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Nature Ecology & Evolution
nature ecology & evolution
https://doi.org/10.1038/s41559-023-02235-1Article
Meta-analysis reveals less sensitivity of
non-native animals than natives to extreme
weather worldwide
Shimin Gu 1,4, Tianyi Qi 1,2,4, Jason R. Rohr 3 & Xuan Liu 1,2
Extreme weather events (EWEs; for example, heatwaves, cold spells,
storms, oods and droughts) and non-native species invasions are two
major threats to global biodiversity and are increasing in both frequency
and consequences. Here we synthesize 443 studies and apply multilevel
mixed-eects metaregression analyses to compare the responses of 187
non-native and 1,852 native animal species across terrestrial, freshwater
and marine ecosystems to dierent types of EWE. Our results show that
marine animals, regardless of whether they are non-native or native, are
overall insensitive to EWEs, except for negative eects of heatwaves on
native mollusks, corals and anemone. By contrast, terrestrial and freshwater
non-native animals are only adversely aected by heatwaves and storms,
respectively, whereas native animals negatively respond to heatwaves,
cold spells and droughts in terrestrial ecosystems and are vulnerable
to most EWEs except cold spells in freshwater ecosystems. On average,
non-native animals displayed low abundance in terrestrial ecosystems, and
decreased body condition and life history traits in freshwater ecosystems,
whereas native animals displayed declines in body condition, life history
traits, abundance, distribution and recovery in terrestrial ecosystems, and
community structure in freshwater ecosystems. By identifying areas with
high overlap between EWEs and EWE-tolerant non-native species, we also
provide locations where native biodiversity might be adversely aected by
their joint eects and where EWEs might facilitate the establishment and/or
spread of non-native species under continuing global change.
Climate change and invasive species are two major threats to global
biodiversity
1,2
. Understanding how climate change influences inva-
sions of non-native species is crucial for mitigating their joint impacts
in the context of accelerating global change
3
. In addition to gradual
shifts in temperature and precipitation, scientists have recognized that
the increasing frequency and magnitude of extreme weather events
(EWEs), such as heatwaves, cold spells, storms, floods and droughts4,
can result in even greater biological consequences than changes to
climate means
5
. Comparison of the responses of native and non-native
species to EWEs is crucial for developing early and effective strategies
for native species conservation and non-native species prevention
under accelerating EWEs associated with climate change6.
Considerable evidence from native species has shown that EWEs
can cause declines in population abundances and species richness,
Received: 16 March 2023
Accepted: 21 September 2023
Published online: xx xx xxxx
Check for updates
1Key Laboratory of Animal Ecology and Conservation Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing, China. 2University of Chinese
Academy of Sciences, Beijing, China. 3Department of Biological Sciences, Environmental Change Initiative, University of Notre Dame, Notre Dame, IN,
USA. 4These authors contributed equally: Shimin Gu, Tianyi Qi. e-mail: liuxuan@ioz.ac.cn
Nature Ecology & Evolution
Article https://doi.org/10.1038/s41559-023-02235-1
Sevastopol Bay
26
. Non-native species showed less susceptibility and
recovered more quickly than native species in the marine epibenthic
fouling community of Bodega Harbor, California, USA
27
. Despite these
striking case studies, a thorough understanding of the general effect
of EWEs on non-native and native species across ecosystems, types of
EWE and multiple taxonomic groups is still lacking, impeding forecasts
of the responses of non-native species to climate change and their
joint impacts on native species. It is critical to fill this literature gap
because resources for managing and mitigating biological invasions
and climate change are limited. Thus, it is crucial to identify the most
affected regions and problematic taxa so that those resources are
targeted properly.
Here we applied a multilevel mixed-effects metaregression to
conduct a global synthesis of non-native and native animal responses
to EWEs (Supplementary Fig. 1). These species spanned terrestrial,
freshwater (mammals, birds, amphibians, reptiles, fish and inverte-
brates) and marine ecosystems (surface and benthic fishes and benthic
invertebrates). Each measured effect size was assigned to one of eight
major response categories: physiology, body condition, behaviour,
restructure community composition and limit post-event recovery
across ecosystems
7–13
. However, published studies also found that
non-native arthropods, mammals, shellfishes and fishes might be
relatively tolerant of, or even respond positively to EWEs
14–17
. There
are several possible mechanisms to explain different responses of
non-native and native species to EWEs
18
. First, EWEs often result in
considerable mortality of native species and could thus create more
vacant niches to facilitate non-native species invasions19,20. For exam-
ple, severe drought events decreased native invertebrates and fishes by
increasing water salinity, facilitating the establishment of non-native
salt-tolerant counterparts
14,15
. Second, invaders can have more rapid
growth rates, stronger competitive abilities, higher phenotypic plastic-
ity, broader tolerance of disturbance and quicker recovery and prolif-
eration than natives
21–24
. For example, the abundance of most native
fish in the Rio Minho estuary, Portugal, declined but abundance of
non-native fish increased after extreme droughts and floods, and thus
the fish assemblage there was dominated by a few invasive fish species
after extreme weather events25. Non-native mesozooplankton species
exhibit higher flexibility to marine heatwaves than native species in the
84
Number of studies
47
31
24 21
74
32 47
76
Number of sample
eect sizes
0
100
300
500
0
500
1,500
Number of sample
eect sizes
129
Heatwave
Cold spell
Storm
Flood
Drought
EWEs
a
b
c
d
e
Amphibia
Anthozoa
Ascidiacea
Aves
Bivalvia
Branchiopoda
Clitellata
Euchelicerata
Gastropoda
Gymnolaemata
Insecta
Malacostraca
Mammalia
Maxillopoda
Polychaeta
Reptilia
Teleostei
Proportion of sample
eect sizes (%)
0
5
15
25
35 Non-native
Native
Fig. 1 | Distribution of non-native and native species under EWEs from
443 studies. a–e, Point colours indicate different types of EWE in 235 locations
for non-native species (a) and 394 locations for native species (b). The bar chart
shows the number of effect sizes for different EWE groups of non-native (c) and
native species (d), and the proportions of sample effect sizes across taxa (e).
Animal silhouettes in e were obtained from PhyloPic (www.phylopic.org).
Nature Ecology & Evolution
Article https://doi.org/10.1038/s41559-023-02235-1
life history traits, abundance, distribution, community structure and
recovery after EWEs. Our analyses covered five main types of EWEs:
heatwaves, cold spells, storms, floods and droughts. Furthermore,
on the basis of the results of our meta-analyses, we quantified the
spatial overlap between the distributions of EWE-tolerant non-native
species and the EWE hotspots. These overlap analyses should identify
locations where native biodiversity might be adversely affected by the
joint effects of non-native species and EWEs, and where EWEs might
facilitate the future establishment and/or spread of non-native species.
Results
Overall EWE distributions
Across the globe, there were a total of 973 measured effect sizes from
177 peer-reviewed studies across 187 non-native species and 4,330
measured effect sizes from 335 peer-reviewed studies across 1,852
native species (Supplementary Fig. 1). These reported studies on the
effects of EWEs on animals were mainly distributed in North America
and Europe, and sporadically distributed in South America, southern
Africa, East Asia and southeast Australia (Fig. 1a,b). Eighty four per-
cent of studies on non-native species (149/177) and 95% of studies on
native species (317/335) focused on responses to only one type of EWE
(Fig. 1c,d and Supplementary Data 1). Overall, our analyses included
effect sizes of EWEs on non-native animals and native animals span-
ning 6, 7 and 10 classes of terrestrial, freshwater and marine organ-
isms, respectively (Fig. 1e) and three orders of magnitude in body size
(for example, smallest mean body size, Insecta: 0.81 ± 0.22 mm; largest
Mammalia: 1,531.33 ± 211.00 mm).
Species can differ in their exposure to EWEs that may influence
selection for EWE tolerance. We assessed exposure differences by
comparing the average magnitude of the EWEs within the geographic
ranges of each native and non-native species in our database. We
found limited evidence that non-native and native species experi-
ence significantly different magnitudes of EWE exposures (Sup-
plementary Fig. 2). We also found little evidence in our samples that
ecosystem types differed significantly in their magnitudes of EWEs
(Supplementary Fig. 2), except that oceans have more days of heat-
waves and cold spells than terrestrial and freshwater ecosystems
(Supplementary Fig. 2).
Responses of non-native and native animals to EWEs
Overall, we found that non-native species had 24.8% positive, 31.8%
negative and 43.4% neutral responses (confidence intervals (CIs) cross-
ing zero) to EWEs. Native species had 12.7% positive, 20.5% negative
and 66.8% neutral responses to EWEs. Both non-native and native
species exhibited positive, negative and neutral responses to each
type of EWE (Fig. 2). Further multilevel mixed-effects metaregression
models showed that non-native species only responded negatively
to heatwaves in terrestrial ecosystems, whereas native species were
adversely affected by heatwaves, cold spells and droughts (Fig. 3a). In
freshwater ecosystems, non-native species only responded negatively
to storms, but native species responded negatively to heatwaves,
storms, floods and droughts. We even observed positive effects of
heatwaves and cold spells on freshwater non-native species (Fig. 3b).
Marine animal species overall were insensitive to EWEs, regardless
of whether they were non-native or native (Fig. 3c). Egger’s test indi-
cated limited evidence for publication bias associated with the overall
responses of non-native and native animals to EWEs (Supplementary
Table 1). In addition, the omnibus Wald-type test showed a good fit of
the model to the data (Supplementary Table 4). Hence, the greater
tolerance of non-native animals than natives to EWEs does not appear
to be artefactual.
To assess whether the responses of non-native and native species
were dependent on certain taxa or biogeographic realms (Nearctic,
Neotropic, Palaearctic, Indomalayan, Afrotropic and Australasian
in terrestrial and freshwater ecosystems; Agulhas, Cold Temperate
Northeast Pacific, Lusitanian, Northern European Seas, Tropical North-
western Atlantic, Warm Temperate Northeast Pacific and Warm Tem-
perate Northwest Atlantic in marine ecosystems), we reconducted the
analyses above including taxonomic group and realm as independent
variables interacting with non-native/native status (Supplementary
Figs. 3 and 4). Analyses across taxonomic groups (Supplementary
Fig. 3) and biogeographic realms (Supplementary Fig. 4) produced sim-
ilar results as the overall analyses. One insight revealed from this sepa-
rate analysis was that the negative response of terrestrial non-native
animals to heatwaves was only a product of the sensitivity of non-native
insects (mean effect size: −1.188, P < 0.001, Supplementar y Fig. 3).
Among response variables, in terrestrial ecosystems, EWEs only
had negative effects on abundance of non-native species, but adversely
affected body condition, life history traits, abundance, distribution
and post-event recovery of native species (Fig. 4a). In freshwater eco-
systems, EWEs had negative effects on body condition and life history
traits of non-native species, and on community structure of native
species (Fig. 4b). Across terrestrial and freshwater ecosystems, we did
not observe negative effects of EWEs on the distribution, abundance
(except terrestrial insects: mean effect size −0.844, P = 0.004), commu-
nity structure or recovery of non-native animals (Fig. 4a,b), which thus
appear to maintain population stability and community structure dur-
ing and after EWEs. We even observed a positive response of non-native
species’ physiology, behaviour and recover y to EWEs in terrestrial and
freshwater ecosystems (Fig. 4a,b). In marine ecosystems, non-native
species presented overall positive responses to EWEs except for body
condition and life history traits (Fig. 4c).
Overlap between non-native species and EWEs
We further conducted spatial overlap analyses between EWE hotspots
and suitable habitat for non-native animals to identify where native spe-
cies might be particularly vulnerable to the combined effects of EWEs
and non-native species. To do so, we first applied species distribution
modelling to predict those grids with suitable areas for establishment of
non-native animals and overlaid these grids with maps of EWE hotspots
(see more details in Supplementary Methods). We then calculated the
net effect of each non-native animal to EWEs in each overlapped grid
as the proportions of positive plus neutral responses minus negative
response on the basis of the sample effect sizes in the meta-analyses.
The accumulative net effect for each grid was obtained to reflect the
overall tolerance of all potential non-native species to EWEs.
Our analyses show that overlapping areas of highly EWE-tolerant
non-native species and EWEs hotspots are generally distributed in
mid-to-high latitudes, but these patterns did depend on EWE type. For
heatwaves, overlapping areas were mainly distributed in mid-latitude
regions, including west and east-southern United States, southern
Brazil, southern Mediterranean, South Africa, east-southern Asia,
south Australia, New Zealand, west-northern coast and islands in
the Indian Ocean, and west coast and islands in the Pacific Ocean
(Fig. 5a). For cold spells, overlapping areas were mainly distributed in
high-latitude regions, including northern areas of the United States
and Canada, southern Argentina, northern Europe, western coastal
regions of Australia, east coast of the North Atlantic Ocean, south
coast of the Baltic Sea and east coast of the Arctic Ocean (Fig. 5b). For
storms, overlapping areas were sporadically distributed from low to
high latitudes, including Latin America, India, high-latitude European
countries (that is, the United Kingdom and Norway), south-western
and north-eastern Australia, Northern Atlantic Ocean and the west
coast of the Pacific Ocean (Fig. 5c). For floods and droughts, overlap-
ping areas were distributed in mid latitudes of the Mediterranean
region, mid-Asia, southern Australia, and East and Southeast Asia.
In South America, overlap was associated with floods in western
Amazon and southern Brazil but with droughts in northern Amazon
and southern Argentina. In Africa, overlap coincided with floods in
the middle of Africa but with droughts in northern Africa (Fig. 5d,e).
Nature Ecology & Evolution
Article https://doi.org/10.1038/s41559-023-02235-1
Heatwave events
a
b
c
Cold-spell events Storm events Flood events
−40
−20
0
20
40
−100
−300
−200
1 187
−60
−40
−20
0
1 109
−20
−10
0
10
1 80
0
5
10
1 22
−50
−10
30
−120
−80
1 233
−10
−5
0
5
1 437
−20
−10
0
10
1 866
−10
0
10
1 108
−40
−20
0
20
40
−1,700
−1,200
1 121
−4
16
−1,000
−500
1 16
−10
0
10
1 43
Drought events
−20
−10
0
10
20
−60
−40
−200
−100
−600
−400
1 52
2,000
6,000
−20
0
20
−1,000
−500
1 301
−30
−20
−10
0
10
20
30
−1,200
−700
1 33
−20
−10
0
−60
−40
1 286
−10
0
10
−1,800
−800
1 345
−5
0
5
10
1 63
−15
−10
−5
0
5
1 459
−20
−10
0
10
20
30
−430
−230
1 140
−10
0
10
1 55
0
20
40
1 50
−20
0
20
40
1 207
190
390
85
125
−35
−15
5
25
1 76
−20
−10
0
10
20
1 676
Number of sample eect sizes
Number of sample eect sizes
Number of sample eect sizes
0
0.4
0.8
0
0.4
0.8
0
0.4
0.8
0
0.4
0.8
0
0.4
0.8
0
0.4
0.8
0
0.4
0.8
0
0.4
0.8
0
0.4
0.8
0
0.4
0.8
0
0.4
0.8
0
0.4
0.8
0
0.4
0.8
0
0.4
0.8
0
0.4
0.8
0
0.4
0.8
0
0.4
0.8
0
0.4
0.8
0.0
0.4
0.8
0
0.4
0.8
0.0
0.4
0.8
0
0.4
0.8
0
0.4
0.8
0
0.4
0.8
Sample eect sizes
for non-natives
Sample eect sizes
for non-natives
Sample eect sizes
for natives
Sample eect sizes
for natives
Sample eect sizes
for non-natives
Sample eect sizes
for natives
Terrestrial ecosystemFreshwater ecosystemMarine ecosystem
Fig. 2 | Sample effect sizes of non-native and native species in responding to
EWEs. a–c, Sample effect sizes in terrestrial (a), freshwater (b) and marine (c)
ecosystems. The horizontal dashed lines represent the position where the sample
effect size is zero. The heights of barplots are relative proportions of positive
(blue), negative (pink) and neutral (grey) (CIs crossing zero) effect sizes, and were
standardized, ranging from 0 to 1.
Nature Ecology & Evolution
Article https://doi.org/10.1038/s41559-023-02235-1
Non-native × heatwave (24; 140)
Native × heatwave (21; 207)
Non-native × cold-spell (9; 55)
Native × cold-spell (7; 76)
Non-native × storm (7; 50)
Native × storm (24; 676)
−3 −2 −1 0 1 2 3
Hedges’ d (95% confidence interval)
Non-native × heatwave (27; 121)
Native × heatwave (26; 301)
Non-native × cold-spell (4; 16)
Native × cold-spell (6; 33)
Non-native × storm (7; 43)
Native × storm (22; 286)
Non-native × flood (20; 63)
Native × flood (38; 459)
Non-native × drought (14; 52)
Native × drought (41; 345)
Non-native × heatwave (35; 187)
a
b
c
Native × heatwave (28; 233)
Non-native × cold-spell (29; 109)
Native × cold-spell (19; 437)
Non-native × storm (18; 80)
Native × storm (86; 866)
Non-native × drought (7; 22)
Native × drought (34; 108)
Terrestrial ecosystemFreshwater ecosystemMarine ecosystem
*
***
NS
**
***
**
NS
NS
***
NS
***
NS
Fig. 3 | A comparison of non-native (circle) and native species (triangle)
responses to five different types of EWE. a–c, Effect sizes (Hedges’ d) for non-
native and native species’ responses to heatwave, cold-spell, storm, flood and
drought events in terrestrial (a), freshwater (b) and marine (c) environments,
estimated from metafor. Error bars are 95% CIs. A Wald-type test was used to
detect whether a mean effect size estimate was significant when the 95% CI did
not encompass zero. In a, P values of non-native species responses to EWEs
were: heatwave (0.0001), cold spell (0.004), storm (0.298) and drought (0.763);
P values of native species responses to EWEs were: heatwave (<0.0001), cold
spell (<0.0001), storm (0.079) and drought (<0.0001). In b, P values of non-
native species responses to EWEs were: heatwave (0.0002), cold spell (0.002),
storm (0.027), flood (0.842) and drought (0.698); P values of native species
responses to EWEs were: heatwave (0.042), cold spell (0.635), storm (0.023),
flood (0.032) and drought (0.011). In c, P values of non-native species responses
to EWEs were: heatwave (0.592), cold spell (0.079) and storm (0.001); P values
of native species responses to EWEs were: heatwave (0.442), cold spell (0.856)
and storm (0.132). Numbers in parentheses represent the number of studies
and measured effect sizes, respectively. Blue, significantly positive mean effect
sizes; pink, significantly negative mean effect sizes; grey, non-significant mean
effect sizes. The asterisks and ‘NS’ indicate significant and non-significant
differences, respectively, between non-native and native species to the particular
EWE; *P < 0.05, **P < 0.01, ***P < 0.001, performed using an omnibus test
(Supplementary Table 2). Multiple comparisons were not performed in data
analyses. The two-sided P value was used to judge significance.
Nature Ecology & Evolution
Article https://doi.org/10.1038/s41559-023-02235-1
Our results were robust to different criteria used to define overlap hot
-
spots (Supplementary Fig. 5, see details in Supplementary Methods).
Discussion
The present study provided a comparative evaluation of the responses
of non-native and native animals to historical EWEs across taxa and
ecosystems at the global scale. Although there were both ‘winners’
and ‘losers’ across both non-native and native species and ecosys-
tems (Fig. 2), proportionally there were more positive responses of
non-native than native animals to EWEs, making the mean response to
EWEs less negative for non-native than for native species. Our further
meta-analyses that controlled for spatial and taxonomic pseudorep-
lication generally showed that non-native species are less sensitive to
most EWEs than their native counterparts, especially in terrestrial and
freshwater ecosystems. This high tolerance of non-native species to
EWEs compared with native species particularly represented a strong
capacity of non-native species to maintain population stability after
EWEs across ecosystems. We found limited evidence of publication
bias associated with the overall responses of non-native and native
animals to EWEs. However, there was detectable publication bias for
non-native animal responses to terrestrial cold spells, and for native
animal responses to terrestrial heatwaves and cold spells, and fresh-
water floods and droughts (Supplementary Table 1), which is a com-
mon phenomenon in meta-analyses when disciplines are partial to
studying certain effects28.
There are several possible explanations for why non-native animals
tend to be less sensitive to most EWEs than native species within the
same taxonomic class. First, many non-native species exhibit rapid
growth rates, long spawning seasons, short longevities, high competi-
tive abilities, rapid population recolonization and trophic preference
for detritus that could help them take advantage of limited resources
and maintain population sizes during and after EWEs
18,29,30
. Non-native
species also often have higher plasticity than native species18,31,32. For
example, the abundance of the invasive South American tomato pin-
worm was tolerant of acute and chronic temperature stress because
of high thermal plasticity in invaded ranges33. As another example, an
invasive prawn showed higher plasticity of upper thermal limits than
native prawns and was thus less vulnerable to extreme thermal events34.
Finally, the high propagule pressure and meta-population structure
(that is, connectivity) of many non-native species
35
often make their
populations more resilient to the adverse effects of EWEs than native
species
18,36
. Indeed, population-level response variables of non-native
species, such as their abundance, distribution and recovery, were gen-
erally insensitive to EWEs (Fig. 4). Nevertheless, we also observed some
negative responses of terrestrial non-native animals to heatwaves,
particularly for Insecta (Fig. 3 and Supplementary Fig. 3). Additional
analyses further showed that heatwaves could negatively impact insect
body size, development time, growth rate, longevity, reproduction
and survival rate (Supplementary Table 5). These findings support a
previous insect study revealing that life history plasticity was weak in
insect responses to extreme temperatures37.
Freshwater non-native animals responded positively to heat-
waves and cold spells, consistent with some previous studies on fresh-
water crustaceans
38
and mussels
39,40
. Given that 90.8% (109/120) of
non-native freshwater animals in heatwave studies are warm-adapted
and cold-adapted fishes and invertebrates (including Bivalvia, Gas-
tropoda and Malacostraca) introduced through aquaculture (Supple-
mentary Data 1)
41
, one potential explanation for the positive response
of freshwater non-native animals to heatwaves and cold spells is eco-
logical memory theory42. This theory predicts that adaptations to
environmental change are positively related to the past disturbance
events experienced by a species
43,44
. Future studies should test whether
native species exposed to more severe historical EWEs are indeed more
tolerant of EWEs.
Terrestrial ecosystem
aFreshwater ecosystem
bMarine ecosystem
c
Physiology (13; 42)
Physiology (10; 81)
Body condition (9; 34)
Body condition (17; 61)
Behaviour (8; 38)
Behaviour (11; 31)
Life history traits (32; 203)
Life history traits (59; 244)
Abundance (26; 51)
Abundance (74; 932)
Distribution (8; 11)
Distribution (12; 21)
Recovery (5; 32)
Recovery (27; 379)
−3 −2 −1 0 1 2 3
Hedges’ d (95% confidence interval)
Physiology (6; 33)
Physiology (8; 73)
Body condition (10; 24)
Body condition (13; 145)
Behaviour (8; 20)
Behaviour (13; 59)
Life history traits (15; 37)
Life history traits (14; 37)
Abundance (35; 133)
Abundance (72; 708)
Community structure (9; 19)
Community structure (45; 105)
Recovery (6; 20)
Recovery (18; 302)
−3 −2 −1 0 1 2 3
Hedges’ d (95% confidence interval)
Physiology (10; 41)
Physiology (11; 126)
Body condition (6; 25)
Body condition (5; 14)
Behaviour (4; 19)
Behaviour (5; 33)
Life history traits (17; 62)
Life history traits (15; 103)
Abundance (18; 71)
Abundance (31; 481)
Recovery (5; 24)
Recovery (12; 218)
−3 −2 −1 0 1 2 3
Hedges’ d (95% confidence interval)
**
***
NS
***
***
NS
***
NS
*
*
**
NS
*
**
*
***
NS
***
**
***
Non-native Native
Fig. 4 | A comparison of non-native (circle) and native (triangle) species
responses to EWEs for eight response variables. a–c, Effect sizes (Hedges’
d) for the non-native and native species responding to EWEs in terrestrial (a),
freshwater (b) and marine (c) ecosystems, estimated from metafor. Error
bars are 95% CIs. A Wald-type test was used to detect whether a mean effect
size estimate was significant when the 95% CI did not encompass zero. In a,
P values of non-native species response variables to EWEs were: physiology
(<0.0001), body condition (<0.0001), behaviour (<0.0001), life history traits
(<0.0001), abundance (0.0003), distribution (0.597) and recovery (<0.0001);
P values of native species response variables to EWEs were: physiology (0.854),
body condition (<0.0001), behaviour (<0.0001), life history traits (<0.0001),
abundance (<0.0001), distribution (0.003) and recovery (<0.0001). In b, P values
of non-native species response variables to EWEs were: physiology (0.026),
body condition (0.0004), behaviour (<0.0001), life history traits (<0.0001),
abundance (0.630), community structure (0.839) and recovery (0.021); P values
of native species response variables to EWEs were: physiology (<0.0001), body
condition (0.0004), behaviour (0.882), life history traits (0.337), abundance
(0.224), community structure (<0.0001) and recovery (0.463). In c, P values of
non-native species response variables to EWEs were: physiology (0.003), body
condition (0.003), behaviour (0.011), life history traits (0.005), abundance
(0.0005) and recovery (<0.0001); P values of native species response variables
to EWEs were: physiology (0.009), body condition (0.487), behaviour (0.003),
life history traits (0.143), abundance (0.950) and recovery (0.690). Numbers
in parentheses represent the number of studies and measured effect sizes,
respectively. Blue, significantly positive mean effect sizes; pink, significantly
negative mean effect sizes; grey, non-signif icant mean effect sizes. The asterisks
and ‘NS’ indicate significant and non-significant differences, respectively,
between non-native and native species in their responses to EWEs; *P < 0.05,
**P < 0.01, ***P < 0.001, performed using an omnibus test (Supplementary Table 3).
Multiple comparisons were not performed in data analyses. The two-sided
P value was used to judge significance.
Nature Ecology & Evolution
Article https://doi.org/10.1038/s41559-023-02235-1
Interestingly, in contrast to terrestrial and freshwater species,
both non-native and native marine species were insensitive to EWEs.
Importantly, this finding was not a product of the lower magnitude of
EWEs in marine than in terrestrial and freshwater environments, as we
observed few differences in the magnitude of EWEs among ecosystem
types within the geographic ranges of each native and non-native
species in our meta-analysis (Supplementary Fig. 2). The only differ-
ence we did observe suggested that oceans had significantly more
days experiencing heatwaves and cold spells than terrestrial and
freshwater ecosystems (Supplementary Fig. 2). The tolerance of
non-native marine species to EWEs supports previous findings that
marine invaders were generally insensitive to ocean heatwaves
26,27
,
cold spells
45,46
and storms
16,47
. For instance, non-native bryozoans and
crustaceans maintained their community composition and popula-
tion abundance, respectively, in response to marine heatwaves
26,27
.
In contrast, it has been reported extensively that marine heatwaves
are pervasive stressors to native ocean species, especially anemones
and corals (Anthozoa)
7,48
. Indeed, we observed a negative response
of native Anthozoa to marine heatwaves (mean effect size −1.632,
P < 0.001), consistent with past studies
7,48
. In addition, our results
support a recent review on the negative response of benthic inver-
tebrates (that is, Bivalvia) to marine heatwaves (mean effect size
−0.869, P = 0.028), which was possibly due to their limited abilities
to disperse to more suitable habitats7. Regarding the insensitivity of
marine native and non-native species to cold spells, Maxillopoda and
Polychaeta dominated the effect sizes for this test and the literature
reports that these taxa tend to be cold-adapted species and thus
have high performance at low temperatures
45,46
. Finally, we found
that marine non-native and native species were also insensitive to
storm events. Teleostei and Bivalvia dominated the effect sizes for
this test. Our finding is consistent with previous studies that showed
that fishes and Bivalvia were insensitive to storms, possibly because
they are either mobile enough
49
or use ocean currents
50
to seek refuge
during storms, respectively.
Our global analysis of spatial overlap between non-native species
and EWE hotspots identified several vulnerable areas in mid-to-high
latitudes including North America, Europe, Oceania, temperate
Asia inland, East and Southeast Asia, South America and Africa and
marine regions in low-to-mid latitude areas of the Atlantic Ocean,
west-northern coast of the Indian Ocean, south coast of the Baltic
Sea, east coast of the Arctic Ocean and west coast of the Pacific Ocean
where native species might face joint impacts of invasive species and
EWEs. Although the invasion hotspots we identified were only based
on habitat suitability for establishment, we found that these predicted
hotspots have also been reported as areas with frequent non-native spe-
cies introductions35,51, which imply a potentially high overall invasion
dc
b
a
e
Cumulative net eect of
EWEs on non-native species
13.9
0
–3.2
Cumulative net eect of
EWEs on non-native species
5.2
0
–6.9
Cumulative net eect of
EWEs on non-native species
19.3
0
–2.0
Cumulative net eect of
EWEs on non-native species
12.6
0
–2.0
Cumulative net eect of
EWEs on non-native species
16.3
0
Fig. 5 | Overlapping areas between potential distributions of non-native
species that are tolerant of EWEs and EWE hotspots worldwide. a–e, Global
maps showing the accumulative net effects of predicted non-native animals in
areas with the top 20% occurrences of heatwaves (a), cold spells (b), storms (c),
100-yr floods (d) and extreme droughts (SPI ≤ −1.5) (e) at 5-arcmin resolution.
Higher values indicate greater combined risks of invasions and EWEs, and
negative values mean that there are more negative responses of non-native
species to EWEs than positive and neutral responses in those areas. The ‘white’
colour in the maps indicates land areas without overlaps between predicted
distributions of non-native species and EWEs. Taxonomic information for
animals in each corresponding EWE type used in the overlap analyses: for
heatwaves, terrestrial (Amphibia, Aves, Euchelicerata and Insecta), freshwater
(Bivalvia, Branchiopoda, Gastropoda, Malacostraca and Teleostei) and marine
(Ascidiacea, Bivalvia, Gastropoda, Gymnolaemata, Malacostraca, Maxillopoda,
Polychaeta and Teleostei) species were included; for cold spells, terrestrial
(Amphibia, Insecta, Mammalia and Reptilia), freshwater (Gastropoda and
Teleostei) and marine (Bivalvia, Malacostraca, Maxillopoda and Polychaeta)
species were included; for storms, terrestrial (Amphibia, Aves, Insecta,
Mammalia and Reptilia), freshwater (Bivalvia, Clitellata, Gastropoda and
Teleostei) and marine (Malacostraca and Teleostei) species were included;
for floods, terrestrial (Amphibia and Aves) and freshwater (Bivalvia, Insecta,
Malacostraca and Teleostei) species were included; for droughts, terrestrial
(Insecta) and freshwater (Bivalvia, Gastropoda, Malacostraca and Teleostei)
species were included.
Nature Ecology & Evolution
Article https://doi.org/10.1038/s41559-023-02235-1
risk in these regions. Furthermore, our identified EWE epicentres have
also been validated by several predictive models52–55.
Our present study also provided some useful directions for future
studies. First, this study focused on the direct effect of EWEs to native
and non-native species, but EWEs can also have indirect impacts on
biota. For example, prolonged heatwaves can promote lethal hypoxic/
anoxic conditions56. EWEs can cause severe population declines by
damaging habitat-forming species, such as corals, forests, mangroves
and mussel7, or by removing key prey species from food webs57. Further-
more, for marine species, the effects of EWEs might be more severe in
intertidal and shallow subtidal zones than in deeper/offshore marine
waters owing to increased exposure to EWEs. Indeed, we found that
non-native species in deeper water (species recorded maximum depth
>200 m) exhibited positive responses to EWEs (mean effect size 2.262,
P = 0.009). However, we did not detect the negative effect of EWEs on
either non-native or native species in intertidal and shallow subtidal
zones. As we only have 41 samples (3.3% of all marine species samples)
for deeper/offshore species, a larger sample size would be useful to
more rigorously compare the responses of nearshore vs offshore spe-
cies. Finally, the invasion and EWE overlap areas in the present study
were based on non-native animal tolerance to EWEs. We acknowledge
that some EWE-sensitive non-native species might still have the poten-
tial to exert ecological forces on existing ecosystems. However, under
the limited resources that can be used to manage biological invasions
and climate change, we suggest that future studies should prioritize
these less-sensitive animals in locations of overlap so that timely mitiga-
tion strategies can be implemented if native species exhibit declines
associated with biological invasions and intensified EWEs driven by
global change. Our present analyses could facilitate early prevention
schemes against biological invasions and climate change globally and
improve the development of sustainable policies in the era of global
change.
Methods
Literature search
We conducted a systematic literature search on ISI Web of Science (all
databases) and Scopus to collect published papers from the year 1864
to 24 April 2023. The following search terms were entered into the
‘Topic’ field in ISI Web of Science and in ‘All fields’ for Scopus: (‘storm’
OR ‘hurricane’ OR ‘cyclone’ OR ‘typhoon’ OR ‘tornado’ OR ‘wildfire’
OR ‘extreme snow’ OR ‘extreme ice’ OR ‘extreme heat’ OR ‘heat wave’
OR ‘extreme high temperature’ OR ‘extreme cold’ OR ‘cold wave’ OR
‘extreme’ OR ‘extreme drought’ OR ‘extreme rainfall’ OR ‘extreme
precipitation’ OR ‘flood’) AND (‘abundance’ OR ‘behaviour’ OR ‘rich-
ness’ OR ‘reproduction’ OR ‘mating’ OR ‘*diversity’ OR ‘composition’
OR ‘predation’ OR ‘parasit’ OR ‘herbivory’ OR ‘activity’ OR ‘timing’ OR
‘physiology’ OR ‘development’ OR ‘trophic’ OR ‘biomass’ OR ‘survival’
OR ‘growth’) AND (‘species’ OR ‘population’ OR ‘ecological community’
OR ‘ecosystem*’). This resulted in a total of 147,212 unique studies that
were screened for inclusion in our meta-analysis. We also combined
studies from four previous meta-analyses of the animals’ responses
to EWEs8,13,58,59 (Supplementary Fig. 1).
Screening process and data exclusion criteria
First, we screened the title, key words and abstract to determine can-
didate studies that focused on effects of EWEs on non-native or native
species. Review papers and those without quantitative analyses were
excluded. We excluded studies on the basis of the following criteria:
(1) no statistical comparisons of EWE effects to controls, insufficient
information on sample size, mean or variance, or no reporting of
the animal species; (2) only lab work simulating the EWE-associated
changes in salinity but no direct test of the EWE effects on aquatic or
saltmarsh living organisms; (3) intra- or interspecific interactions under
changed microclimatic or soil habitats induced by EWEs; (4) sea-level
or manipulated water-level rise that resulted in further submergence
or inundation; (5) human burning practices in managed grassland or
forests; and (6) comparison of differences in litter or carrion of species
along a gradient of EWEs. We excluded these studies because there
were either no measured response variables of species to EWEs (2 to 5),
or the reported measured variables were only based on the species’
litter or carrion but not the living organisms (6). We then divided the
studies14–16,25–27,38,39,45–47,50,60–490 that passed this screening into those on
non-native and native species.
Data extraction and measurable categories of response
variables
We extracted sample size, mean and variance values in the control (that
is, those samples that did not experience EWEs) and treatment groups
(that is, those samples that experienced EWEs) from each study. Par-
ticularly, for studies based on successive or long-term observational
data, the value at the closest time before EWEs was the control, and the
averaged value around the time of EWE was the treatment491. We only
extracted the most extreme EWE level from manipulative experiments
testing more than two EWE levels. GetData graph Digitizer (v.2.24)
was used to extract values from figures in the studies. We extracted
median and interquartile range in boxplots to quantify the mean and
deviation values when studies reported statistical results of parametric
tests or when the data had been transformed to meet normality in the
literature492. From each study, we also recorded species name, taxon,
ecosystem, type of EWE, coordinates of study/sampling sites and refer-
ence information.
We categorized response variables into eight categories. At the
population level, categories included life history traits (that is, sur-
vival rate, reproduction, longevity, development time, growth rate),
abundance (that is, population density or size, capture or encounter
rate, number count and relative abundance), distribution (that is, occu-
pancy, home range, spatial distribution, foraging zone, territory size),
biodiversity (that is, number of species, richness index, population
genetic structure) and recovery (that is, recovery of population abun-
dance and/or community composition after EWEs). At the individual
level, categories included physiology (that is, gene expression, immune
responses, protein and hormone-related chemical compounds, respi-
ration and critical thermal limits), body condition (that is, body mass
and size) and behaviour (that is, activity, dietary, feeding or foraging
amount, inter-/intraspecific competition, migration or movement and
habitat selection) (Supplementary Table 6). These eight groups were
only included in our main analyses if they contained at least 10 effect
sizes from multiple studies for each class or biogeographic realm
493
.
The response variables were standardized before the analyses to ensure
that all reported responses were in the same direction; that is, larger
was always better and smaller worse for each response variable.
Meta-analysis
We used a standardized mean difference with heteroscedastic popu-
lation variances (SMDH) in the two groups, which is a widely used
and robust method to calculate effect sizes494. Hedges’ d effect sizes
were obtained after correcting for sample bias in SMDH using the
‘escalc’ function in the ‘metafor’ (v.3.0-2) package495. To evaluate
responses of mean effect sizes to moderator variables, we ran multi-
level mixed-effects metaregression models using the ‘rma.mv’ function
in the ‘metafor’ (v.3.0-2) package, which allowed us to account for the
nested structure and non-independence of observations from a single
study. To control for non-independence among variables within a
study, we adopted the method used in ref. 28 and set paper ID (a set of
numbers used to distinguish different studies) as a random intercept.
In addition, we included different taxonomic levels (Class, Order and
Family) as a random effect to control for phylogenetic covariance in
EWE tolerances among species. We used Family in our main analysis
because of its lower Akaike information criterion value than models
using Class or Order as random intercept (Supplementary Table 7).
Nature Ecology & Evolution
Article https://doi.org/10.1038/s41559-023-02235-1
We also included response variable category as a random effect to
control for the pseudoreplication issue of different samples among
categories of variables. We included interaction between non-native/
native status and the occurrence of a given EWE as a fixed effect to test
for differences in responses of native and non-native species to EWEs.
We considered the mean effect size estimate to be significant when the
95% confidence interval (CI) did not encompass zero. The approximate
residual heterogeneity of models was assessed using Cochran’s Q (Q
E
),
and the omnibus Wald-type test (Q
M
) was used to assess model perfor-
mance in explaining the heterogeneity attributed to a given moderator
variable
496
. We ran Egger’s regression test for publication bias
497
and
an omnibus test to compare the responses of non-native and native
species to each EWE498.
Sensitivity analyses
Previous studies suggested that sample outliers might influence the
results of meta-analyses
499
. To test the robustness of our results to
sample outliers, we removed those outliers and re-ran meta-analytic
models to check the outcome of mean effect sizes. Outliers were clas-
sified as any standardized residual for a study whose absolute value
was >3 (ref. 500) and were determined using the ‘metaoutliers’ func-
tion in the ‘altmeta’ (v.4.1) package501. Neither the direction nor the
significance of mean effect sizes changed when outliers were removed
(see details in Supplementary Tables 8 and 9) except for the following:
a significant negative response of native species to terrestrial storms
became non-significant (Supplementary Table 8), and two significant
positive responses (behaviour and life history traits) and one significant
negative response (abundance) of native freshwater species to EWEs
became non-significant (Supplementary Table 9).
To test whether the overall response to different EWEs was robust
across taxa and biogeographic realms (Nearctic, Neotropic, Palaearctic,
Afrotropic, Australasian) for terrestrial and freshwater species, and
across provinces (Agulhas, Cold Temperate Northeast Pacific, Lusita-
nian, Northern European Seas, Tropical Northwestern Atlantic, Warm
Temperate Northeast Pacific and Warm Temperate Northwest Atlantic)
for marine species, we conducted two additional sets of sensitivity anal-
yses specifically focusing only on those taxonomic classes and realms
reporting both non-native and native animals (Supplementary Data 1).
Identifying areas of overlap between hotspots of invasions
and EWEs
We finally explored overlap areas suitable for establishment of
EWE-tolerant non-native animals and frequent EWEs. To achieve this,
we first collected occurrence data for each non-native species and pre-
dicted their habitat suitability for establishment worldwide. We then
overlapped those grids with suitable habitats for non-native species
establishment with EWE hotspots (10%, 20% and 30% grids at a spatial
resolution of 5 arcmin with the highest frequency of EWEs in history).
For these overlapped grids, we calculated the net effect of positive,
negative and neutral responses for each non-native animal to focal
EWEs (that is, net effect = proportion of positive response + proportion
of neutral response − proportion of negative response) on the basis of
the sample effect sizes in the meta-analyses above. The accumulative
net effect of EWEs on non-native species in each grid was obtained, with
higher values indicating greater potential combined risks of invasions
and EWEs. Details for predicting non-native species habitat suitability
and the distributions of historical EWEs are summarized below.
Habitat suitability for non-native animal establishment. We first
generated a non-native species list from the literature used in the
meta-analysis (see non-native species list in Supplementary Data 2).
Species occurrence records were then gathered from the online data-
base of the Global Biodiversity Information Facility502, and we added
additional records from the literature (see distribution data source in
Supplementary Data 2). We excluded those records without precise
coordinates and withunclear establishment status. Next, we applied
the ‘scrubr’ R package to remove duplicate coordinates
503
. For further
spatial modelling analysis, occurrence data were thinned to 5-arcmin
resolution (~9.2 km at the equator) using the ‘spThin’ package
504
to
reduce sampling bias from disproportional survey efforts among taxa
or regions505. We identified the native and non-native ranges for each
of species on the basis of the following databases: Global Invasive Spe-
cies Database (GISD, http://www.iucngisd.org/gisd/), Invasive Species
Compendium on CABI (https://www.cabi.org/ISC/), World Register of
Introduced Marine Species (WRiMS, https://www.marinespecies.org/
introduced/), SeaLifeBase (https://www.sealifebase.se/search.php),
IUCN (https://www.iucnredlist.org/), and extra information from Wiki-
pedia, Google Scholar and published literature (Supplementary Data
3). We further quantified the potential distribution of the non-native
species using ecological niche modelling (ENM), which is a widely
used method to provide robust predictions of potential distributions
of species506. ENMs for potential species distributions under current
climatic conditions were constructed using MaxEnt
507
on the basis of a
standard protocol following a previous study
508
. Details on modelling
steps, predictor selection, method to account for sample bias and
assessments of model performance are provided below.
ENM
To quantify potential distributions of non-native species, the Max
-
Ent algorithm was used to fit the models. The MaxEnt algorithm has
generally shown high predictive performance and has been exten-
sively applied in conservation, invasion and biogeography studies,
and recent research shows that tuned MaxEnt models can perform
comparably to ensemble models
509
. Training data contained both of a
species’ native and non-native ranges to eliminate biases in evaluating
species’ realized niches as some non-native species can shift their real-
ized climatic niches in invaded areas510,511. A minimum convex polygon
with two-degree buffers was chosen to define the background extent
where distribution occurrences of non-native species are located512.
A target-group method was used to account for the potential effect of
sampling bias in species occurrence data on results513.
For land species, both climate and habitat factors including vegeta-
tion and water availability were used to predict their potential distribu-
tions, considering the important role of habitat variables in reflecting
species’ requirements for food and reproduction
514
. Details on variable
selection differed across taxa on the basis of their main physiological
requirements following previous studies (Supplementary Table 10).
For marine non-native species, the Bio-ORACLE database (v.2.2,
https://www.bio-oracle.org/downloads-to-email.php) was used to col-
lect current environmental data for both surface and benthic species
515
.
Sea water depth information was accessed from Global Marine Envi-
ronment Datasets (https://gmed.auckland.ac.nz/)516. The Bio-ORACLE
database supplied averaged outputs of predic tors on the basis of three
atmosphere–ocean general circulation models (AOGCMs) including
CCSM4, HadGEM2-ES and MIROC5 at 5-arcmin (~9.2 km at the equator)
resolution that was then used for further analyses
515
. As climate warm-
ing effects on marine ecosystems depend on ocean depths
517
, potential
distributions of benthic and shallow-water species were predicted
separately. Water depth, salinity and seasonal water temperature were
necessarily used to predict distributions of benthic invertebrates
and fishes518,519. Specifically, a total of six candidate predictors were
used to predict benthic species distributions, including water depth
(m), annual mean current velocity (m−1 yr−1), annual mean sea benthic
salinity (PSS yr−1), annual range of sea benthic salinity (PSS yr−1), annual
mean sea benthic temperature (°C yr−1) and annual range of sea ben-
thic temperature (°C yr
−1
). For surface water fishes, water depth, sea
surface temperature and salinity, and sea ice were used to predict
spatial distributions
520–522
. Potential distributions of marine surface
fishes were predicted by seven candidate predictors, including water
depth (m), annual mean current velocity (m
−1
yr
−1
), annual mean ice
Nature Ecology & Evolution
Article https://doi.org/10.1038/s41559-023-02235-1
thickness (m yr−1), annual sea surface salinity (PSS yr−1), annual range
of sea surface salinity (PSS yr
−1
), annual mean sea surface temperature
(°C yr−1) and annual range of sea surface temperature (°C yr−1). These
predictor variables did not show high correlations (Pearson’s correla-
tion coefficient |r| < 0.70)523.
Multiple predictor combinations from simple to full models were
fitted using the MaxEnt algorithm. Cross-validations for the fitted
models were performed on the basis of a spatial partitioning strat-
egy using the ‘block’ method524. Three representative measures (area
under the receiver operating characteristic curve (AUC), true skill
statistic (TSS) and Boyce index) were used to evaluate the performance
of fitted models
525–527
. First, AUC is a threshold-independent meas-
ure; an AUC value between 0.7 and 0.9 indicates good model perfor-
mance and a value >0.9 indicates excellent performance
528
. Second,
TSS is a threshold-dependent measure with summing of sensitivity
and specificity minus one529; a TSS value from 0.4 to 0.8 indicates
good model performance and a value >0.8 indicates excellent perfor-
mance. Third, the Boyce index is useful for evaluating fitted models
with presence-only data to overcome potential overfitting issues. This
index ranges from −1 to 1 and a higher value indicates better model
performance527. All ENMs analyses were conducted using the ‘ENMeval’
package in R530. Overall, the ENMs used in our present study had good
performance in predicting potential distributions of the non-native
species (with minimum values of AUC > 0.75; TSS > 0.40; more than 83%
of species with Boyce > 0.70; see details in Supplementary Table 11).
EWEs distribution. Distributions of different types of EWEs were col-
lected from open data sources and publications.
Heatwave and cold-spell events on land
HadEX3 is a newly updated product generated through the coordina-
tion of the joint World Meteorological Organization (WMO) Expert
Team on Climate Change Detection and Indices (ETCCDI). HadEX3
(https://www.metoffice.gov.uk/hadobs/hadex3/) supplies a set of 17
monthly metrics of extreme weather events gridded (1.875° × 1.25°
longitude–latitude) for global land surfaces from 1901 to 2018 (ref. 531).
Four of those metrics were selected owing to their long-term record-
ings by stations and representation of the frequency and intensity of
thermal extremes531. Proportions of extreme warm days and duration
of warm days are commonly used to evaluate global-scale heatwave
conditions532,533. TX90p (percentage of time when daily maximum
temperature is >90th percentile) and WSDI (annual count when at least
6 consecutive days of maximum temperature is >90th percentile) were
used to quantify heatwave events in terrestrial and freshwater systems.
TN10p (percentage of time when daily minimum temperature is <10th
percentile) and CSDI (annual count when at least 6 consecutive days
of minimum temperature is <10th percentile) were used to quantify
cold-spell events.
Marine heatwave and cold-spell events
Historical marine heatwave events from 1980 to 2019 were recently
reported
534
as averaged days of heatwaves per decade at 1° × 1° resolu-
tion at the global scale. Reference 535 provides mean annual frequency of
marine cold-spell (days) from 1982 to 2020 at 0.2498264° × 0.2496528°
resolution globally.
Storm events
The Global Risk Data Platform supplies historical recorded storm
events and tracks from satellite remote-sensing from 1970 to 2015
(https://preview.grid.unep.ch/index.php?preview=data&events=
cyclones&evcat=1&lang=eng). Available polygon layers in this plat-
form contain information on country names, the year of storm events,
starting and ending dates and the category per event. In addition, the
coordinates of storm tracks per event are provided. Therefore, duration
and category data of storm events at 0.5° × 0.5° resolution were used.
Extreme flood events
Aqueduct Flood Hazard Maps provide global historical flood haz-
ard grid datasets at 5’ × 5’ resolution (https://www.wri.org/data/
aqueduct-floods-hazard-maps). The historical dataset supplies times
of recorded coastal and riverine floods with returning periods of 2, 5,
10, 25, 50, 100, 250 and 1,000 yr (ref. 536). Sums of times of coastal
and riverine flooding events with 100-yr returning periods were used
in the data analysis.
Extreme drought events
The global monthly average standardized precipitation index (SPI)
dataset is available from the National Center for Atmospheric Research
(NCAR)/University Corporation for Atmosphere Research (UCAR)
platform (https://www.ucar.edu/) at 1° × 1° resolution for the years
1942–2012. Monthly SPI is a widely used index to describe meteoro-
logical drought, and monthly SPI ≤ −1.5 was used to define an extreme
drought event537. The SPI data for a 12-month timescale were selected
to assess drought events. Fur thermore, to better quantify multiple-year
averages of drought events, we calculated the frequency of extreme
dryness per year (that is, (1/12) × number of month(s) with SPI ≤ −1.5).
The annual mean frequency of extreme dryness from January 1950 to
December 2012 was used in the data analysis. We standardized all the
EWEs layers with different to the same 5-arcmin resolution using the
‘resample’ function in the ‘raster’ (v.3.5-21) package538. Animal silhou-
ettes in the PhyloPic database (www.phylopic.org) were accessed and
visualized using the ‘add_phylopic_base’ function in the ‘rphylopic’
(v.1.1.1) package539. All data540 analyses were conducted in R (4.2.1)541.
Reporting summary
Further information on research design is available in the Nature Port-
folio Reporting Summary linked to this article.
Data availability
All data have been deposited in a public structured data depository
(https://doi.org/10.6084/m9.figshare.23587695). Source data are pro-
vided with this paper.
Code availability
The R code for running the main analyses is available at https://doi.
org/10.6084/m9.figshare.23587695.
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Acknowledgements
X.L. was supported by the Third Xinjiang Scientiic Expedition Program
(2022xjkk0800 and 2021xjkk0600), the National Science Foundation
of China (32171657), grants from the Youth Innovation Promotion
Association of the Chinese Academy of Sciences (Y201920) and grants
from the High Quality Economic and Social Development in Southern
Xinjiang (NFS2101). J.R.R. was supported by funding provided by the
US National Science Foundation (EEID-1518681, DEB-2017785) and the
US Department of Agriculture (NRI 2009-35102-0543).
Author contributions
X.L. conceived the project. X.L., S.G. and J.R.R. designed the study. X.L.
supervised the project. S.G., T.Q. and X.L. collected the data. S.G., T.Q.
and X.L. performed data analyses. S.G. and X.L. wrote the manuscript
draft and all authors contributed to manuscript revisions.
Competing interests
The authors declare no competing interests.
Additional information
Supplementary information The online version
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Correspondence and requests for materials should be addressed to
Xuan Liu.
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