Procellariiform Species Research Articles

Unusual Mass Stranding of Atlantic Yellow-Nosed Albatross (Thalassarche chlororhynchos), Petrels and Shearwaters in Southern Brazil

Abstract. Mass strandings of seabirds occur frequently on many beaches worldwide and commonly involve penguins, petrels, shearwaters, and prions, among others. Large numbers of stranded albatrosses are rarely reported. In this paper, an unusual stranding event that involved five species of Procellariiformes, predominantly the Atlantic Yellow-nosed Albatross (Thalassarche chlororhynchos), is described in southern Brazil. Carcasses and debilitated specimens of Atlantic Yellow-nosed Albatrosses (n = 125), unidentified petrels/shearwaters (Procellariidae; n = 63), White-chinned Petrels (Procellaria aequinoctialis; n = 52), Great Shearwaters (Puffinus gravis; n = 11), Manx Shearwaters (Puffinus puffinus; n = 4) and Cory's Shearwater (Calonectris borealis; n = 1) were found stranded between 15 and 22 March 2013. Atlantic Yellow-nosed Albatrosses (n = 20) and White-chinned Petrel (n = 1) were found alive and remained in the rehabilitation center for a few days before being released. A total of at least 256 birds...

Release of constraints on nest-site selection in burrow-nesting petrels following invasive rat eradication

Introduced mammals have been eradicated from many offshore islands around the world, removing predation pressure from burrow-nesting seabirds and other affected wildlife. Nest-site selection in procellariiform seabirds is mediated by nesting habitat characteristics and social information, although it is unclear if, or how, nest-site selection will affect post-eradication colony growth. Using a Bayesian hierarchical modeling approach we assessed how nest-site selection differs among burrow-nesting seabird colonies at different stages of recovery after Pacific rat (Rattus exulans) eradication. We compared nest-site selection in a community of seven procellariiform species among six offshore islands in northeastern New Zealand: four designated rat-free over a continuum within the last 26 years, an island which never had rats, and an island with rats present. We hypothesized that, immediately after eradication, birds would be constrained to nesting habitat where they were less vulnerable to predation, and as time since eradication increased birds would eventually spread to new habitat. We found a positive relationship between mean burrow density and time since rat eradication. Soil depth was the most important predictor of burrow presence, abundance, and occupancy in plots among islands, with more burrows found in deeper soil. We found that the relationships between habitat covariates and nest-site selection decreased with increasing time since eradication. The probability of a covariate having a significant effect on nest-site selection decreased with increasing time since eradication and decreasing variability in the covariate across an island. Our results suggest that the eradication of rodents reduced constraints on petrel nesting distribution and that nest-site selection in burrow-nesting petrels may be influenced by burrow density, where selection of particular nesting habitat characteristics may be relatively more important in small recovering populations. We conclude that colony expansion immediately after predator removal is complex, influenced by numerous interacting factors, but may be partly limited by the availability of suitable nesting habitat.

Interspecific variations in the faecal microbiota ofProcellariiformseabirds

Despite the enormous amount of data available on the importance of gut microbiota in vertebrates (especially mammals), there is no information available on the microbiota of seabirds. Procellariiformes are long-lived seabirds that consume a diet high in lipids and are characterised by their ability to produce and store large amount of stomach oils through the partial digestion of prey (with the exception of the Pelecanoididae). Examining the faecal microbiota of three Procellariiform species (short-tailed shearwater, common diving petrel and fairy prion) provided a unique opportunity to not only characterise the gastrointestinal (GI) microbial composition of seabirds but to also examine the influence of stomach oils on the microbial community. The results indicated that Procellariiform seabirds host a highly diverse community of faecal microorganisms, dominated by three phyla (Firmicutes, Proteobacteria and Bacteroidetes) and that each species has its own species-specific GI microbiota. In addition, significant differences were observed in the microbial communities of oil-producing and non-oil-producing seabirds. This study is the first whole-community examination and classification of the faecal microbiota of Procellariiform seabirds.

Importance of accounting for phylogenetic dependence in multi-species mark–recapture studies

Species in comparative demography studies often have a common phylogenetic or evolutionary ancestry and hence, they cannot fully be treated as independent samples in the statistical analysis. Although the serious implication of ignoring phylogeny has long been recognized, no attempt has been made so far to account for the lack of statistical independence due to phylogeny in multi-species mark–recapture comparative demography studies. In this paper, we propose a Bayesian hierarchical model that explicitly accounts for phylogenetic dependence among species, and to correct for imperfect detection, which is a common phenomenon in free-ranging species. We illustrate the method using individual mark–recapture data collected from 16 seabird species of the order Procellariiformes. Data on body mass and phylogeny of these species are compiled from literature. We investigate the relationship between adult survival and body mass with and without accounting for phylogeny. If we ignore phylogeny, we obtain a positive survival–body mass relationship. However, this relationship is no longer statistically significant once phylogenetic dependence is taken into account, implying that survival may actually depend on an unmeasured variable that is correlated with body mass due to a shared dependence on phylogeny. The proposed model allows the integration of multi-species mark–recapture data and phylogenetic information, and it is therefore a valuable tool in ecological and evolutionary biology.

Delimiting shades of gray: phylogeography of theNorthernFulmar,Fulmarus glacialis

The Northern Fulmar (Fulmarus glacialis) is a common tube-nosed seabird with a disjunct Holarctic range. Taxonomic divisions within the Northern Fulmar have historically been muddled by geographical variation notably including highly polymorphic plumage. Recent molecular analyses (i.e., DNA barcoding) have suggested that genetic divergence between Atlantic and Pacific populations could be on par with those typically observed between species. We employ a multigene phylogenetic analysis to better explore the level of genetic divergence between these populations and to test an old hypothesis on the origin of the modern distribution of color morphs across their range. Additionally, we test whether mutations in the melanocortin-1 receptor gene (MC1R) are associated with dark plumage in the Northern Fulmar. We confirmed that mitochondrial lineages in the Atlantic and Pacific populations are highly divergent, but nuclear markers revealed incomplete lineage sorting. Genetic divergence between these populations is consistent with that observed between many species of Procellariiformes and we recommend elevating these two forms to separate species. We also find that MC1R variation is not associated with color morph but rather is better explained by geographical divergence.

Back home at night or out until morning? Nycthemeral variations in homing of anosmic Cory's shearwaters in a diurnal colony

Olfactory cues have been shown to be important to homing petrels at night, but apparently those procellariiform species that also come back to the colony during the day are not impaired by smell deprivation. However, the nycthemeral distribution of homing, i.e. whether displaced birds released at night return to their burrow by night or during daylight, has never been investigated. To explore this question, we studied the homing behaviour of Cory's shearwater (Calonectris borealis) in the only known population where these birds are active at the colony both during the day and at night. Here, we compared the nocturnal versus diurnal homing schedule of birds treated with zinc sulphate (to induce a reversible but complete anosmia) with that of controls. Our results show that anosmic shearwaters were unable to home in the dark and were constrained to wait for the daylight to find their burrow again. Our results confirm that olfaction is the basic sensory input for homing by night even in a petrel species that is diurnally active at the colony.

Foraging over Sargassum by Western North Atlantic Seabirds

Drifting reefs of Sargassum (a brown alga) are used by a variety of pelagic seabirds in the western Atlantic Ocean. We examined gut contents from 964 individuals of 39 seabird species collected 5 to 60 km off the coast of North Carolina for evidence of Sargassum use. Sargassum pieces or Sargassum-associated prey were found in nine of 10 Procellariiformes species and less frequently among Charadriiformes (12 of 25 species). No Sargassum-associated prey was found in Pelecaniformes examined, but observational data indicated that Atlantic tropicbirds (Phaethon lepturus and P. aethereus) and Masked Boobies (Sula dactylatra) commonly foraged over Sargassum. Four species were considered Sargassum specialists, having frequencies of occurrence >25% and high volumes of Sargassum-associated prey: Audubon's Shearwater (Puffinus lherminieri), Royal Tern (Thalasseus maximus), Bridled Tern (Onychoprion anaethetus), and Red-necked Phalarope (Phalaropus lobatus). Seven species fed in Sargassum to a lesser extent, and nine species had ingested Sargassum pieces, but contained no Sargassum-associated prey. It is likely that other seabird species forage regularly over Sargassum, as our conclusions are based on relatively small sample sizes taken during random sampling in the open ocean. Our conservative analysis and extensive observational data indicate the Sargassum community is critical for feeding for some western North Atlantic seabirds. Degradation of Sargassum habitats by oil development, harvest, and/or ocean acidification would undoubtedly have negative effects on fitness of these birds.

Assessing the location and stability of foraging hotspots for pelagic seabirds: An approach to identify marine Important Bird Areas (IBAs) in Spain

Protected areas play a key role in the preservation of biodiversity, but their implementation at sea is lagged behind terrestrial environments, especially in offshore areas. Here we describe the identification of foraging hotspots off the Mediterranean Iberian coast using three Procellariiform species as examples, and assess the stability of these sites. Then, we show how these foraging hotspots contributed to the delimitation of marine Important Bird Areas (IBAs). The whole process consisted of: (1) seabird data collection (extensive boat-based surveys and seabird tracking, conducted in 1999–2010) and compilation of relevant spatial descriptors of the marine environment; (2) species distribution modeling (SDM) aimed at identifying areas with high habitat quality for the different seabird species (3); identification and delineation of the main seabird hotspots, based on models, supported by direct seabird data, and mediated by expert opinion; (4) application of BirdLife International IBA criteria for hotspot validation; and (5) combination of hotspots from different species to set the final limits of the marine IBAs. This approach allowed to identify a series of hotspots for pelagic species in the study area, and provided nice examples of stability assessment, which slightly differed in performance between seabird species. They contributed to the Spanish marine IBA inventory, which is in the process of receiving legal protection. Future work should be directed at confirming the stability of the marine IBAs in the long term, and to address the development of management plans to make effective the protection of these sites.

Assessment of Trace Metal Concentrations in Feathers of White-chinned Petrels, Procellaria Aequinoctialis, from the Patagonian Shelf

Cd, Cr, Cu, Fe, Ni, Pb, and Zn were measured in feathers from male and female White-chinned petrels Procelllaria aequinoctialis accidentally killed in longliners off Argentina in 2005. Cd, Pb, and Ni concentrations in adult feathers were below detection limits regardless of the birds' sex. Metal concentrations did not vary with sex for Cu, Fe and Zn in feathers of adult birds despite significant differences in body size between males and females. The Cu and Fe concentrations differed significantly between the type of feather within individual birds. The mean concentrations of metals determined here were within the range of concentrations reported in feather tissues of other related Procellariiformes species from different biogeographic areas. However, the concentrations of Cr were similar to those reported for other petrels from polluted areas of the North Pacific. Thus, it appears likely that levels of pollution in Patagonia may not be as negligible as previously thought for some trace metals.

Maternal antibody persistence: a neglected life-history trait with implications from albatross conservation to comparative immunology.

The evolution of different life-history strategies has been suggested as a major force constraining physiological mechanisms such as immunity. In some long-lived oviparous species, a prolonged persistence of maternal antibodies in offspring could thus be expected in order to protect them over their long growth period. Here, using an intergenerational vaccination design, we show that specific maternal antibodies can display an estimated half-life of 25 days post-hatching in the nestlings of a long-lived bird. This temporal persistence is much longer than previously known for birds and it suggests specific properties in the regulation of IgY immunoglobulin catabolism in such a species. We also show that maternal antibodies in the considered procellariiform species are functional as late as 20 days of age. Using a modelling approach, we highlight that the potential impact of such effects on population viability could be important, notably when using vaccination for conservation. These results have broad implications, from comparative immunology to evolutionary eco-epidemiology and conservation biology.

Organochlorine contaminants in albatrosses and petrels during migration in South Atlantic Ocean

Albatrosses and petrels (Procellariiformes) are migratory oceanic birds of considerable conservational interest. Polychlorinated biphenyls (PCBs) and organochlorine pesticides (OCPs) were assessed in the subcutaneous fat, liver and muscle of 100 birds belonging to eight species of Procellariiformes collected during their migration period in southern Brazil, one of the most important feeding areas for these species. Although the profiles of PCBs and OCPs were similar among the individuals, with predominance of penta, hexa and heptachlorobiphenyls and p′p-DDE, organochlorine concentrations exhibited a high degree of intra-species variability. The influence of body condition during the migration period in the distribution of organochlorine contaminants was also evaluated, showing that it is a significant factor in the variation and redistribution of these compounds in the tissues of these birds. The intense use of lipid reserves associated to the contamination from organochlorine compounds could be a troubling factor for seabirds with extended breeding periods and that spend most of their lives at sea migrating long distances, such as most of Procellariiformes. Studies on contamination are necessary to improve the knowledge of the threats to these birds and their populations as well as to contribute with information about persistent organic pollutants in the South Atlantic marine environment.

New haematological data in Cory's shearwater, Calonectris diomedea (Aves, Procellariiformes)

Haematology can provide useful information to assess the health of free-ranging animals. In seabirds, many procellariiform (albatrosses and petrels) species undertake long-distance migrations during which individuals may get in contact with birds and pathogens of different biogeographic origin. Although checking whether procellariiformes might play a role in large-scale spread of diseases is desirable, haematological data have been published in very few species. For the first time, we determined blood cell counts in Cory's shearwater, Calonectris diomedea, a petrel which breeds in the western Palearctic but overwinters off Brazil and South Africa. Forty-five adult Cory's shearwaters were captured in their burrows in the Azores archipelago during the pre-laying period in March 2008, measured, weighed, and a blood sample was taken from each of them. Haematocrit, polychromasia, leukocyte and thrombocyte counts did not differ significantly between sexes, but total leukocyte number was significantly (positively) correlated with body condition.

Trophic versus geographic structure in stable isotope signatures of pelagic seabirds breeding in the northeast Atlantic

Feeding ecology and geographic location are 2 major factors influencing animal stable isotope sig- natures, but their relative contributions are poorly un- derstood, which limits the usefulness of stable isotope analysis in the study of animal ecology. To improve our knowledge of the main sources of isotopic variability at sea, we determined δ 15 N and δ 13 C signatures in the first primary feather of adult birds from 11 Procellariiform species (n = 609) across 16 northeast Atlantic localities, from Cape Verde (20° N) to Iceland (60° N). Post-breed- ing areas (where the studied feather is thought to be grown) were determined using light-level geolocation for 6 of the 11 species. Isotopic variability was geograph- ically unstructured within the mid-northeast Atlantic (Macaronesian archipelagos), but trophically structured according to species and regardless of the breeding location, presumably as a result of trophic segregation among species. Indeed, the interspecific isotopic overlap resulting from combining δ 15 N and δ 13 C signatures of seabirds was low, which suggests that most species ex- ploited exclusive trophic resources consistently across their geographic range. Species breeding in north tem- perate regions (Iceland, Scotland and Northern Ireland) showed enriched δ 15 N compared to the same or similar species breeding in tropical and subtropical regions, suggesting some differences in baseline levels between these regions. The present study illustrates a noticeable trophic segregation of northeast Atlantic Procellari- iformes. Our results show that the isotopic approach has limited applicability for the study of animal movements in the northeast Atlantic at a regional scale, but is poten- tially useful for the study of long-distance migrations between large marine systems.

Recoveries of juvenile Giant Petrels in regions of ocean productivity: potential implications for population change

Explaining long-term population change for migratory seabirds such as Giant Petrels (Macronectes spp.) has proven elusive because only aspects of adult life-histories have been studied. There is a paucity of demographic data for juveniles however; there is a considerable amount of leg-band recovery location data for younger age-classes. Nestlings were leg-banded at two sub-Antarctic islands, and at two higher latitude Antarctic breeding colonies. Bands were most often recovered in winter within six months of liberation. Banded fledglings were recovered in known productive upwelling biomes. The birds had travelled between 350 and 6150 km downwind from their natal colonies to reach these biomes. The distances fledglings travelled to reach the biomes were correlated with the observed population trends at their natal colonies; negative/positive population trends were correlated with great/lesser distances travelled. This study highlights the potential importance juvenile life-history attributes when considering population change for long-lived seabird species, and identifies rich upwelling regions such as the Humboldt and Benguelen Currents that might be important foraging areas for this and other Procellariiform species with high conservation values.

New Skeleton from the Early Oligocene of Germany Indicates a Stem-Group Position of Diomedeoidid Birds

We report a new specimen of the extinct procellariiform species Diomedeoides brodkorbi (Aves, Diomedeoididae) from the early Oligocene (Rupelian) of Rheinweiler in southwestern Germany. The well-preserved partial skeleton allows the recognition and reassessment of new osteological details that bear on the phylogenetic affinities of diomedeoidids. The presence on the coracoid of a deeply excavated, cup-like facies articularis for the scapula suggests a stem group position of the Diomedeoididae within Procellariiformes, because this trait also occurs in stem-group representatives of several avian groups, as well as in Mesozoic non-neornithine birds, and is a plesiomorphic character. We hypothesize that the similarities of Diomedeoides to extant southern storm-petrels (Oceanitinae), such as the long mandibular symphysis, the small processus supracondylaris dorsalis and the long legs are plesiomorphic for Procellariiformes.

Polychlorinated biphenyls and organochlorine pesticides in plastics ingested by seabirds

The occurrence of plastic objects in the digestive tract was assessed in eight species of Procellariiformes collected in southern Brazil and the occurrence of polychlorinated biphenyls (PCBs) and organochlorine pesticides (OCPs) in the ingested plastics pellets and plastic fragments was evaluated. PCBs were detected in plastic pellets (491ngg−1) and plastic fragments (243–418ngg−1). Among the OCPs, p,p′-DDE had the highest concentrations, ranging from 68.0 to 99.0ngg−1. The occurrence of organic pollutants in post-consumer plastics supports the fact that plastics are an important source carrying persistent organic pollutants in the marine environment. Although transfer through the food chain may be the main source of exposure to POPs to seabirds, plastics could be an additional source for the organisms which ingest them, like Procellariiformes which are the seabirds most affected by plastic pollution.

Ambient, productive and wind energy, and ocean extent predict global species richness of procellariiform seabirds

ABSTRACTAims Tests of the energy hypothesis for the large‐scale distribution of species richness have largely been concerned with the influence of two alternative forms of environmental energy, temperature and energy from primary productivity, both of which (at least in terrestrial systems) peak within the tropics. Taxa showing extra‐tropical diversity peaks present a potential challenge to the generality of species–energy theory. One such group are pelagic seabirds of the order Procellariiformes that show not only an extra‐tropical diversity peak but one confined to the Southern Ocean, hence a highly asymmetric one. They are distinct in being exceptionally adapted to take advantage of wind energy, which they may rely on for long‐distance ocean foraging for the patchy resources needed to meet their energetic needs. Wind represents a readily available source of kinetic energy, shows a strong latitudinal gradient, and has been largely omitted from species–energy theory. Moreover, maximal benefits of wind are likely to be afforded in areas of greatest available contiguous ocean extent. We compare the relative importance of wind speed, ocean productivity (chlorophyll concentration), air temperature and available ocean extent (distance) in explaining large‐scale global distribution of procellariiform species richness across the world's oceans.Location Global, oceanic.Methods Hierarchical partitioning, model selection, ordinary least squares (OLS) and spatial generalized least squares (GLS) regression.Results Hierarchical partitioning of non‐spatial regression models indicates that ocean distance is the most important predictor of procellariiform species richness followed by wind speed and then temperature. In contrast, that of spatial regression models indicates the roughly equal importance of ocean distance and temperature, followed by wind speed. Although contributing additional model fit, ocean productivity is consistently the weakest predictor. Best‐fit models include all four predictors and explain 67% of observed variation. The species–productivity relationship is negative overall, while the species–temperature relationship is hump‐shaped. In contrast, ocean distance and wind speed are positively associated with species richness.Conclusions Large‐scale procellariiform species richness distribution may represent a trade‐off in the use of different energy forms, being highest in Southern Ocean areas where productive energy and temperature are relatively low, but where available ocean foraging extent and wind energy required to utilize it are near‐maximal.

Attraction of petrels to artificial lights in the Canary Islands: effects of the moon phase and age class

The extent and intensity of artificial night lighting has increased with urban development worldwide. The resulting light pollution is responsible for mortality among many Procellariiformes species which show nocturnal activity on their breeding grounds. Here, we report light‐induced mortality of Procellariiformes during a 9‐year study (1998–2006) on Tenerife, the largest island of the Canary archipelago. A total of 9880 birds from nine species were found grounded, the majority being Cory’s Shearwaters Calonectris diomedea (93.4%). For this species the majority of grounded birds were fledglings (96.4%), which fall apparently while leaving their nesting colony for the first time; for the smaller species (storm‐petrels) adult birds were more often grounded than fledglings. For almost all species, grounding showed a seasonal pattern linked with their breeding cycle. Certain phases of the moon influenced grounding of Cory’s Shearwater, with the extent of grounding being reduced during phases of full moon. The percentage of fledglings attracted to lights in relation to the fledglings produced annually varied between species and years (0–1.3% for the Madeiran Storm‐petrel Oceanodroma castro; 41–71% for Cory’s Shearwater). Mean adult mortality rates also varied between species (from 0.4% for the European Storm‐petrel Hydrobates pelagicus and the Cory’s Shearwater, to 2.3% for the Manx Shearwater Puffinus puffinus). Here we show that light‐induced mortality rates are of concern, at least for petrels and small shearwaters. Thanks to efforts involving civil cooperation, 95% of grounded birds have been returned to the wild. To minimize the impact of artificial lights on petrels we recommend several conservation measures: continuing rescue campaigns, alteration of light signatures and reduction of light emissions during the fledging peaks. Furthermore, we recommend that a monitoring program for petrel populations be implemented, as well as further studies to assess the fate of released fledglings and continued research to address why petrels are attracted to lights.

Plastic ingestion by Procellariiformes in Southern Brazil

The Procellariiformes are the birds most affected by plastic pollution. Plastic fragments and pellets were the most frequent items found in the digestive tract of eight species of Procellariiformes incidentally caught by longline fisheries as well as beached birds in Southern Brazil. Plastic objects were found in 62% of the petrels and 12% of the albatrosses. The Great shearwater, Manx shearwater, Cory’s shearwater and Antarctic fulmar were found to have greater quantities and frequencies of occurrence of plastic. There was no significant difference in the number of plastics between the birds from longline fisheries and beached birds. No correlation was found between the number of prey and number of plastics in the digestive tract of the birds analyzed, but this does not discard the hypothesis that, in some cases, the presence of plastic in the digestive tract has a negative effect on the feeding efficiency of these birds.

Differences in stable isotopes in blood and feathers of seabirds are consistent across species, age and latitude: implications for food web studies

Stable isotopes of growing feathers and blood both represent assimilated diet, and both tissues are used to study the diet and foraging distribution of marine and terrestrial birds. Although most studies have assumed that both tissues represent a difference of one trophic level to diet, the enrichment factors of blood and feathers may differ, especially where endogenous reserves are used as precursors during feather synthesis. In this study, we compare carbon and nitrogen stable isotopes of blood and simultaneously growing feathers of five species of Procellariiformes, representing five genera, different geographical regions and different life stages (chicks and adults). In all species, feathers were enriched in 15N and 13C compared with blood. Isotopic values of carbon and nitrogen were correlated in different tissues growing simultaneously for most species analyzed, suggesting that mathematical corrections could be used to compare different tissues. Our results imply that more care needs to be taken when comparing stable isotope signatures across studies assuming different tissues are equivalent indicators of trophic ecology.