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 environment 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 reproduction. 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 negatively related to their clutch size. Other environmental 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 breeding conditions (Reznick 1985
). In the presence of a highly virulent infectious disease, whatever the condition 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 energetically demanding (Thomson et al. 1998
; Williams 2005
) and affect immune function of individuals (Gustafsson et al. 1994
; Hanssen et al. 2004
). 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. Bêty 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 predator 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 reproduction and survival.