Biol. Lett. (2009) 5, 278–281
Published online 20 February 2009
Costs of reproduction in a
long-lived bird: large
clutch size is associated
with low survival in the
presence of a highly
Se ´bastien Descamps1,2,3,*, H. Grant Gilchrist2,
Joe ¨l Be ˆty3, E. Isabel Buttler1,2and Mark R. Forbes1
1Department of Biology, Carleton University, Ottawa, Ontario,
2NWRC, Environment Canada, Ottawa, Ontario, Canada K1A0H3
3De ´partement de Biologie, UQAR-CEN, Rimouski, Que ´bec,
*Author and address for correspondence: De ´partement de Biologie,
UQAR-CEN, 300 alle ´e des Ursulines, Rimouski, Que ´bec,
Canada G5L3A1 (email@example.com).
Fitness costs of reproduction are expected to be
more pronounced when the environmental con-
ditions deteriorate. We took advantage of a
natural experiment to investigate the costs of
reproduction among common eiders (Somateria
mollissima) nesting at a site in the Arctic, where
an avian cholera epizootic appeared at different
magnitudes. We tested the predictions that
larger reproductive effort (clutch size) is associ-
ated with lower survival or breeding probability
the following year, and that this relationship was
more pronounced under heightened exposure to
the disease. Our results indicate that large clutch
sizes were associated with lower survival of
female eider ducks, but only when there was
heightened exposure to avian cholera, as indexed
by eider mortality on site. No cost was observed
when cholera was absent or when lesser exposure
was evident. This supports the hypothesis that
fitness costs of high reproductive effort are
higher under unfavourable conditions such as a
disease epizootic, and further indicates that
being a conservative breeder can increase survi-
val probability, given the presence of a highly
Keywords: avian cholera; clutch size; common eider;
reproductive effort; survival
The existence of trade-offs between life-history traits,
and in particular of fitness costs of reproduction, is at
the core of life-history theory (Roff 2002). As costs of
reproduction generate covariation between demo-
graphic rates, a comprehensive understanding of
population dynamic processes requires examination
of the costs of reproduction (Proaktor et al. 2008).
Fitness costs of reproduction have proven difficult
to study in the wild because variation in individual
quality often overrides the costs of reproduction,
and leads to apparent positive associations between
demographic components (Reznick 1985). Given the
difficulty of studying the costs of reproduction, it is
particularly challenging to understand how they vary
with environmental conditions. It has been suggested
that under unfavourable conditions, fitness costs of
reproduction should be more pronounced (Reznick
1985), but empirical evidence is extremely rare.
Unfavourable conditions often originate from high
population density (Festa-Bianchet et al. 1998), star-
vation (Penn & Smith 2007) and harsh weather
(Tavecchia et al. 2005). Infectious disease can have
dramatic effects on individuals’ life histories, but its
influence on reproductive costs has rarely been investi-
gated (but see Festa-Bianchet 1989).
We took advantage of the appearance of an avian
cholera epizootic in a nesting colony of common
eiders (Somateria mollissima) in the Canadian Arctic
(hereafter called the East Bay colony) to study
variation in fitness costs of conservative versus higher
investment in reproduction in relation to the magni-
tude of a disease epidemic. Common eiders are long-
lived, iteroparous sea ducks, whose females exhibit a
strong philopatry to breeding areas (Goudie et al.
2000). Female eiders incubate alone, do not feed
during the entire incubation period and can lose more
than 40 per cent of their body mass during laying and
incubation (e.g. Parker & Holm 1990). It has been
shown in common eiders that an increase in repro-
ductive effort decreases their immune function, with
potential cascading effects on future fitness prospects
(Hanssen et al. 2004, 2005).
Female common eiders nesting at the East Bay
colony offer a rare opportunity to investigate variation
in fitness costs of reproduction as a function of environ-
mental conditions (i.e. degree of exposure to a disease),
and to test the hypothesis that costs of reproduction
increase under conditions of heightened exposure.
2. MATERIAL AND METHODS
Our study was done at East Bay, Southampton Island, Nunavut,
Canada, where between 4000 and 8000 eider pairs breed depend-
ing on the year. This site is the largest known common eider colony
in the Canadian Arctic. An avian cholera (Pasteurella multocida)
epidemic first appeared in 2005, but its impact at first was very
limited (5% of the breeding female eiders died during this breeding
season); in comparison, the cholera epidemic had a very large to
moderate impact on eider survival during the 2006 and 2007
breeding seasons (2006: approx. 32% of the breeding females died
versus approx. 14% in 2007; I. Buttler & H. G. Gilchrist 2008,
In precocial birds, maternal energetic allocation to reproduction,
or reproductive effort (sensu Evans 1990), mainly corresponds to
egg production and incubation. Energetic costs of egg production
and incubation are influenced by clutch size and both can have
fitness costs (Erikstad & Tveraa 1995; Thomson et al. 1998;
Williams 2005). As a consequence, we used the clutch size of
female eiders as a proxy of their reproductive effort.
To study whether costs of reproduction varied with respect to
lesser or heightened exposure to the disease, we used the modelling
of capture–mark–recapture (CMR) data (Lebreton et al. 1992) of
158 females of known clutch size banded between 2004 and 2007
(70 were banded in 2004, 29 in 2005, 28 in 2006 and 31 in 2007)
and model selection based on AICc (Akaike Information Criterion
corrected for small sizes; Burnham & Anderson 2002). Our procedure
is detailed in appendix 1 of the electronic supplementary material.
As non-breeders are less likely to be spotted on the island when
compared with breeders (see details in appendix 1 of the electronic
supplementary material), a lower recapture probability in a given
year can be interpreted in terms of a lower breeding probability.
Using our CMR modelling, we tested for a relationship between
Electronic supplementary material is available at http://dx.doi.org/
10.1098/rsbl.2008.0704 or via http://rsbl.royalsocietypublishing.org.
Received 26 November 2008
Accepted 12 January 2009
This journal is q 2009 The Royal Society
clutch size and either survival or breeding probability at three
different periods: 2004–2006, where there was no (or extremely
limited) effect of avian cholera on mortality; 2006–2007, which was
the year following the largest cholera outbreak; and 2007–2008,
where cholera had a limited effect on eider mortality. Any difference
in survival estimates could correspond to an actual difference in
survival and/or permanent emigration, and CMR survival analyses
do not allow disentangling these two alternatives. Thus, we also
used the data on female eiders recovered dead during the breeding
season of the year of the largest cholera outbreak (nZ28) to
determine, using a logistic regression, whether mortality on the
island in 2006 was linked to clutch size (no female of known clutch
size was found dead during the 2007 breeding season).
Additional details on methods are presented in appendix 1 of
the electronic supplementary material.
Recapture probabilities were relatively constant
throughout the period of our study and equal to
0.63G0.05 s.e. (appendix 2 in the electronic supple-
mentary material). Recapture probabilities were not
related to the clutch size of females, whether they
bred before or during a cholera outbreak (table 1a;
figure 1a; appendix 3 in the electronic supplementary
material). Annual survival of female eider ducks
varied with the period considered (2004–2006:
0.89G0.03 s.e.; 2006–2007:
2007–2008: 0.68G0.08 s.e.; appendix 2 in the
electronic supplementary material). Annual survival
was not related to clutch size before the severe
cholera epidemic or during the period of moderate
cholera effect, but was strongly and negatively associ-
ated with clutch size during the period of intense
cholera effect (table 1b; figure 1b; appendix 3 in the
electronic supplementary material). An increase of
one egg in the clutch was associated with an
estimated average decrease of 15 per cent in survival.
The probability of mortality on the island in 2006
increased significantly with clutch size (slope of 0.85
on a logit scale; effect of clutch size: score-test
statisticZ3.93, pZ0.048; figure 2).
In the years prior to cholera outbreak, the survival of
female eiders was independent of clutch size. Similar
results have been found for females breeding in 2007,
a year with apparently lessened exposure of eiders to
avian cholera. This suggests that, when the environ-
ment was not unfavourable (no avian cholera
epizootic or limited exposure to avian cholera), no
cost was detectable. This probably reflects that the
costs of reproduction, if any, were limited and masked
by individual heterogeneity (van Noordwijk & de Jong
1986). In favourable environmental conditions,
females could adjust their reproductive effort in
relation to their pre-breeding body condition so that
females in good condition could deal with the higher
energetic demands required by laying and incubating
a larger clutch without paying extra cost of reproduc-
tion. This led to no association, or a positive
association, between clutch size and return rates
(Yoccoz et al. 2002).
In the year of the greatest exposure of eiders to
avian cholera, as indexed by on-site estimates of eider
mortality, survival of females was strongly and nega-
tively related to their clutch size. Other environmental
Table 1. Effects of clutch size on survival and recapture probabilities of female common eiders, East Bay colony, Southampton Island, Nunavut, Canada. (np indicates the number of
estimated parameters for each model, AICc is the Akaike information criterion corrected for small sample sizes and DAICc is the difference in AICc between the model with the lowest
AICc and the model considered. wiindicates the AICc weight of a given model among the whole set of models fitted.)
(a) clutch size effect on recapture probabilities (survival and recapture probabilities were modelled as: f04–06,06–07,07–08p.; see appendix 2 in the electronic supplementary material for
no effect of clutch size
linear effect of clutch size on recapture probabilities in 2004 and 2005
linear effect of clutch size on recapture probabilities in 2007
linear effect of clutch size on recapture probabilities in 2006
(b) clutch size effect on survival probabilities (survival and recapture probabilities were modelled as: f04–06,06–07,07–08p.; see appendix 2 in the electronic supplementary material for
linear effect of clutch size on survival between 2006 and 2007
no effect of clutch size
linear effect of clutch size on survival between 2007 and 2008
linear effect of clutch size on survival between 2004 and 2006
Cost of reproduction and avian cholera
S. Descamps et al.
Biol. Lett. (2009)
parameters (e.g. temperature and precipitation) were
not worse during the 2006 breeding seasons when
compared with other years, and density was lower in
2006 than in 2005. Therefore, an increase in the costs
of reproduction because of the presence of a highly
virulent pathogen remains the most likely explanation.
We found no effect of clutch size on recapture
probabilities, either before or during the cholera
epizootic, which suggests that the probability of
breeding was not a function of the size of the clutch
laid in the previous year. Consequently, it seems that
the clutch size affected only the survival ability of
females but for those who survived, there was no
long-lasting effect of previous reproduction on the
current breeding propensity.
Our study thus supports the hypothesis of higher
costs of reproduction under very unfavourable breed-
ing conditions (Reznick 1985). In the presence of a
highly virulent infectious disease, whatever the con-
dition or quality of female eiders, a higher energetic
allocation to reproduction required by laying and
incubating a larger clutch led to higher survival costs
of reproduction. Three non-exclusive mechanisms
can be proposed for this observed relationship. First,
laying and incubating a large clutch may be energeti-
cally demanding (Thomson et al. 1998; Williams
2005) and affect immune function of individuals
(Gustafsson et al. 1994; Hanssen et al. 2004, 2005).
Such effects could have few, if any, consequences
when environmental conditions are good but could be
exacerbated under unfavourable conditions such as
the presence of a disease, leading thus to increased
mortality. Second, clutch size is correlated with arrival
date and breeding success, so that females laying a large
clutch tend to arrive earlier on the colony (H. G.
Gilchrist & J. Be ˆty 2004, unpublished data) and are
more likely to complete the incubation (Bourgeon et al.
2006). Consequently, female eiders laying a small
clutch may have spent a shorter time on the island.
Such females could have been less exposed to the
disease either because they arrived and laid later or
because they left the island earlier after nesting failure.
A third possibility is that females laying larger clutches
require more recesses to replenish water reserves;
freshwater on the island can be the source of
P . multocida, so that a greater fresh water consumption
could be associated to a greater exposure to the disease.
Whatever the underlying mechanism behind the
relationship between survival and clutch size, our
main results and conclusions remain the same: an
increase in reproductive effort led to a decrease in
survival in the year when avian cholera outbreak had
the greatest magnitude. This relationship might be
due to the physiological and/or ecological costs of
reproduction (e.g. decrease in immune function and
thus, higher susceptibility to the disease once infected
versus longer or greater exposure to the disease and
thus, higher risk of infection).
Our study supports previous theoretical findings,
which suggest that ‘during poor breeding conditions,
maximum fitness is achieved either by not breeding at
all or by abandoning the brood’ (Erikstad et al. 1998,
p. 1781). Erikstad et al. (1998) proposed that breeding
conditions are determined by variables such as territory
quality, weather conditions, food supply and/or pre-
dator density. Our study indicates that the presence of a
disease might be another important determinant of
breeding conditions, which can affect the survival of
breeding individuals and trade-offs between reproduc-
tion and survival.
probability of mortality on the island
Figure 2. Relationship between clutch size and the probability
of mortality on the island for female common eiders breeding
during a severe avian cholera outbreak at East Bay,
Southampton Island, Nunavut, Canada. The line represents
the estimated relationship from a logistic regression. Numbers
correspond to sample sizes for each clutch size category.
clutch size effect
2004–2006 2006–2007 2007–2008
clutch size effect
Figure 1. Slopes (GCI 95%) of the estimated relationships
(on a logit scale) between clutch size and (a) recapture
probabilities or (b) apparent survival for female common
eidersbreeding atEast Bay, Southampton
280S. Descamps et al.Cost of reproduction and avian cholera
Biol. Lett. (2009)
The study has been approved by the Canadian Council on Download full-text
This study was supported by the Canadian Wildlife Service,
Nunavut Wildlife Management
Institute of Nature, Polar Continental Shelf Project, Fonds
Que ´be ´cois de la Recherche sur la Nature et les Tech-
nologies, Canadian Network of Centres of Excellence
ArcticNet, Natural Sciences and Engineering Research
Council of Canada and the Department of Indian Affairs
and Northern Canada. We thank all of the summer research
assistants, and Maureen Kay, Myra Robertson and Mark
Mallory for their help at different stages of the study.
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Cost of reproduction and avian cholera
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Biol. Lett. (2009)