causes of low breeding success and survival
Breeding success at the Isle of May was high during the late 1980s, very low during the 1990s and showed a partial recovery 2000–02 (Fig. 2). Very similar patterns occurred at many British kittiwake colonies along the North Sea during this period (Mavor et al. 2003). The high breeding success observed during 1986–89 was comparable with the long-term mean at the very productive North Shields colony in north-east England (Thomas & Coulson 1988), whereas the worst years during the 1990s were similar to observed values in Alaska (Dragoo, Byrd & Irons 2001). The range observed over our 17-year study was thus comparable with that found for the species over its entire range. The period of low breeding success coincided with the activity of the Wee Bankie sandeel fishery (compare Appendix 1 and Fig. 2), but when the 2 years with very low catches (1990 and 1999) were excluded the correlation was less strong (Table 1). However, when winter SST during the previous year was included in the model, a very large part of the variation was explained (Table 1 and Fig. 3).
The highest ranked models for adult survival all included a decline with ‘age’ in either survival or resighting probabilities (Table 2). This could indicate senescence of either birds or colour-rings. However, an analysis of the subset of known-age birds provided strong evidence in favour of a quadratic trend in survival with true age rather than any effect of the age of the colour-ring (Frederiksen, Wanless & Harris 2004), and we used this result in conjunction with year-specific estimates from the model presented here as input for the population model. Adult survival declined substantially from the high values observed early in the study and subsequently stabilized (Fig. 4). The decline was less pronounced than in a previous analysis where the effect of ‘age’ was not taken into account (Harris, Wanless & Rothery 2000) but nevertheless substantial. The population model provided an estimate of the mean survival of all adults (aged ≥ 2 years) in the population, ranging from 0·98 in 1986–87 to 0·82 in 1998–99. Again, this range contains most estimates of kittiwake survival from other populations, from very high in Alaska (Hatch, Roberts & Fadely 1993; Golet, Irons & Estes 1998) to low in Brittany (Danchin & Monnat 1992) and at North Shields (Aebischer & Coulson 1990). Survival was low when the Wee Bankie fishery was active and when breeding success was also low (compare Appendix 1 and Figs 2 and 4), and when the previous winter's SST was included in the model a high proportion of the variation was explained (Table 1 and Fig. 5). Furthermore, there was a strong correlation between survival and breeding success in the following season (see Appendix 4).
It seems clear that the effect of SST on kittiwake breeding success and survival must be mediated through sandeel availability, and the changing importance of sandeel age classes to kittiwakes through the breeding season provides a clue to the mechanism. We propose the following scenario: warm winters lead to low sandeel recruitment, perhaps by reducing the food supplies available to larval sandeels (Arnott & Ruxton 2002). Kittiwakes start feeding on this weak year class of 0 group sandeel during chick rearing in June. This is too late to have a major effect on breeding success in the current year, but adults (and presumably fledglings) are in poor condition at the end of the breeding season and overwinter survival is correspondingly low. Next spring, breeding adults again feed mainly on the same weak year class in the early part of the breeding season (sandeels older than 1 group constitute a small proportion of kittiwake diet; Lewis et al. 2001) and their poor condition leads to low reproductive investment and correspondingly low breeding success. After a cold winter, the opposite situation occurs. The observed correlation between independent estimates of survival and breeding success in the following season (r = 0·67; see Appendix 4) was sufficiently strong to lend some credence to this hypothesis. The sharp decline in breeding success in 1990 occurred soon after a ‘regime shift’ in the North Sea, when an increased influx of warm Atlantic water had major ecological consequences, including a change in plankton community composition (Beaugrand 2004). Sandeel size and quality declined markedly over the study period (Wanless et al. 2004), perhaps as a response to changes in ocean climate, and this may also have affected kittiwakes adversely.
The Wee Bankie sandeel fishery also appears to have had a large effect on kittiwake performance (Figs 3 and 5). The exact mechanism is unclear, because the fishery is only likely to have had a strong direct effect on sandeel abundance in 1993, the peak year (Rindorf, Wanless & Harris 2000). Also, the fishery mainly took 1+ group sandeel in June and July, i.e. after the kittiwakes had switched to 0 group as their main prey (Lewis et al. 2001). However, it is possible that the fishery affected the behaviour of all sandeel age classes, so that they spent less time near the surface and thus became less available for surface feeders such as kittiwakes. Clearly, detailed studies of the behavioural responses of sandeels to fishing activity are required to elucidate the precise mechanism.
Kittiwake performance and population size declined at the same time as other sandeel-dependent seabirds were more successful on the Isle of May. As an extreme example, numbers of Atlantic puffins Fratercula arctica (L.), which to a large extent also feed their young on 0 group sandeels, increased by about 10% year−1 during the 1990s (Wanless et al. 2003). However, kittiwakes appear more sensitive to food shortages than many seabirds (Furness & Tasker 2000).
At Foula in Shetland, Oro & Furness (2002) found that kittiwake survival was associated with sandeel abundance, kittiwake body condition and breeding success of great skuas Catharacta skua Brünnich, an important predator of kittiwakes. The two first findings are consistent with our results, but great skuas are absent from the Isle of May and predation by great black-backed gulls Larus marinus L., for example, is rare. At the same time, kittiwake survival may also be affected by factors operating outside the breeding season. Identifying such factors is problematic, because only fragmentary data exist about the wintering areas of British kittiwakes: some individuals winter in the North Sea while others are dispersed in the North Atlantic (Coulson 2002). We found practically no correlation between adult survival and the winter NAO index (Table 1), a widely used indicator of winter conditions in the North Atlantic (Hurrell et al. 2003). In the future, application of lightweight data loggers (Wilson et al. 2002) may allow us to identify wintering areas more precisely and test whether survival is correlated with environmental conditions in these areas.
predictions of future population growth
The dynamics of the Isle of May kittiwake population have changed dramatically over the study period, from an approximately 8% increase year−1 in the late 1980s to a 11% decline year−1 in the late 1990s (Fig. 1). Our model showed that this change could be explained by the observed declines in adult survival and breeding success (Fig. 6), and that both factors were important. There was no need to invoke changes in net recruitment, i.e. juvenile survival including emigration/immigration, as the model was rather insensitive to variation in this parameter (Fig. 6). Large changes in emigration or immigration also seem unlikely if kittiwakes, as evidence from other studies suggest, preferentially recruit to successful colonies (Danchin, Boulinier & Massot 1998): breeding success for all major colonies within approximately 150 km of the Isle of May was closely correlated with our study colony (Harris & Wanless 1997), and these colonies have also shown similar declining trends (Heubeck 2004). Both the deterministic and stochastic models also indicated that the kittiwake population was unlikely to increase under current environmental conditions, and that a reopening of the Wee Bankie fishery would probably lead to a marked decline in numbers (see Appendix 5 and Fig. 7). Furthermore, if climate change, as predicted by climate models, should lead to increases in North Sea temperatures in winter, this is predicted to exacerbate the already critical situation for kittiwakes, particularly if the fishery is active.
implications for management
In the North Sea, kittiwakes are almost completely dependent on sandeels during the breeding season. Therefore, any factor reducing the abundance or availability of sandeels is likely to have a negative effect and lead to population declines. We have identified two factors associated with low performance in kittiwakes at the Isle of May: high winter sea temperatures and an industrial sandeel fishery. It is unclear exactly how the fishery would affect the availability of sandeels to kittiwakes. Nevertheless, in a situation where kittiwakes are declining not only in the North Sea but throughout most of their range (Hatch, Roberts & Fadely 1993; Barrett 2001), any activities that endanger their main food supply should be avoided. Although sea temperatures are also to some extent within human control, any policy changes aimed at reversing the warming trend will be very slow to take effect. Thus, it seems prudent and in accordance with the precautionary principle to extend indefinitely the closure of sandeel fisheries within the feeding range of kittiwake colonies in the western North Sea.
Our results suggest that kittiwake performance is strongly dependent on sandeel availability, and therefore reflects the general health of marine ecosystems in terms of their ability to produce sufficient amounts of forage fish to sustain thriving populations of top predators. Monitoring kittiwake performance (breeding success and survival) could therefore be an efficient way of monitoring marine ecosystem health. Furthermore, intensive long-term studies remain the only source of consistent data allowing evaluation of both population trends and extensive monitoring programmes, and maintaining such studies should be a high priority for research and management.