Jaume Forcada

Spatial and temporal operation of the Scotia Sea ecosystem: a review of large-scale links in a krill centred food web

The Scotia Sea ecosystem is a major component of the circumpolar Southern Ocean system, where productivity and predator demand for prey are high. The eastward-flowing Antarctic Circumpolar Current (ACC) and waters from the Weddell–Scotia Confluence dominate the physics of the Scotia Sea, leading to a strong advective flow, intense eddy activity and mixing. There is also strong seasonality, manifest by the changing irradiance and sea ice cover, which leads to shorter summers in the south. Summer phytoplankton blooms, which at times can cover an area of more than 0.5 million km2, probably result from the mixing of micronutrients into surface waters through the flow of the ACC over the Scotia Arc. This production is consumed by a range of species including Antarctic krill, which are the major prey item of large seabird and marine mammal populations. The flow of the ACC is steered north by the Scotia Arc, pushing polar water to lower latitudes, carrying with it krill during spring and summer, which subsidize food webs around South Georgia and the northern Scotia Arc. There is also marked interannual variability in winter sea ice distribution and sea surface temperatures that is linked to southern hemisphere-scale climate processes such as the El Niño–Southern Oscillation. This variation affects regional primary and secondary production and influences biogeochemical cycles. It also affects krill population dynamics and dispersal, which in turn impacts higher trophic level predator foraging, breeding performance and population dynamics. The ecosystem has also been highly perturbed as a result of harvesting over the last two centuries and significant ecological changes have also occurred in response to rapid regional warming during the second half of the twentieth century. This combination of historical perturbation and rapid regional change highlights that the Scotia Sea ecosystem is likely to show significant change over the next two to three decades, which may result in major ecological shifts.

Female fur seals show active choice for males that are heterozygous and unrelated.

Much debate surrounds the exact rules that influence mating behaviour, and in particular the selective forces that explain the evolution of female preferences. A key example is the lek paradox, in which female choice is expected rapidly to become ineffective owing to loss of additive genetic variability for the preferred traits. Here we exploit a remarkable system in which female fur seals exert choice by moving across a crowded breeding colony to visit largely static males. We show that females move further to maximize the balance between male high multilocus heterozygosity and low relatedness. Such a system shows that female choice can be important even in a strongly polygynous species, and at the same time may help to resolve the lek paradox because heterozygosity has low heritability and inbreeding avoidance means there is no single ‘best’ male for all females.

Environmental forcing and Southern Ocean marine predator populations: effects of climate change and variability

The Southern Ocean is a major component within the global ocean and climate system and potentially the location where the most rapid climate change is most likely to happen, particularly in the high-latitude polar regions. In these regions, even small temperature changes can potentially lead to major environmental perturbations. Climate change is likely to be regional and may be expressed in various ways, including alterations to climate and weather patterns across a variety of time-scales that include changes to the long interdecadal background signals such as the development of the El Niño–Southern Oscillation (ENSO). Oscillating climate signals such as ENSO potentially provide a unique opportunity to explore how biological communities respond to change. This approach is based on the premise that biological responses to shorter-term sub-decadal climate variability signals are potentially the best predictor of biological responses over longer time-scales. Around the Southern Ocean, marine predator populations show periodicity in breeding performance and productivity, with relationships with the environment driven by physical forcing from the ENSO region in the Pacific. Wherever examined, these relationships are congruent with mid-trophic-level processes that are also correlated with environmental variability. The short-term changes to ecosystem structure and function observed during ENSO events herald potential long-term changes that may ensue following regional climate change. For example, in the South Atlantic, failure of Antarctic krill recruitment will inevitably foreshadow recruitment failures in a range of higher trophic-level marine predators. Where predator species are not able to accommodate by switching to other prey species, population-level changes will follow. The Southern Ocean, though oceanographically interconnected, is not a single ecosystem and different areas are dominated by different food webs. Where species occupy different positions in different regional food webs, there is the potential to make predictions about future change scenarios.

Climatically driven fluctuations in Southern Ocean ecosystems

Determining how climate fluctuations affect ocean ecosystems requires an understanding of how biological and physical processes interact across a wide range of scales. Here we examine the role of physical and biological processes in generating fluctuations in the ecosystem around South Georgia in the South Atlantic sector of the Southern Ocean. Anomalies in sea surface temperature (SST) in the South Pacific sector of the Southern Ocean have previously been shown to be generated through atmospheric teleconnections with El Niño Southern Oscillation (ENSO)-related processes. These SST anomalies are propagated via the Antarctic Circumpolar Current into the South Atlantic (on time scales of more than 1 year), where ENSO and Southern Annular Mode-related atmospheric processes have a direct influence on short (less than six months) time scales. We find that across the South Atlantic sector, these changes in SST, and related fluctuations in winter sea ice extent, affect the recruitment and dispersal of Antarctic krill. This oceanographically driven variation in krill population dynamics and abundance in turn affects the breeding success of seabird and marine mammal predators that depend on krill as food. Such propagating anomalies, mediated through physical and trophic interactions, are likely to be an important component of variation in ocean ecosystems and affect responses to longer term change. Population models derived on the basis of these oceanic fluctuations indicate that plausible rates of regional warming of 1oC over the next 100 years could lead to more than a 95% reduction in the biomass and abundance of krill across the Scotia Sea by the end of the century.

THE EFFECTS OF GLOBAL CLIMATE VARIABILITY IN PUP PRODUCTION OF ANTARCTIC FUR SEALS

Climate variability has strong effects on marine ecosystems, with repercussions that range in scale from those that impact individuals to those that impact the entire food web. Climate-induced changes in the abundance of species in lower trophic levels can cascade up to apex predators by depressing vital rates. However, the characteristics and predictability of predator demographic responses remain largely unexplored. We investigated the detectability, limits, and nonlinearity of changes in Antarctic fur seal pup production at South Georgia over a 20-year period in response to environmental autocorrelation created by global climate perturbations; these were identified in time series of monthly averaged sea surface temperature (SST). Environmental autocorrelation at South Georgia was evident with frequent SST anomalies between 1990 and 1999, during a decade of warm background (time-averaged) conditions. SST anomalies were preceded by, and cross-correlated with, frequent El Nino-La Nina events between 1987 and 1998, which was also a decade of warm background conditions in the tropical Pacific Ocean. Nonlinear mixed-effects models indicated that positive anomalies at South Georgia explained extreme reductions in Antarctic fur seal pup production over 20 years of study. Simulated environmental time series suggested that the effect of anomalies on Antarctic fur seals was only detectable within a narrow range of positive SST, regardless of the distribution, variance, and autocorrelation structure in SST; this explained the observed nonlinearity in responses in pup production, which were observed only under persistent high SST levels. Such anomalies at South Georgia were likely associated with low availability of prey, largely krill, which affected Antarctic fur seal females over time scales longer than their breeding cycle. Reductions in Antarctic fur seal pup production could thus be predicted in advance by the detection of large-scale anomalies, which appeared to be driven by trends in global climate perturbation.

Bayesian inference of a historical bottleneck in a heavily exploited marine mammal

Emerging Bayesian analytical approaches offer increasingly sophisticated means of reconstructing historical population dynamics from genetic data, but have been little applied to scenarios involving demographic bottlenecks. Consequently, we analysed a large mitochondrial and microsatellite dataset from the Antarctic fur seal Arctocephalus gazella, a species subjected to one of the most extreme examples of uncontrolled exploitation in history when it was reduced to the brink of extinction by the sealing industry during the late eighteenth and nineteenth centuries. Classical bottleneck tests, which exploit the fact that rare alleles are rapidly lost during demographic reduction, yielded ambiguous results. In contrast, a strong signal of recent demographic decline was detected using both Bayesian skyline plots and Approximate Bayesian Computation, the latter also allowing derivation of posterior parameter estimates that were remarkably consistent with historical observations. This was achieved using only contemporary samples, further emphasizing the potential of Bayesian approaches to address important problems in conservation and evolutionary biology.

Bet‐hedging response to environmental variability, an intraspecific comparison

A major challenge in ecology is to understand the impact of increased environmental variability on populations and ecosystems. To maximize their fitness in a variable environment, life history theory states that individuals should favor a bet-hedging strategy, involving a reduction of annual breeding performance and an increase in adult survival so that reproduction can be attempted over more years. As a result, evolution toward longer life span is expected to reduce the deleterious effects of extra variability on population growth, and consequently on the trait contributing the most to it (e.g., adult survival in long-lived species). To investigate this, we compared the life histories of two Black-browed Albatross (Thalassarche melanophrys) populations breeding at South Georgia (Atlantic Ocean) and Kerguelen (Indian Ocean), the former in an environment nearly three times more variable climatically (e.g., in sea surface temperature) than the latter. As predicted, individuals from South Georgia (in the more variable environment) showed significantly higher annual adult survival (0.959, SE = 0.003) but lower annual reproductive success (0.285 chick per pair, SE = 0.039) than birds from Kerguelen (survival = 0.925, SE = 0.004; breeding success = 0.694, SE = 0.027). In both populations, climatic conditions affected the breeding success and the survival of inexperienced breeders, whereas the survival of experienced breeders was unaffected. The strength of the climatic impact on survival of inexperienced breeders was very similar between the two populations, but the effect on breeding success was positively related to environmental variability. These results provide rare and compelling evidence to support bet-hedging underlying changes in life history traits as an adaptive response to environmental variability.

Climate change selects for heterozygosity in a declining fur seal population

Global environmental change is expected to alter selection pressures in many biological systems, but the long-term molecular and life history data required to quantify changes in selection are rare. An unusual opportunity is afforded by three decades of individual-based data collected from a declining population of Antarctic fur seals in the South Atlantic. Here, climate change has reduced prey availability and caused a significant decline in seal birth weight. However, the mean age and size of females recruiting into the breeding population are increasing. We show that such females have significantly higher heterozygosity (a measure of within-individual genetic variation) than their non-recruiting siblings and their own mothers. Thus, breeding female heterozygosity has increased by 8.5% per generation over the last two decades. Nonetheless, as heterozygosity is not inherited from mothers to daughters, substantial heterozygote advantage is not transmitted from one generation to the next and the decreasing viability of homozygous individuals causes the population to decline. Our results provide compelling evidence that selection due to climate change is intensifying, with far-reaching consequences for demography as well as phenotypic and genetic variation.

Whales from Space: Counting Southern Right Whales by Satellite

We describe a method of identifying and counting whales using very high resolution satellite imagery through the example of southern right whales breeding in part of the Golfo Nuevo, Península Valdés in Argentina. Southern right whales have been extensively hunted over the last 300 years and although numbers have recovered from near extinction in the early 20th century, current populations are fragmented and are estimated at only a small fraction of pre-hunting total. Recent extreme right whale calf mortality events at Península Valdés, which constitutes the largest single population, have raised fresh concern for the future of the species. The WorldView2 satellite has a maximum 50 cm resolution and a water penetrating coastal band in the far-blue part of the spectrum that allows it to see deeper into the water column. Using an image covering 113 km2, we identified 55 probable whales and 23 other features that are possibly whales, with a further 13 objects that are only detected by the coastal band. Comparison of a number of classification techniques, to automatically detect whale-like objects, showed that a simple thresholding technique of the panchromatic and coastal band delivered the best results. This is the first successful study using satellite imagery to count whales; a pragmatic, transferable method using this rapidly advancing technology that has major implications for future surveys of cetacean populations.

No relationship between microsatellite variation and neonatal fitness in Antarctic fur seals, Arctocephalus gazella

Published studies of wild vertebrate populations have almost universally reported positive associations between genetic variation measured at microsatellite loci and fitness, creating the impression of ubiquity both in terms of the species and the traits involved. However, there is concern that this picture may be misleading because negative results frequently go unpublished. Here, we analyse the relationship between genotypic variation at nine highly variable microsatellite loci and neonatal fitness in 1070 Antarctic fur seal pups born at Bird Island, South Georgia. Despite our relatively large sample size, we find no significant association between three different measures of heterozygosity and two fitness traits, birth weight and survival. Furthermore, increasing genetic resolution by calculating parental relatedness also yields no association between genetic variation and fitness. Our findings are consistent with necropsy data showing that most pups die from starvation or trauma, conditions that are unlikely to be influenced strongly by genetic factors, particularly if the benefits of high heterozygosity are linked to immune‐related genes.