Was the removal of rabbits and house mice from Selvagem Grande beneficial to the breeding of Cory's shearwaters Calonectris diomedea borealis?

Abstract

The breeding success of Cory's shearwaters Calonectris diomedea borealis at its important Atlantic colony on Selvagem Grande has been monitored periodically at two study plots since 1982. A successful eradication programme was implemented to remove two alien invasive mammals, rabbits Oryctolagus cuniculus and house mice Mus musculus, from the island during 2002. The availability of long-term breeding data for Cory's shearwaters on Selvagem Grande provided a unique opportunity to study the effects of the removal of rabbits and mice on seabird breeding. Annual observation of approximately 400 Cory's nests showed that significantly more birds fledged from both study sites in the five breeding seasons after the eradication than in the 13 seasons prior to it for which reliable breeding data were available. The numbers of young birds present at the time of fledging were an average of 47 and 23% greater than pre-eradication numbers at the two study sites. The eradication of rabbits and mice was simultaneous and, therefore, it was impossible to attribute the increased breeding success of Cory's shearwaters to the removal of one or other species. However, both are known to have adverse impacts on the breeding of nesting seabirds. These observations provide important justification for the implementation of further programmes for the removal of alien invasive mammals from oceanic islands.

Selvagem Grande (30°09′N, 15°52′W) is the largest island of the Portuguese sub-archipelago of the Selvagens and lies between Madeira and the Canary Islands in the north-east Atlantic. The island supports one of the most important Atlantic colonies of Cory's shearwaters Calonectris diomedea borealis (Granadeiro et al., 2006) and the birds have been studied intensively since the expedition organised by the Museu Municipal do Funchal (História Natural) in 1963 (Pickering & Maul, 1965; Zino, 1971, 1985; Zino et al., 1987; Mougin et al., 2002a,b; Granadeiro et al, 2006). Two study areas of c. 15 * 100 m (site EFGH) and 16 * 140 m (site ABCD) on the island's cliff slopes have been defined for long-term monitoring (Zino et al., 1987). These areas are on opposite sides of the island, one facing the north-east trade wind and one in the lee of it. Frequent expeditions were made to the sites in order to conduct the monitoring, with special emphasis on the time of egg laying (late May to mid June) and prior to fledging (late October). The breeding cycle of the birds on the island is remarkably consistent and predictable. After a period of recovery following a devastating illegal cull of birds in 1976 (Zino, 1985), demonstrated in the increasing number of nests monitored in the years between 1984 to 1989, the numbers of nests studied did not vary appreciably among the annual study periods (Fig. 1).

Fig. 1 Percentage of monitored Cory's shearwaters nests on Selvagem Grande that produced fledged chicks (means for study areas ABCD and EFGH combined). Stippled bars are before eradication of mice and rabbits, and black bars after eradication. Values at the top of bars are the numbers of nests monitored. Rabbits and mice were eradicated during the 2002 breeding season. In breeding seasons for which no data are presented, logistical problems prevented adequate study. The number of nests studied in 2005 represents c. 1.5% of the total number of breeding pairs estimated to be present on the island in that year (Granadeiro et al., 2006.).

Populations of the rabbit Oryctolagus cuniculus and the house mouse Mus musculus inhabited the island, probably the result of ancient introductions by mariners, but were removed in a successful eradication programme carried out by the Parque Natural da Madeira involving the intensive application of baits containing the anticoagulant rodenticide brodifacoum (Oliveira et al., 2003). The removal of the majority of mammals occurred during August 2002, coinciding with the period of hatching of Cory's shearwater chicks. Rabbits and house mice were the only alien mammals present on the island.

The removal of rats (Rattus spp.) from breeding colonies of seabirds can result in significant rises in productivity and survival because of their predation of adults, eggs and young (Zino et al., 2001; Courchamp et al., 2003; Buckle, 2004). Mice, mainly house mice, but also Peromyscus spp. and others, also inhabit many oceanic islands and in spite of their small size are able to predate nesting seabirds and their eggs and chicks (Blight et al., 1999: Drever et al., 2000; Cuthbert & Hilton, 2004; Wanless et al., 2007). The removal of rabbits has also been shown to be beneficial in terms of island conservation (Courchamp et al., 2003). However, the principal biota that benefit are plants and the major effects on breeding seabirds are probably indirect, mediated by vegetation changes, reduced soil erosion and the removal of the prey base of raptors that may take seabirds as secondary prey items (Priddel et al., 2000; Bullock et al., 2002).

The existence of a long-term data set on the breeding success of Cory's shearwater on Selvagem Grande provided a unique opportunity to study the benefits of the removal of the two alien invasive species, rabbits and house mice. Ideally, in breeding studies of seabirds, nests are monitored throughout the breeding season, the breeders ringed, the date of laying observed, and losses throughout incubation and the dates of hatching and fledging are noted (Zino et al., 1987). It has not been possible, however, to obtain such complete data sets in every breeding season of Cory's shearwaters on Selvagem Grande due to the difficulty of access to the island. In most years the ringing of the juveniles took place after late September and losses of juveniles after this date and prior to fledging are known to be minimal. Therefore, the numbers of nests monitored and of chicks ringed are used in this study as indicators of annual productivity in the two study areas.

A significant increase in Cory's shearwater productivity was observed in the years following the eradication programme in both study areas. (Table 1, Fig. 1). Fledgling productivity in study area ABCD increased from a mean of 36.5 fledglings per 100 nests monitored in 13 breeding seasons before eradication to one of 53.7 per 100 nests in the 5 subsequent seasons. A similar effect was observed in study area EFGH, with fledgling productivity increasing from a mean of 45.4 to one of 55.7 per 100 nests. These increases represent, respectively, 47 and 23% more young birds in nests immediately prior to fledging after rabbit and mouse eradication.

Table 1 The mean percentage of Cory's shearwater nests that produced fledglings in two study areas of Selvagem Grande before and after the eradication of rabbits and mice, together with two-tailed t-tests for the difference of means with unequal variances, hence the different degrees of freedom.

Until Selvagem Grande was classified as a Nature Reserve in 1971, and permanently wardened from 1980, the island's Cory's shearwaters were intensively, and latterly illegally, exploited for meat, oil and feathers (Mougin & Stahl, 1982; Zino, 1985). This resulted in a population decline from an estimated 130,000-150,000 breeding pairs to 7,000 pairs in 1980 (Mougin & Mougin, 2000). Since the last extensive culls in 1975 and 1976 the population of Cory's shearwaters on Selvagem Grande appears to have been increasing at an annual rate of c. 5% and has now recovered to an estimated 29,540 breeding pairs (Granadeiro et al., 2006). It is also clear, however, that a highly significant increase in the number of fledglings produced in the two study areas in the last five consecutive breeding seasons has coincided with the removal of rabbits and mice from Selvagem Grande. If the increase seen in the study plots is typical of the nests on the island as a whole it is likely that the rate of growth of the island's population will also increase. A similar increase in the breeding success of Cory's shearwater was found by Igual et al. (2006) who controlled, but did not eliminate, black rats Rattus rattus at Cory's shearwater breeding sites on the Chafarinas Islands in the Mediterranean.

Our observations do not prove a causative link between the eradication of alien mammals and improved breeding success of Cory's shearwaters. However, competition between rabbits and seabirds for burrows has been noted on some oceanic islands (Courchamp et al., 2003) but, as previously stated, Selvagem Grande once supported, in the presence of rabbits, a much larger population of Cory's shearwater than it does now. Thus, the removal of competition for burrows seems an unlikely explanation for their increased breeding success, although disturbance may have been important. Also, if the eradication of rabbits resulted in a benefit to the birds through reduced soil erosion and vegetation recovery we would have anticipated a more gradual change in breeding success than was apparent. Mice may have direct impact on breeding seabirds through predation (Blight et al., 1999; Cuthbert & Hilton, 2004; Wanless et al., 2007). However, while very high densities of mice frequently occurred on Selvagem Grande, no obvious sign of their predation of Cory's adults, chicks and eggs was ever seen. Therefore, attributing the increased fledging rate of Cory's shearwater either to mouse or rabbit removal, or to a combination of both, must remain speculative. Nevertheless, the adverse impacts of both rabbits and mice on the breeding of nesting seabirds is well established (Courchamp et al., 2003) and their removal from Selvagem Grande appears to have had an immediate and dramatic effect in increased breeding productivity of Cory's shearwater. The increase was apparent in the 2002 breeding season during which the rabbit and mouse eradication took place. This suggests that the impact of the alien mammals may have been on the birds’ chicks, rather than their eggs, because the mammals were present throughout laying and incubation in 2002 and effective removal occurred only around the time of hatching. In spite of their necessarily speculative nature, these observations will provide encouragement and stimulus to those planning programmes for the removal of alien vertebrates from other oceanic islands.