LETTERS
PUBLISHED ONLINE: 1 SEPTEMBER 2013 | DOI: 10.1038/NCLIMATE1990
Crop pests and pathogens move polewards in a
warming world
Daniel P. Bebber1 , Mark A. T. Ramotowski2 and Sarah J. Gurr1 *
Global food security is threatened by the emergence and spread
of crop pests and pathogens. Spread is facilitated primarily
by human transportation, but there is increasing concern that
climate change allows establishment in hitherto unsuitable
regions. However, interactions between climate change, crops
and pests are complex, and the extent to which crop pests
and pathogens have altered their latitudinal ranges in response
to global warming is largely unknown. Here, we demonstrate
an average poleward shift of 2.7 ± 0.8 km yr−1 since 1960, in
observations of hundreds of pests and pathogens, but with
significant variation in trends among taxonomic groups. Ob-
servational bias, where developed countries at high latitudes
detect pests earlier than developing countries at low latitudes,
would result in an apparent shift towards the Equator. The
observed positive latitudinal trends in many taxa support the
hypothesis of global warming-driven pest movement.
Since crop domestication 10,000 years ago, farmers have been
plagued by multitudes of pests and pathogens (hereafter termed
pests) causing starvation and social upheaval1–4 . Classic examples
include the 1840s Irish potato famine caused by the oomycete
Phytophthora infestans and the 1943 Great Bengal Famine due to the
fungus Helminthosporium oryzae 3 . The threat persists. Between 10
and 16% of crop production is lost to pests, with similar losses post-
harvest1,4,5 . Indeed, losses of major crops to fungi and oomycetes
alone amount to enough to feed 8.5% of today’s population2 . The
diversity of crop pests is daunting (fungi, bacteria, viruses, viroids,
oomycetes, insects and nematodes) and continues to expand
through evolution and dissemination of new pathotypes2,6–8 .
Recently emerged strains of the rusts Puccinia graminis and
P. striiformis are among the most virulent and rapidly spreading
pathogens ever seen9,10 , and a new and invasive lineage of P. infestans
has rapidly displaced other late blight genotypes11 .
Dissemination occurs through both natural and anthropogenic
processes, facilitated by the increasing interconnectedness of the
global food chain. More than half of all emerging diseases of
plants are spread by introduction6 . Weather is the second most
important factor6 . For example, fusarium head blight of wheat
has re-emerged in the USA, favoured by warm, wet weather
at anthesis5 . Insect pests are also influenced by weather, with
chewing insects responding negatively to drought and borers
positively12 . Warming generally stimulates insect herbivory at
higher latitudes, primarily through increased winter survival13 ,
as seen in mountain pine beetle (Dendroctonus ponderosae)
outbreaks in the US Pacific Northwest14 . The effects of weather
are dependent on both host and pest responses. For example,
drought stress can decrease plant resistance15 , but infection
probability is lower in dry conditions16 . Although pests are
1 Department of Biosciences, University of Exeter, Stocker Road, Exeter EX4 4QD, UK, 2 Christ Church College, University of Oxford, St Aldates, Oxford OX1
1DP, UK. *e-mail: s.j.gurr@exeter.ac.uk
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spread by human activities and aerial dispersal6,8 , prevailing
climatic conditions are likely to determine their subsequent
establishment and growth.
The influence of weather on crop disease has led to speculation
about the effects of anthropogenic climate change on global
food security5,6,17,18 . Projections are complicated by the interacting
influences of increasing atmospheric CO2 concentrations, changing
climatic regimes, altered frequency/intensity of extreme weather
events, and differing responses of the plant and its enemies17–19 .
However, a general pattern of increasing latitudinal range with
mean global temperature is anticipated6 , either through direct
effects of climate change on the pests, or on the availability of
host crops. Latitudinal shifts in species distributions, as organisms
track temperature optima, have been detected in thousands of wild
populations20–22 . However, a comprehensive analysis of latitudinal
range shifts of crop pests has not hitherto been attempted. Here,
we undertake this analysis using published observations of 612
crop pests and pathogens (Supplementary Table S1 and Fig. S1).
The data were investigated for the presence of observational biases,
caused by latitudinal gradients in the abilities of countries to detect,
identify and report pests, and latitudinal trends in observations for
individual pest species.
Identification of reporting biases is central to the analysis of
latitudinal trends in pest observation. The earliest observation for
a particular pest in a particular region is equal to the true date
of arrival plus a delay due to observation, identification, reporting
and selection of a reliable record for inclusion in the database. In a
regression of the latitude of observation against observation date,
the regression coefficient will be positive if there is an observed
increase over time, negative if there is a decrease, and statistically
undifferentiated from zero if no trend is detected. A bias will arise
if the delay period is related to latitude. Scientific and technical
capacity are greater for countries at high latitudes23 , and these
countries also report more pests (see Supplementary Information).
Therefore, countries at high latitudes should report earlier than
low latitudes, and the regression coefficient of latitude on year of
observation should be negative in the absence of any real latitudinal
trend in observations.
Two-thirds of pests were observed either solely in the Northern
Hemisphere (restricted above 23.4◦ N) or northern and tropical
(between 23.4◦ S and 3.4◦ N) zones for the first decade of
observations (Supplementary Table S2). Around one-tenth of the
pests were found solely outside the tropics, and another tenth
within the tropics, with the remainder global (in both tropical and
extra-tropical zones). Only two pests were restricted to the south
(below 23.4◦ S). By the end of the observation period more than
half were global in distribution, a third were either northern or
1
LETTERS
120
100
Latitudinal range (°)
80
60
40
20
0 South
0 100 200 300
Longitudinal range (°)
Figure 1 | Latitudinal range versus longitudinal range. Grey points show
values for individual pests in each year. The curves show fitted values (solid
line) (±s.e.m., shown by dashed curves) from generalized additive mixed
models, with random slopes and intercepts for individual pest species. The
straight dashed line shows the 1:1 relationship for scale.
northern and tropical, and less than one-tenth of the pests were
restricted to the tropical or tropical and southern zones. Of those
originally restricted to the tropics, more than two-thirds spread out,
most becoming global. Of those originally found outside the tropics,
half were later found in the tropics. The latitudinal range (the
difference between the most-northerly and most-southerly known
latitudes) for a pest in a given year increased roughly linearly with
the longitudinal range (Fig. 1). However, this occurred more rapidly
over smaller ranges, such that, on average, the rate of increase was
approximately equal for latitude and longitude.
Latitudinal trends in observations varied greatly among in-
dividual pest species (Supplementary Fig. S2), but taking all
species together, significant positive latitudinal trends were detected
(Fig. 2). For Northern Hemisphere observations, the Acari, Bacte-
ria, Coleoptera, Diptera, Fungi, Hemiptera, Isoptera, Lepidoptera
and Oomycota show increased detection towards the north since
1960 (Fig. 3). In contrast, Nematoda and viruses show the opposite
trend, towards the Equator. Randomization tests showed that no
trend should be detected, if no temporal pattern were present (see
Supplementary Information). Linear mixed-effects models of coun-
try (or region) latitude against year of first observation showed an
average poleward shift in recorded incidences of 2.7 ± 0.8 km yr−1
(t -test versus zero, t = 3.3, df = 22,387, p = 0.0009) since 1960
for both hemispheres combined, 2.2 ± 0.8 km yr−1 in the Northern
Hemisphere (t = 2.7, df = 18,769, p = 0.007) and 1.7±1.7 km yr−1
in the Southern Hemisphere (t = 1.0, df = 3,222, p = 0.3).
Linear mixed-effects models were also fitted to detect average
trends within pest species or pathotypes. For all pests combined,
the mean latitudinal shifts were not significant (Supplementary
Table S3), but this seemed to be due to large variability among
pest groups (Supplementary Tables S4 and S5). For all years,
observations of Coleoptera and Lepidoptera shifted north in the
Northern Hemisphere, whereas Nematoda and viruses shifted
south (Fig. 4). From 1960 onwards, Acari, Coleoptera, Fungi,
Hemiptera and Lepidoptera shifted north and Nematoda and
viruses shifted south, towards the Equator (Fig. 4). Taking multiple
comparisons into account, significant trends were found in a few
pests (Supplementary Table S6). From 1960 onwards, 12 pests
(of which ten were fungi) showed significant trends towards the
Equator, and 17 pests (of which six were nematodes) away.
The results indicate significant positive latitudinal shifts for
many important groups of crop pests and pathogens. Overall, there
has been a significant trend of increasing numbers of pest and
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© 2013 Macmillan Publishers Limited. All rights reserved.
NATURE CLIMATE CHANGE DOI: 10.1038/NCLIMATE1990
North
35
34
33
32
Latitude (°)
¬18
¬20
¬22
¬24
1900 1920 1940 1960 1980 2000
Year
Figure 2 | Latitude versus year of earliest observation for all pests, in the
Northern and Southern hemispheres. Fitted values (solid line) and
standard errors (dashed lines) are derived from generalized additive mixed
models of latitude against year of observation.
pathogen observations at higher latitudes, globally and in both the
Northern and Southern hemispheres. The mean shift in detection
since 1960 (26.6 km per decade) is more rapid than that reported
for many wild species (17.6 km per decade; ref. 22), but is nearly
identical to that expected by temperature changes (27.3 km per
decade; ref. 21). Latitudinal variation in countries’ abilities to report
pests would probably bias the data towards earlier detection at
higher latitudes. Therefore, the positive trends cannot be explained
by likely latitudinal variation in the ability to detect pathogens.
Overall trends in new observations could include increased
detection probabilities at high latitudes unrelated to predictors such
as gross domestic product (GDP), or result from real shifts in pests
that have not yet been detected at lower latitudes. Therefore, models
for mean shifts within species were also fitted. Within-species shifts
were significant for some groups, particularly ‘mobile invertebrate
pests such as Lepidoptera, Coleoptera and Hemiptera, but also
Fungi. The viruses and Nematoda showed clear observational shifts
towards the Equator. Both viruses and Nematoda lack the means
for airborne dispersal, and the trend could therefore be due to
trade alone, whereas the aerially dispersed groups exhibit poleward
shifts. Other possibilities are that viruses and Nematoda are difficult
to identify in the field, being soil-borne, and their symptoms
potentially misidentifiable as abiotic stresses. Therefore, reporting
bias due to latitudinal variation scientific and technical capacity
could explain these negative trends.
It is likely that movements of wild species are hampered by
habitat fragmentation, dispersal limitation, and some by long
generation times. A climatic debt can be incurred, whereby species
do not move as rapidly as expected given shifting climatic regimes24 .
In contrast, pathogens have evolved to disperse and grow rapidly,
and their spread is facilitated by the global trade in seeds and
agricultural produce. It is likely that anthropogenic6 and aerial8
dispersal continuously introduce pathogens to new areas, and in
NATURE CLIMATE CHANGE DOI: 10.1038/NCLIMATE1990 LETTERS
All Acari Bacteria Coleoptera Diptera
1,000

500

¬500

¬1,000

Fungi Hemiptera Hymenoptera Isoptera Lepidoptera

Distance from Equator (km)

1,000

500

¬500

¬1,000

Nematoda Oomycota Protozoa Thysanoptera Viruses

1,000

500

¬500

¬1,000

1960 1980 2000 1960 1980 2000 1960 1980 2000 1960 1980 2000 1960 1980 2000
Year

Figure 3 | Latitude versus year of observation for pest taxonomic groups in the Northern Hemisphere from 1960 onwards. Fits for all pests combined are
shown for comparison. Fitted values (solid line) and standard errors (dashed lines) are derived from generalized additive mixed models.

many cases only inclement weather prevents their establishment All 1960 onwards
in a new habitat. As such, an unwanted assisted colonization Lep.
programme is taking place for plant pests and pathogens25 . Pro.
Observed changes in pest distributions accord with observations Col.
of wild species20,22 , direct responses of pests to warming14 , Hem.
and with expectations for expanding pest ranges under climate Fun.
change6 . Although recent climate change is implicated as an Hym.
important driver of these observations, other factors could bias Aca.
the results. New crop varieties and agricultural technologies Bac.
have extended the agricultural margin northward in the USA26 , Iso.
and deforestation has increased production in the tropics, thus Oom.
providing new opportunities for pest invasions at high and low Dip.
latitudes. Correlations between land use change and climate change All.
can obscure analyses based on species temperature ranges20,24,27 . Thy.
Range expansions could be biased in one direction if equatorial Vir.
barriers, such as the Sahara desert, were more restrictive to pest Nem.
movement than poleward barriers such as permafrost. However, ¬40 ¬20 0 20 40 60 ¬40 ¬20 0 20 40 60
randomization tests demonstrated that no latitudinal shift would be Rate (km yr¬1)
expected in the absence of a directional temporal trend. Although
factors such as land use change do influence species distributions, Figure 4 | Mean latitudinal shift (km yr−1 ) for pest taxonomic groups in
the influence of such confounding factors decreases in large-scale the Northern Hemisphere for all years, and for 1960 onwards. Estimates
studies, and detecting climate signals in noisy data is unlikely in the are from linear mixed-effects models of latitude against observation year
absence of real climate drivers20 . for centred species-level data. Positive values denote a poleward shift,
Global food security is dependent on numerous physical, negative values a shift towards the Equator. Error bars show 95%
agronomic and socioeconomic factors. There is little doubt, confidence intervals of the mean. Taxonomic groups are abbreviated, and
however, that climate change and its effects on plant health combined observations (All) included for comparison. Groups are ordered
will increasingly threaten human populations, particularly those by the mean of the coefficients.
living in poorer regions1,18,28,29 . We have shown that reported
observations of hundreds of pests and pathogens are consistent their transport will be critical in controlling this growing threat to
with the hypothesis of climate change drivers, and contrary to the global food security1,2,6 .
hypothesis of greater detection capability in developed countries.
Although countries at higher latitudes are better able to monitor Methods
and manage emerging pests and diseases, these countries also The latitudes and dates of the earliest record of 612 crop pests and pathogens were
tend to have the greatest productivity per unit land area, and abstracted from two exhaustive historical databases—the CABI Distribution Maps
of Plant Pests, and of Plant Diseases30 (Supplementary Table S1). The maps are
the threat to food security is troubling. If climate change will available from CABI (www.cabi.org). Pest observations were at country level, and
make it easier for crop-destroying organisms to spread, renewed regional for some large countries (USA, Brazil, India, China, Japan, Russia and
efforts to monitor the occurrence of pests and diseases and control Australia); therefore, latitudes of country or region centroids were used in analyses,

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LETTERS
to determine whether the latitude of new observations has changed significantly
over time, and whether any shift was consistent either with any observational bias
or with the expected effect of climate change.
The presence of a record for a particular geographical region in a given year
depends on numerous factors, including the presence of the pest, occurrence at a
detectable and economically significant level, and scientific and technical capacity
to sample, identify and publish a report in a source abstracted by CABI. The data
are therefore likely to suffer from strong observational bias. When considering the
potential impact of climate change on crop pest distributions, any observational
bias linked to latitude must be investigated.
Let L be the latitude of earliest observation, and Do be the year of earliest
observation in the map. Do is not the date of arrival, but includes both the delay
in reporting and selection of a record for the map, that is, Do = Da + Dd , where
Da is the true date of arrival, and Dd is a random variable describing the delay
between arrival and reporting in the map. If there has been a real latitudinal shift
in pest distributions, we propose a relationship E(L) ∼ aDa , where the coefficient a
is positive. Estimation of a will be biased if delay in observation varies with latitude
E(Dd ) ∼ bL, such that E(L) ∼ aDa + bL, where b is non-zero. If b is positive, then
regression of L on Do will overestimate a, and if b is negative then the regression
will underestimate a. In other words, if countries at higher latitudes delay reporting
longer than those at low latitudes, it will seem as though pests arrived at higher
latitudes later, and a poleward latitudinal shift could be erroneously inferred. If
countries at low latitudes report later, the situation is reversed, and a latitudinal
shift towards the Equator would be inferred. On the basis of known biases in
species observational capacity towards higher latitudes, correlation between per
capita GDP and scientific capacity23 , increases in per capita GDP with latitude,
and increase in pest detection number with latitude, we infer that countries at
higher latitudes are likely to have better pest detection capacity, meaning that Dd
is smaller and b < 0. Therefore, the likely bias in observational capacity means
that a positive latitudinal shift in observations is unlikely in the absence of a real
climate change signal.
The data were tested for the presence of non-Gaussian errors and spatial
autocorrelation before linear mixed-effects models and generalized additive mixed
models were applied, to estimate latitudinal shifts in observations of the entire data
set, taxonomic groups and individual species. Linear mixed-effects models on 1,000
randomizations of year against latitude, with pest as a random effect, were used
to remove any temporal trend in the pest observations and thereby determine the
latitudinal shift expected in the absence of a global trend such as climate change.
The latitudes of the centroids of countries or regions were used in the analysis.
Randomization tests gave an expected latitudinal shift of −0.011 ± 0.017 km yr−1 ,
that is, no significant shift under the null hypothesis of no temporal trend
affecting pest observations.
Full methods are described in the Supplementary Information.
Received 15 December 2012; accepted 31 July 2013;
published online 1 September 2013
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Acknowledgements
The authors thank Earthwatch and the HSBC Climate Partnership for financially
supporting D.P.B.
Author contributions
M.A.T.R. collected the data, D.P.B. analysed the data and following discussion with
S.J.G., D.P.B. and S.J.G. wrote the paper.
Additional information
Supplementary information is available in the online version of the paper. Reprints and
permissions information is available online at www.nature.com/reprints. Correspondence
and requests for materials should be addressed to S.J.G.
Competing financial interests
The authors declare no competing financial interests.