Weimerskirch Diseases threaten Southern Ocean albatrosses

Infectious diseases have the potential to cause rapid declines and extinction in vertebrate populations, and are likely to be spreading with increased globalisation and climate warming. In the Southern Ocean and Antarctica, no major outbreaks of infectious diseases have been reported to date, perhaps because of isolation and cold climate, although recent evidence suggests their presence. The major threat for the Southern Ocean environment is today considered to be fishing activities, and especially controversial long-lining which is assumed to be the cause of the major decreases in albatross and large petrel populations observed recently. Here we show that the worldwide spread of avian cholera is probably the major cause of the decrease on Amsterdam Island of the large yellow-nosed albatross (Diomedea chlororhynchos) population, which was previously attributed to long-line fishing. Another pathogenic bacterium, Erysipelas, was also present. The diseases affect mainly young chicks, with a cyclic pattern between years, but also kill adult birds. The outbreak of the disease probably occurred in the mid-1980s when chick mortality increased, adult survival decreased and the population started to decrease. The diseases may be currently threatening the very rare Amsterdam albatross (D. amsterdamensis) with extinction, and are probably also affecting sooty albatrosses (Phoebetria fusca). The spread of diseases to the most remote areas of the world raises major concern for the conservation of the Southern Ocean environment. Introduction Diseases have probably played a major role in the regulation and evolution of animal populations, including humans (May 1988; Stearns 1999). Infectious diseases have the potential to cause rapid decrease and ultimately extinction in vertebrate populations (Grenfell and Dobson 1995), and their role has only been recently fully acknowledged, especially for the potential major conservation problems they may pose. Today, they are likely to be spreading with increased globalisation and climate warming (Harvell et al. 2002). Because they spend most of their life at sea and return to land only to breed, the impact of diseases on seabirds is perhaps more difficult to detect than in terrestrial species. Although there is some evidence of mass mortalities in seabirds, they generally result from trophic problems, poisoning or pollution, rather than from diseases (e.g. Coulson 1968; Sileo et al. 1990; Burger 1993; Work and Smith 1996). In the Southern Ocean and Antarctica, there are no records of major disease outbreaks causing mass mortality reported to date, possibly because of isolation, low temperatures and reduced human interference. However, recent evidence suggests the presence of pathogens in penguins in Antarctica, but no major mortality has been noted so far (Gardner et al. 1997). Available data are, however, currently inadequate, and the recent presence of humans on scientific bases or the increasing numbers of tourists may be potential vectors for future disease outbreaks (Gardner et al. 1997). The major threat for the Southern Ocean environment is today considered to be fishing activities, and especially controversial longlining, which is assumed to be the cause for the major decreases in albatross and petrel populations observed recently (Gales 1998), and much focus of present research has been directed logically towards research on this issue (Croxall 1998). Amsterdam Island is one of the most isolated islands in the world, located in the middle of the H. Weimerskirch Centre d’Etudes Biologiques de Chizé, UPR 1934 Centre National de la Recherche Scientifique, 79360 Villiers en Bois, France E-mail: henri.weimerskirch@la-reunion.ird. fr Polar Biol (2004) 27: 374–379 DOI 10.1007/s00300-004-0600-x southern Indian Ocean, and is the sole nesting ground of the minute population of the critically endangered Amsterdam albatross, Diomedea amsterdamensis (Weimerskirch et al. 1997; Inchausti and Weimerskirch 2001), but also of a large population of yellow-nosed albatrosses, D. chlororhynchos. The population of yellow-nosed albatrosses has halved during the past 20 years from 37,000 to 18,000 pairs (Weimerskirch and Jouventin 1998), resulting in its listing as a Vulnerable Species, and upgraded as Endangered by IUCN. The decrease was attributed to long-line fishing, which indeed causes the mortality of yellow-nosed albatrosses around Australia (Gales et al. 1998) where Amsterdam yellow-nosed albatrosses are known to winter (Weimerskirch et al. 1985). Off South Africa, Atlantic yellow-nosed albatrosses are also caught in small numbers in long-line fishing (Ryan et al. 2002). However, there has been a tendency to attribute decrease of albatross populations to long-line fishing whereas very few studies so far have tried to estimate the potential effect of long-lining on the dynamics of populations affected by this type of fishery (e.g. Weimerskirch et al. 1997; Tuck et al. 2001). For example, on Amsterdam, yellow-nosed albatrosses have suffered heavy mortalities of chicks during their first weeks of life that cannot be attributed to long-line fishing at sea, suggesting that other factors might be involved in the population decrease. Here, we have studied in detail the cause of mortality that affected the populations of yellow-nosed albatrosses on Amsterdam Island, and have looked especially whether causes other than longlining could have induced the observed decrease of the population. Our observations in the field have suggested to us that the cause of mortality might involve diseases, and we present here the results of this research. Materials and methods A long-term study colony of around 200 pairs of yellow-nosed albatrosses has been monitored annually since 1979 at Pointe d’Entrecasteaux, on the western coast of Amsterdam island (37 S, 70 E). In this colony, the number of breeding pairs is counted, and all adults and chicks are banded. Banded birds are recaptured for identification in mark-recapture studies, allowing us to estimate adult and juvenile survival. During a study focusing on the foraging ecology of yellow-nosed albatrosses in December-March 1995/1996 and 1996/1997, colonies were observed continuously from dawn to dusk (Weimerskirch et al. 2001), allowing detailed study of the timing, occurrence and cause (predation, starvation or other) of chicks’ deaths. From 1995/1996, long-term study colonies and neighbouring colonies were monitored for breeding success, and fresh corpses of adults and chicks were collected. The fresh corpses of 25 individuals (21 chicks and 4 adults) collected within a few minutes to 1 h after death in the colonies were rapidly frozen, and returned frozen to France for autopsies and tissue analyses. Laboratory analyses, including necropsy, bacteriology and histopathology, were performed at the National Centre for Avian Diseases (LDA 22, Ploufragan, France). The serotype of the Erysipelas bacteria was determined by Merial Laboratories (Lyon, France). Survival of adults was estimated following Lebreton et al. (1992), using Program Mark (White and Burnham 1999). Results Yellow-nosed albatross During the 1995/1996 breeding season, we investigated the causes of mortality through continuous observation of a study colony of ca. 100 pairs during 1 month from hatching. We found that during this period in the study plot, 31 healthy well-fed chicks died within a few minutes after convulsions, apparently from a disease that spread progressively between neighbouring nests, and from low to high altitude in the colonies. Laboratory analyses of 25 individuals (21 chicks and 4 adults) found dead under these circumstances during the 1995/1996 season and during the following seasons, indicate that 2 chicks were infected by the bacterium Erysipelothrix rhusiopathidae, during a year of lower mortality (1996). The serotype of the bacteria is 1b. Four adults and the remaining chicks collected in 1999 and 2000 (during years of very high chick mortality) were infected by the bacterium Pasteurella multicida, which is responsible for avian cholera. The high mortality of healthy chicks attended by their parents within a few weeks of hatching is the major cause of the low breeding success of the colony. The typical pattern of increased mortality just after hatching is shown in Fig. 1. The population started to decrease in the mid-1980s (Fig. 2a). Breeding success decreased from 1983/1984, showing since this period a cyclical pattern, peaking with complete failure at 3to 4-year intervals (Fig. 2b). The mortality of chicks was not distributed evenly in the colonies. Whereas it was extremely high in the lower-altitude colonies, and in some isolated colonies, it was lower in other colonies at higher altitudes (Table 1). The rate of breeding failure due to chick mortality was similar among subcolonies in two successive seasons (Table 1, R=0.945, P<0.001) The long-term records of demographic parameters show that adult mortality increased from the early Fig. 1 Change in breeding success over the 2000–2001 breeding season from laying till fledging (n=1,273 eggs laid). Hatching occurred 60 days after laying 375