Molecular responses of a key Antarctic species to sedimentation due to rapid climate change.

Rapid regional warming causing glacial retreat and melting of ice caps in Antarctica leads benthic filter-feeders to be exposed to periods of food shortage and high respiratory impairment as a consequence of seasonal sediment discharge in the West Antarctic Peninsula coastal areas. The molecular physiological response and its fine-tuning allow species to survive acute environmental stress and are thus a prerequisite to longer-term adaptation to changing environments. Under experimental conditions, we analyzed here the metabolic response to changes in suspended sediment concentrations, through transcriptome sequencing and enzymatic measurements in a highly abundant Antarctic ascidian. We found that the mechanisms underlying short-term response to sedimentation in Cnemidocarpa verrucosa sp. A involved apoptosis, immune defense, and general metabolic depression. These mechanisms may be understood as an adaptive protection against sedimentation caused by glacial retreat. This process can strongly contribute to the structuring of future benthic filter-feeder communities in the face of climate change.

Parallel shape divergence between ecotypes of the limpet Nacella concinna along the Antarctic Peninsula: a new model species for parallel evolution?

Parallel phenotypic divergence is the independent differentiation between phenotypes of the same lineage or species occupying ecologically similar environments in different populations. We tested in the Antarctic limpet Nacella concinna the extent of parallel morphological divergence in littoral and sublittoral ecotypes throughout its distribution range. These ecotypes differ in morphological, behavioural and physiological characteristics. We studied the lateral and dorsal outlines of shells and the genetic variation of the mitochondrial gene Cytochrome Oxidase subunit I from both ecotypes in 17 sample sites along more than 2,000 km. The genetic data indicate that both ecotypes belong to a single evolutionary lineage. The magnitude and direction of phenotypic variation differ between ecotypes across sample sites; completely parallel ecotype-pairs (i.e., they diverge in the same magnitude and in the same direction) were detected in 84.85% of lateral and 65.15% in dorsal view comparisons. Besides, specific traits (relative shell height, position of shell apex, and elliptical/pear-shape outline variation) showed high parallelism. We observed weak morphological covariation between the two shape shell views, indicating that distinct evolutionary forces and environmental pressures could be acting on this limpet shell shape. Our results demonstrate there is a strong parallel morphological divergence pattern in N. concinna along its distribution, making this Antarctic species a suitable model for the study of different evolutionary forces shaping the shell evolution of this limpet.

Hidden diversity in Antarctica: Molecular and morphological evidence of two different species within one of the most conspicuous ascidian species.

The Southern Ocean is one of the most isolated marine ecosystems, characterized by high levels of endemism, diversity, and biomass. Ascidians are among the dominant groups in Antarctic benthic assemblages; thus, recording the evolutionary patterns of this group is crucial to improve our current understanding of the assembly of this polar ocean. We studied the genetic variation within Cnemidocarpa verrucosa sensu lato, one of the most widely distributed abundant and studied ascidian species in Antarctica. Using a mitochondrial and a nuclear gene (COI and 18S), the phylogeography of fifteen populations distributed along the West Antarctic Peninsula and Burdwood Bank/MPA Namuncurá (South American shelf) was characterized, where the distribution of the genetic distance suggested the existence of, at least, two species within nominal C. verrucosa. When reevaluating morphological traits to distinguish between genetically defined species, the presence of a basal disk in one of the genotypes could be a diagnostic morphological trait to differentiate the species. These results are surprising due to the large research that has been carried out with the conspicuous C. verrucosa with no differentiation between species. Furthermore, it provides important tools to distinguish species in the field and laboratory. But also, these results give new insights into patterns of differentiation between closely related species that are distributed in sympatry, where the permeability of species boundaries still needs to be well understood.

Benthic colonization in newly ice-free soft-bottom areas in an Antarctic fjord.

Extended glacier retreat is among the main consequences of the rapid warming of the West Antarctic Peninsula. Particularly, in the inner part of Potter Cove (South Shetland Islands, Antarctica) large areas are now exposed to open sea conditions owing to the retreat of Fourcade glacier. During the 2010 austral summer, underwater photographic surveys were undertaken by SCUBA diving up to 30 m in these new ice-free areas 80 m from the glacier front. Our main aim was to investigate colonization and early succession of the benthic assemblages on soft-bottom areas. Here, we reported a total of 1,146 animals belonging to 13 taxa. Filter-feeders comprised the largest trophic group and sessile fauna showed much higher coverages and densities than mobile fauna at all depths. The most abundant groups were ascidians and bryozoans, which together comprised ~90% of all taxa documented. In a region where most of marine-terminating glaciers are in retreat, these results are an important contribution to improve our knowledge on colonization in the newly ice-free areas.

Reproductive Seasonality of the Antarctic Sea Pen Malacobelemnon daytoni (Octocorallia, Pennatulacea, Kophobelemnidae).

The pennatulid Malacobelemnon daytoni is one of the dominant species in Potter Cove, Antarctica. Its abundance and range of distribution have increased in recent years probably related to climate change mediated alterations of environmental factors. This work is the second part of a study dealing on the reproductive ecology of Malacobelemnon daytoni, and aims to assess its reproductive seasonality over a two-year period. Sampling was carried out every month during 2009-2010 and samples were examined by histological analysis. Gametogenesis exhibited a seasonal pattern evidenced by the maturity stage index (MSI) and the number of mature oocytes and cysts throughout the year. Immature oocytes and spermatocytes were present year-round, but maturation was seasonal and it seems that more than one spawning per year was possible. These spawnings could be more linked with suspended particulate matter (SPM) (probably available via resuspension events) than with primary production pulses. This idea reinforces the hypothesis that winter time is not so stressful, in energy terms, in Potter Cove, which seems to depend on energy sources other than local phytoplankton production. There was not a strong inter-annual variability between the reproductive characteristics analyzed in 2009 and 2010; the only variable different was the size of oocytes (higher in 2009), suggesting different energy availability in each year, related with a higher concentration of SPM in 2009 (although it was not significant). Malacobelemnon daytoni could be the first reported Antarctic suspension feeder species that presents a reproductive cycle with more than a spawning event per year. This strategy would help to explain the success of this species in the Potter Cove ecosystem and in high ice-impacted areas.

Climate change and glacier retreat drive shifts in an Antarctic benthic ecosystem.

The Antarctic Peninsula (AP) is one of the three places on Earth that registered the most intense warming in the last 50 years, almost five times the global mean. This warming has strongly affected the cryosphere, causing the largest ice-shelf collapses ever observed and the retreat of 87% of glaciers. Ecosystem responses, although increasingly predicted, have been mainly reported for pelagic systems. However, and despite most Antarctic species being benthic, responses in the Antarctic benthos have been detected in only a few species, and major effects at assemblage level are unknown. This is probably due to the scarcity of baselines against which to assess change. We performed repeat surveys of coastal benthos in 1994, 1998, and 2010, analyzing community structure and environmental variables at King George Island, Antarctica. We report a marked shift in an Antarctic benthic community that can be linked to ongoing climate change. However, rather than temperature as the primary factor, we highlight the resulting increased sediment runoff, triggered by glacier retreat, as the potential causal factor. The sudden shift from a "filter feeders-ascidian domination" to a "mixed assemblage" suggests that thresholds (for example, of tolerable sedimentation) and alternative equilibrium states, depending on the reversibility of the changes, could be possible traits of this ecosystem. Sedimentation processes will be increasing under the current scenario of glacier retreat, and attention needs to be paid to its effects along the AP.

Benthic Trophic Interactions in an Antarctic Shallow Water Ecosystem Affected by Recent Glacier Retreat.

The western Antarctic Peninsula is experiencing strong environmental changes as a consequence of ongoing regional warming. Glaciers in the area are retreating rapidly and increased sediment-laden meltwater runoff threatens the benthic biodiversity at shallow depths. We identified three sites with a distinct glacier-retreat related history and different levels of glacial influence in the inner part of Potter Cove (King George Island, South Shetland Islands), a fjord-like embayment impacted since the 1950s by a tidewater glacier retreat. We compared the soft sediment meio- and macrofauna isotopic niche widths (δ13C and δ15N stable isotope analysis) at the three sites to investigate possible glacier retreat-related influences on benthic trophic interactions. The isotopic niches were locally shaped by the different degrees of glacier retreat-related disturbance within the Cove. Wider isotopic niche widths were found at the site that has become ice-free most recently, and narrower niches at the older ice-free sites. At an intermediate state of glacier retreat-related disturbance (e.g. via ice-growler scouring) species with different strategies could settle. The site at the earliest stage of post-retreat development was characterized by an assemblage with lower trophic redundancy. Generally, the isotopic niche widths increased with increasing size spectra of organisms within the community, excepting the youngest assemblage, where the pioneer colonizer meiofauna size class displayed the highest isotopic niche width. Meiofauna at all sites generally occupied positions in the isotopic space that suggested a detrital-pool food source and/or the presence of predatory taxa. In general ice scour and glacial impact appeared to play a two-fold role within the Cove: i) either stimulating trophic diversity by allowing continuous re-colonization of meiofaunal species or, ii) over time driving the benthic assemblages into a more compact trophic structure with increased connectedness and resource recycling.

When shape matters: strategies of different Antarctic ascidians morphotypes to deal with sedimentation.

Climate change leads to increased melting of tidewater glaciers in the Western Antarctic Peninsula region and sediment bearing glacial melt waters negatively affects filter feeding species as solitary ascidians. In previous work the erect-forms Molgula pedunculata and Cnemidocarpa verrucosa (Order Stolidobranchiata) appeared more sensitive than the flat form Ascidia challengeri (Order Phlebobranchiata). Sedimentation exposure is expected to induce up-regulation of anaerobic metabolism by obstructing the organs of gas exchange (environmental hypoxia) or causes enhanced squirting activity (functional hypoxia). In this study we evaluated the possible relationship between ascidian morphotype and their physiological response to sedimentation. Together with some behavioural observations, we analysed the response of anaerobic metabolic parameters (lactate formation and glycogen consumption) in different tissues of three Antarctic ascidians, exposed to high sediment concentrations (200 mgL(-1)). The results were compared to experimental hypoxia (10% pO2) and exercise (induced muscular contraction) effects, in order to discriminate the effect of sediment on each species and morpho-type (erect vs. flat forms). Our results suggest that the styled (erect) C. verrucosa increases muscular squirting activity in order to expulse excessive material, while the flat-form A. challengeri reacts more passively by down-regulating its aerobic metabolism under sediment exposure. Contrary, the erect ascidian M. pedunculata did not show any measurable response to the treatments, indicating that filtration and ingestion activities were not reduced or altered even under high sedimentation (low energetic material) which could be disadvantageous on the long-term and could explain why M. pedunculata densities decline in the study area.