Large‐scale oceanographic fluctuations drive Antarctic petrel survival and reproduction

Polar Regions are experiencing environmental changes at unprecedented rates. These changes can spread throughout entire food webs from lower trophic levels to apex predators. As many top predators forage over large areas, these indirect effects may be associated with large‐scale patterns of climate variability. Using global climate indices that are known to impact the Southern Ocean ecosystem (the El Niño Southern Oscillation and Antarctic Oscillation Indices) we assessed their efficacy to predict variation in the demographic parameters of Antarctic seabirds. First, we used a long‐term dataset on adult survival (estimated from capture–mark–recapture data) and reproduction of Antarctic petrel Thalassoica antarctica, from the largest known breeding colony (Svarthamaren, Dronning Maud Land) and examined whether large‐scale oceanographic fluctuations impact survival and reproduction. Second, we conducted an exhaustive literature review to determine whether the effects of large‐scale environmental variability on Antarctic seabirds have a coherent fingerprint across the Antarctic continent and nearby islands. We found that most of the variation in both reproductive success, timing of hatching, and survival of Antarctic petrels can be accurately modeled using the two modes of large‐scale climate variability in Antarctica. The literature review, combined with the results from our field study, suggests that while the anticipated trends in the global patterns of climatic variability will generally have detrimental effects on populations of top predators in the Southwest Atlantic, these conclusions cannot be extrapolated to all seabird populations in Antarctica without additional data.     

A latitudinal gradient in climate effects on seabird demography: results from interspecific analyses

For an understanding of the effect of climate change on animal population dynamics, it is crucial to be able to identify which climatologic parameters affect which demographic rate, and what the underlying mechanistic links are. An important reason for why the interactions between demography and climate still are poorly understood is that the effects of climate vary both geographically and taxonomically. Here, we analyse interspecifically how different climate variables affect the breeding success of North Atlantic seabird species along latitudinal and longitudinal gradients. By approaching the problem comparatively, we are able to generalize across populations and species. We find a strong interactive effect of climate and latitude on breeding success. Of the climatic variables considered, local sea surface temperatures during the breeding season tend to be more relevant than the North Atlantic Oscillation (NAO). However, the effect of NAO on breeding success shows a clear geographic pattern, changing in sign from positive in the south to negative in the north. If this interaction is taken account of, the model explains more variation than any model with sea surface temperature. This superiority of the NAO index is due to its ability to capture effects of more than one season in a single parameter. Mechanistically, however, several lines of evidence suggest that sea surface temperature is the biologically most relevant explanatory variable.     

Diverging phenological responses of Arctic seabirds to an earlier spring

The timing of annual events such as reproduction is a critical component of how free‐living organisms respond to ongoing climate change. This may be especially true in the Arctic, which is disproportionally impacted by climate warming. Here, we show that Arctic seabirds responded to climate change by moving the start of their reproduction earlier, coincident with an advancing onset of spring and that their response is phylogenetically and spatially structured. The phylogenetic signal is likely driven by seabird foraging behavior. Surface‐feeding species advanced their reproduction in the last 35 years while diving species showed remarkably stable breeding timing. The earlier reproduction for Arctic surface‐feeding birds was significant in the Pacific only, where spring advancement was most pronounced. In both the Atlantic and Pacific, seabirds with a long breeding season showed a greater response to the advancement of spring than seabirds with a short breeding season. Our results emphasize that spatial variation, phylogeny, and life history are important considerations in seabird phenological response to climate change and highlight the key role played by the species’ foraging behavior.     

Global climate patterns explain range-wide synchronicity in survival of a migratory seabird

To predict the impact of climate change over the whole species distribution range, comparison of adult survival variations over large spatial scale is of primary concern for long-lived species populations that are particularly susceptible to decline if adult survival is reduced. In this study, we estimated and compared adult survival rates between 1989 and 1997 of six populations of Cory's shearwater ( Calonectris diomedea ) spread across 4600 km using capture–recapture models. We showed that mean annual adult survival rates are different among populations along a longitudinal gradient and between sexes. Variation in adult survival is synchronized among populations, with three distinct groups: (1) both females and males of Corsica, Tremiti, and Selvagem (annual survival range 0.88–0.96); (2) both females and males of Frioul and females from Crete (0.82–0.92); and (3) both females and males of Malta and males from Crete (0.74–0.88). The total variation accounted for by the common pattern of variation is on average 71%, suggesting strong environmental forcing. At least 61% of the variation in survival is explained by the Southern Oscillation Index fluctuations. We suggested that Atlantic hurricanes and storms during La Niña years may increase adult mortality for Cory's shearwater during winter months. For long-lived seabird species, variation in adult survival is buffered against environmental variability, although extreme climate conditions such as storms significantly affect adult survival. The effect of climate at large spatial scales on adult survival during the nonbreeding period may lead to synchronization of variation in adult survival over the species' range and has large effects on the meta-population trends. One can thus worry about the future of such long-lived seabirds species under the predictions of higher frequency of extreme large-scale climatic events.     

Variable exposure and immunological response to Lyme disease Borrelia among North Atlantic seabird species

Colonial seabirds often breed in large aggregations. These individuals can be exposed to parasitism by the tick Ixodes uriae, but little is known about the circulation of pathogens carried by this ectoparasite, including Lyme disease Borrelia. Here we investigated the prevalence of antibodies (Ab) against Borrelia burgdorferi sensu lato in seabird species sampled at eight locations across the North Atlantic. Using enzyme-linked immunosorbent assay tests, we found that the prevalence of anti-Borrelia Ab in adult seabirds was 39.6% on average (over 444 individuals), but that it varied among colonies and species. Common guillemots showed higher seroprevalence (77.1%+/-5.9) than black-legged kittiwakes (18.6%+/-6.7) and Atlantic puffins (22.6%+/-6.3). Immunoblot-banding patterns of positive individuals, reflecting the variability of Borrelia antigens against which Ab were produced, also differed among locations and species, and did not tightly match the prevalence of Borrelia phylogroups previously identified in ticks collected from the same host individuals. These results represent the first report of the widespread prevalence of Ab against Borrelia within an assemblage of seabird species and demonstrate that Borrelia is an integrated aspect in the interaction between seabirds and ticks. More detailed studies on the dynamics of Borrelia within and among seabird species at different spatial scales will now be required to better understand the implications of this interaction for seabird ecology and the epidemiology of Lyme disease.     

At-sea surveys confirm a North Atlantic biodiversity hotspot

Capsule A number of tracking studies have shown an area of the North Atlantic, south of the Charlie-Gibbs Fracture Zone, to be an important overwintering location for seabirds. We conducted seabird observations along a trans-Atlantic transect from Ireland to Canada in April 2014 to test the hypothesis that seabird species richness and abundance will peak in the area of the Mid-Atlantic Ridge. At-sea survey results agreed with previous tracking studies, highlighting the importance of the Mid-Atlantic Ridge area for seabirds.     

North Atlantic climate variation influences survival in adult fulmars

There is increasing evidence that large scale climate variation influences reproductive parameters of seabirds, but fewer studies have investigated possible effects on adult survival. Previous work has shown that climate variation reflected by the winter North Atlantic oscillation (WNAO) influences reproductive success in northern fulmars. Here, we use a 34 year long (1962–1995) individual‐based data set to investigate inter‐annual and inter‐individual variation in adult survival in this species. Breeding success in the previous and current seasons, and both the WNAO and one‐year lagged WNAO indexes, were considered as potential sources of inter‐annual variation in survival and recapture probabilities. Sex and an index of body size were considered as potential sources of inter‐individual variation in survival and recapture probabilities. Body size effects were not significant, but males and females differed in both their survival and recapture probabilities. Probability of recapture of females was positively correlated with breeding success in both the current and previous breeding seasons, whereas male recapture probabilities were correlated only with previous breeding success. Male and female survival decreased over the study period, suggesting that there had been a degradation of environmental conditions. This hypothesis was supported by the detection of a negative correlation between survival and the WNAO, which, in turn, showed a positive increase over this period. The negative correlation between female adult survival and WNAO did not result only from the long term behaviour of the two time series, but persisted for higher frequency fluctuations. In contrast, the correlation between male survival and WNAO seemed to result only from the long term behaviour of the two time series. Despite uncertainties over causal mechanisms, these findings add to the body of evidence that large scale climate variation could dramatically affect seabird population dynamics. Furthermore our results suggest that climate variation can differentially influence individuals with distinct phenotypic characteristics.     

Targeting efforts in rescue programmes mitigating light-induced seabird mortality: First the fat,then the skinny

Oceanic conditions determine food availability to seabirds and affect seabird reproductive parameters, such as breeding success, chick growth, and survival rates. In seabirds, juvenile survival at sea is positively correlated with body condition at fledging. In addition, in several seabird species, especially petrels and shearwaters (Order Procellariiformes), fledglings are disoriented by artificial lights during their maiden flights from their nests to the sea, and many of them fall on the ground and are rescued by volunteers to mitigate light-induced mortality. We studied variations in body condition and body mass in Cory’s Shearwater (Calonectris borealis) fledglings on Faial Island (Azores), using data from rescue campaigns conducted over 15 consecutive years. We checked if body condition was related to oceanic conditions. Late fledglings were in poorer body condition than early ones. Significant inter-annual variations in fledging body condition were observed. These were not related to North Atlantic Oscillation fluctuations. However, annual mean fledgling body condition was positively correlated with sea surface temperatures measured in the autumn of the previous year in a northern feeding area used by adults throughout the breeding season. This study broadens our knowledge of the factors affecting fledgling body condition in Procellariiformes and provides advice to better manage the rescue campaigns. Optimal management of rescue campaigns is essential given the limited economic or human resources allocated to such an aim.     

Physiological effects of climate on distributions of endothermic species

Aim Determining the mechanisms underlying climatic limitation of species distributions is essential for understanding responses to current climatic change. Disentangling direct (e.g. physiological) and indirect (e.g. trophic) effects of climate on distributions through occurrence‐based modelling is problematic because most species use the same area for both shelter and food acquisition. By focusing on marine birds that breed on land but feed at sea, we exploit a rare opportunity to dissociate direct from indirect climatic effects on endothermic species. Location Coastal Europe. Methods We developed climate‐response surfaces (CRS) for 13 seabird species in coastal Europe, linking terrestrial climatic variables considered important for heat transfer with presence/absence data across each species’ entire European breeding range. Agreement between modelled and actual distribution was assessed for jackknifed samples using area under the curve (AUC) of receiver operating characteristic plots. Higher AUC values indicated closer correspondence between observed breeding distribution and terrestrial climate. We assessed the influence of several ecological factors on model performance across species. Results Species maximum foraging range and breeding latitude explained the greatest proportion of variation in AUC across species. AUC was positively related to both latitude and foraging range. Main conclusions The positive relationship between foraging range and AUC suggests that species foraging further are more likely to be constrained by environmental heat stress conditions at the breeding site. One plausible explanation is that long foraging trips result in one parent spending long periods in continuous nest attendance, exposed to such conditions. These may include negative impacts through predation and parasitism in addition to physiological responses to the thermal environment, which probably explains why our models performed better for species breeding at higher latitudes, where such species interactions are considered less important. These data highlight the importance of considering physiological impacts of climate for endothermic species, and suggest that widespread oceanographic changes that reduce prey quality and quantity for seabirds at sea may be exacerbated by additional impacts of climate at the breeding site.     

Differential reproductive responses to stress reveal the role of life-history strategies within a species

Life-history strategies describe that ‘slow’- in contrast to ‘fast’-living species allocate resources cautiously towards reproduction to enhance survival. Recent evidence suggests that variation in strategies exists not only among species but also among populations of the same species. Here, we examined the effect of experimentally induced stress on resource allocation of breeding seabirds in two populations with contrasting life-history strategies: slow-living Pacific and fast-living Atlantic black-legged kittiwakes. We tested the hypothesis that reproductive responses in kittiwakes under stress reflect their life-history strategies. We predicted that in response to stress, Pacific kittiwakes reduce investment in reproduction compared with Atlantic kittiwakes. We exposed chick-rearing kittiwakes to a short-term (3-day) period of increased exogenous corticosterone (CORT), a hormone that is released during food shortages. We examined changes in baseline CORT levels, parental care and effects on offspring. We found that kittiwakes from the two populations invested differently in offspring when facing stress. In response to elevated CORT, Pacific kittiwakes reduced nest attendance and deserted offspring more readily than Atlantic kittiwakes. We observed lower chick growth, a higher stress response in offspring and lower reproductive success in response to CORT implantation in Pacific kittiwakes, whereas the opposite occurred in the Atlantic. Our findings support the hypothesis that life-history strategies predict short-term responses of individuals to stress within a species. We conclude that behaviour and physiology under stress are consistent with trade-off priorities as predicted by life-history theory. We encourage future studies to consider the pivotal role of life-history strategies when interpreting inter-population differences of animal responses to stressful environmental events.     

Inter‐oceanic variation in patterns of host‐associated divergence in a seabird ectoparasite

Aim Parasites with global distributions and wide host spectra provide excellent models for exploring the factors that drive parasite diversification. Here, we tested the relative force of host and geography in shaping population structure of a widely distributed and common ectoparasite of colonial seabirds, the tick Ixodes uriae. Location Two natural geographic replicates of the system: numerous seabird colonies of the North Pacific and North Atlantic Ocean basins. Methods Using eight microsatellite markers and tick samples from a suite of multi‐specific seabird colonies, we examined tick population structure in the North Pacific and compare patterns of diversity and structure to those in the Atlantic basin. Analyses included population genetic estimations of diversity and population differentiation, exploratory multivariate analyses, and Bayesian clustering approaches. These different analyses explicitly took into account both the geographic distance among colonies and host use by the tick. Results Overall, little geographic structure was observed among Pacific tick populations. However, host‐related genetic differentiation was evident, but was variable among host types and lower than in the North Atlantic. Main conclusions Tick population structure is concordant with the genetic structure observed in seabird host species within each ocean basin, where seabird populations tend to be less structured in the North Pacific than in the North Atlantic. Reduced tick genetic structure in the North Pacific suggests that host movement among colonies, and thus tick dispersal, is higher in this region. In addition to information on parasite diversity and gene flow, our findings raise interesting questions about the subtle ways that host behaviour, distribution and phylogeographic history shape the genetics of associated parasites across geographic landscapes.     

Climate warming decreases the survival of the little auk (Alle alle), a high Arctic avian predator

Delayed maturity, low fecundity, and high adult survival are traits typical for species with a long‐life expectancy. For such species, even a small change in adult survival can strongly affect the population dynamics and viability. We examined the effects of both regional and local climatic variability on adult survival of the little auk, a long‐lived and numerous Arctic seabird species. We conducted a mark‐resighting study for a period of 8 years (2006‐2013) simultaneously at three little auk breeding sites that are influenced by the West Spitsbergen Current, which is the main carrier of warm, Atlantic water into the Arctic. We found that the survival of adult little auks was negatively correlated with both the North Atlantic Oscillation (NAO) index and local summer sea surface temperature (SST), with a time lag of 2 and 1 year, respectively. The effects of NAO and SST were likely mediated through a change in food quality and/or availability: (1) reproduction, growth, and development of Arctic Calanus copepods, the main prey of little auks, are negatively influenced by a reduction in sea ice, reduced ice algal production, and an earlier but shorter lasting spring bloom, all of which result from an increased NAO; (2) a high sea surface temperature shortens the reproductive period of Arctic Calanus, decreasing the number of eggs produced. A synchronous variation in survival rates at the different colonies indicates that climatic forcing was similar throughout the study area. Our findings suggest that a predicted warmer climate in the Arctic will negatively affect the population dynamics of the little auk, a high Arctic avian predator.     

Climate,copepods and seabirds in the boreal Northeast Atlantic – current state and future outlook

The boreal Northeast Atlantic is strongly affected by current climate change, and large shifts in abundance and distribution of many organisms have been observed, including the dominant copepod Calanus finmarchicus, which supports the grazing food web and thus many fish populations. At the same time, large‐scale declines have been observed in many piscivorous seabirds, which depend on abundant small pelagic fish. Here, we combine predictions from a niche model of C. finmarchicus with long‐term data on seabird breeding success to link trophic levels. The niche model shows that environmental suitability for C. finmarchicus has declined in southern areas with large breeding seabird populations (e.g. the North Sea), and predicts that this decline is likely to spread northwards during the 21st century to affect populations in Iceland and the Faroes. In a North Sea colony, breeding success of three common piscivorous seabird species [black‐legged kittiwake (Rissa tridactyla), common guillemot (Uria aalge) and Atlantic puffin (Fratercula arctica)] was strongly positively correlated with local environmental suitability for C. finmarchicus, whereas this was not the case at a more northerly colony in west Norway. Large seabird populations seem only to occur where C. finmarchicus is abundant, and northward distributional shifts of common boreal seabirds are therefore expected over the coming decades. Whether or not population size can be maintained depends on the dispersal ability and inclination of these colonial breeders, and on the carrying capacity of more northerly areas in a warmer climate.     

Detecting population heterogeneity in effects of North Atlantic Oscillations on seabird body condition: get into the rhythm

Climatic influences on animal populations, mediated by changes in condition‐dependent survival or reproduction, have long intrigued ecologists. We analyzed links between winter North Atlantic Oscillations (NAO), a large scale climatic phenomenon affecting weather conditions over the North Atlantic and the Arctic, and average pre‐laying body mass in common eiders. Body mass is a good proxy for condition‐dependent reproductive output in this species. Time series links were assessed for two eider populations breeding at high latitudes, over a 10‐ and a 21‐year time series. Winter NAO affected body mass in both populations and these effects were easier to detect when changes in the series rhythm were assessed using a novel method based on data discretization and information theory, rather than detection based on changes in amplitude, assessed using traditional linear models. Winter conditions affected body condition of eiders in both populations. Different mechanisms, however, are likely to be involved in the two populations, one being presumably affected by direct effects of climate and the other by effects through the food chain. Therefore, the same species can respond along different pathways to the same large scale climatic pattern, an important consideration when seeking to understand or manage the response of species to present and future climate change.     

The devil is in the detail: Nonadditive and context‐dependent plant population responses to increasing temperature and precipitation

In climate change ecology, simplistic research approaches may yield unrealistically simplistic answers to often more complicated problems. In particular, the complexity of vegetation responses to global climate change begs a better understanding of the impacts of concomitant changes in several climatic drivers, how these impacts vary across different climatic contexts, and of the demographic processes underlying population changes. Using a replicated, factorial, whole‐community transplant experiment, we investigated regional variation in demographic responses of plant populations to increased temperature and/or precipitation. Across four perennial forb species and 12 sites, we found strong responses to both temperature and precipitation change. Changes in population growth rates were mainly due to changes in survival and clonality. In three of the four study species, the combined increase in temperature and precipitation reflected nonadditive, antagonistic interactions of the single climatic changes for population growth rate and survival, while the interactions were additive and synergistic for clonality. This disparity affects the persistence of genotypes, but also suggests that the mechanisms behind the responses of the vital rates differ. In addition, survival effects varied systematically with climatic context, with wetter and warmer + wetter transplants showing less positive or more negative responses at warmer sites. The detailed demographic approach yields important mechanistic insights into how concomitant changes in temperature and precipitation affect plants, which makes our results generalizable beyond the four study species. Our comprehensive study design illustrates the power of replicated field experiments in disentangling the complex relationships and patterns that govern climate change impacts across real‐world species and landscapes.     

Climatic variables influence the temporal dynamics of an anuran metacommunity in a nonstationary way

Understanding the temporal dynamics of communities is crucial to predict how communities respond to climate change. Several factors can promote variation in phenology among species, including tracking of seasonal resources, adaptive responses to other species, demographic stochasticity, and physiological constraints. The activities of ectothermic vertebrates are sensitive to climatic variations due to the effect of temperature and humidity on species physiology. However, most studies on temporal dynamics have analyzed multi‐year data and do not have resolution to discriminate within‐year patterns that can determine community assembly cycles. Here, we tested the temporal stability and synchrony of calling activity and also how climatic variables influence anuran species composition throughout the year in a metacommunity in the Atlantic Forest of southern Brazil. Using a multivariate method, we described how the relationship between species composition and climatic variables changes through time. The metacommunity showed a weak synchronous spatial pattern, meaning that species responded independently to environmental variation. Interestingly, species composition exhibited a nonstationary response to climate, suggesting that climate affects species composition differently depending on the season. The species‐climate relationship was stronger during the spring, summer, and winter, mainly influenced by temperature, rainfall, and humidity. Thus, temporal community dynamics seem to be mediated by species life‐history traits, in which independent fluctuations promote community stability in temporally varying environments.     

Basal metabolic rates of North Atlantic seabirds

Basal metabolic rates (BMR) were measured for 11 species of North Atlantic seabirds, ranging in size from the Kittiwake Rissa tridactyla to the Gannet Sula bassana. BMRs for all species were higher than those predicted from the allometric equations of Lasiewski and Dawson (1967), Aschoff and Pohl (1970) and Ellis (1984). The equations of Ellis (1984), incorporating a latitude correction, and of Bennett and Harvey (1987), involving deviations by seabird families from a general avian trend line, gave predictions for BMR which were closer to, but respectively lower and higher than, those observed in this study. BMR for seabirds in Scotland (55–60^oN) is described by the equation: BMR (kj/d) = 2.30W⁰⁷⁷⁴. The principal sources of variability in BMR amongst seabirds and the selective forces shaping the differences between seabirds and most other birds with lower BMRs remain unclear but deserve further study.     

Teleconnections and local weather orchestrate the reproduction of tit species in the Carpathian Basin

Variation in climatic conditions is an important driving force of ecological processes. Populations are under selection to respond to climatic changes with respect to phenology of the annual cycle (e.g. breeding, migration) and life‐history. As teleconnections can reflect climate on a global scale, the responses of terrestrial animals are often investigated in relation to the El Niño‐Southern Oscillation and North Atlantic Oscillation. However, investigation of other teleconnections and local climate is often neglected. In this study, we examined over a 33‐year period the relationships between four teleconnections (El Niño‐Southern Oscillation, North Atlantic Oscillation, Arctic Oscillation, East Atlantic Pattern), local weather parameters (temperature and precipitation) and reproduction in great tits Parus major and blue tits Cyanistes caeruleus in the Carpathian Basin, Hungary. Furthermore, we explored how annual variations in the timing of food availability were correlated with breeding performance. In both species, annual laying date was negatively associated with the Arctic Oscillation. The date of peak abundance of caterpillars was negatively associated with local temperatures in December–January, while laying date was negatively related to January–March temperature. We found that date of peak abundance of caterpillars and laying date of great tits advanced, while in blue tits clutch size decreased over the decades but laying date did not advance. The results suggest that weather conditions during the months that preceded the breeding season, as well as temporally more distant winter conditions, were connected to breeding date. Our results highlight that phenological synchronization to food availability was different between the two tit species, namely it was disrupted in blue tits only. Additionally, the results suggest that in order to find the climatic drivers of the phenological changes of organisms, we should analyze a broader range of global meteorological parameters.     

Seabird diversity hotspot linked to ocean productivity in the Canary Current Large Marine Ecosystem

Upwelling regions are highly productive habitats targeted by wide-ranging marine predators and industrial fisheries. In this study, we track the migratory movements of eight seabird species from across the Atlantic; quantify overlap with the Canary Current Large Marine Ecosystem (CCLME) and determine the habitat characteristics that drive this association. Our results indicate the CCLME is a biodiversity hotspot for migratory seabirds; all tracked species and more than 70% of individuals used this upwelling region. Relative species richness peaked in areas where sea surface temperature averaged between 15 and 20°C, and correlated positively with chlorophyll a, revealing the optimum conditions driving bottom-up trophic effects for seabirds. Marine vertebrates are not confined by international boundaries, making conservation challenging. However, by linking diversity to ocean productivity, our research reveals the significance of the CCLME for seabird populations from across the Atlantic, making it a priority for conservation action.