Aggregative versus solitary settlement in Spirobranchus cariniferus gray, 1843 (serpulinae). What is the trade-off?

Sessile marine invertebrates usually follow a distinct pattern of living in dense aggregations or as solitary individuals. However, at least some serpulins, including Spirobranchus cariniferus, seem to be able to settle aggregative or solitary. To understand how living solitary or in aggregation is beneficial, it is essential to understand the advantages and disadvantages of both settlement strategies for sessile invertebrates. Benefits of living in aggregations include securing suitable habitat, improving the probability of survival by mitigating physical stress and increasing reproductive success. However, living in patches also comes with some disadvantages for the individual, such as higher intra- and interspecific competition for food, space and oxygen. Increased physiological stress can lead to increased mortality and decreased reproductive success, whereas solitary individuals could produce more gametes because of a lack of competition for food and space. On the other hand, predators would have easier access to them, and the possibility of fertilisation success may be lower because of a lack of synchronisation and a greater distance between individuals of different sexes. These issues have not been sufficiently addressed, particularly for serpulids. Individuals of the New Zealand endemic polychaete Spirobranchus cariniferus can be found solitary and aggregative in the same habitat. Therefore, this study is the first on serpulids comparing the growth and mortality of individuals living alone or in aggregations. Hence, bi-monthly observation of mortality and growth measurements were conducted on tagged individuals in the field, and weekly observations were conducted in a laboratory-based study on individuals of both settlement configurations. A final comparison of body metrics to tube dimensions was made by removing an individual from their tube. My findings revealed that while solitary and aggregative individuals elongate their tubes at a similar rate, further correlations of the body to tube sizes lead to the conclusion that solitary worms focus more of their energy on tube growth rather than body size increment than aggregative conspecifics. Mortality is highly variable and seems not to differ between both configurations. However, individuals living in a patch can better recover from damage to their tubes. Here presented observations hopefully initiated further studies into the effects of aggregation size and density on individual growth. Results of this and subsequent studies can inform the management efforts for reefs of serpulins, bivalves and other invertebrates.

Ultrastructure of the Jurassic serpulid tubes-phylogenetic and paleoecological implications.

The ultrastructural diversity of the Middle and Late Jurassic serpulid tubes from the Polish Basin has been investigated. The inspection of 12 taxa representing the two major serpulid clades allowed for the identification of three ultrastructure types-irregularly oriented prismatic structure (IOP), spherulitic prismatic structure (SPHP), and simple prismatic structure (SP). Six of the studied species are single-layered and six species possess two distinct layers. Ultrastructural diversity corresponds to certain serpulid clades. The members of Filograninae have single-layered tube walls composed of possibly plesiomorphic, irregularly oriented prismatic structure (IOP). Two-layered tubes occur solely within the clade Serpulinae, where the external, denser layer is built of either the ordered spherulitic (SPHP) or simple prismatic microstructure (SP), and the internal layer is composed of irregularly oriented prismatic structure (IOP). Apart from phylogenetic signals provided by the tube ultrastructure, it can be used in analyzing paleoecological aspects of tube-dwelling polychaetes. Compared to the more primitive, irregularly oriented microstructures of Filograninae, the regularly oriented microstructures of Serpulinae need a higher level of biological control over biomineralization. The advent of the dense outer protective layer (DOL) in serpulids, as well as the general increase in ultrastructure diversity, was likely a result of the evolutionary importance of the tubes for serpulids. Such diversity of the tube ultrastructural fabrics allowed for maximizing functionality by utilizing a variety of morphogenetic programs. The biomineralization system of serpulids remains more complex compared to other tube-dwelling polychaetes. Physiologically more expensive tube formation allows for mechanical strengthening of the tube by building robust, strongly ornamented tubes and firm attachment to the substrate. Contrary to sabellids, which perform a fugitive strategy, an increased tube durability allows serpulids a competitive advantage over other encrusters.

Serpulid reefs and their role in aquatic ecosystems: A global review.

The Serpulidae are a large family of sedentary polychaetes, characterized by a calcareous habitation tube, which they cannot leave. The calcium carbonate tube is in the form of both aragonite and calcite, in fairly constant ratio for each taxon. Tubes are cemented firmly to any hard substrate (in only few species tubes are free). Although in the majority of the species the tubes encrust the substrate for all their length, the distal part may eventually detach and grow erectly. Certain species in dense populations build tubes vertical to the substrate in clumps and cement the tubes to each other. This gives serpulids the capability of forming reef-life structures when densely settling. Despite the relative smallness of the individual tubes (rarely longer than 15cm and wider than 1cm), such reef-like structures may cover tens of m2, with a layer more than 1m thick. Serpulid reefs can be divided roughly into seven groups, according to the building modality and the type of habitat they occupy: (i) pseudocolonies; (ii) littoral belts; (iii) subtidal to deep-water reefs; (iv) reefs in coastal lakes and harbours; (v) brackish water reefs; (vi) tapestries in freshwater caves; (vii) biostalactites inside marine caves. The role of serpulid reefs in the ecosystems they inhabit is multifarious and may be distinguished in functions (biomass and production, benthic pelagic coupling, resistance and resilience, reproductive and survivorship strategies, trophodynamics, bioconstruction, living space and refuge, nursery, sediment formation and retention, food for other species, carbonate deposition and storage) and services (water clearance, reef associated fishery, cultural benefits). On the other hand, many serpulids are important constituents of biological fouling, and their calcareous masses damage submerged artefacts, causing huge economic costs. Positive and negative roles of serpulid reefs need to be compared with common metrics; the overall balance, however, is still to be assessed.

Another blow to the conserved gene order in Annelida: Evidence from mitochondrial genomes of the calcareous tubeworm genus Hydroides.

Mitochondrial genomes are frequently applied in phylogenetic and evolutionary studies across metazoans, yet they are still poorly represented in many groups of invertebrates, including annelids. Here, we report ten mitochondrial genomes from the annelid genus Hydroides (Serpulidae) and compare them with all available annelid mitogenomes. We detected all 13 protein coding genes in Hydroides spp., including the atp8 which was reported as a missing gene in the Christmas Tree worm Spirobranchus giganteus, another annelid of the family Serpulidae. All available mitochondrial genomes of Hydroides show a highly positive GC skew combined with a highly negative AT skew - a feature consistent with that found only in the mitogenome of S. giganteus. In addition, amino acid sequences of the 13 protein-coding genes showed a high genetic distance between the Hydroides clade and S. giganteus, suggesting a fast rate of mitochondrial sequence evolution in Serpulidae. The gene order of protein-coding genes within Hydroides exhibited extensive rearrangements at species level, and were different from the arrangement patterns of other annelids, including S. giganteus. Phylogenetic analyses based on protein-coding genes recovered Hydroides as a monophyletic group sister to Spirobranchus with a long branch, and sister to the fan worm Sabellidae. Yet the Serpulidae + Sabellidae clade was unexpectedly grouped with Sipuncula, suggesting that mitochondrial genomes alone are insufficient to resolve the phylogenetic position of Serpulidae within Annelida due to its high base substitution rates. Overall, our study revealed a high variability in the gene order arrangement of mitochondrial genomes within Serpulidae, provided evidence to question the conserved pattern of the mitochondrial gene order in Annelida and called for caution when applying mitochondrial genes to infer their phylogenetic relationships.

More is needed-Thousands of loci are required to elucidate the relationships of the 'flowers of the sea' (Sabellida, Annelida).

Sabellida is a well-known clade containing tube-dwelling annelid worms with a radiolar crown. Iterative phylogenetic analyses over three decades have resulted in three main clades being recognized; Fabriciidae, Serpulidae and Sabellidae, with Fabriciidae proposed as the sister group to Serpulidae. However, relationships within Sabellidae have remained poorly understood, with a proliferation of genera. In order to obtain a robust phylogeny with optimal support, we conducted a large-scale phylogenomic analysis with 19 new sabellid transcriptomes for a total of 21 species. In contrast to earlier findings based on limited DNA data, our results support the position of Fabriciidae as sister taxon to a Sabellidae + Serpulidae clade. Our large sampling within Sabellidae also allows us to establish a stable phylogeny within this clade. We restrict Sabellinae to a subclade of Sabellidae and broaden the previously monotypic Myxicolinae to include Amphicorina and Chone. We tested the robustness of species tree reconstruction by subsampling increasing numbers of genes to uncover hidden support of alternative topologies. Our results show that inclusion of more genes leads to a more stable topology with higher support, and also that including higher divergence genes leads to stronger resolution.

Soluble esterases as biomarkers of neurotoxic compounds in the widespread serpulid Ficopomatus enigmaticus (Fauvel, 1923).

The characterization of soluble cholinesterases (ChEs) together with carboxylesterases (CEs) in Ficopomatus enigmaticus as suitable biomarkers of neurotoxicity was the main aim of this study. ChEs of F. enigmaticus were characterized considering enzymatic activity, substrate affinity (acetyl-, butyryl-, propionylthiocholine), kinetic parameters (Km and Vmax) and in vitro response to model inhibitors (eserine hemisulfate, iso-OMPA, BW284C51), and carbamates (carbofuran, methomyl, aldicarb, and carbaryl). CEs were characterized based on enzymatic activity, kinetic parameters and in vitro response to carbamates (carbofuran, methomyl, aldicarb, and carbaryl). Results showed that cholinesterases from F. enigmaticus showed a substrate preference for acetylthiocholine followed by propionylthiocholine; butyrylthioline was not hydrolyzed differently from other Annelida species. CE activity was in the same range of cholinesterase activity with acetylthiocholine as substrate; the enzyme activity showed high affinity for the substrate p-nytrophenyl butyrate. Carbamates inhibited ChE activity with propionylthiocholine as substrate to a higher extent than with acetylthiocoline. Also CE activity was inhibited by all tested carbamates except carbaryl. In vitro data highlighted the presence of active forms of ChEs and CEs in F. enigmaticus that could potentially be inhibited by pesticides at environmentally relevant concentration.

An in situ assessment of local adaptation in a calcifying polychaete from a shallow CO2 vent system.

Ocean acidification (OA) is likely to exert selective pressure on natural populations. Our ability to predict which marine species will adapt to OA and what underlies this adaptive potential is of high conservation and resource management priority. Using a naturally low-pH vent site in the Mediterranean Sea (Castello Aragonese, Ischia) mirroring projected future OA conditions, we carried out a reciprocal transplant experiment to investigate the relative importance of phenotypic plasticity and local adaptation in two populations of the sessile, calcifying polychaete Simplaria sp. (Annelida, Serpulidae, Spirorbinae): one residing in low pH and the other from a nearby ambient (i.e. high) pH site. We measured a suite of fitness-related traits (i.e. survival, reproductive output, maturation, population growth) and tube growth rates in laboratory-bred F2 generation individuals from both populations reciprocally transplanted back into both ambient and low-pH in situ habitats. Both populations showed lower expression in all traits, but increased tube growth rates, when exposed to low-pH compared with high-pH conditions, regardless of their site of origin suggesting that local adaptation to low-pH conditions has not occurred. We also found comparable levels of plasticity in the two populations investigated, suggesting no influence of long-term exposure to low pH on the ability of populations to adjust their phenotype. Despite high variation in trait values among sites and the relatively extreme conditions at the low pH site (pH < 7.36), response trends were consistent across traits. Hence, our data suggest that, for Simplaria and possibly other calcifiers, neither local adaptations nor sufficient phenotypic plasticity levels appear to suffice in order to compensate for the negative impacts of OA on long-term survival. Our work also emphasizes the utility of field experiments in natural environments subjected to high level of pCO 2 for elucidating the potential for adaptation to future scenarios of OA.

Sperm swimming in the polychaete Galeolaria caespitosa shows substantial inter-individual variability in response to future ocean acidification.

The rapidity of ocean acidification intensifies selection pressure for resilient phenotypes, particularly during sensitive early life stages. The scope for selection is greater in species with greater within-species variation in responses to changing environments, thus enhancing the potential for adaptation. We investigated among-male variation in sperm swimming responses (percent motility and swimming speeds) of the serpulid polychaete Galeolaria caespitosa to near- (ΔpH -0.3) and far-future ocean acidification (ΔpH -0.5). Responses of sperm swimming to acidification varied significantly among males and were overall negative. Robust sperm swimming behavior under near-future ocean acidification in some males may ameliorate climate change impacts, if traits associated with robustness are heritable, and thereby enhance the potential for adaptation to far-future conditions. Reduced sperm swimming in the majority of male G. caespitosa may decrease their fertilization success in a high CO2 future ocean. Resultant changes in offspring production could affect recruitment success and population fitness downstream.