Waders in winter: long-term changes of migratory bird assemblages facing climate change.
ABSTRACT Effects of climate change on species occupying distinct areas during their life cycle are still unclear. Moreover, although effects of climate change have widely been studied at the species level, less is known about community responses. Here, we test whether and how the composition of wader (Charadrii) assemblages, breeding in high latitude and wintering from Europe to Africa, is affected by climate change over 33 years. We calculated the temporal trend in the community temperature index (CTI), which measures the balance between cold and hot dwellers present in species assemblages. We found a steep increase in the CTI, which reflects a profound change in assemblage composition in response to recent climate change. This study provides, to our knowledge, the first evidence of a strong community response of migratory species to climate change in their wintering areas.
Article: Large-scale changes in community composition: determining land use and climate change signals.[show abstract] [hide abstract]
ABSTRACT: Human land use and climate change are regarded as the main driving forces of present-day and future species extinction. They may potentially lead to a profound reorganisation of the composition and structure of natural communities throughout the world. However, studies that explicitly investigate both forms of impact--land use and climate change--are uncommon. Here, we quantify community change of Dutch breeding bird communities over the past 25 years using time lag analysis. We evaluate the chronological sequence of the community temperature index (CTI) which reflects community response to temperature increase (increasing CTI indicates an increase in relative abundance of more southerly species), and the temporal trend of the community specialisation index (CSI) which reflects community response to land use change (declining CSI indicates an increase of generalist species). We show that the breeding bird fauna underwent distinct directional change accompanied by significant changes both in CTI and CSI which suggests a causal connection between climate and land use change and bird community change. The assemblages of particular breeding habitats neither changed at the same speed and nor were they equally affected by climate versus land use changes. In the rapidly changing farmland community, CTI and CSI both declined slightly. In contrast, CTI increased in the more slowly changing forest and heath communities, while CSI remained stable. Coastal assemblages experienced both an increase in CTI and a decline in CSI. Wetland birds experienced the fastest community change of all breeding habitat assemblages but neither CTI nor CSI showed a significant trend. Overall, our results suggest that the interaction between climate and land use changes differs between habitats, and that comparing trends in CSI and CTI may be useful in tracking the impact of each determinant.PLoS ONE 01/2012; 7(4):e35272. · 4.09 Impact Factor
published online 23 March 2011
Laurent Godet, Mikaël Jaffré and Vincent Devictor
assemblages facing climate change
Waders in winter: long-term changes of migratory bird
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Waders in winter:
of migratory bird
Laurent Godet1,2,*, Mikae ¨l Jaffre ´3
and Vincent Devictor4
1CNRS, Laboratoire Ge ´olittomer–UMR 6554 LETG,
Nantes University, Nantes, France
2CNRS, Marine Station of Dinard–UMR 7208 BOREA,
Muse ´um National d’Histoire Naturelle, Paris, France
3Universite ´ Lille 1, UMR CNRS 8187 LOG, Wimereux, France
4CNRS, UMR 5554 ISEM, Montpellier University, Montpellier, France
*Author for correspondence (firstname.lastname@example.org).
Effects of climate change on species occupying
distinct areas during their life cycle are still
unclear. Moreover, although effects of climate
change have widely been studied at the species
level, less is known about community responses.
Here, we test whether and how the composition of
wader (Charadrii) assemblages, breeding in high
latitude and wintering from Europe to Africa,
is affected by climate change over 33 years. We cal-
culated the temporal trend in the community
temperature index (CTI), which measures the bal-
ance between cold and hot dwellers present in
species assemblages. We found a steep increase
in the CTI, which reflects a profound change in
assemblage composition in response to recent
climate change. This study provides, to our knowl-
edge, the first evidence of a strong community
response of migratory species to climate change
in their wintering areas.
Keywords: climate change; waders; assemblages;
community temperature index; estuaries
Climate warming is unevenly distributed around the
globe , being particularly severe in high latitudes
. Resident species living in high latitudes are there-
fore expected to suffer from a range contraction of
their distribution . By contrast, migratory species
that breed only in high latitudes but winter in lower
latitudes should have different responses to climate
change, as they experience climate change unequally
during their life cycle . Yet, beyond changes of
species ranges, the response of species breeding in
high latitudes but wintering in temperate areas is still
Effect of climate change on migratory species has
mainly been studied using species-by-species ap-
proaches (e.g. [5–7]). However, species responses do
not necessarily correspond to the responses of species
assemblages taken as a whole. In this respect,
monitoring changes in the composition of wader
assemblages provide an interesting means to investi-
gate climate change impacts on migratory species
assemblages. Indeed, in their European wintering
grounds, local wader assemblages are composed of
species breeding in very distinct areas, mainly (sub)-
arctic regions . Some of these long-distance
migrants tend to winter further north in Europe, as a
response to climate change [5,6]. However, the conse-
quences of these changes at the community level
Here, we used wader counts over 33 years in 69
French estuaries in order to test the long-term changes
in the composition of wader assemblages in response to
2. MATERIAL AND METHODS
(a) Bird data
We used the French data from the wintering wader monitoring pro-
gramme conducted from 1977 to 2009 in the context of the
European wetland bird survey (EWBS; electronic supplementary
material, S1). Here, we considered the 23 estuarine wader species
wintering in France. We further selected all French sites monitored
in the EWBS, excluding Mediterranean sites, gathering populations
with different migratory routes (i.e. a total of 69 sites).
(b) Community temperature index
For each species, we calculated a species temperature index (STI)
(table 1) that corresponds to the mean temperature within the winter-
temperature averaged over the wintering range of this species is 58C).
STI was shown to be a straightforward niche metric for predicting
long-term [9,10] and short-term  responses of bird species to cli-
mate change. STIs were obtained on a geographical information
system from the overlapping of the wintering range of each species
at the same time, obtained from Delanyet al.  and the spatial distri-
bution of the mean temperature in winter (averaged from 1950 to
2000 from WorldClim database: http://www.worldclim.org). For
each species, we considered only population(s) wintering in the
monitored sites (table 1).
The community temperature index (CTI) of a given assem-
blage corresponds to the STIs of each species within this
assemblage weighted by the respective species abundances (e.g. in
an assemblage ‘A’ composed of one individual of the species ‘x’
with an STI of 108C and two individuals of the species ‘y’ with an
STI of 208C, the CTI will be (1 ? 10 þ 2 ? 20)/(1 þ 2) ¼
16.678C). In a given place, following temperature increase, we thus
expect an increase in CTI resulting from the faster relative increase
in abundances of individuals belonging to species with high STIs.
As waders are gregarious species and can change from very low to
very high numbers locally (table 1), CTI was calculated from the log
(x þ 1)-transformed abundances to account for high variations in
species abundances. Taking the same example as above, the CTI
of the assemblage ‘A’ will be:
logð1 þ 1Þ?10 þ logð2 þ 1Þ?20
logð1 þ 1Þ þ logð2 þ 2Þ
We also calculated CTI from the presence/absence transformed
abundances (by replacing by one any species abundance exceeding
one individual) to check whether the potential observed change in
CTI resulted only from variation in species abundances or also
from local colonizations and extinctions of individual species.
We used the CRUTEM3 database (http://www.hadobs.org) to
assess change in winter temperature from 1977 to 2009 (averaged
from October to December) within the whole wintering area of all
the studied populations. These data give the temperature anomalies
using the period 1961–1990 as a reference .
(d) Data analysis
CTI was calculated for each site each year. Then, the temporal (year-
to-year) trend in CTI was calculated with a linear model, using data
from all monitored sites between 1977 and 2009. In this model, site
was considered as a fixed factor and year as a continuous variable.
This model thus provides the average trend in CTI, accounting for
variation among sites in CTI.
Electronic supplementary material is available at http://dx.doi.org/
10.1098/rsbl.2011.0152 or via http://rsbl.royalsocietypublishing.org.
Received 8 February 2011
Accepted 3 March 2011
This journal is q 2011 The Royal Society
on March 24, 2011rsbl.royalsocietypublishing.orgDownloaded from
The trend in CTI could also result from variation in the presence
or abundance of only a few species rather than mirroring a real
change in the composition of species assemblages. We therefore
tested the robustness of the temporal trend in CTI to changes in
the presence or absence of particular species. To do so, we randomly
and gradually removed species from the total pool of 23 species, and
calculated the trend in CTI for the remaining species (bootstrap
algorithm). This was done for 1000 random removals of 1–17
species (i.e. 75% of the 23 species). If the overall trend in CTI was
dependent on the dynamics of only few species, we expected to
find a poor robustness of the simulated trends to the change in the
The latitudinal trend in CTI (in kilometres) was calculated with
a linear model using all sites, and the mean CTI of the period 1977–
2009 for each site. In this model, site was considered as a random
factor and latitude as a continuous variable. Beyond the temporal
(year-to-year) and the latitudinal (in kilometres) trends in CTI, a
latitudinal shift of the CTI over the period (in km yr21) can be cal-
culated using the combination of both the temporal and spatial trend
in CTI . Indeed, using the spatial trend (8C km21) and the tem-
poral trend in CTI (8C yr21), and providing that these trends are
linear, one can estimate the spatial shift in assemblage composition
from the ratio of these two estimates (8C yr21/8C km21¼ km yr21).
The temporal trend in temperature was estimated with a linear
model, using all temperature stations provided by the CRUTEM3
database that overlap the wintering range of at least one of the
studied wader species. In this model, temperature station was
considered as a fixed factor and year as a continuous variable.
During the period 1977–2009, the CTI increased
steeply (þ0.02888C yr21+0.0022 s.e., F1,31¼ 174.4,
p , 0.00001, r2¼ 0.84; figure 1). A similar trend
wasfound with the
(þ0.05098C yr21+0.0048 s.e.,
0.00001, r2¼ 0.78; electronic supplementary material,
figure S1). The trend in CTI was also highly robust to
the presence or absence of particular species: it
remained stable even when up to 75 per cent of
the species were randomly excluded from the assem-
observed after the removal of one-third of the species
species were biased towards highly positive resulting
trends in CTI (electronic supplementary material,
The increase in the temperature anomaly over the
same period and within the whole wintering area of
the waders was highly significant (F1,31¼ 68.43, p ,
0.00001, r2¼ 0.68) and increased by 0.03578C
(+0.0043 s.e.) per year (figure 1).
inCTI could onlybe
Table 1. STIs, populations and subspecies of the wader species monitored in France in the context of the European Wetland
Bird Survey. (Populations and subspecies wintering ranges were selected from Delany et al. . N, Northern; S, Southern;
W, Western; E, Eastern; C, Central.)
speciessubspecies or populations considered in this study
per site and per years.e.
nominal subspecies ostralegus
populations breeding from SW Europe and NWAfrica
populations breeding in W Europe
east Atlantic populations
nominal subspecies hiaticula
populations breeding from Wand C Europe to
NWAfrica of the subspecies curonicus
populations breeding from E Atlantic and
nominal subspecies lapponica
subspecies islandicus and populations breeding from
NE Europe of the nominal subspecies phaeopus
nominal subspecies arquata
European breeding populations
subspecies britannica and robusta
populations breedings in NW Europe 21.7902.5180.038
European breeding populations
populations breeding in NWand C Europe
populations breeding in NE Canada and Greenland
populations breeding from Ellesmere to Taymyr and
migrating/wintering in E Atlantic
populations breeding in Europe
populations breeding in N Europe and W Siberia, and
populations breeding in NE Canada an N Greenland
nominal subspecies alpina; Baltic, Britain and Ireland
breeding populations of the subspecies schinzii
western populations breeding from Taymyr to W Europe,
and wintering from Europe to WAfrica
2 L. Godet et al. Waders assemblages and climate warming
on March 24, 2011rsbl.royalsocietypublishing.org Downloaded from
CTI also significantly decreased in space from
southern to northern France (20.00148C km21+
4.9 ? 1024s.e.,
1977 to 2009, the temporal increase in CTI thus
corresponded to a 20.15 km (+7.14 s.e.) northwards
shift per year. Using presence–absence data, the
spatial trend was comparable (20.00208C+0.0008
s.e. km21, F1,67¼ 6.69, p ¼ 0.0119) and the corres-
ponding northwards shift in CTI was similar (27.45
p ¼ 0.0052). From
We found a consistent and important change in the
composition of wader assemblages over 33 years
towards species more dependent on high temperatures.
This temporal trend was robust to the removal of 75
per cent of the species from the initial pool and similar
when estimated with presence–absence data. These
results demonstrate an important reassembly of the
wader assemblages at large spatio-temporal scale on
their wintering grounds.
Focusing on wintering wader assemblages provides
new insights on climate change impact on bird as-
semblages. Not only do changes in the temperature
in the breeding grounds affect the composition of
bird assemblages , but the migratory behaviours of
long-distance migratory species may also be affected
by changes in temperatures in their wintering grounds.
Such changes in assemblage composition may result
from different, albeit non-exclusive, mechanisms.
First, MacLean et al.  suggested that, following
climate warming, young waders (that have not yet
become established in favoured wintering sites) could
tend to reduce their migration routes and to winter
further north in contrast to adults that are site faithful
to their traditional wintering grounds . We can
expect that these young birds predominantly belong
to species with high STIs that do not have to winter
in the southernmost sites anymore to thrive during
very cold winters. Second, we can expect that hot
dwellers (with high STIs), which are potentially more
sensitive to cold temperatures, benefit more than cold
dwellers from midler winters, by reducing their
winter mortality to a greater extent than cold dwellers.
Third, some cold dwellers (all generations pooled),
which used to winter in northern France in the past,
may have shifted northwards recently, and now tend
to winter even further north (e.g. in the past, many
oystercatchers wintered in France when tidal flats of
the Wadden Sea froze over ). These three mechan-
isms could contribute to a faster relative increase in hot
dweller abundance and presence in local wader assem-
blages, and therefore to an increase in CTI. Finally, the
increase in temperature may have both direct impacts
on waders (e.g. on their physiology) and indirect
impacts such as changes in the abundance, distribution
or accessibility of macrobenthic preys.
Maclean et al.  found a northward shift for seven
wader species in Northwest Europe that was five times
slower than our result. The northwards shift we found
of ca 20 km yr21however, is only based on a latitudinal
gradient between the southernmost and northernmost
monitored French estuaries that represent a tiny part
of the wader wintering range, which stretches from
the Baltic Sea to tropical Africa.
This study further suggests that CTI is a suitable in-
dicator for assessing the response of local animal
assemblages to climate change. Moreover, measuring
the change in assemblage composition can reveal
trends that are masked at the species level. For instance,
almost all wader species are increasing in France (elec-
tronic supplementary material, figure S3) and seem to
be progressively shifting northwards in Europe [5,6].
However, our results suggest that different species have
different dynamics within communities, which results
in important changes in local assemblage compositions.
In the future, because waders are among the main
predators of the benthic compartment, this change in
wader assemblages may have serious consequences for
estuarine functions in Western Europe.
We thank volunteers involved in wader counts in France, four
anonymous referees who improved this manuscript and Paul
Norwood who improved the English of this text. Special
thanks to Patrick Le Mao and Christophe Luczak who
helped us in our data query. V.D. received financial support
from the Fondation pour la Recherche sur la Biodiversite ´
(projects FABIO and COPHY).
1 Loarie, S. R., Duffy, P. B., Hamilton, H., Asner, G. P.,
Field, C. B. & Ackerly, D. D. 2009 The velocity of
climate change. Nature 462, 1052–1055. (doi:10.1038/
2 Callaghan, T. V. et al. 2005 Arctic tundra and polar
ecosystems. In Arctic climate impact assessment, ACIA
1977 1981 1985 1989 1993 1997 2001 2005 2009
temperature anomaly (°C)
community temperature index (°C)
Figure 1. (a) Temporal trend of the CTI from 1977 to 2009
(first year set to zero). (b) Temporal trend of the average
October–January temperature anomaly in the whole winter-
ing area of the waders from 1977 to 2009. Dashed lines
represent standard errors around the means.
Waders assemblages and climate warming
L. Godet et al.
on March 24, 2011 rsbl.royalsocietypublishing.orgDownloaded from
(eds C. Symon, L. Arris & B. Heal), pp. 243–351.
Cambridge, UK: Cambridge University Press.
3 Hickling, R., Roy, D. B., Hill, J. K., Fox, R. & Thomas,
C. D. 2006 The distributions of a wide range of taxonomic
groups are expanding polewards. Glob. Change Biol. 12,
4 Lemoine, N., Schaefer, H.-C. & Bo ¨hning-Gaese, K.
2007 Species richness of migratory birds is influenced
by global climate change. Glob. Ecol. Biogeogr. 16,
5 Austin, G. E. & Rehfish, M. M. 2005 Shifting distri-
butions of migratory fauna in relation to climatic
change. Glob. Change Biol. 11, 31–38. (doi:10.1111/j.
6 Maclean, I. M. D. et al. 2008 Climate change causes
rapid changes in the distribution and site abundance of
birds in winter. Glob. Change Biol. 14, 2489–2500.
7 Rehfish, M. M., Austin, G. E., Freeman, S. N.,
Armitage, M. J. S. & Burton, N. H. K. 2004 The possible
impact of climate change on the future distributions and
numbers of waders on Britain’s non-estuarine coast. Ibis
146, 70–81. (doi:10.1111/j.1474-919X.2004.00330.x)
8 Delany, S., Scott, D., Dodman, T. & Stroud, D. 2009 An
atlas of wader populations in Africa and Western Europe.
Wageningen, The Netherlands: Wetlands International.
9 Devictor, V., Julliard, R., Couvet, D. & Jiguet, F. 2008
Birds are tracking climate warming, but not fast
enough. Proc. R. Soc. B 275, 2743–2748. (doi:10.
10 Jiguet, F., Gadot, A. S., Julliard, R., Newson, S. E. &
Couvet, D. 2007 Climate envelope, life history traits
and the resilience of birds facing global change. Glob.
11 Jiguet, F., Julliard, R., Thomas, C. D., Dehorter, O.,
Newson, S. E. & Couvet, D. 2006 Thermal range pre-
dicts bird resilience to extreme temperatures. Ecol. Lett.
9, 1321–1330. (doi:10.1111/j.1461-0248.2006.00986.x)
12 Brohan, P., Kennedy, J. J., Harris, I., Tett, S. F. B. &
Jones, P. D. 2006 Uncertainty estimates in regional and
global observed temperature changes: a new data set
from 1850. J. Geophys. Res. 111, D12 106. (doi:10.
13 Townshend, D. J. 1985 Decisions for a lifetime: establish-
ment of spatial defence and movement patterns by
juvenile grey plovers (Pluvialis squatarola). J. Anim. Ecol.
54, 267–274. (doi:10.2307/4637)
der Meer, J. & Smit, C. J. 1996 Oystercatcher Haematopus
ostralegus winter mortality in the Netherlands: the effect of
severe weather and food supply. Ardea 84A, 469–492.
4L. Godet et al.Waders assemblages and climate warming
on March 24, 2011 rsbl.royalsocietypublishing.orgDownloaded from