Audrey Jaeger

Patterns of aging in the long-lived wandering albatross

How does an animal age in natural conditions? Given the multifaceted nature of senescence, identifying the effects of age on physiology and behavior remains challenging. We investigated the effects of age on a broad array of phenotypic traits in a wild, long-lived animal, the wandering albatross. We studied foraging behavior using satellite tracking and activity loggers in males and females (age 6–48+ years), and monitored reproductive performance and nine markers of baseline physiology known to reflect senescence in vertebrates (humoral immunity, oxidative stress, antioxidant defenses, and hormone levels). Age strongly affected foraging behavior and reproductive performance, but not baseline physiology. Consistent with results of mammal and human studies, age affected males and females differently. Overall, our findings demonstrate that age, sex, and foraging ability interact in shaping aging patterns in natural conditions. Specifically, we found an unexpected pattern of spatial segregation by age; old males foraged in remote Antarctica waters, whereas young and middle-aged males never foraged south of the Polar Front. Old males traveled a greater distance but were less active at the sea surface, and returned from sea with elevated levels of stress hormone (corticosterone), mirroring a low foraging efficiency. In contrast to findings in captive animals and short-lived birds, and consistent with disposable soma theory, we found no detectable age-related deterioration of baseline physiology in albatrosses. We propose that foraging efficiency (i.e., the ability of individuals to extract energy from their environment) might play a central role in shaping aging patterns in natural conditions.

Wide range of mercury contamination in chicks of southern ocean seabirds.

Using top predators as sentinels of the marine environment, Hg contamination was investigated within the large subantarctic seabird community of Kerguelen Islands, a remote area from the poorly known Southern Indian Ocean. Chicks of 21 sympatric seabirds presented a wide range of Hg concentrations, with the highest contaminated species containing ∼102 times more feather Hg than the less contaminated species. Hence, Kerguelen seabirds encompass the whole range of chick feather Hg values that were previously collected worldwide in poorly industrialized localities. Using stable isotopes, the effects of foraging habitats (reflected by δ13C) and trophic positions (reflected by δ15N) on Hg concentrations were investigated. Species-related Hg variations were highly and positively linked to feather δ15N values, thus highlighting the occurrence of efficient Hg biomagnification processes within subantarctic marine trophic webs. By contrast, Hg contamination overall correlated poorly with feeding habitats, because of the pooling of species foraging within different isotopic gradients corresponding to distinct seabird habitats (benthic, pelagic, neritic and oceanic). However, when focusing on oceanic seabirds, Hg concentration was related to feather δ13C values, with species feeding in colder waters (lower δ13C values) south of Kerguelen Islands being less prone to be contaminated than species feeding in northern warmer waters (higher δ13C values). Within the context of continuous increase in global Hg emissions, Kerguelen Islands that are located far away from anthropogenic sources can be considered as an ideal study site to monitor the temporal trend of global Hg contamination. The present work helps selecting some seabird species as sentinels of environmental pollution according to their high Hg concentrations and their contrasted foraging ecology.

Isotopic investigation of contemporary and historic changes in penguin trophic niches and carrying capacity of the southern Indian ocean.

A temperature-defined regime shift occurred in the 1970s in the southern Indian Ocean, with simultaneous severe decreases in many predator populations. We tested a possible biological link between the regime shift and predator declines by measuring historic and contemporary feather isotopic signatures of seven penguin species with contrasted foraging strategies and inhabiting a large latitudinal range. We first showed that contemporary penguin isotopic variations and chlorophyll a concentration were positively correlated, suggesting the usefulness of predator δ13C values to track temporal changes in the ecosystem carrying capacity and its associated coupling to consumers. Having controlled for the Suess effect and for increase CO2 in seawater, δ13C values of Antarctic penguins and of king penguins did not change over time, while δ13C of other subantarctic and subtropical species were lower in the 1970s. The data therefore suggest a decrease in ecosystem carrying capacity of the southern Indian Ocean during the temperature regime-shift in subtropical and subantarctic waters but not in the vicinity of the Polar Front and in southward high-Antarctic waters. The resulting lower secondary productivity could be the main driving force explaining the decline of subtropical and subantarctic (but not Antarctic) penguins that occurred in the 1970s. Feather δ15N values did not show a consistent temporal trend among species, suggesting no major change in penguins’ diet. This study highlights the usefulness of developing long-term tissue sampling and data bases on isotopic signature of key marine organisms to track potential changes in their isotopic niches and in the carrying capacity of the environment.

Celestial moderation of tropical seabird behavior.

Most animals, including birds, have cyclic life histories and numerous studies generally conducted on captive animals have shown that photoperiod is the main factor influencing this periodicity. Moon cycles can also affect periodic behavior of birds. Few studies have investigated the influence of these environmental cues in natural settings, and particularly in tropical areas where the change in photoperiod is slight and some bird species keep cyclic behaviors. Using miniaturized light sensors, we simultaneously investigated under natural conditions the influence of photoperiod and moon phases on the migration dates and at-sea activity of a tropical seabird species, the Baraus petrel, throughout its annual cycle. Firstly, we found that birds consistently started their pre- and post-breeding migrations at precise dates corresponding in both cases to a day-duration of 12.5 hours, suggesting a strong influence of the photoperiod in the regulation of migration behavior. We also found that mean population arrival dates to the colony changed from year to year and they were influenced by moon phases. Returns at their colonies occurred around the last full moon of the austral winter, suggesting that moon cycle is used by birds to synchronize their arrival. Secondly, variations of day-time activity were sinusoidal and correlated to seasonal changes of daylength. We thus hypothesize that the photoperiod could directly affect the behavior of the birds at sea. Night-time at-sea activity exhibited a clear cycle of 29.2 days, suggesting that nocturnal foraging was highly regulated by moon phase, particularly during the non-breeding season. To our knowledge, this is the first study to document a mixed regulation of the behavior of a wild bird by photoperiod and moon phases throughout its annual cycle.

Age, sex, and breeding status shape a complex foraging pattern in an extremely long‐lived seabird

Evidence of age-dependent changes in foraging behavior of free-ranging individuals is scarce, especially at older stages. Using the isotopic niche as a proxy of the trophic niche during both the breeding (blood) and inter-nesting (feather) periods, we report here empirical evidence for age-, gender-, and breeding status-dependent foraging ecology and examine its potential consequences on subsequent reproduction and survival in an extremely long-lived species, the Wandering Albatross (Diomedea exulans). Immature Wandering Albatrosses of both sexes forage in the subtropics (delta13C) and feed at the same trophic position (delta15N) as the adults. In contrast to immature birds, adult females forage, on average, at more northern latitudes than males, with both sexes feeding in the subtropics during the internesting period, and males, not females, favoring subantarctic waters during incubation. In contrast to adult females, males show a unique pattern among birds and mammals of a continuous change with age in their main feeding habitat by foraging progressively farther south in colder waters during both the breeding and inter-nesting periods. In males, foraging at higher latitudes (lower feather delta13C values) is associated with a lower probability of breeding during the following years compared to other birds, but with no effect on their probability of surviving. Foraging in cold and windy waters may be linked to foraging impairment that might explain different life history trade-offs and lower investment in reproduction with age. This key point requires further longitudinal investigations and/or studies examining foraging success and the energy budget of birds feeding in different water masses.

Massive infection of seabird ticks with bacterial species related to Coxiella burnetii.

ABSTRACT Seabird ticks are known reservoirs of bacterial pathogens of medical importance; however, ticks parasitizing tropical seabirds have received less attention than their counterparts from temperate and subpolar regions. Recently, Rickettsia africae was described to infect seabird ticks of the western Indian Ocean and New Caledonia, constituting the only available data on bacterial pathogens associated with tropical seabird tick species. Here, we combined a pyrosequencing-based approach with a classical molecular analysis targeting bacteria of potential medical importance in order to describe the bacterial community in two tropical seabird ticks, Amblyomma loculosum and Carios (Ornithodoros) capensis. We also investigated the patterns of prevalence and host specificity within the biogeographical context of the western Indian Ocean islands. The bacterial community of the two tick species was characterized by a strong dominance of Coxiella and Rickettsia. Our data support a strict Coxiella-host tick specificity, a pattern resembling the one found for Rickettsia spp. in the same two seabird tick species. Both the high prevalence and stringent host tick specificity suggest that these bacteria may be tick symbionts with probable vertical transmission. Detailed studies of the pathogenicity of these bacteria will now be required to determine whether horizontal transmission can occur and to clarify their status as potential human pathogens. More generally, our results show that the combination of next generation sequencing with targeted detection/genotyping approaches proves to be efficient in poorly investigated fields where research can be considered to be starting from scratch.

Rickettsia spp. in seabird ticks from western Indian Ocean islands, 2011-2012.

We found a diversity of Rickettsia spp. in seabird ticks from 6 tropical islands. The bacteria showed strong host specificity and sequence similarity with strains in other regions. Seabird ticks may be key reservoirs for pathogenic Rickettsia spp., and bird hosts may have a role in dispersing ticks and tick-associated infectious agents over large distances.

Influenza A Virus on Oceanic Islands: Host and Viral Diversity in Seabirds in the Western Indian Ocean

Ducks and seabirds are natural hosts for influenza A viruses (IAV). On oceanic islands, the ecology of IAV could be affected by the relative diversity, abundance and density of seabirds and ducks. Seabirds are the most abundant and widespread avifauna in the Western Indian Ocean and, in this region, oceanic islands represent major breeding sites for a large diversity of potential IAV host species. Based on serological assays, we assessed the host range of IAV and the virus subtype diversity in terns of the islands of the Western Indian Ocean. We further investigated the spatial variation in virus transmission patterns between islands and identified the origin of circulating viruses using a molecular approach. Our findings indicate that terns represent a major host for IAV on oceanic islands, not only for seabird-related virus subtypes such as H16, but also for those commonly isolated in wild and domestic ducks (H3, H6, H9, H12 subtypes). We also identified strong species-associated variation in virus exposure that may be associated to differences in the ecology and behaviour of terns. We discuss the role of tern migrations in the spread of viruses to and between oceanic islands, in particular for the H2 and H9 IAV subtypes.

Absence of coronaviruses, paramyxoviruses, and influenza A viruses in seabirds in the southwestern Indian Ocean.

Abstract We investigated circulation of coronaviruses, paramyxoviruses, and influenza A viruses in eight seabird species of the southwestern Indian Ocean. Viruses were not detected by real-time polymerase chain reactions in the 338 tested cloacal swab samples, supporting that they did not circulate in the studied colonies at the time of sampling.

The role of seabirds of the Iles Eparses as reservoirs and disseminators of parasites and pathogens

Abstract The role of birds as reservoirs and disseminators of parasites and pathogens has received much attention over the past several years due to their high vagility. Seabirds are particularly interesting hosts in this respect. In addition to incredible long-distance movements during migration, foraging and prospecting, these birds are long-lived, site faithful and breed in dense aggregations in specific colony locations. These different characteristics can favor both the local maintenance and large-scale dissemination of parasites and pathogens. The Iles Eparses provide breeding and feeding grounds for more than 3 million breeding pairs of seabirds including at least 13 species. Breeding colonies on these islands are relatively undisturbed by human activities and represent natural metapopulations in which seabird population dynamics, movement and dispersal can be studied in relation to that of circulating parasites and pathogens. In this review, we summarize previous knowledge and recently-acquired data on the parasites and pathogens found in association with seabirds of the Iles Eparses. These studies have revealed the presence of a rich diversity of infectious agents (viruses, bacteria and parasites) carried by the birds and/or their local ectoparasites (ticks and louse flies). Many of these agents are widespread and found in other ecosystems confirming a role for seabirds in their large scale dissemination and maintenance. The heterogeneous distribution of parasites and infectious agents among islands and seabird species suggests that relatively independent metacommunities of interacting species may exist within the western Indian Ocean. In this context, we discuss how the patterns and determinants of seabird movements may alter parasite and pathogen circulation. We conclude by outlining key aspects for future research given the baseline data now available and current concerns in eco-epidemiology and biodiversity conservation.