Biologging of emperor penguins-Attachment techniques and associated deployment performance.

An increasing number of marine animals are equipped with biologgers, to study their physiology, behaviour and ecology, often for conservation purposes. To minimise the impacts of biologgers on the animals' welfare, the Refinement principle from the Three Rs framework (Replacement, Reduction, Refinement) urges to continuously test and evaluate new and updated biologging protocols. Here, we propose alternative and promising techniques for emperor penguin (Aptenodytes forsteri) capture and on-site logger deployment that aim to mitigate the potential negative impacts of logger deployment on these birds. We equipped adult emperor penguins for short-term (GPS, Time-Depth Recorder (TDR)) and long-term (i.e. planned for one year) deployments (ARGOS platforms, TDR), as well as juvenile emperor penguins for long-term deployments (ARGOS platforms) in the Weddell Sea area where they had not yet been studied. We describe and qualitatively evaluate our protocols for the attachment of biologgers on-site at the colony, the capture of the animals and the recovery of the devices after deployment. We report unprecedented recaptures of long-term equipped adult emperor penguins (50% of equipped individuals recaptured after 290 days). Our data demonstrate that the traditional technique of long-term attachment by gluing the biologgers directly to the back feathers causes excessive feather breakage and the loss of the devices after a few months. We therefore propose an alternative method of attachment for back-mounted devices. This technique led to successful year-round deployments on 37.5% of the equipped juveniles. Finally, we also disclose the first deployments of leg-bracelet mounted TDRs on emperor penguins. Our findings highlight the importance of monitoring potential impacts of biologger deployments on the animals and the need to continue to improve methods to minimize disturbance and enhance performance and results.

Devonian agglutinated polychaete tubes: all in all it's just another grain in the wall.

Biomineralized and organic metazoan tubular skeletons are by far the most common in the fossil record. However, several groups of organisms are also able to agglutinate particles to construct more rigid structures. Here we present a novel type of agglutinated tube from the austral and endemic palaeobiota of the Malvinokaffric realm (Devonian, Brazil). This fossil is characterized by an agglutinated tube made of silt-sized particles forming an unusual flanged morphology that is not known from the fossil record. Besides being able to select specific particles, these organisms probably lived partially buried and were detritus/suspension feeders. Comparisons across different modern groups show that these fossils are strongly similar to tubes made by polychaetes, specifically from the family Maldanidae. If this interpretation is correct, then an early divergence of the Sedentaria clade may have occurred before the Devonian.

Linking multiple facets of biodiversity and ecosystem functions in a coastal reef habitat.

Reef-building species play key roles in promoting local species richness and regulating ecosystem functions like biogeochemical fluxes. We evaluated the functioning of a habitat engineered by the reef-building polychaete Sabellaria alveolata, by measuring oxygen and nutrient fluxes in the reef structures and in the soft-sediments nearby. Then, we investigated the relative importance of temperature, the engineer S. alveolata, and different facets of macrofauna diversity (taxonomic, functional diversity and identity), on the reef biogeochemical fluxes using multiple linear regressions and effect sizes. The reef fluxes were more intense than the soft-sediment fluxes and mainly driven by the engineer biomass and abundance, stressing the importance of these biogenic structures. Higher water temperatures and an intermediate level of associated macrofauna functional dispersion weighted only by abundance (i.e. intermediate biological trait variability) maximized the reef's global biogeochemical functioning. Ultimately, the physical degradation of the reefs could lead to lower levels of functioning.

Recent trend reversal for declining European seagrass meadows.

Seagrass meadows, key ecosystems supporting fisheries, carbon sequestration and coastal protection, are globally threatened. In Europe, loss and recovery of seagrasses are reported, but the changes in extent and density at the continental scale remain unclear. Here we collate assessments of changes from 1869 to 2016 and show that 1/3 of European seagrass area was lost due to disease, deteriorated water quality, and coastal development, with losses peaking in the 1970s and 1980s. Since then, loss rates slowed down for most of the species and fast-growing species recovered in some locations, making the net rate of change in seagrass area experience a reversal in the 2000s, while density metrics improved or remained stable in most sites. Our results demonstrate that decline is not the generalised state among seagrasses nowadays in Europe, in contrast with global assessments, and that deceleration and reversal of declining trends is possible, expectingly bringing back the services they provide.

Increased sea ice cover alters food web structure in East Antarctica.

In recent years, sea ice cover along coasts of East Antarctica has tended to increase. To understand ecological implications of these environmental changes, we studied benthic food web structure on the coasts of Adélie Land during an event of unusually high sea ice cover (i.e. two successive austral summers without seasonal breakup). We used integrative trophic markers (stable isotope ratios of carbon, nitrogen and sulfur) to build ecological models and explored feeding habits of macroinvertebrates. In total, 28 taxa spanning most present animal groups and functional guilds were investigated. Our results indicate that the absence of seasonal sea ice breakup deeply influenced benthic food webs. Sympagic algae dominated the diet of many key consumers, and the trophic levels of invertebrates were low, suggesting omnivore consumers did not rely much on predation and/or scavenging. Our results provide insights about how Antarctic benthic consumers, which typically live in an extremely stable environment, might adapt their feeding habits in response to sudden changes in environmental conditions and trophic resource availability. They also show that local and/or global trends of sea ice increase in Antarctica have the potential to cause drastic changes in food web structure, and therefore to impact benthic communities.

Adhesive gland transcriptomics uncovers a diversity of genes involved in glue formation in marine tube-building polychaetes.

Tube-building sabellariid polychaetes are hermatypic organisms capable of forming vast reefs in highly turbulent marine habitats. Sabellariid worms assemble their tube by gluing together siliceous and calcareous clastic particles using a polyelectrolytic biocement. Here, we performed transcriptomic analyses to investigate the genes that are differentially expressed in the parathorax region, which contains the adhesive gland and tissues, from the rest of the body. We found a large number of candidate genes to be involved in the composition and formation of biocement in two species: Sabellaria alveolata and Phragmatopoma caudata. Our results indicate that the glue is likely to be composed by a large diversity of cement-related proteins, including Poly(S), GY-rich, H-repeat and miscellaneous categories. However, sequences divergence and differences in expression profiles between S. alveolata and P. caudata of cement-related proteins may reflect adaptation to the type of substratum used to build their tube, and/or to their habitat (temperate vs tropical, amplitude of pH, salinity …). Related to the L-DOPA metabolic pathways and linked with the genes that were differentially expressed in the parathorax region, we found that tyrosinase and peroxidase gene families may have undergone independent expansion in the two Sabellariidae species investigated. Our data also reinforce the importance of protein modifications in cement formation. Altogether these new genomic resources help to identify novel transcripts encoding for cement-related proteins, but also important enzymes putatively involved in the chemistry of the adhesion process, such as kinases, and may correspond to new targets to develop biomimetic approaches. STATEMENTS OF SIGNIFICANCE: The diversity of bioadhesives elaborated by marine invertebrates is a tremendous source of inspiration to develop biomimetic approaches for biomedical and technical applications. Recent studies on the adhesion system of mussel, barnacle and sea star had highlighted the usefulness of high-throughput RNA sequencing in accelerating the development of biomimetic adhesives. Adhesion in sandcastle worms, which involves catechol and phosphate chemistries, polyelectrolyte complexes, supramolecular architectures, and a coacervation process, is a useful model to develop multipurpose wet adhesives. Using transcriptomic tools, we have explored the diversity of genes encoding for structural and catalytic proteins involved in cement formation of two sandcastle worm species, Sabellaria alveolata and Phragmatopoma caudata. The important genomic resource generated should help to design novel "blue" adhesives.

Latitudinal Patterns in European Seagrass Carbon Reserves: Influence of Seasonal Fluctuations versus Short-Term Stress and Disturbance Events.

Seagrass meadows form highly productive and valuable ecosystems in the marine environment. Throughout the year, seagrass meadows are exposed to abiotic and biotic variations linked to (i) seasonal fluctuations, (ii) short-term stress events such as, e.g., local nutrient enrichment, and (iii) small-scale disturbances such as, e.g., biomass removal by grazing. We hypothesized that short-term stress events and small-scale disturbances may affect seagrass chance for survival in temperate latitudes. To test this hypothesis we focused on seagrass carbon reserves in the form of starch stored seasonally in rhizomes, as these have been defined as a good indicator for winter survival. Twelve Zostera noltei meadows were monitored along a latitudinal gradient in Western Europe to firstly assess the seasonal change of their rhizomal starch content. Secondly, we tested the effects of nutrient enrichment and/or biomass removal on the corresponding starch content by using a short-term manipulative field experiment at a single latitude in the Netherlands. At the end of the growing season, we observed a weak but significant linear increase of starch content along the latitudinal gradient from south to north. This agrees with the contention that such reserves are essential for regrowth after winter, which is more severe in the north. In addition, we also observed a weak but significant positive relationship between starch content at the beginning of the growing season and past winter temperatures. This implies a lower regrowth potential after severe winters, due to diminished starch content at the beginning of the growing season. Short-term stress and disturbances may intensify these patterns, because our manipulative experiments show that when nutrient enrichment and biomass loss co-occurred at the end of the growing season, Z. noltei starch content declined. In temperate zones, the capacity of seagrasses to accumulate carbon reserves is expected to determine carbon-based regrowth after winter. Therefore, processes affecting those reserves might affect seagrass resilience. With increasing human pressure on coastal systems, short- and small-scale stress events are expected to become more frequent, threatening the resilience of seagrass ecosystems, particularly at higher latitudes, where populations tend to have an annual cycle highly dependent on their storage capacity.

Integrating Ecosystem Engineering and Food Web Ecology: Testing the Effect of Biogenic Reefs on the Food Web of a Soft-Bottom Intertidal Area.

The potential of ecosystem engineers to modify the structure and dynamics of food webs has recently been hypothesised from a conceptual point of view. Empirical data on the integration of ecosystem engineers and food webs is however largely lacking. This paper investigates the hypothesised link based on a field sampling approach of intertidal biogenic aggregations created by the ecosystem engineer Lanice conchilega (Polychaeta, Terebellidae). The aggregations are known to have a considerable impact on the physical and biogeochemical characteristics of their environment and subsequently on the abundance and biomass of primary food sources and the macrofaunal (i.e. the macro-, hyper- and epibenthos) community. Therefore, we hypothesise that L. conchilega aggregations affect the structure, stability and isotopic niche of the consumer assemblage of a soft-bottom intertidal food web. Primary food sources and the bentho-pelagic consumer assemblage of a L. conchilega aggregation and a control area were sampled on two soft-bottom intertidal areas along the French coast and analysed for their stable isotopes. Despite the structural impacts of the ecosystem engineer on the associated macrofaunal community, the presence of L. conchilega aggregations only has a minor effect on the food web structure of soft-bottom intertidal areas. The isotopic niche width of the consumer communities of the L. conchilega aggregations and control areas are highly similar, implying that consumer taxa do not shift their diet when feeding in a L. conchilega aggregation. Besides, species packing and hence trophic redundancy were not affected, pointing to an unaltered stability of the food web in the presence of L. conchilega.

Ephemeral bio-engineers or reef-building polychaetes: how stable are aggregations of the tube worm Lanice conchilega (Pallas, 1766)?

Dense aggregations of tube-worms can stabilize sediments and generate oases for benthic communities that are different and often more diverse and abundant than those of the surroundings. If these features are to qualify as biogenic reefs under nature-conservation legislation such as the EC Habitats Directive, a level of stability and longevity is desirable aside from physical and biological attributes. Lanice conchilega (Pallas, 1766) is widely distributed around the European coast and aggregations of this tube-dwelling polychaete are known to have a positive effect on the biodiversity of associated species in inter- and sub-tidal areas. This increases the value of L. conchilega-rich habitats for higher trophic levels such as birds and fish. However, L. conchilega is currently not recognized as a reef builder primarily due to uncertainty about the stability of their aggregations. We carried out three studies on different spatial and temporal scales to explore a number of properties relating to stability: (1) Individual aggregations of L. conchilega of ∼1 m(2) were monitored for up to 1 year, (2) records of L. conchilega from a 258-ha area over a 35-year period were analyzed, (3) the recovery of a population of L. conchilega subjected to disturbances by cultivation of Manila clams (Ruditapes philippinarum) was followed over 3 years. The studies provided evidence about the longevity of L. conchilega aggregations, their resistance to disturbance, their resilience in recovering from negative impact and their large-scale persistence. The results showed that populations of L. conchilega were prone to considerable fluctuation and the stability of aggregations depended on environmental factors and on recruitment. The tube-worms proved to be susceptible to disturbance by cultivation of Manila clams but demonstrated the potential to recover from that impact. The long-term monitoring of a large L. conchilega population in the Bay of Mont Saint Michel (France) indicated that aggregations can persist over many decades with a constant, densely populated core area and an expanding and contracting more thinly populated fringe zone. The stability of aggregations of L. conchilega and the structures they form do not unequivocally fit the currently accepted definition of a reef. However, given L. conchilega's accepted reef-like potential to influence diversity and abundance in benthic communities, we suggest clarifying and expanding the definition of reefs so that species with records of significant persistence in particular areas and which otherwise meet expectations of reefs are included within the definition.

Clam farmers and Oystercatchers: effects of the degradation of Lanice conchilega beds by shellfish farming on the spatial distribution of shorebirds.

The Manila clam Ruditapes philippinarum cultivation is an original shellfish farming activity strongly mechanized. In the Chausey archipelago (France) this activity settles on the Lanice conchilega beds, habitat known to host a rich and diversified benthic macrofauna and which is an attractive feeding ground for birds. A first study highlighted that this activity had strong negative effects on the L. conchilega beds and their associated benthic macrofauna. Here we assess the impacts of such an activity on the Eurasian Oystercatcher Haematopus ostralegus for which Chausey is one of the most important national breeding sites and which is also a common species in winter, spring and autumn migrations. We found that Oystercatchers significantly selected the L. conchilega beds to feed and that their spatial distribution was significantly modified after the creation of new clam concessions. In a context of a growing disappearance of pristine coastal ecosystems for the benefit of anthropo-ecosystems, we discuss the problem of the degradation of such benthic habitats with a low resilience which may loose their high functional value.

Considering the functional value of common marine species as a conservation stake: the case of sandmason worm Lanice conchilega (Pallas 1766) (Annelida, Polychaeta) beds.

Conservation of the marine environment mainly focuses on threatened elements and more precisely on vulnerable and endangered species like birds and mammals. When dealing with the conservation of marine habitats, the scientific community is mainly interested in hot spots of diversity, like seagrass beds in Europe, or hot spots of endemism, like coral reefs in tropical areas. Nevertheless, using the example of a common and widespread marine invertebrate, the sandmason worm (Lanice conchilega, Polychaeta, Terebellidae), we show that vulnerability and rarity are not the only criteria to take into account in order to select the best natural element for conservation. This species can form dense beds that increase biodiversity, are attractive feeding grounds for birds and fishes, and have a high socioeconomic value. In consequence, they have a high functional value that should be considered as an important conservation stake. Through the example of the Chausey archipelago and the Bay of the Mont Saint-Michel (France), we propose a synthetic interdisciplinary approach to evaluate the conservation needs of these beds. The issue is even more pressing when one considers that these natural elements and many similar ones still do not benefit from any legal protection in Europe despite their high heritage value.

Before and after wasting disease in common eelgrass Zostera marina along the French Atlantic coasts: a general overview and first accurate mapping.

We examined the original manuscripts of a French national survey conducted in 1933 on the state of common eelgrass Zostera marina beds along the French Atlantic coasts during the period when wasting disease struck the entire North Atlantic population in the 1930s. Based on GIS related techniques and old sets of aerial photographs, we present the first accurate mapping of the Z. marina beds before wasting disease occurred and assess their spatial recolonization since the 1950s in the Chausey Archipelago (France), which contains large Z. marina beds. The national survey confirmed that the Z. marina beds almost totally disappeared from the French coasts during the 1930s. However, the disease symptoms seem to have begun locally a few years before. On the study site, we found that the Z. marina beds were more than twice as extended than as they are today, and covered both subtidal and intertidal areas. By the 1950s, 20 yr after the onset of the disease, the beds had hardly recolonized, and contrary to the recolonization patterns reported elsewhere in Europe, they were mainly restricted to subtidal areas. The subtidal and intertidal Z. marina beds on the site are now rapidly expanding.

Does Manila clam cultivation affect habitats of the engineer species Lanice conchilega (Pallas, 1766)?

The major French site of Manila clam Ruditapes philippinarum (Adams and Reeves, 1850) cultivation is located in the Chausey Archipelago where the associated practices are highly mechanized: every steps of production are made with tractor-driven machinery. The Manila clam concessions are concentrated on Lanice conchilega (Pallas, 1766) bioherms, which are known to increase alpha-diversity and to locally modify sediment dynamics. This study focus on the impacts of Manila clam cultivation on (i) the natural populations of L. conchilega and on (ii) the structure of the associated benthic assemblages during the different steps of the farming production cycle. We found that the L. conchilega populations are significantly affected within the concessions where their total abundances drastically decrease, their spatial patterns are modified and the associated benthic assemblages are significantly altered. Our results are discussed in a context of a sustainable management of the Manila clam cultivation in coastal areas.