Climate and Dispersal: Black-Winged Stilts Disperse Further in Dry Springs

Abstract

Climate affects the abundance and distribution of many species of wildlife. Nevertheless, the potential effects of climate on dispersive behaviour remain unstudied. Here, I combine data from (i) a long-term Black-winged Stilt (Himantopus himantopus) monitoring program, (ii) a capture-recapture marking program in Doñana, and (iii) reports from the Rare Birds Committee in the United Kingdom to analyse at different geographical scales the relationship between climate, survival, philopatry, and dispersive behaviour. Black-winged Stilt populations varied in size in consonance with changes in both the North Atlantic Oscillation (NAO) and local rainfall during the breeding season. Changes in population size are related to changes in philopatry and increases in dispersal beyond the traditional range of the species. The results indicate that climatic conditions influence the dispersive behaviour of individual birds, explaining rapid changes in the local population of this species breeding in unstable Mediterranean wetlands.

Full text

Climate and Dispersal: Black-Winged Stilts Disperse
Further in Dry Springs
Jordi Figuerola*
Department of Wetland Ecology, Estacio
´
n Biolo
´
gica de Don
˜
ana, Consejo Superior de Investigaciones Cientı
´
ficas (CSIC), Seville, Spain
Climate affects the abundance and distribution of many species of wildlife. Nevertheless, the potential effects of climate on
dispersive behaviour remain unstudied. Here, I combine data from (i) a long-term Black-winged Stilt (Himantopus himantopus)
monitoring program, (ii) a capture-recapture marking program in Don
˜
ana, and (iii) reports from the Rare Birds Committee in
the United Kingdom to analyse at different geographical scales the relationship between climate, survival, philopatry, and
dispersive behaviour. Black-winged Stilt populations varied in size in consonance with changes in both the North Atlantic
Oscillation (NAO) and local rainfall during the breeding season. Changes in population size are related to changes in philopatry
and increases in dispersal beyond the traditional range of the species. The results indicate that climatic conditions influence
the dispersive behaviour of individual birds, explaining rapid changes in the local population of this species breeding in
unstable Mediterranean wetlands.
Citation: Figuerola J (2007) Climate and Dispersal: Black-Winged Stilts Disperse Further in Dry Springs. PLoS ONE 2(6): e539. doi:10.1371/
journal.pone.0000539
INTRODUCTION
Climate affect the abundance and distribution of many species of
wildlife. Impacts of last decades changes in climate include
reduction in population size, survival, and/or productivity, and
a northward shift in the distribution of a variety of different
organisms [1]. North Atlantic Oscillation (NAO) index is one of
the main cyclical climatic forces. During positive phases of the
NAO, westerly winds increase temperature and rainfall over
Northern Europe, and drought in the Mediterranean region [2].
Both ecological processes in the Sea (i.e. fish growth and survival)
and the continent (i.e. competition between sympatric species,
survival and productivity) seem affected by NAO phases [2].
Nevertheless, the potential effects of NAO and climate in general
on dispersive behaviour remain unstudied. Theoretical studies
predict major changes in the distribution of animals and plants in
response to climate, although the validity of these models has yet
to be established [3]. How do highly mobile organisms such as
birds respond to changes in climate? I investigated the case of the
Black-winged Stilt Himantopus himantopus, a common breeding
wader in European and, in particular, in southern European
wetlands [4]. The breeding population in Don˜ana (southwest
Spain) is very variable, ranging from 50 pairs in dry years to over
14,000 pairs in wet years. Given that the total European
population is estimated at 33,500–49,800 pairs, up to 28–42%
of European Black-winged Stilts breed in some years in Don˜ana.
Since 1988 the breeding population of Black-winged Stilts has
been monitored by means of censuses of breeding pairs, the
ringing of chicks with PVC rings, and the resighting of marked
individuals.
RESULTS
I used capture-mark-resighting data spanning the years 1988–
2003 to estimate Black-winged Stilt survival and resighting rates.
Survival estimates are affected by mortality and permanent
emigration, while resighting rates are affected by mark observation
effort and temporal dispersal to other areas [5]. Survival is low
during the first year of life (1
st
year: 28.11%612.75; 1+ year:
69.65%64.78), although it was constant from one year to another.
Resighting varied greatly with time and did not depend on age
(Table 1). Time-dependent variation in resighting rates was better
explained by local rainfall (45.1% variance explained) than by the
NAO (33.5% variance explained, Figure 1a). The simultaneous
combination of NAO and rainfall did not improve the fit on
models including only rainfall. Breeding population size increased
with resighting rates (r = 0.56, F = 5.95, df = 1, 13, p = 0.03) and
rainfall during the breeding season (r = 0.64, F = 10.82, df = 1, 16,
p = 0.005), but decreased with NAO (Figure 1b). Combining
simultaneously NAO and rainfall increased the fit of the model
(r = 0.86, F = 20.47, df = 2, 15, p,0.0001) and both factors
remained significantly related to population size in Don˜ana
(NAO, F = 18.37, df = 1, 15, p = 0.0006; rainfall, F = 10.01,
df = 1, 15, p = 0.006). NAO (but not local rainfall in Don˜ ana,
r = 20.12, F = 0.22, df = 1, 14, p = 0.65) tended to be positively
related, and Don˜ ana population size negatively related to the
frequency of observations of dispersing Black-winged Stilts in the
United Kingdom, a country outside the range of the species
(Figures. 1c and 2).
DISCUSSION
Considerable attention has been focused on the incidence of
climatic factors on survival, reproduction, and/or phenology [6,7].
However, the impact of climate on philopatry and dispersal has
received much less attention [8,9]. The results of this study suggest
that climatic conditions have important effects on birds’
philopatry, which is in turn related to changes in breeding
populations. Ultimately these changes lead to an increase in
Academic Editor: Peter Jones, University of Edinburgh, United Kingdom
Received February 21, 2007; Accepted May 22, 2007; Published June 20, 2007
Copyright: ß 2007 Jordi Figuerola. This is an open-access article distributed
under the terms of the Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided the
original author and source are credited.
Funding: The Junta de Andalucı
´
a funded this study via the project contract ‘Las
aves acua
´
ticas de Don
˜
ana y el cultivo del arroz: la interaccio
´
n entre la agricultura y
la conservacio
´
n de las zonas hu
´
medas’. The Spanish Ministry of Science and
Technology provides support for my research with a Ramo
´
n y Cajal contract for
young researchers.
Competing Interests: The author has declared that no competing interests exist.
* To whom correspond ence should be addressed. E-mail: jordi@ebd.csic.es
PLoS ONE | www.plosone.org 1 June 2007 | Issue 6 | e539

dispersive behaviour and an improved capacity for colonizing new
breeding localities. NAO, one of the Earth’s main large-scale
cyclical climatic patterns, is negatively associated to rainfall in
Spain and North Africa [10]. Both local rainfall and NAO have
been related by multivariate analyses to breeding population size
in Don˜ana: the former is a better estimator of habitat availability
for birds migrating into Don˜ana, while the latter may affect the
probability that birds wintering in Africa will breed closer to their
wintering grounds. Unfortunately, no information is available on
numbers of Black-winged Stilts breeding in North African
countries to directly test this relation between NAO and African
breeding distribution. The resighting rate is not only affected by
philopatry, but also by other factors such as research effort and
consequently analyses of this factor should be considered
conservative (and may explain the moderate amount of variance
explained by the models). Despite this, the resighting rate is clearly
associated with population changes in the study area and in
a region more than 1500 kilometres from Don˜ana, a fact that
increases confidence in the soundness of results.
Temperature increases leading to rising sea-levels [11] and
changes in rainfall patterns [12] will harm coastal wetlands. In
addition to cyclical fluctuations, a long term trend towards more
positive NAO is occurring [2]. While rain will probably increase in
northern Europe, the Mediterranean region will become drier [12]
and under this scenario information on how weather influences the
demographic parameters of organisms is urgently needed. In terms
of survival I found no direct costs of dispersal, although the effects
on individuals fitness cannot be excluded given that other studies
have found a relationship between dispersal and delayed breeding
[13,9].
Understanding how species’ ranges are modified in light of
climate change is an important issue in ecology. Travis & Dytham
[14] have recently produced a model that suggests that during
range expansion selection may favour individuals with a higher
propensity for dispersal. A paradoxical result of my study is that
climate itself can modify the propensity of individuals to disperse,
thereby increasing the probability of range expansion in species
that live, for example, in unstable environments such as
Mediterranean wetlands.
MATERIALS AND METHODS
The data
Since 1988 the number of breeding pairs of Black-winged Stilts has
been counted every year in the Don˜ana National Park and the
resulting figures have been found to be closely correlated to the
numbers counted in the whole of Don˜ ana (r = 0.93, F = 69.03,
df = 1, 10, p,0.0001), which are available for far fewer years.
The observation of rare birds outside their normal ranges has
long been a common hobby in many countries and the British
Birds Rarities Committee revised and evaluated all observations of
rare birds in Great Britain since 1959. This task provides valuable
information regarding the frequency of the rare bird species that
wander to Great Britain and can be consulted on the Internet
(http://www.bbrc.org.uk/waders.htm). Observations from all
years between 1988 and 2004 were included in the analyses.
The number of observations in any given year or territory will
clearly depend on the number of ornithologists living or visiting
that area. To control for differences in observer effort, the number
of any other rare species of waders (Infraorder Charadriides,
excluding the family Laridae; 15) observed in the UK was included
as a covariate in the analyses. Both the numbers of Black-winged
Stilts and waders observed in UK were log transformed.
Two different indicators of environmental conditions were used
in the analyses: rainfall in Don˜ana from March to August (the
Black-winged Stilt breeding season) (available at http://www-rbd.
ebd.csic.es/Seguimiento/mediofisico/parametrosmeteorologicos/
em05.htm), and the mean winter NAO-index (available at http://
www.cgd.ucar.edu/cas/jhurrell/indices.html). NAO is a major
source of interannual variability in atmospheric circulation and the
NAO index is estimated on the basis of differences in pressure at
sea-level between Lisbon and Reykjavik from December to
March.
Modelling survival and resighting rates
Chicks have been ringed in Don˜ ana since 1988 with metal rings
and white plastic DARVIC rings marked with a black, three-digit
code. These rings can be read from a distance with the aid of
a telescope. I conducted a capture-resighting analysis to estimate
survival and resighting rate using the program MARK and
information pertaining to 2964 individuals ringed and observed in
Table 1. Modelling the survival and resighting rates of Black-
winged Stilts during the period 1988–2003 using capture-
resighting data gathered in Don
˜
ana (southwest Spain).
......................................................................
a) Testing for age and time variation in survival and recapture parameters
Model QAICc Parameters QDeviance
Ø(age) p(time) 949.370 17 75.323
Ø(constant) p(time) 950.148 16 78.124
Ø(age) p(constant) 953.888 3 108.038
Ø(constant) p(constant) 954.072 2 110.226
Ø(age) p(age) 955.872 4 108.017
Ø(constant) p(age) 956.042 3 110.192
Ø(time) p(constant) 956.700 16 84.676
Ø(time) p(age) 958.550 17 84.503
Ø(age) p(age*time) 963.328 31 60.818
Ø(time) p(time) 968.177 29 69.750
Ø(age*time) p(constant) 968.765 30 68.297
Ø(age*time) p(age) 970.756 31 68.247
Ø(time) p(age*time) 983.817 44 54.637
Ø(age*time) p(time) 985.683 44 56.503
Ø(age*time) p(age*time) 1000.515 58 42.349
Ø(constant) p(age*time) 1036.888 30 136.421
b) Testing for the effects of weather on model parameters in the model Ø(age)
p(time)
Ø(age) p(rain March–August) 941.131 4 93.275
Ø(age) p(NAO+rain March–August) 941.183 5 91.321
Ø(age) p(NAO) 944.958 4 97.103
Ø(age) p(time) 949.370 17 75.323
c) Testing for effects of weather on model parameters in the model Ø(constant)
p(time)
Ø(constant) p(rain March–August) 941.497 3 95.647
Øconstant) p(NAO+rain March–August) 941.472 4 93.617
Ø(constant) p(NAO) 944.997 3 99.147
Ø(constant) p(time) 950.148 16 78.124
Models are defined in terms of survival (Ø) and recapture rates (p) that vary
between first-year and adult birds (age) and between years (time). AIC was
adjusted for a c-hat value of 1.12. The models supported by the AIC criterion
during the model selection process are marked in bold.
doi:10.1371/journal.pone.0000539.t001
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Don˜ ana during the period 1988–2003. Only captures and
observations occurring between March and August were included
in the analyses so as to estimate the probability of a bird alive in
one breeding season being still alive during the next breeding
season.
Survival analysis was based on the Cormack-Jolly-Seber models
(CJS). Survival rates are affected both by mortality and by
permanent emigration from the study area and resighting rates
reflect both variation in observation/capture effort and the
temporary emigration of individuals from the study area [16].
The relationship between climatic variables and survival and/or
recapture parameters was tested using a capture-recapture model
selection and simplification approach [5]. Model selection was
based upon a fully parameterized model in which both survival
and recapture probabilities varied with age and time. Models
incorporating age-dependent effects only allowed parameters to be
different from adults during the year after capture as chicks. The
adjustment of the CJS model to the data was assessed with the
RELEASE programme’s goodness-of-fit test [17] and with a para-
metric bootstrap approach. The parameteric estimates from the
Figure 1. North Atlantic Oscillation and Black-winged Stilt population dynamics. a, Philopatry to breeding grounds estimated as resighting rates
from the model Ø(age) p(time), r = 0.58, F = 6.49, df = 1, 13, p = 0.02, 1989–2003. b, Number of pairs breeding in Don
˜
ana National Park, r = 0.74,
F = 19.78, df = 1, 16, p = 0.0004, 1988–2005. c, Frequency of Black-winged Stilt observations in the United Kingdom after controlling for the number of
rare waders observed in the UK, a country outside the actual range of this species, r = 0.48, F = 4.15, df = 1, 14, p = 0.06, 1977–2004.
doi:10.1371/journal.pone.0000539.g001
Climate, Survival & Dispersal
PLoS ONE | www.plosone.org 3 June 2007 | Issue 6 | e539

model were used to simulate data in line with the assumptions
contained in the CJS models (individuals were independent and no
overdispersion of data occurred). This process was repeated 1000
times and the deviance of each model was calculated to determine
whether the deviance of the observed model exceeded that of the
simulated data. The overdispersion parameter (c-hat) was
calculated as the ratio between the mean deviance of simulated
models and the deviance of the observed model [18]. We found no
evidence of significant overdispersion (c-hat = 1.12) and thus no
evidence for the assumption that fates of individual birds were
independent of each other [19]. We adjusted results to a c-hat of
1.12 (ideally c-hat should be 1.00), although this adjustment had
no qualitative effect on the results.
Model simplification was based on an analysis of the factors
affecting survival and resighting probabilities and constructed
models with variation between age and time, and the age*time
interaction. Finally, using the simplified capture and survival
model, we tested the possible relationships between resighting
rates, which were found to vary annually, local rainfall and NAO.
I used a small sample size adjusted by Akaike’s information
criterion (AICc) for model selection. AICc is considered to be
a simple, effective, and objective means for model selection [20].
Models with lower AICc values are assumed to best fit the data
with the least possible number of parameters. Models with AICc
values differing by less than 2 were considered to be equivalent.
The amount of variance explained by climatic variables was
calculated as Deviance(model constant) - Deviance(model with
covariate) / Deviace(model constant) - Deviance(model with time
dependent parameter), as per [21].
Statistical analyses
A Pearson regression was used to analyse the relationship between
NAO and rainfall in Don˜ana, and breeding population size and
frequency of observations in the UK.
ACKNOWLEDGMENTS
Manolo Man˜ ez supplied information on the breeding populations in
Don˜ ana National Park. The Equipo de Seguimiento de Procesos Naturales
and many volunteer ringers and observers in Don˜ ana and the United
Kingdom have contributed to the databases analysed and have made
possible this paper. Tama´s Sze´kely provided useful comments on a first
draft of the manuscript.
Author Contributions
Conceived and designed the experiments: JF. Analyzed the data: JF. Wrote
the paper: JF.
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