Genetic structuring among colonies of a pantropical seabird: Implication for subspecies validation and conservation.

Investigations of the genetic structure of populations over the entire range of a species yield valuable information about connectivity among populations. Seabirds are an intriguing taxon in this regard because they move extensively when not breeding, facilitating intermixing of populations, but breed consistently on the same isolated islands, restricting gene flow among populations. The degree of genetic structuring of populations varies extensively among seabird species but they have been understudied in their tropical ranges. Here, we address this across a broad spatial scale by using microsatellite and mitochondrial data to explore the population connectivity of 13 breeding populations representing the six subspecies of the white-tailed tropicbird (Phaethon lepturus) in the Atlantic, Indian, and Pacific Oceans. Our primary aim was to identify appropriate conservation units for this little known species. Three morphometric characters were also examined in the subspecies. We found a clear pattern of population structuring with four genetic groups. The most ancient and the most isolated group was in the northwestern Atlantic Ocean. The South Atlantic populations and South Mozambique Channel population on Europa were genetically isolated and may have had a common ancestor. Birds from the Indo-Pacific region showed unclear and weak genetic differentiation. This structuring was most well defined from nuclear and mtDNA markers but was less well resolved by morphological data. The validity of classifying white-tailed tropicbirds into six distinct subspecies is discussed in light of our new findings. From a conservation standpoint our results highlight that the three most threatened conservation units for this species are the two subspecies of the tropical North and South Atlantic Oceans and that of Europa Island in the Indian Ocean.

Sex-Specific Habitat Utilization and Differential Breeding Investments in Christmas Island Frigatebirds throughout the Breeding Cycle.

In seabirds, equal bi-parental care is the rule, as it is considered crucial for raising chicks successfully because seabirds forage in an environment with unpredictable and highly variable food supply. Frigatebirds forage in poor tropical waters, yet males reduce and even stop parental care soon after chick brooding, leaving the female to provision the chick alone for an extended fledging period. Using bird-borne tracking devices, male and female Christmas Island Frigatebirds (Fregata andrewsi) were investigated during the brooding, late chick rearing and post-fledging period to examine whether sexes exhibit foraging strategies that may be linked to differential breeding investments. During brooding, males and females showed similar foraging behaviour under average marine productivity of oceanic waters close to the colony, but males shifted to more distant and more productive habitats when conditions deteriorated to continue with reduced chick provisioning. During the late chick rearing period, females progressively increased their foraging range to the more distant but productive marine areas that only males had visited during brooding. Birds spent the non-breeding period roosting in highly productive waters of the Sunda Shelf. The sex-specific utilisation of three different foraging habitats with different primary productivity (oceanic, coastal, and shelf areas) allowed for temporal and spatial segregation in the exploitation of favourable habitats which seems to enable each sex to optimise its foraging profitability. In addition, post-fledging foraging movements of females suggest a biennial breeding cycle, while limited information on males suggests the possibility of an annual breeding cycle.

Infection by Haemoproteus parasites in four species of frigatebirds and the description of a new species of Haemoproteus (Haemosporida: Haemoproteidae).

Among seabirds, the fregatids stand out with a high prevalence of blood parasites. Four of 5 species in this family have been found to be infected with Haemoproteus; however, complete species descriptions with molecular phylogeny are lacking. Seventy-five samples from 4 species of frigatebirds, i.e., Fregata andrewsi, Fregata minor, Fregata magnificens, and Fregata aquila, were screened for infections caused by species of Haemoproteus. Four different parasite haplotypes were found infecting frigatebirds based on the sequencing of a fragment of the cytochrome b gene. Two haplotypes belong to the subgenus Parahaemoproteus, and the other 2 correspond to haplotypes within the subgenus Haemoproteus . The more prevalent and cosmopolitan Parahaemoproteus haplotype (FregPHae1) was phylogenetically grouped with other Haemoproteus parasites infecting non-passerine birds, but it could not be detected from the single sample from F. aquila. The other Parahaemoproteus haplotype (FregPHae2) was not phylogenetically clustered with parasites infecting non-passerine birds, and it was sequenced from a single (1 each) F. andrewsi and F. minor. Blood smears from F. andrewsi infected only by FregPHae1 haplotype showed sufficient gametocytes to allow description of a new species, Haemoproteus valkiunasi sp. nov. In contrast to Haemoproteus iwa, the only previously known blood parasite infecting frigatebirds and described from F. minor from Galapagos Islands, parasites from F. andrewsi (1) are shorter with no contact of gametocyte with host cell membrane, (2) have fewer pigment granules, and (3) have wider microgametocytes, with a smaller host nuclear displacement. In contrast, patent single infections corresponding to the cosmopolitan haplotype of the subgenus Haemoproteus (FregHae1) were also found in samples from 1 F. andrewsi, 1 F. minor, and 1 F. aquila. In all these cases, the number of microgametocytes was very low, resembling H. iwa, which lacks microgametocytes in the original description. Macrogametocytes of haplotype FregHae1 in F. andrewsi differ significantly from all the characteristics measured from H. valkiunasi. In addition, it also differs from all characteristics of H. iwa despite being genetically identical in the analyzed fragment.

Leucocyte profiles and H/L ratios in chicks of Red-tailed Tropicbirds reflect the ontogeny of the immune system.

Immune defence is fundamentally important for the survival prospects of young animals. While innate immunity offers initial protection from a variety of pathogens, acquired immunity responds more specifically to pathogens, but is considered to be more costly and to respond slower. Moreover, the acquired immunity is not yet fully developed in neonatal chicks. Little is known about the ontogeny of the immune system of wild birds. Long-lived seabirds, with their slow chick development, are good models to investigate how young birds invest in both arms of their immune system. We determined leucocyte profiles and heterophil to lymphocyte (H/L) ratios of Red-tailed Tropicbirds (Phaeton rubricauda westralis) on Christmas Island, Indian Ocean. Young chicks (N = 10) had significantly higher H/L ratios than older chicks (N = 19), while adults (N = 47) showed intermediate values and did not differ from either chick age class. High H/L ratios in young chicks were caused by high initial numbers of heterophils per 10,000 erythrocytes that declined with age. In contrast, the number of lymphocytes per 10,000 erythrocytes was similar for young and older chicks. These data suggest that young chicks invested heavily in innate immunity to protect themselves from pathogens, while investment into acquired immunity became more important in older chicks with a functional acquired immune response. Body condition did not have a significant influence on any leucocyte parameter.

Hemosporidian blood parasites in seabirds--a comparative genetic study of species from Antarctic to tropical habitats.

Whereas some bird species are heavily affected by blood parasites in the wild, others reportedly are not. Seabirds, in particular, are often free from blood parasites, even in the presence of potential vectors. By means of polymerase chain reaction, we amplified a DNA fragment from the cytochrome b gene to detect parasites of the genera Plasmodium, Leucocytozoon, and Haemoproteus in 14 seabird species, ranging from Antarctica to the tropical Indian Ocean. We did not detect parasites in 11 of these species, including one Antarctic, four subantarctic, two temperate, and four tropical species. On the other hand, two subantarctic species, thin-billed prions Pachyptila belcheri and dolphin gulls Larus scoresbii, were found infected. One of 28 thin-billed prions had a Plasmodium infection whose DNA sequence was identical to lineage P22 of Plasmodium relictum, and one of 20 dolphin gulls was infected with a Haemoproteus lineage which appears phylogenetically clustered with parasites species isolated from passeriform birds such as Haemoproteus lanii, Haemoproteus magnus, Haemoproteus fringillae, Haemoproteus sylvae, Haemoproteus payevskyi, and Haemoproteus belopolskyi. In addition, we found a high parasite prevalence in a single tropical species, the Christmas Island frigatebird Fregata andrewsi, where 56% of sampled adults were infected with Haemoproteus. The latter formed a monophyletic group that includes a Haemoproteus line from Eastern Asian black-tailed gulls Larus crassirostris. Our results are in agreement with those showing that (a) seabirds are poor in hemosporidians and (b) latitude could be a determining factor to predict the presence of hemosporidians in birds. However, further studies should explore the relative importance of extrinsic and intrinsic factors on parasite prevalence, in particular using phylogenetically controlled comparative analyses, systematic sampling and screening of vectors, and within-species comparisons.