Piecing together the global population puzzle of wandering albatrosses: genetic analysis of the Amsterdam albatross Diomedea amsterdamensis

Wandering albatrosses have been subjected to numerous taxonomic revisions due to discoveries of new species, analyses of morphological data and, more recently, the inclusion of genetic data. The small population of albatrosses (170 individuals including 26 pairs breeding annually) on Amsterdam Island in the Indian Ocean, Diomedea amsterdamensis, has been given species status based on plumage and morphometrics, but genetic data published to date provide weak support and its specific status remains controversial for some authors. We used mitochondrial control region sequence data to elucidate the relationship of the Amsterdam albatross within the wandering albatross complex (Diomedea amsterdamensis, D. antipodensis, D. dabbenena and D. exulans). Three novel haplotypes were present in 35 individuals from Amsterdam Island, and were highly divergent (3.6–7.3%) from haplotypes found in the other three members of the wandering albatross complex. Low levels of genetic variation in Amsterdam albatross likely resulted, at least in part, from a population bottleneck. Geographic isolation in the wandering albatross complex is maintained by high natal philopatry. As Amsterdam Island is the only breeding ground for this critically endangered species, we strongly urge conservation efforts in the area, especially in relation to long line fisheries and other threats such as disease and introduced predators, and it be listed as a distinct species.     

The occurrence of two bill morphs of prions Pachyptila vittata on Gough Island

Prions Pachyptila are abundant seabirds in the Southern Ocean that have been used to infer environmental change, but this relies on an understanding of their morphological diversity. Species limits among prions are largely defined by the size and structure of their bills. The broad-billed prion P. vittata, which breeds at temperate islands in the central South Atlantic Ocean and around New Zealand, is the largest species with adult bill widths averaging 21–22 mm. We report local differences in bill sizes on Gough Island, with typical adults breeding in some areas and narrower-billed birds in other areas (average bill width 18–19 mm, although at one site there was a second mode at bill widths of 16–17 mm). The narrow-billed birds have slightly shorter bills, heads and wings (averaging 1–2 % smaller than typical adult broad-billed prions), but the difference in bill width is much more marked (15 %). The small-billed birds differ from typical broad-billed prions in having blue colouration in the upper mandible and are similar in size to MacGillivray’s prion P. [salvini/vittata] macgillivrayi from Amsterdam and St Paul islands in the temperate Indian Ocean. The occurrence of two prion morphs on Gough Island raises intriguing questions about their ecology and systematics. Small-billed birds breed 3 months later than large-billed birds, suggesting that they are a separate species, not an example of bill polymorphism.     

Can predation by invasive mice drive seabird extinctions?

The house mouse, Mus musculus, is one of the most widespread and well-studied invasive mammals on islands. It was thought to pose little risk to seabirds, but video evidence from Gough Island, South Atlantic Ocean shows house mice killing chicks of two IUCN-listed seabird species. Mouse-induced mortality in 2004 was a significant cause of extremely poor breeding success for Tristan albatrosses, Diomedea dabbenena (0.27 fledglings/pair), and Atlantic petrels, Pterodroma incerta (0.33). Population models show that these levels of predation are sufficient to cause population decreases. Unlike many other islands, mice are the only introduced mammals on Gough Island. However, restoration programmes to eradicate rats and other introduced mammals from islands are increasing the number of islands where mice are the sole alien mammals. If these mouse populations are released from the ecological effects of predators and competitors, they too may become predatory on seabird chicks.     

The impacts of introduced House Mice on the breeding success of nesting seabirds on Gough Island

Invasive species are the main threat to island biodiversity; seabirds are particularly vulnerable and are one of the most threatened groups of birds. Gough Island, a UNESCO World Heritage Site in the South Atlantic Ocean, is an Important Bird and Biodiversity Area, and one of the most important seabird colonies globally. Invasive House Mice Mus musculus depredate eggs and chicks of most seabird species on the island, but the extent of their impact has not been quantified. We used field data and bootstrapped normal distributions to estimate breeding success and the number of surviving chicks for 10 seabird species on Gough Island, and compared estimates with those of analogous species from predator‐free islands. We examined the effects of season and nest‐site location on the breeding success of populations on Gough Island, predicting that the breeding success of Gough birds would be lower than that of analogues, particularly among small burrow‐nesting species. We also predicted that winter‐breeding species would exhibit lower breeding success than summer‐breeding species, because mice have fewer alternative food sources in winter; and below‐ground nesters would have lower breeding success than surface nesters, as below‐ground species are smaller so their chicks are easier prey for mice. We did indeed find that seabirds on Gough Island had low breeding success compared with analogues, losing an estimated 1 739 000 (1 467 000–2 116 000) eggs/chicks annually. Seven of the 10 focal species on Gough Island had particularly high chick mortality and may have been subject to intense mouse predation. Below‐ground and winter breeders had lower breeding success than surface‐ and summer‐breeders. MacGillivray's Prion Pachyptila macgillivrayi, Atlantic Petrel Pterodroma incerta and Tristan Albatross Diomedea dabbenena are endemic or near‐endemic to Gough Island and are likely to be driven to extinction if invasive mice are not removed.     

Unexpectedly high genetic diversity of mtDNA control region through severe bottleneck in vulnerable albatross <Emphasis Type="Italic">Phoebastria albatrus</Emphasis>

In the late part of the nineteenth century and the early part of the last century, the short-tailed albatross Phoebastria albatrus was in danger of extinction owing to feather hunting. In the middle of the last century, the total number of this species was inferred to be approximately 50–60 with breeding occurring only on Torishima Island of the Izu Islands. Recently, the number of individuals has increased to more than 2,000 and that of their breeding islands to three, namely, Torishima Island, and Minami- and Kita-kojima Islands of the Senkaku Islands. Here, we show that the 44 short-tailed albatrosses we examined represent 29 haplotypes in the control region of mitochondrial DNA, and have a considerably higher genetic diversity than most avian species, but not very high in albatross species; the h and π were 0.96 and 0.013, respectively. However, the parsimony network clearly showed that many intermediate haplotypes were lost. It was concluded that the majority of the haplotypes in the founder population have been maintained. Judging from these findings and the exponential increase in the number of individuals, the present population of the short-tailed albatross seems not to be affected by inbreeding depression through a severe bottleneck. The conservation and expansion of their breeding grounds, and effective protection from bycatch mortality in foraging areas are important for the future survival of this species.     

Influences of status and recent breeding experience on the moult strategy of the yellow-nosed albatross Diomedea chlororhynchos

The primary moult of individually colour-ringed, adult yellow-nosed albatrosses at nests on Gough Island was examined in 1983 and related to the status of each bird and its breeding history in the previous year. Adults renew only about half of their primaries each winter and suspend moult while breeding. Birds that bred successfully renewed fewer primaries than did unsuccessful birds or nonbreeders. There were no differences in primary moult between the sexes or in relation to size. Yellow-nosed albatrosses show complex wave moult as an adaptation to slow renewal of flight feathers. The energy, nutrient or time requirements for feather renewal may conflict with breeding annually so that there is a trade-off between the extent of moult desirable to maintain flight efficiency and the benefits of breeding in successive seasons.     

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.     

Notes on New Zealand mammals 8. Predation on nesting southern royal albatrosses Diomedea epomophora by a New Zealand sea lion Phocarctos hookeri

Abstract

This note documents unusual predation of southern royal albatrosses Diomedea epomophora on land by an individual New Zealand sea lion Phocarctos hookeri. During a survey of albatross nests on Campbell Island in the New Zealand sub‐antarctic in January 2005, 128 corpses of adult albatrosses were found at or near nests within a 230 ha area. Flattened vegetation and flipper prints near the nests suggested sea lion predation, and subsequently a male sea lion was found near a line of freshly killed birds. The predation rate was estimated to be at least seven birds per day over a number of weeks; similar skeletal remains from the previous year were observed in a neighbouring area. The impact of one threatened species on another can be a dilemma for conservation managers. In this case, apparently only one male sea lion was involved and, because of the ongoing impact to the albatross population, permission was obtained to cull that individual on 17 January 2005. No further incidents were observed over the following three seasons (2006–08).     

Species delimitation and the origin of populations in island representatives of Phylica (Rhamnaceae)

Abstract Relationships between the closely related island species of Phylica (Rhamnaceae) and a mainland species, P. paniculata , were elucidated using amplified fragment length polymorphisms (AFLPs). Parsimony, neighbor joining, and principal coordinate (PCO) analyses indicated that each of the species studied is distinct. AFLPs were also useful in elucidating the genetic relationships and possible infraspecific origins of different island populations in the Atlantic and Indian Oceans. Phylica nitida on Réunion is likely to have been derived from P. nitida on Mauritius. Although the sampling on New Amsterdam is not extensive, the data are also consistent with the hypothesis that P. arborea on New Amsterdam was derived from a single colonization of P. arborea from Gough Island. Similarly, the Gough Island population appears to have been derived from a single colonization event, but it is so distinct from those on Tristan da Cunha, that there may have been two separate dispersals to Gough and Tristan/Nightingale from different lines of the mainland progenitor. There is also evidence of a recolonization from Gough to Tristan da Cunha. Thus, Phylica arborea is capable of repeated long distance dispersal, up to 8000 km, even though the fruits and seeds are not of a type normally associated with this phenomenon.     

Long distance breeding dispersal of a southern elephant seal

Southern elephant seals range extensively during regular foraging excursions. Despite this they are highly philopatric and long range dispersal is rare. At Gough Island, southern Atlantic Ocean, we observed a breeding adult male elephant seal during September 2009, which had been tagged on its natal beach at Marion Island, southern Indian Ocean, in November 1998. The individual was resighted only once on Marion Island, 6 months after tagging. This 3,860 km movement represents dispersal (and likely gene flow) between distinct populations from different elephant seal geographical provinces. Given the polygynous breeding system of this species, the presence of this single male may have a disproportionate genetic effect on the small number of southern elephant seals breeding at Gough Island.     

Effects of Climate Change and Fisheries Bycatch on Shy Albatross (Thalassarche cauta) in Southern Australia

The impacts of climate change on marine species are often compounded by other stressors that make direct attribution and prediction difficult. Shy albatrosses (Thalassarche cauta) breeding on Albatross Island, Tasmania, show an unusually restricted foraging range, allowing easier discrimination between the influence of non-climate stressors (fisheries bycatch) and environmental variation. Local environmental conditions (rainfall, air temperature, and sea-surface height, an indicator of upwelling) during the vulnerable chick-rearing stage, have been correlated with breeding success of shy albatrosses. We use an age-, stage- and sex-structured population model to explore potential relationships between local environmental factors and albatross breeding success while accounting for fisheries bycatch by trawl and longline fisheries. The model uses time-series of observed breeding population counts, breeding success, adult and juvenile survival rates and a bycatch mortality observation for trawl fishing to estimate fisheries catchability, environmental influence, natural mortality rate, density dependence, and productivity. Observed at-sea distributions for adult and juvenile birds were coupled with reported fishing effort to estimate vulnerability to incidental bycatch. The inclusion of rainfall, temperature and sea-surface height as explanatory variables for annual chick mortality rate was statistically significant. Global climate models predict little change in future local average rainfall, however, increases are forecast in both temperatures and upwelling, which are predicted to have detrimental and beneficial effects, respectively, on breeding success. The model shows that mitigation of at least 50% of present bycatch is required to offset losses due to future temperature changes, even if upwelling increases substantially. Our results highlight the benefits of using an integrated modeling approach, which uses available demographic as well as environmental data within a single estimation framework, to provide future predictions. Such predictions inform the development of management options in the face of climate change.     

Speciation chronology of rockhopper penguins inferred from molecular, geological and palaeoceanographic data

Aim The Southern Ocean is split into several biogeographical provinces between convergence zones that separate watermasses of different temperatures. Recent molecular phylogenies have uncovered a strong phylogeographic structure among rockhopper penguin populations, Eudyptes chrysocome sensu lato, from different biogeographical provinces. These studies suggested a reclassification as three species in two major clades, corresponding, respectively, to warm, subtropical and cold sub‐Antarctic watermasses rather than to geographic proximity. Such a phylogeographic pattern, also observed in plants, invertebrates and fishes of the Southern Ocean, suggests that past changes in the positions of watermasses may have affected the evolutionary history of penguins. We calculated divergence times among various rockhopper penguin clades and calibrated these data with palaeomagmatic and palaeoceanographic events to generate a speciation chronology in rockhopper penguins. Location Southern Ocean. Methods Divergence times between populations were calculated using five distinct mitochondrial DNA loci, and assuming a molecular clock model as implemented in mdiv . The molecular evolution rate of rockhopper penguins was calibrated using the radiochronological age of St Paul Island and Amsterdam Island in the southern Indian Ocean. Separations within other clades were correlated with palaeoceanographic data using this calibrated rate. Results The split between the Atlantic and Indian populations of rockhopper penguins was dated as 0.25 Ma, using the date of emergence of St Paul and Amsterdam islands, and the divergence between sub‐Antarctic and subtropical rockhopper penguins was dated as c. 0.9 Ma (i.e. during the mid‐Pleistocene transition, a major change in the Earth’s climate cycles). Main conclusions The mid‐Pleistocene transition is known to have caused a major southward shift in watermasses in the Southern Ocean, thus changing the environment around the northernmost rockhopper penguin breeding sites. This ecological isolation of northernmost populations may have caused vicariant speciation, splitting the species into two major clades. After the emergence of St Paul and Amsterdam islands in the subtropical Indian Ocean 0.25 Ma, these islands were colonized by penguins from the subtropical Atlantic, 6000 km away, rather than by penguins from the sub‐Antarctic Indian Ocean, 5000 km closer.     

Environmental heterogeneity and the evolution of foraging behaviour in long ranging greater albatrosses

Habitat selection in heterogeneous environments is assumed to allow diversification. Wide‐ranging species like pelagic seabirds present a paradox, in that their diversity appears difficult to reconcile with a frequent lack of geographical isolation between populations. We studied the foraging strategies of three closely related species of greater albatrosses, wandering albatross, Diomedea exulans, Amsterdam albatrosses D. amsterdamensis and royal albatross, D. epomophora, in relation to environmental heterogeneity at coarse‐grained and fine‐grained scales. During the incubation period the three species foraged at long distances from their colonies. We observed significant differences between the species in the duration of foraging trips and the distance travelled per day. There were significant differences in preference for habitat types in relation to bathymetric features, and in chlorophyll a concentrations in the waters traversed. Royal albatross preferred shallower waters (<1500 m depth), which were rich in chlorophyll (>0.5 mg/m³), while the other species spent on average 80% of their time in waters deeper than this, where chlorophyll levels were lower. Wandering albatrosses foraged in colder waters than Amsterdam albatrosses. Patterns of activity divided the species into two groups: those exploiting oceanic habitats (wandering and Amsterdam albatrosses) spent high proportions of time on the water (49%), and had on average 1.35 takeoffs and landings per hour, while royal albatross, which foraged mainly over neritic waters spent only 35% of their time sitting on the water, and made on average 2.6 takeoff per hour. Further, royal albatross showed a similar pattern of activity during all periods of the day, while wandering and Amsterdam albatrosses were mostly inactive during the night. We link these differences in activity to prey patch availability in two contrasting habitats – continental shelf areas compared to open ocean habitats. The divergent styles of foraging observed in this study suggest that these closely‐related and wide‐ranging species could effectively co‐exist by dividing the resources available to them by different modes of exploitation.     

The Evangelistas Islets,Chile: a new breeding site for black-browed albatrosses

A previously undescribed population of black-browed albatrosses (Thalassarche melanophrys) is reported at the Evangelistas Islets, Straits of Magellan, Chile. The population was censused from aerial photographs taken on 13 October 2002 that yielded an estimate of the number of breeding pairs. A combined total of 4,670 pairs of black-browed albatrosses were found nesting at Elcano and Lobos Islets, 2 of the 4 islets in the Evangelistas group. This new record raises to four the number of breeding islands of this albatross species in Chile.     

Surviving with low genetic diversity: the case of albatrosses

Low genetic diversity is predicted to negatively impact species viability and has been a central concern for conservation. In contrast, the possibility that some species may thrive in spite of a relatively poor diversity has received little attention. The wandering and Amsterdam albatrosses (Diomedea exulans and Diomedea amsterdamensis) are long-lived seabirds standing at an extreme along the gradient of life strategies, having traits that may favour inbreeding and low genetic diversity. Divergence time of the two species is estimated at 0.84 Myr ago from cytochrome b data. We tested the hypothesis that both albatrosses inherited poor genetic diversity from their common ancestor. Within the wandering albatross, per cent polymorphic loci and expected heterozygosity at amplified fragment length polymorphisms were approximately one-third of the minimal values reported in other vertebrates. Genetic diversity in the Amsterdam albatross, which is recovering from a severe bottleneck, was about twice as low as in the wandering albatross. Simulations supported the hypothesis that genetic diversity in albatrosses was already depleted prior to their divergence. Given the generally high breeding success of these species, it is likely that they are not suffering much from their impoverished diversity. Whether albatrosses are unique in this regard is unknown, but they appear to challenge the classical view about the negative consequences of genetic depletion on species survival.     

Molecular provenance analysis for shy and white-capped albatrosses killed by fisheries interactions in Australia, New Zealand, and South Africa

Shy and white-capped albatrosses, Thalassarche cauta and T. steadi, respectively, are phenotypically similar and are known to suffer fisheries-related bycatch mortality across their foraging range. Assessments of the extent or scale of impact of bycatch mortality on these species have previously been precluded by difficulties identifying bycatch carcasses to species level. In this study, a fast and simple molecular test based on a single nucleotide polymorphism in mtDNA of shy and white-capped albatrosses was used to determine the species composition of fisheries bycatch carcasses recovered from Australian, New Zealand, and South African waters. The only area where bycatch mortality of both species co-occurred was in Tasmanian waters; in all other zones the bycatch was exclusively comprised of white-capped albatrosses. Genotypic provenance assignment tests of shy albatrosses, a species with significant genetic structure between island colonies, correctly assigned 72% to their island of origin. These data are the first to provide insight into the relative vulnerability of shy and white-capped albatrosses to bycatch mortality across their foraging range, and to establish the vast differences in the at-sea distributions of these two species.     

Field metabolic rates of black-browed albatrosses Thalassarche melanophrys during the incubation stage

Field metabolic rates (FMR) and activity patterns of black-browed albatrosses Thalassarche melanophrys were measured while at sea and on nest during the incubation stage at Kerguelen Island, southwestern Indian Ocean. Activity-specific metabolic rates of five albatrosses at sea (FMR_at-sea) were measured using doubly labeled water (DLW), and by equipping birds with wet-dry activity data loggers that determined when birds were in flight or on the water. The metabolic rates of four birds incubating their eggs (FMR_on-nest) were also measured using DLW. The mean±SD FMR_at-sea of albatrosses was 611±96 kJ kg⁻¹ d⁻¹ compared to FMR_on-nest of 196±52 kJ kg⁻¹ d⁻¹. While at sea, albatrosses spent 52.9±8.2% (N=3) of their time in flight and they landed on the water 41.2±13.9 times per day. The FMR of black-browed albatrosses appear to be intermediate to that of three other albatross species. Based on at-sea activity, the power requirement of flight was estimated to be 8.7 W kg⁻¹ (or 4.0×predicted BMR), which is high compared to other albatross species, but may be explained by the high activity levels of the birds when at sea. The FMR_at-sea of albatrosses, when scaled with body mass, are lower than other seabirds of similar body size, which probably reflects the economical nature of their soaring flight.     

Demographic history of a recent invasion of house mice on the isolated Island of Gough

Island populations provide natural laboratories for studying key contributors to evolutionary change, including natural selection, population size and the colonization of new environments. The demographic histories of island populations can be reconstructed from patterns of genetic diversity. House mice (Mus musculus) inhabit islands throughout the globe, making them an attractive system for studying island colonization from a genetic perspective. Gough Island, in the central South Atlantic Ocean, is one of the remotest islands in the world. House mice were introduced to Gough Island by sealers during the 19th century and display unusual phenotypes, including exceptionally large body size and carnivorous feeding behaviour. We describe genetic variation in Gough Island mice using mitochondrial sequences, nuclear sequences and microsatellites. Phylogenetic analysis of mitochondrial sequences suggested that Gough Island mice belong to Mus musculus domesticus, with the maternal lineage possibly originating in England or France. Cluster analyses of microsatellites revealed genetic membership for Gough Island mice in multiple coastal populations in Western Europe, suggesting admixed ancestry. Gough Island mice showed substantial reductions in mitochondrial and nuclear sequence variation and weak reductions in microsatellite diversity compared with Western European populations, consistent with a population bottleneck. Approximate Bayesian computation (ABC) estimated that mice recently colonized Gough Island (~100 years ago) and experienced a 98% reduction in population size followed by a rapid expansion. Our results indicate that the unusual phenotypes of Gough Island mice evolved rapidly, positioning these mice as useful models for understanding rapid phenotypic evolution.     

Reproductive endocrinology of the Black-browed albatross Diomedea melanophris and the Grey-headed albatross D. chrysostoma

Gonadal size and the circulating concentrations of two pituitary hormones (luteinizing hormone and prolactin) and three gonadal steroids (testosterone, progesterone and oestradiol-17β) were measured in two closely related Diomedea albatrosses at South Georgia. The Grey-headed albatross D. chrysostoma , if successful in rearing a chick, usually breeds biennially, whilst the Black-browed albatross D. melanophris normally breeds annually. Direct examination (by laparoscopy) of the gonads showed that the testes of both species underwent annual cycles, whilst endocrine data confirmed that those male Grey-headed albatrosses at the colony in the pre-laying period but not breeding in that year (having bred successfully the previous year) were apparently in full reproductive condition with elevated testosterone levels typical of breeding birds. However, the females of the two species differed markedly. Grey-headed albatrosses, in a year following successful breeding, had undeveloped ovaries with low levels of circulating oestradiol but high levels of progesterone, whereas the Black-browed albatrosses showed a pattern consistent with annual ovarian development. The profiles of gonadal steroids through the breeding season were similar for the males of both species but differences existed between the females. In the female Grey-headed albatrosses, transient peaks of progesterone were present throughout chick rearing but these were absent from Black-browed albatrosses. Prolactin had a similar profile in both species, with uniformly high levels throughout incubation and a rapid fall near the end of the brood-guard period. It is suggested that Grey-headed, like Black-browed, albatrosses are intrinsically annual breeders. However, if a female Grey-headed albatross breeds successfully in one year, then nutritional factors operate to ensure that in the following year the female does not show ovarian development, although the ovary is active in terms of progesterone secretion.     

A northern rockhopper penguin unveils dispersion pathways in the Southern Ocean

We report the first record of a northern rockhopper penguin Eudyptes moseleyi on the Kerguelen Islands, Southern Indian Ocean. The penguin must have crossed the subtropical convergence to reach the island. This species was recently proved to be genetically different from the subantarctic eastern rockhopper penguin E. filholi that normally breeds on the Kerguelen Islands. The sequencing of a part of the mitochondrial control region shows that this bird may come from the population of Gough Island, 6,000 km away, in the south Atlantic Ocean. This finding confirms that the genetic isolation between these two penguin species is complete, although some individuals may sporadically disperse between the breeding sites. This first direct observation of a disperser from the Atlantic to the Indian Ocean also adds further support to a biogeographic dispersion pattern already suggested by phylogeographic patterns in other species from the Southern Ocean.