Christophe Barbraud

Emperor penguins and climate change

Variations in ocean–atmosphere coupling over time in the Southern Ocean have dominant effects on sea-ice extent and ecosystem structure, but the ultimate consequences of such environmental changes for large marine predators cannot be accurately predicted because of the absence of long-term data series on key demographic parameters. Here, we use the longest time series available on demographic parameters of an Antarctic large predator breeding on fast ice and relying on food resources from the Southern Ocean. We show that over the past 50 years, the population of emperor penguins (Aptenodytes forsteri) in Terre Adélie has declined by 50% because of a decrease in adult survival during the late 1970s. At this time there was a prolonged abnormally warm period with reduced sea-ice extent. Mortality rates increased when warm sea-surface temperatures occurred in the foraging area and when annual sea-ice extent was reduced, and were higher for males than for females. In contrast with survival, emperor penguins hatched fewer eggs when winter sea-ice was extended. These results indicate strong and contrasting effects of large-scale oceanographic processes and sea-ice extent on the demography of emperor penguins, and their potential high susceptibility to climate change.

Assessing the impact of climate variation on survival in vertebrate populations

The impact of the ongoing rapid climate change on natural systems is a major issue for human societies. An important challenge for ecologists is to identify the climatic factors that drive temporal variation in demographic parameters, and, ultimately, the dynamics of natural populations. The analysis of long‐term monitoring data at the individual scale is often the only available approach to estimate reliably demographic parameters of vertebrate populations. We review statistical procedures used in these analyses to study links between climatic factors and survival variation in vertebrate populations.

Trends in bird and seal populations as indicators of a system shift in the Southern Ocean

Although world oceans have been warming over the past 50 years, the impact on biotic components is poorly understood because of the difficulty of obtaining long-term datasets on marine organisms. The Southern Ocean plays a critical role in global climate and there is growing evidence of climate warming. We show that air temperatures measured by meteorological stations have steadily increased over the past 50 years in the southern Indian Ocean, the increase starting in mid 1960s and stabilizing in mid 1980s, being particularly important in the sub-Antarctic sector. At the same time, with a time lag of 2–9 years with temperatures, the population size of most seabirds and seals monitored on several breeding sites have decreased severely, whilst two species have increased at the same time. These changes, together with indications of a simultaneous decrease in secondary production in sub-Antarctic waters and the reduction of sea-ice extent further south, indicate that a major system shift has occurred in the Indian Ocean part of the Southern Ocean. This shift illustrates the high sensitivity of marine ecosystems, and especially upper trophic level predators, to climatic changes.

Demographic models and IPCC climate projections predict the decline of an emperor penguin population

Studies have reported important effects of recent climate change on Antarctic species, but there has been to our knowledge no attempt to explicitly link those results to forecasted population responses to climate change. Antarctic sea ice extent (SIE) is projected to shrink as concentrations of atmospheric greenhouse gases (GHGs) increase, and emperor penguins (Aptenodytes forsteri) are extremely sensitive to these changes because they use sea ice as a breeding, foraging and molting habitat. We project emperor penguin population responses to future sea ice changes, using a stochastic population model that combines a unique long-term demographic dataset (1962–2005) from a colony in Terre Adélie, Antarctica and projections of SIE from General Circulation Models (GCM) of Earths climate included in the most recent Intergovernmental Panel on Climate Change (IPCC) assessment report. We show that the increased frequency of warm events associated with projected decreases in SIE will reduce the population viability. The probability of quasi-extinction (a decline of 95% or more) is at least 36% by 2100. The median population size is projected to decline from ≈6,000 to ≈400 breeding pairs over this period. To avoid extinction, emperor penguins will have to adapt, migrate or change the timing of their growth stages. However, given the future projected increases in GHGs and its effect on Antarctic climate, evolution or migration seem unlikely for such long lived species at the remote southern end of the Earth.

LONG-TERM CONTRASTED RESPONSES TO CLIMATE OF TWO ANTARCTIC SEABIRD SPECIES

We examined the population dynamics of two Antarctic seabirds and the influence of environmental variability over a 40-year period by coupling the estimation of demographic parameters, based on capture-recapture data, and modeling, using Leslie ma- trix population models. We demonstrated that the demographic parameters showing the greatest contribution to the variance of population growth rate were adult survival for both species. Breeding success showed the same contribution as adult survival for Emperor Penguins, whereas the proportion of breeders had the next stronger contribution for Snow Petrels. The sensitivity of population growth rate to adult survival was very high and the adult survival variability was weak for both species. Snow Petrel males survived better than females, whereas Emperor Penguin males had lower survival than females. These differ- ences may be explained by the different investment in breeding. Emperor Penguin adult survival was negatively affected by air temperature during summer and winter for both sexes; male survival was negatively affected by sea ice concentration during summer, autumn, and winter. On the other hand, there was no effect of environmental covariates on Snow Petrel adult survival. The Emperor Penguin population has declined by 50% because of a decrease in adult survival related to a warming event during a regime shift in the late 1970s, whereas Snow Petrels showed their lowest numbers in 1976, but were able to skip reproduction. Indeed, the retrospective analysis of projection population matrix entries indicated that breeding abstention played a critical role in the population dynamics of Snow Petrels but not Emperor Penguins. Snow Petrels did not breed either when air temperature decreased during spring (probably reducing nest attendance and laying) or when sea ice decreased during autumn (reducing food availability). Emperor Penguin and Snow Petrel breeding population sizes were positively influenced by sea ice through its effect on adult survival for Emperor Penguins and on the proportion of breeders for Snow Petrels. Therefore, we hypothesize that the population sizes of the two species could be negatively affected by reduced sea ice in the context of global warming.

Climate and density shape population dynamics of a marine top predator

Long-term studies have documented that climate fluctuations affect the dynamics of populations, but the relative influence of stochastic and density–dependent processes is still poorly understood and debated. Most studies have been conducted on terrestrial systems, and lacking are studies on marine systems explicitly integrating the fact that most populations live in seasonal environments and respond to regular or systematic environmental changes. We separated winter from summer mortality in a seabird population, the blue petrel Halobaena caerulea, in the southern Indian Ocean where the El Niño/Southern Oscillation effects occur with a 3–4–year lag. Seventy per cent of the mortality occurred in winter and was linked to climatic factors, being lower during anomalous warm events. The strength of density dependence was affected by climate, with population crashes occurring when poor conditions occurred at high densities. We found that an exceptionally long–lasting warming caused a ca. 40% decline of the population, suggesting that chronic climate change will strongly affect this top predator. These findings demonstrate that populations in marine systems are particularly susceptible to climate variation through complex interactions between seasonal mortality and density–dependent effects.

Climate change and Southern Ocean ecosystems I: how changes in physical habitats directly affect marine biota

Antarctic and Southern Ocean (ASO) marine ecosystems have been changing for at least the last 30 years, including in response to increasing ocean temperatures and changes in the extent and seasonality of sea ice; the magnitude and direction of these changes differ between regions around Antarctica that could see populations of the same species changing differently in different regions. This article reviews current and expected changes in ASO physical habitats in response to climate change. It then reviews how these changes may impact the autecology of marine biota of this polar region: microbes, zooplankton, salps, Antarctic krill, fish, cephalopods, marine mammals, seabirds, and benthos. The general prognosis for ASO marine habitats is for an overall warming and freshening, strengthening of westerly winds, with a potential pole-ward movement of those winds and the frontal systems, and an increase in ocean eddy activity. Many habitat parameters will have regionally specific changes, particularly relating to sea ice characteristics and seasonal dynamics. Lower trophic levels are expected to move south as the ocean conditions in which they are currently found move pole-ward. For Antarctic krill and finfish, the latitudinal breadth of their range will depend on their tolerance of warming oceans and changes to productivity. Ocean acidification is a concern not only for calcifying organisms but also for crustaceans such as Antarctic krill; it is also likely to be the most important change in benthic habitats over the coming century. For marine mammals and birds, the expected changes primarily relate to their flexibility in moving to alternative locations for food and the energetic cost of longer or more complex foraging trips for those that are bound to breeding colonies. Few species are sufficiently well studied to make comprehensive species-specific vulnerability assessments possible. Priorities for future work are discussed.

SEX DIFFERENCES IN PARENTAL INVESTMENT AND CHICK GROWTH IN WANDERING ALBATROSSES: FITNESS CONSEQUENCES

Parents should adjust expenditure on parental care so as to maximize fitness, but quantitative data are sparse, particularly for sexually dimorphic species. We use data from two breeding seasons to investigate the fitness consequences of variation in parent provisioning behavior and chick growth in a sexually dimorphic seabird, the Wandering Albatross (Diomedea exulans). Male parents brought more food to their single offspring than females did, and male chicks (sons) received more food than female chicks (daughters). The study of growth parameters indicates that sons had faster growth rates, reached higher asymptotic mass, and were heavier and larger at fledging than daughters. Male chicks that survived to adult age were larger than those that disappeared, whereas the females that survived were those in better condition at fledging, indicating that different factors affect survival of each sex during the first years of independence at sea. Survival to adult age seems to be influenced by the ability of parents to provision the offspring adequately, especially in the case of male chicks, whose costs appear to be higher. The age and ex- perience of parents did not influence the amount of food delivered to the chick, but older birds rearing male chicks were more synchronized on a within-pair basis than younger parents, and consequently their sons grew faster, attaining both higher asymptotic mass and higher mass at fledging. Old adult males appeared to have a higher mortality rate than younger males when rearing a son. There was no such tendency for adult males rearing a daughter or for females rearing a son. Younger, less experienced pairs may tend to produce more sons than daughters when compared to older and more experienced pairs. If valid, this tendency for an age-related sex ratio could be the result of higher costs of raising the more expensive sex. These findings indicate that the optimal age-related investment by parents varies between males and females but also depends to a large degree on whether they are rearing a son or a daughter.

Phenological changes in the southern hemisphere.

Current evidence of phenological responses to recent climate change is substantially biased towards northern hemisphere temperate regions. Given regional differences in climate change, shifts in phenology will not be uniform across the globe, and conclusions drawn from temperate systems in the northern hemisphere might not be applicable to other regions on the planet. We conduct the largest meta-analysis to date of phenological drivers and trends among southern hemisphere species, assessing 1208 long-term datasets from 89 studies on 347 species. Data were mostly from Australasia (Australia and New Zealand), South America and the Antarctic/subantarctic, and focused primarily on plants and birds. This meta-analysis shows an advance in the timing of spring events (with a strong Australian data bias), although substantial differences in trends were apparent among taxonomic groups and regions. When only statistically significant trends were considered, 82% of terrestrial datasets and 42% of marine datasets demonstrated an advance in phenology. Temperature was most frequently identified as the primary driver of phenological changes; however, in many studies it was the only climate variable considered. When precipitation was examined, it often played a key role but, in contrast with temperature, the direction of phenological shifts in response to precipitation variation was difficult to predict a priori. We discuss how phenological information can inform the adaptive capacity of species, their resilience, and constraints on autonomous adaptation. We also highlight serious weaknesses in past and current data collection and analyses at large regional scales (with very few studies in the tropics or from Africa) and dramatic taxonomic biases. If accurate predictions regarding the general effects of climate change on the biology of organisms are to be made, data collection policies focussing on targeting data-deficient regions and taxa need to be financially and logistically supported.

ENVIRONMENTAL CONDITIONS AND BREEDING EXPERIENCE AFFECT COSTS OF REPRODUCTION IN BLUE PETRELS

Using data from a 17-year study of individually marked Blue Petrels, we examined how survival and breeding probability varied with experience and breeding status, and looked for costs of first reproduction, taking into account environmental and individual variability. Using multistate capture-recapture models with four states (inexperienced non- breeders, first-time breeders, experienced breeders, and experienced nonbreeders), we found that first-time breeders had a lower probability of surviving and breeding in the next year than experienced breeders. Survival of first-time breeders was lower than that of inexpe- rienced nonbreeders, indicating a cost of first reproduction. Survival of inexperienced in- dividuals (both breeders and nonbreeders), but not of experienced ones, was negatively affected by poor environmental oceanographic conditions. The costs of reproduction for first-time breeders were particularly marked during harsh weather conditions. Survival and the probability of breeding in the next year for experienced birds were higher for breeders than for nonbreeders. Similarly, the probability of breeding in the next year for first-time breeders was higher than for inexperienced nonbreeders. This suggests heterogeneity in quality among individuals. Experienced breeders had a higher body condition than first- time breeders and nonbreeders. Body condition did not affect the probability of surviving or breeding in the next year. These results can be interpreted in the light of a change in the proportion of individuals with different survival (selection hypothesis: low-quality individuals die sooner). The inferiority of first-time breeders may be linked to a higher proportion of lower-quality individuals in younger age classes. First reproduction may act as a filter, selecting individuals of higher quality. Sea surface height, reflecting food avail- ability, is probably a key selective agent.