS
Database of observed changes. We developed a database of observations from
peer-reviewed papers (primarily published since the IPCC Third Assessment
Report38), specifically documenting the data series in terms of system, region,
longitude and latitude, dates and duration, statistical significance, type of
impact, and whether or not land use was identified as a driving factor (see
Supplementary Table 1). Data for the system changes were taken from ,80
studies (of which ,75 are new since the Third Assessment Report) containing
.29,500 data series. Studies were selected that demonstrate a statistically significant trend in change in either direction in systems related to temperature or
to other climate change variables as described by the authors, and that contain
data for at least 20 years between 1970 and 2004 (although study periods may
extend earlier or later). Observations in the studies were characterized as a
‘change consistent with warming’ or a ‘change not consistent with warming’.
Spatial analysis. Databases of the observed significant changes in the natural
systems and the regional temperature trends over the period 1970–2004 were
overlaid in a geographical information system. For Europe, even though there
were very large numbers of observed response data series in some cells, these were
counted as single cells in the spatial analysis. Two different gridded observed
temperature data sets were used: HadCRUT3 (ref. 35) and GHCN-ERSST
(ref. 39), both of which were used in the IPCC Fourth Assessment Report. In
each 5u 3 5u grid cell, the observed system responses were assessed as consistent
with warming or not consistent with warming—based on a decision rule of 80%
or more of data series consistent with warming within a cell—providing a binary
pattern of 183 (HadCRUT3) and 203 (GHCN-ERSST) cells across the globe.
There are fewer cells with temperature data in the HadCRUT3 data set because it
does not use any infilling of data from adjacent cells, unlike GHCN-ERSST. All
cells with observed temperature data are included from each of the data sets,
irrespective of the sign of the temperature trend.
The spatial patterns of the observed system changes were compared with the
observed temperature trends using two different pattern-comparison measures.
To assess the significance of these observed measures of pattern agreement,
global temperature trend data were obtained from long control simulations with
seven different climate models from the WCRP CMIP3 multi-model database at
PCMDI, to represent the range of 35-year temperature trends across the globe
resulting from natural climate variations. Details of the different models used are
included in Supplementary Table 3. The global temperature trend fields from the
climate models represent the spatial coherence and decadal variability of natural
internal temperature variations.
Two different pattern-comparison measures were used: a binary pattern congruence (uncentred pattern correlation) between the gridded binary field of
system responses consistent (or not consistent) with warming and the gridded
field of positive (or negative) temperature trends; and a pattern congruence
between the gridded binary field of system responses and the gridded field of
standardized temperature trends (the 35-year temperature trends divided by the
standard deviation of 35-year temperature trends caused by natural internal
climate variations). For each of these measures, the observed values for the
two different observed temperature-trend data sets were compared with the
distributions obtained using temperature trends caused by natural internal
climate variability, as represented by the climate models. Significant attribution
was assigned when both spatial statistics methods and both temperature data sets
showed significant results. Detailed results are presented in the Supplementary
Information and are summarized in the section ‘Spatial analyses at global and
continental scales’ above.
38. IPCC (ed.) Climate Change 2001: Impacts, Adaptation, and Vulnerability:
Contribution of Working Group II to the Third Assessment Report to the International
Panel on Climate Change (Cambridge Univ. Press, Cambridge, UK, 2001).
39. Smith, T. M. & Reynolds, R. W. A global merged land and sea surface temperature
reconstruction based on historical observations (1880–1997). J. Clim. 18,
2021–2036 (2005).
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