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Abstract Mollusca is a morphologically diverse phylum, exhibiting an immense variety of calcium carbonate structures. Proteomic studies of adult shells often report high levels of rapidly-evolving, ‘novel’ shell matrix proteins (SMPs), which are hypothesized to drive shell diversification. However, relatively little is known about the phylogenetic distribution of SMPs, or about the function of individual SMPs in shell construction. To understand how SMPs contribute to shell diversification a thorough characterization of SMPs is required. Here, we build tools and a foundational understanding of SMPs in the marine gastropod species Crepidula fornicata and Crepidula atrasolea because they are genetically-enabled mollusc model organisms. First, we established a staging system of shell development in C. atrasolea for the first time. Next, we leveraged previous findings in C. fornicata combined with phylogenomic analyses of 95 metazoan species to determine the evolutionary lineage of its adult SMP repertoire. We found that 55% of C. fornicata’s SMPs belong to molluscan orthogroups, with 27% restricted to Gastropoda, and only 5% restricted at the species level. The low percentage of species-restricted SMPs underscores the importance of broad-taxon sampling and orthology inference approaches when determining homology of SMPs. From our transcriptome analysis, we found that the majority of C. fornicata SMPs that were found conserved in C. atrasolea were expressed in both larval and adult stages. We then selected a subset of SMPs of varying evolutionary ages for spatial-temporal analysis using in situ hybridization chain reaction (HCR) during larval shell development in C. atrasolea. Out of the 18 SMPs analyzed, 12 were detected in the larval shell field. These results suggest overlapping larval vs. adult SMP repertoires. Using multiplexed HCR, we observed five SMP expression patterns and three distinct cell populations within the shell field. These patterns support the idea that modular expression of SMPs could facilitate divergence of shell morphological characteristics. Collectively, these data establish an evolutionary and developmental framework in Crepidula that enables future comparisons of molluscan biomineralization to reveal mechanisms of shell diversification.

In order to investigate the serendipitous find of a gastropod encrusted by the symbiont-bearing colonial coral Oculina patagonica, we examined several specimens of cnidarian-encrusted gastropods, ranging in age from the Pliocene to the Recent, and characterized in detail their sclerobiont cover. The results of our analysis suggest that gastropod shells can be encrusted by symbiont-bearing colonial corals at various times: (1) when the gastropod is alive; (2) when the shell is being used by a secondary inhabitant (e.g., hermit crabs or sipunculid worms); (3) when the shell is discarded but yet to be buried. The relationship between the symbiont-bearing coral and the inhabitant(s) of the encrusted shell is an example of facultative mutualism, i.e., it is non-obligate yet beneficial for both ends as the former obtains the capability to move, and the latter improves the resistance and resilience of its armor, thus obtaining extra protection from predators. Being able to move could prove particularly useful for a symbiont-bearing coral because, in addition to removing the risk of being smothered by sediment, it would also favor the photosynthetic activity of its algal endosymbionts by allowing the coral to be always clean of sedimentary particles. Although the resulting epibiotic association would be limited in size by the ability of either the gastropod or the secondary inhabitant of the shell to move at the seafloor, these small and easy-to-miss benthic islands might become the seeds that allow sessile carbonate producers such as hermatypic colonial corals to colonize unconsolidated substrates. [ABSTRACT FROM AUTHOR]

Abstract Background One hundred years ago, marine organisms were the dominant systems for the study of developmental biology. The challenges in rearing these organisms outside of a marine setting ultimately contributed to a shift towards work on a smaller number of so-called model systems. Those animals are typically non-marine organisms with advantages afforded by short life cycles, high fecundity, and relative ease in laboratory culture. However, a full understanding of biodiversity, evolution, and anthropogenic effects on biological systems requires a broader survey of development in the animal kingdom. To this day, marine organisms remain relatively understudied, particularly the members of the Lophotrochozoa (Spiralia), which include well over one third of the metazoan phyla (such as the annelids, mollusks, flatworms) and exhibit a tremendous diversity of body plans and developmental modes. To facilitate studies of this group, we have previously described the development and culture of one lophotrochozoan representative, the slipper snail Crepidula atrasolea, which is easy to rear in recirculating marine aquaria. Lab-based culture and rearing of larger populations of animals remain a general challenge for many marine organisms, particularly for inland laboratories. Results Here, we describe the development of an automated marine aquatic rack system for the high-density culture of marine species, which is particularly well suited for rearing filter-feeding animals. Based on existing freshwater recirculating aquatic rack systems, our system is specific to the needs of marine organisms and incorporates robust filtration measures to eliminate wastes, reducing the need for regular water changes. In addition, this system incorporates sensors and associated equipment for automated assessment and adjustment of water quality. An automated feeding system permits precise delivery of liquid food (e.g., phytoplankton) throughout the day, mimicking real-life feeding conditions that contribute to increased growth rates and fecundity. Conclusion This automated system makes laboratory culture of marine animals feasible for both large and small research groups, significantly reducing the time, labor, and overall costs needed to rear these organisms.

In order to investigate the serendipitous find of a gastropod encrusted by the symbiont-bearing colonial coral Oculina patagonica, we examined several specimens of cnidarian-encrusted gastropods, ranging in age from the Pliocene to the Recent, and characterized in detail their sclerobiont cover. The results of our analysis suggest that gastropod shells can be encrusted by symbiont-bearing colonial corals at various times: (1) when the gastropod is alive; (2) when the shell is being used by a secondary inhabitant (e.g., hermit crabs or sipunculid worms); (3) when the shell is discarded but yet to be buried. The relationship between the symbiont-bearing coral and the inhabitant(s) of the encrusted shell is an example of facultative mutualism, i.e., it is non-obligate yet beneficial for both ends as the former obtains the capability to move, and the latter improves the resistance and resilience of its armor, thus obtaining extra protection from predators. Being able to move could prove particularly useful for a symbiont-bearing coral because, in addition to removing the risk of being smothered by sediment, it would also favor the photosynthetic activity of its algal endosymbionts by allowing the coral to be always clean of sedimentary particles. Although the resulting epibiotic association would be limited in size by the ability of either the gastropod or the secondary inhabitant of the shell to move at the seafloor, these small and easy-to-miss benthic islands might become the seeds that allow sessile carbonate producers such as hermatypic colonial corals to colonize unconsolidated substrates.

Sexual systems are surprisingly diverse, considering the ubiquity of sexual reproduction. Sequential hermaphroditism, the ability of an individual to change sex, has emerged multiple times independently across the animal kingdom. In molluscs, repeated shifts between ancestrally separate sexes and hermaphroditism are generally found at the level of family and above, suggesting recruitment of deeply conserved mechanisms. Despite this, molecular mechanisms of sexual development are poorly known. In molluscs with separate sexes, endocrine disrupting toxins bind the retinoid X receptor (RXR), activating ectopic male development in females, suggesting the retinoid pathway as a candidate controlling sexual transitions in sequential hermaphrodites. We therefore tested the role of retinoic acid signaling in sequentially hermaphroditic Crepidula snails, which develop first into males, then change sex, maturing into females. We show that retinoid agonists induce precocious penis growth in juveniles and superimposition of male development in females. Combining RXR antagonists with retinoid agonists significantly reduces penis length in induced juveniles, while similar treatments using retinoic acid receptor (RAR) antagonists increase penis length. Transcripts of both receptors are expressed in the induced penis. Our findings therefore show that retinoid signaling can initiate molluscan male genital development, and regulate penis length. Further, we show that retinoids induce ectopic male development in multiple Crepidula species. Species-specific influence of conspecific induction of sexual transitions correlates with responsiveness to retinoids. We propose that retinoid signaling plays a conserved role in molluscan male development, and that shifts in the timing of retinoid signaling may have been important for the origins of sequential hermaphroditism within molluscs. [Display omitted] • Retinoid agonists induce penis growth in sequentially hermaphroditic snails. • Blocking RXR or retinoic acid synthesis decreases penis length. • RXR , RAR , and CYP2 6 mRNA are expressed in the induced penis. • Shifts in retinoid timing may be involved in repeated evolution of hermaphroditism. [ABSTRACT FROM AUTHOR]

Mode of development (MOD) is a key feature that influences the rate and direction of evolution of marine invertebrates. Although many groups include species with different MODs, the evolutionary loss of feeding larvae is thought to be irreversible, as the complex structures used for larval feeding and swimming are lost, reduced, or modified in many species lacking feeding larvae. This view is largely based on observations of echinoderms. Phylogenetic analysis suggests that feeding larvae have been re-gained in at least one species of calyptraeid gastropod. Further, its sister species has retained the velum, the structure used for larval feeding and swimming. Here, we document velar morphology and function in calyptraeids with 4 different MODs. Embryos of Crepidula navicella, Crepidula atrasolea, Bostrycapulus aculeatus, Bostrycapulus odites, Bostrycapulus urraca, Crepipatella dilatata, Crepipatella occulta, Crucibulum quiriquinae and Crepidula coquimbensis all hatch as crawling juveniles, yet only Crepidula coquimbensis does not make a well-formed velum during intracapsular development. The velar dimensions of 6 species with non-planktotrophic development were similar to those of planktotrophic species, while the body sizes were significantly larger. All of the species studied were able to capture and ingest particles from suspension, but several non-planktotrophic species may ingest captured particles only occasionally. Video footage suggests that some species with adelphophagic direct development capture but frequently fail to ingest particles compared to species with the other MODs. Together these lines of evidence show that, among calyptraeids at least, species that lack planktotrophic larvae often retain the structures and functions necessary to successfully capture and ingest particles, reducing the barriers to the re-evolution of planktotrophy. [ABSTRACT FROM AUTHOR]

BMP signaling is involved in many aspects of metazoan development, with two of the most conserved functions being to pattern the dorsal-ventral axis and to specify neural versus epidermal fates. An active area of research within developmental biology asks how BMP signaling was modified over evolution to build disparate body plans. Animals belonging to the superclade Spiralia/Lophotrochozoa are excellent experimental subjects for studying the evolution of BMP signaling because a highly conserved, stereotyped early cleavage program precedes the emergence of distinct body plans. In this study we examine the role of BMP signaling in one representative, the slipper snail Crepidula fornicata. We find that mRNAs encoding BMP pathway components (including the BMP ligand decapentaplegic, and BMP antagonists chordin and noggin-like proteins) are not asymmetrically localized along the dorsal-ventral axis in the early embryo, as they are in other species. Furthermore, when BMP signaling is perturbed by adding ectopic recombinant BMP4 protein, or by treating embryos with the selective Activin receptor-like kinase-2 (ALK-2) inhibitor Dorsomorphin Homolog 1 (DMH1), we observe no obvious effects on dorsal-ventral patterning within the posterior (post-trochal) region of the embryo. Instead, we see effects on head development and the balance between neural and epidermal fates specifically within the anterior, pre-trochal tissue derived from the 1q1 lineage. Our experiments define a window of BMP signaling sensitivity that ends at approximately 44–48 ​hours post fertilization, which occurs well after organizer activity has ended and after the dorsal-ventral axis has been determined. When embryos were exposed to BMP4 protein during this window, we observed morphogenetic defects leading to the separation of the anterior, 1q lineage from the rest of the embryo. The 1q-derived organoid remained largely undifferentiated and was radialized, while the post-trochal portion of the embryo developed relatively normally and exhibited clear signs of dorsal-ventral patterning. When embryos were exposed to DMH1 during the same time interval, we observed defects in the head, including protrusion of the apical plate, enlarged cerebral ganglia and ectopic ocelli, but otherwise the larvae appeared normal. No defects in shell development were noted following DMH1 treatments. The varied roles of BMP signaling in the development of several other spiralians have recently been examined. We discuss our results in this context, and highlight the diversity of developmental mechanisms within spiral-cleaving animals. • BMP signaling was examined during development in the snail Crepidula fornicata. • Perturbing BMP signaling does not affect the primary organizer or dorso-ventral axis. • BMP signaling regulates the patterning and morphogenesis of 1st quartet micromeres. • BMP signaling appears to control the balance between neural and epidermal fates. • Comparisons show that BMP signaling differs in different Lophotrochozoan species. [ABSTRACT FROM AUTHOR]

Background: One hundred years ago, marine organisms were the dominant systems for the study of developmental biology. The challenges in rearing these organisms outside of a marine setting ultimately contributed to a shift towards work on a smaller number of so-called model systems. Those animals are typically non-marine organisms with advantages afforded by short life cycles, high fecundity, and relative ease in laboratory culture. However, a full understanding of biodiversity, evolution, and anthropogenic effects on biological systems requires a broader survey of development in the animal kingdom. To this day, marine organisms remain relatively understudied, particularly the members of the Lophotrochozoa (Spiralia), which include well over one third of the metazoan phyla (such as the annelids, mollusks, flatworms) and exhibit a tremendous diversity of body plans and developmental modes. To facilitate studies of this group, we have previously described the development and culture of one lophotrochozoan representative, the slipper snail Crepidula atrasolea, which is easy to rear in recirculating marine aquaria. Lab-based culture and rearing of larger populations of animals remain a general challenge for many marine organisms, particularly for inland laboratories. Results: Here, we describe the development of an automated marine aquatic rack system for the high-density culture of marine species, which is particularly well suited for rearing filter-feeding animals. Based on existing freshwater recirculating aquatic rack systems, our system is specific to the needs of marine organisms and incorporates robust filtration measures to eliminate wastes, reducing the need for regular water changes. In addition, this system incorporates sensors and associated equipment for automated assessment and adjustment of water quality. An automated feeding system permits precise delivery of liquid food (e.g., phytoplankton) throughout the day, mimicking real-life feeding conditions that contribute to increased growth rates and fecundity. Conclusion: This automated system makes laboratory culture of marine animals feasible for both large and small research groups, significantly reducing the time, labor, and overall costs needed to rear these organisms. [ABSTRACT FROM AUTHOR]

Evolution of two novel feeding strategies among caenogastropod molluscs, suspension feeding in calyptraeids such as Crepidula fornicata and predatory feeding with a pleurembolic proboscis among neogastropods, may have both involved elongation of the anterior esophagus. Emergence of predatory feeding with a proboscis is particularly significant because it correlates with the rapid adaptive radiation of buccinoidean and muricoidean neogastropods during the Cretaceous. However, the notion that this important evolutionary transition involved elongation of the anterior esophagus to extend down a long proboscis has been disputed by evidence that it may have been the wall of the buccal cavity that elongated. We undertook a comparative study on foregut morphogenesis during larval and metamorphic development in C. fornicata and in three species of neogastropods with a pleurembolic proboscis to examine the hypothesis that the same region of foregut has elongated in all. We approached this by identifying a conserved marker for the boundary between buccal cavity and anterior esophagus, which was recognizable before the developing foregut showed regional differences in length. A survey of four species of littorinimorph caenogastropods suggested that the site of neurogenic placodes for the buccal ganglia could serve as this marker. Results showed that foregut lengthening in C. fornicata involved elongation posterior to neurogenic placodes for buccal ganglia, an area that corresponded to the anterior esophagus in the other littorinimorphs. However, foregut elongation occurred anterior to neurogenic placodes for buccal ganglia in two buccinoidean and one muricoidean neogastropod. The elongated foregut within the pleurembolic proboscis of these neogastropods qualifies as anterior esophagus only if the definition of the anterior esophagus is expanded to include the dorsal folds that run down the roof of the buccal cavity. Regardless of how the anterior esophagus is defined, comparative developmental data do not support the hypothesis of homology between the elongated adult foregut regions in C. fornicata and in neogastropods with a pleurembolic proboscis. [ABSTRACT FROM AUTHOR]

The anthropogenic introduction in U.K. waters of the north-American marine gastropod Crepidula fornicata (Linné, 1758), commonly called slipper limpet, and its consecutive spreading has led in less than a century to the invasion of a part of benthic grounds along the North-European coasts. Competition for space has hampered the maintenance of the native scallop Pecten maximus , whereas dredge clogging has drastically limited scallop fishing, especially in the Western English Channel. In order to assess the possible future distribution and abundance of both species ( Crepidula and Pecten ), an original model of slipper limpet chains joined to a simple year-class model of the scallop (Ménesguen and Grégoris, 2017) has been coupled to a connectivity matrix summarizing the annual dispersion of emitted larvae in a realistic marine domain. This distributed model can explore the dynamics of both populations at the century scale and has been applied at two different geographical scales: a local one (the bays of Brest and Douarnenez, Western Brittany, France) and a regional one (Bay of Biscay and English Channel). First eigenvectors of the connectivity matrix are used to delineate the main retention areas. For each species taken alone, simulations starting with a few animals in different spots do converge in less than a century towards the same geographic distribution, compatible with the actual field distribution. This suggests that hydrodynamic patterns of larval drift create a strong attractor for these populations; it is reached by different routes of colonization, depending on the initial inoculation. The non-linear interaction created by the lack of space when the populations have filled the benthic area seems to be stronger for scallop populations than for slipper limpets, because of the permanent capacity of Crepidula beds to fix some larvae on the top of existing colonies. Whereas the scallop abundance experiences a rather large limit-cycle, with a dominant 11 years period and a lot of harmonics, the slipper limpet has commonly a stable steady state abundance. Competition between both populations tends to lower the mean scallop abundance and to lengthen and damp its fundamental period of oscillations. Simulated distributions can be locally improved by linking the larval survival to a distributed environmental stressor, as the salinity for scallop or a metallic contamination for the slipper limpet in the case of the bay of Brest. [ABSTRACT FROM AUTHOR]

The American slipper limpet Crepidula fornicata is an invasive, non-native species (INNS) abundant along the European coast. Its further distribution may be facilitated by activities such as dredging and spoil disposal, and the aim of this study was to assess whether C . fornicata is able to survive sediment burial. The slipper limpet was found attached to hard substratum in intertidal areas, but it was absent at a nearby subtidal dredge spoil site. In laboratory experiments 22% of C . fornicata emerged when buried under a 2 cm sediment-layer; only half of them survived. When buried under ≥6 cm none re-surfaced or survived. The results provided evidence that C . fornicata is poorly adapted to adjust its vertical position in sediment and is killed by sudden burial underneath 2 to 6 cm of sediment. The combined laboratory experiments and field surveys suggested that C . fornicata has limited scope to survive the dredge spoil disposal process. [ABSTRACT FROM AUTHOR]

Microplastics exposure could be detrimental to marine organisms especially under high concentrations. However, few studies have considered the multiphasic nature of marine invertebrates' life history and investigated the impact of experiencing microplastics during early development on post-metamorphic stages (legacy effect). Many planktonic larvae can feed selectively and it is unclear whether such selectivity could modulate the impact of algal food-sized microplastic. In this two-stage experiment, veligers of Crepidula onyx were first exposed to additions of algae-sized micro-polystyrene (micro-PS) beads at different concentrations, including ones that were comparable their algal diet. These additions were then either halted or continued after settlement. At environmentally relevant concentration (ten 2-μm microplastic beads ml −1 ), larval and juvenile C. onyx was not affected. At higher concentrations, these micro-PS fed larvae consumed a similar amount of algae compared to those in control but grew relatively slower than those in the control suggesting that ingestion and/or removal of microplastic was/were energetically costly. These larvae also settled earlier at a smaller size compared to the control, which could negatively affect post-settlement success. Juvenile C. onyx receiving continuous micro-PS addition had slower growth rates. Individuals only exposed to micro-PS during their larval stage continued to have slower growth rates than those in the control even if micro-PS had been absent in their surroundings for 65 days highlighting a legacy effect of microplastic exposure. [ABSTRACT FROM AUTHOR]

The calyptraeid gastropod Crepidula fornicata is native to the eastern coast of the United States but has now become an extremely successful invader along much of the European coastline. As the northern limit of its spread is thought to be determined by an inability of adults to tolerate prolonged exposure to low winter temperatures, this study sought to compare the fecundity of females collected from two sites along the Norwegian coastline with that of females collected from Rhode Island, USA. Few other studies have compared the fecundities of marine invertebrates from invasive populations with those found in native populations. For both populations studied, fecundities increased with increasing shell length. However, contrary to expectations, size-related fecundities were significantly higher for Norwegian females than for Rhode Island females, with Norwegian females producing larger egg capsules and a greater number of embryos per capsule, but not a greater number of egg capsules per brood. Current evidence suggests that at the northern extreme of its invaded range, the fecundity of C. fornicata is increased rather than compromised. [ABSTRACT FROM AUTHOR]

During development in metazoan embryos, the fundamental embryonic axes are established by organizing centers that influence the fates of nearby cells. Among the spiralians, a large and diverse branch of protostome metazoans, studies have shown that an organizer sets up the dorsal-ventral axis, which arises from one of the four basic cell quadrants during development (the dorsal, D quadrant). Studies in a few species have also revealed variation in terms of how and when the D quadrant and the organizer are established. In some species the D quadrant is specified conditionally, via cell-cell interactions, while in others it is specified autonomously, via asymmetric cell divisions (such as those involving the formation of polar lobes). The third quartet macromere (3D) typically serves as the spiralian organizer; however, other cells born earlier or later in the D quadrant lineage can serve as the organizer, such as the 2d micromere in the annelid Capitella teleta or the 4d micromere in the mollusc Crepidula fornicata . Here we present work carried out in the snail C. fornicata to show that establishment of a single D quadrant appears to rely on a combination of both autonomous (via inheritance of the polar lobe) and conditional mechanisms (involving induction via the progeny of the first quartet micromeres). Through systematic ablation of cells, we show that D quadrant identity is established between 5th and 6th cleavage stages, as it is in other spiralians that use conditional specification. Subsequently, following the next cell cycle, organizer activity takes place soon after the birth of the 4d micromere. Therefore, unlike the case in other spiralians that use conditional specification, the specification of the D quadrant and the activity of the dorso-ventral organizer are temporally and spatially uncoupled. We also present data on organizer function in naturally-occurring and experimentally-induced twin embryos, which possess multiple D quadrants. We show that supernumerary D quadrants can arise in C. fornicata (either spontaneously or following polar lobe removal); when multiple D quadrants are present these do not exhibit effective organizer activity. We conclude that the polar lobe is not required for D quadrant specification, though it could play a role in effective organizer activity. We also tested whether the inheritance of the small polar lobe by the D quadrant is associated with the ability to laterally inhibit neighboring quadrants by direct contact in order to normally prevent supernumerary organizers from arising. Finally, we discuss the variation of spiralian organizers in a phylogenetic context. [ABSTRACT FROM AUTHOR]

The slipper limpet Crepidula fornicata Linnaeus, 1758 is a major exotic invader of East North Atlantic coasts. Individuals live on top of each other and form stacks with the youngest on the top. Earlier studies reported that one individual typically settles per year. If true, it is a simplified means to provide a “shell length-age” relationship for population dynamics studies, especially Production/Biomass ratio (P/B) assessment. However, estimated P/B ranges between 0.15 and 0.45 yr-1 seem low compared to those of closely-related marine invertebrates and considering the invasiveness of C. fornicata in coastal habitats. In this study, we placed artificial substrates (“tiles”) for one year in the middle of a C. fornicata colony and measured settlement. We sometimes observed more than one individual settling per stack in a year: 4% of stacks were composed by 3 individuals, 27% by 2 individuals and 69% were single specimen. On this basis, we formulated a model to better link the position of each C. fornicata within a stack to its age. In addition, the C. fornicata population was annually sampled for 5 years. Then, population dynamics parameters, density at recruitment, mortality rate, growth performance, production and P/B were estimated. We compared two cases: (i) individual age was defined by its position in stacks; (ii) individual age was corrected by the model. Recalculation moderately increased growth performance expectation (+2 to 8% per year) but greatly enhanced production and P/B (ca. 1.2 to 2.6-fold per year). Recalculated P/B values ranged from 0.55 to 0.72 yr-1. While still low, they were more consistent with published values for similar large marine invertebrates, in particular for invasive species. [ABSTRACT FROM AUTHOR]

In many marine invertebrates, long-distance dispersal is achieved during an extended pelagic larval phase. Although such dispersal should result in high gene flow over broad spatial scales, fine-scale genetic structure has often been reported, a pattern attributed to interfamilial variance in reproductive success and limited homogenization during dispersal. To examine this hypothesis, the genetic diversity of dispersing larvae must be compared with the postdispersal stages, that is benthic recruits and adults. Such data remain, however, scarce due to the difficulty to sample and analyse larvae of minute size. Here, we carried out such an investigation using the marine gastropod Crepidula fornicata. Field sampling of three to four larval pools was conducted over the reproductive season and repeated over 3 years. The genetic composition of larval pools, obtained with 16 microsatellite loci, was compared with that of recruits and adults sampled from the same site and years. In contrast to samples of juveniles and adults, large genetic temporal variations between larval pools produced at different times of the same reproductive season were observed. In addition, full- and half-sibs were detected in early larvae and postdispersal juveniles, pointing to correlated dispersal paths between several pairs of individuals. Inbred larvae were also identified. Such collective larval dispersal was unexpected given the long larval duration of the study species. Our results suggest that each larval pool is produced by a small effective number of reproducers but that, over a reproductive season, the whole larval pool is produced by large numbers of reproducers across space and time. [ABSTRACT FROM AUTHOR]

Precise biodiversity mapping that can be compared over decades would greatly inform the discussion of climate change impacts on species richness and shifts in dominant benthic species. Buzzards Bay, Massachusetts, USA, has a long history of field studies documenting benthic community structure. This bioassessment compares 1955 benthic infaunal sampling results with 2011/2012 samples to determine whether there has been a compositional change. I also compared structural components including grain size and near-bottom temperatures. In addition, benthic temperature rise and fall was logged at 15-min intervals from May to October of consecutive years. There was an observed difference in the benthic compositional structure, substrate and temperature between the 1955 and 2011/2012 station conditions. The 1955 identification of Buzzards Bay as being nutrient poor and having a reported 20.5 °C benthic temperature maximum has changed. Coastal development has brought increased nutrient inputs, and the 2012 bottom temperature maximum was at least 4 °C greater. These conditions contribute to shifts in benthic species dominance, and the substrate itself has been transformed to shell reefs at the stations where the gastropod Crepidula fornicata proliferated. [ABSTRACT FROM AUTHOR]

The slipper limpet Bostrycapulus odites has recently been reported as an introduced species on the Spanish Mediterranean coast. Another species in the family Calyptraeidae, Crepidula fornicata, is a problematic invasive species in the Northeast Atlantic, which makes the closely related Bostrycapulus introduction a matter of concern. Information on the biology of B. odites in its natural environment can facilitate predictions on where the species could find favourable conditions for settlement and expansion. Size and sex were recorded for individuals in four populations over 2600 km of the Southwestern Atlantic shoreline, in Argentina and Brazil, covering the whole native latitudinal range of this widely distributed species. Animals were collected by hand in the intertidal or by SCUBA in subtidal locations; specimens were examined to determine shell length, sex, and the presence and number of brooded egg capsules in females. Mean shell length for the whole population did not differ significantly among populations. However, this species experiences sequential hermaphroditism (protandrism), and the size at sexual maturity (minimum male size) increased significantly with latitude. The fecundity of females at all sites increased with size, and the number of brooded egg capsules as well as the average size of capsules was larger in bigger individual females; however, mean fecundity varied among sites independent of mean female body size. This limpet species modifies its reproductive traits with local conditions, and sexual characters develop earlier in more temperate localities. [ABSTRACT FROM AUTHOR]

Organisms inhabiting coastal waters naturally experience diel and seasonal physico-chemical variations. According to various assumptions, coastal species are either considered to be highly tolerant to environmental changes or, conversely, living at the thresholds of their physiological performance. Therefore, these species are either more resistant or more sensitive, respectively, to ocean acidification and warming. Here, we focused on Crepidula fornicata, an invasive gastropod that colonized bays and estuaries on northwestern European coasts during the 20th century. Small (<3 cm in length) and large (>4.5 cm in length), sexually mature individuals of C. fornicata were raised for 6 months in three different pCO2 conditions (390 μatm, 750 μatm, and 1400 μatm) at four successive temperature levels (10°C, 13°C, 16°C, and 19°C). At each temperature level and in each pCO2 condition, we assessed the physiological rates of respiration, ammonia excretion, filtration and calcification on small and large individuals. Results show that, in general, temperature positively influenced respiration, excretion and filtration rates in both small and large individuals. Conversely, increasing pCO2 negatively affected calcification rates, leading to net dissolution in the most drastic pCO2 condition (1400 μatm) but did not affect the other physiological rates. Overall, our results indicate that C. fornicata can tolerate ocean acidification, particularly in the intermediate pCO2 scenario. Moreover, in this eurythermal species, moderate warming may play a buffering role in the future responses of organisms to ocean acidification. [ABSTRACT FROM AUTHOR]

Theory predicts that genetic variation should be reduced at range margins, but empirical support is equivocal. Here, we used genotyping-by-sequencing technology to investigate genetic variation in central and marginal populations of two species in the marine gastropod genus Crepidula. These two species have different development and dispersal types and might therefore show different spatial patterns of genetic variation. Both allelic richness and the proportion of private alleles were highest in the most central populations of both species, and lower at the margin. The species with low dispersal, Crepidula convexa, showed high degrees of structure throughout the range that conform to the pattern found in previous studies using other molecular markers. The northernmost populations of the high-dispersing species, Crepidula fornicata, are distinct from more central populations, although this species has been previously observed to have little genetic structure over much of its range. Although genetic diversity was significantly lower at the range margin, the absolute reduction in diversity observed with these genomewide markers was slight, and it is not yet known whether there are functional consequences for the marginal populations. [ABSTRACT FROM AUTHOR]

Late Quaternary marine skeletal concentrations from Argentina are rich in molluscs exhibiting a great variety of bioerosion structures. The shells of Crepidula , a characteristic gastropod occurring along more than 2000 km of coastline between the Río de La Plata margin and southern Patagonia, show traces of dwelling, predation and anchoring activities made by porifers, bryozoans, annelids, other gastropods and brachiopods. Caulostrepsis, Entobia, Maeandropolydora, Iramena, Oichnus, Finichnus, Pennatichnus, Pinaceocladichnus, Podichnus and Renichnus occur on the outer shell surface. Finichnus and Oichnus are the only traces present along the entire area and the full time span considered. The most characteristic structures are produced by bryozoans, polychaetes and predatory gastropods. Traces produced by annelids and predatory gastropods occur preferentially in the central shell sector, where predators gained access to the soft parts of the prey. By contrast, encrusting or branching bryozoan colonies are widely distributed as they can attach to any sector regardless of shell features available. No strict correlation is evident between ichnodiversity and either time or latitude, but ichnodiversity is linked to local oceanographical/biotic controls. For Patagonia, with a great majority of ichnotaxa made by bryozoans, the general trend of higher bioerosion degree and ichnodiversity at higher latitudes is controlled by sea surface temperature/productivity: for the modern and the Holocene, several ichnodiversity peaks match with well-constrained conditions (substrate, salinity, thermal fronts). By contrast, this does not hold for the Pleistocene: dissimilar conditions probably prevailed, especially during the Last Interglacial (colder waters richer in nutrients). [ABSTRACT FROM AUTHOR]

Many animals experience periods of feast or famine, which can have major consequences for growth, survival, and reproductive fitness. For animals with complex life histories, the question remains whether a major ontogenetic transition, such as metamorphosis, removes the legacy of early diet variability, or if early stressors persist into later stages. This study examined the effect of constant versus variable food availability and average food concentration during the larval stage on the performance of the marine gastropod Crepidula fornicata (L.) before and after metamorphosis. There was no detectable effect of variable food availability on larval growth, energy stores, survival, and metamorphic competence, or juvenile growth rate and survival. Instead, the average amount of food available during the larval period had the greatest impact on larval size and metamorphic competence. Surprisingly, there were no impacts of larval diet on growth or survival during the juvenile stage. Differences that originated during the larval stage were removed post-metamorphosis. These results suggest that some organisms may be resilient to variations in food availability and that not all early life experiences produce legacy effects. Heterogeneous environments, including variable food availability, should favor flexibility in the timing of ontogenetic transitions that allow individuals to be robust in later life stages. [ABSTRACT FROM AUTHOR]

Sea surface temperatures have been rising and are predicted to continue rising in coming years because of global warming. In addition, salinity has been decreasing in high latitudes and is expected to continue decreasing due to altered precipitation patterns and glacial melting caused by climate change. Many marine organisms that are adapted to the present conditions may be drastically affected by these oceanic changes. Early life stages (larvae and juveniles) should be especially susceptible, since they do not yet have the fully developed morphological defenses of adults. This study investigated the effects of reduced salinity (20 compared to a control of 30) and altered temperature (15, 20, 25, and 29 °C) on the growth, percent inorganic content (representing shell calcification), and feeding rates of larvae and juveniles of the widespread coastal snail Crepidula fornicata . Both larval and juvenile growth rates were significantly depressed at low salinity and lower temperatures. In addition, the salinity that snails were exposed to as larvae significantly impacted their juvenile growth rates in 4 out of 6 treatments, an example of latent effects. The magnitude and direction of this effect were strongly impacted by temperature and parentage. Juvenile feeding rates were significantly depressed following a rapid change in salinity but then gradually recovered to near initial levels over 3 h. There was little difference in the percent inorganic content of juveniles but for larvae that had been reared at 20 °C, percent inorganic content was 27% lower for those reared at a salinity of 20 compared with those reared at 30. In conclusion, the early life stages of C. fornicata may experience more favorable conditions in a warmer future: growth rates will increase, probably making larvae and juveniles less vulnerable to size-specific predation. Conversely, in regions where salinity is decreasing, C. fornicata larvae and juveniles will likely grow more slowly, thereby increasing predation risk by forcing them to spend more time at more vulnerable smaller sizes. Thus, the future of C. fornicata and their potential to continue invading new habitats will depend greatly on the specific salinity and temperature conditions they will be exposed to throughout larval and juvenile development. [ABSTRACT FROM AUTHOR]

Some larval experiences can produce 'latent effects' on post-metamorphic growth or survival. While it is known that periods of starvation during larval development can cause such latent effects, the effect of larval diet on post-metamorphic growth has not been studied. As global climate change and ocean acidification are expected to decrease phytoplankton concentrations and alter both phytoplankton species composition and nutritional characteristics, we examined the impact of 3 phytoplankton species ( Isochrysis galbana, clone T-ISO; Pavlova lutheri, clone MONO; and Dunaliella tertiolecta, clone DUN) on larval growth and subsequent post-metamorphic fitness in the slippersnail Crepidula fornicata. Once larvae metamorphosed, the juveniles were all reared on the diet that produced the fastest growth, T-ISO, to look for latent effects of larval diet on juvenile growth. In all experiments, larvae grew most quickly on T-ISO; diet did not affect relative rates of shell and tissue growth. In 2 of the 4 experiments conducted on the effects of diet quality, larvae reared on T-ISO metamorphosed into juveniles that grew significantly faster than those that had been raised on the other phytoplankton species, indicating clear latent effects of dietary experience and suggesting parent-related genetic variation in susceptibility to this type of stress. Rearing larvae at a very low food concentration of T-ISO (1 × 10 cells ml) until metamorphosis also produced severe latent effects on juvenile growth, reducing juvenile growth rates by more than 30 %. These data provide yet another example of how stresses experienced during larval development can influence post-metamorphic performance, and add another level of complexity to attempts at predicting the future consequences of environmental change on marine community structure and species interactions. [ABSTRACT FROM AUTHOR]

Hermit crabs are notoriously choosy about the gastropod shells they live in. Many periwinkle shells at Nahant, Massachusetts, U.S.A. contain the gastropod Crepidula plana , which forms a thin flat shell inside the periwinkle shell. This study examined how the presence of C. plana affected shell selection behavior by the hermit crab Pagurus longicarpus : naked hermit crabs were offered different combinations of shells, including some containing C. plana and some that had been drilled by naticid gastropods, and their choices were recorded. Because we had to evict hermit crabs from their shells before conducting our choice tests, we also determined rates of recovery from five commonly used shell eviction techniques. No hermit crabs were successfully evicted using low salinity seawater. For the other techniques used, hermit crabs took significantly longer to recover after being removed by gentle but continuous pulling on the carapace and appendages than after being removed by immersion in heated seawater, cracking the shell using a vise, or prodding the hermit crab in the abdomen through a hole drilled in the shell. Even so, most hermit crabs recovered from all of the stresses tested within 20 h, and from at least some stresses within 2–6 h. If shells are to be re-used for experiments, heating seawater is the best technique for evicting P. longicarpus ; otherwise, cracking the shell using a vise is recommended. When provided with intact shells and similarly-sized shells containing adult C. plana , all of the hermit crabs chose shells without C. plana , and did so within only about 30 min. However, given a choice between shells housing C. plana and those bearing drill holes–shells which they normally avoid–the hermit crabs were about evenly divided in their choice of shells, and many of the hermit crabs never made a final decision even after 18 or 19 h, suggesting that the presence of C. plana greatly reduces shell attractiveness and suitability. The presence of C. plana increased total shell weight and reduced internal shell volume considerably, and also weakened the shell substantially, likely making the hermit crabs more vulnerable to predators; all of these factors may play a role in selecting for the intense avoidance behavior exhibited by this species for periwinkle shells bearing C. plana . [ABSTRACT FROM AUTHOR]

In the current context of environmental change, ocean acidification is predicted to affect the cellular processes, physiology and behaviour of all marine organisms, impacting survival, growth and reproduction. In relation to thermal tolerance limits, the effects of elevated pCO2 could be expected to be more pronounced at the upper limits of the thermal tolerance window. Our study focused on Crepidulafornicata, an invasive gastropod which colonized shallow waters around European coasts during the 20th century. We investigated the effects of 10 weeks' exposure to current (380 μatm) and elevated (550, 750, 1,000 μatm) pCO2 on this engineer species using an acute temperature increase (1 °C 12 h -1) as the test. Respiration rates were measured on both males (small individuals) and females (large individuals). Mortality increased suddenly from 34 °C, particularly in females. Respiration rate in C.fornicata increased linearly with temperature between 18 and 34 °C, but no differences were detected between the different pCO2 conditions either in the regressions between respiration rate and temperature or in Q10 values. In the same way, condition indices were similar in all the pCO2 treatments at the end of the experiment, but decreased from the beginning of the experiment. This species was highly resistant to acute exposure to high temperature regardless of pCO2 levels, even though food was limited during the experiment. Crepidulafornicata appears to have either developed resistance mechanisms or a strong phenotypic plasticity to deal with fluctuations of physicochemical parameters in its habitat. This suggests that invasive species may be more resistant to future environmental changes than its native competitors. [ABSTRACT FROM AUTHOR]

Suspension-feeding organisms living in the intertidal zone experience reduced feeding times associated with periodic aerial exposure. The potential morphological and physiological adaptations to this reduced feeding time were investigated for two closely related gastropods, Crepidula fornicata and Crepipatella peruviana. Intertidal C. fornicata had heavier gills than subtidal conspecifics, a difference mediated by larger gill surface areas and greater numbers of gill filaments among intertidal individuals of a given size. In contrast, the gills of intertidal and subtidal C. peruviana were morphologically indistinguishable. Despite relatively larger food-collecting organs, individuals of C. fornicata from the intertidal zone had clearance rates (CR) that were not significantly different from those of subtidal conspecifics. In contrast, the CR of intertidal C. peruviana were significantly lower than those of subtidal conspecifics. The low CR of intertidal C. peruviana may be partially explained by significantly lower measured particle transport velocities across their gills. In the context of feeding, intertidal individuals of C. fornicata performed at least as well as subtidal conspecifics, resulting in a population whose adults were as large as those found subtidally. This suggests that C. fornicata has had a long interaction with the environmental heterogeneity associated with intertidal life. In contrast, intertidal individuals of C. peruviana were on average smaller than subtidal individuals and may be stressed in the intertidal. [ABSTRACT FROM AUTHOR]

Food quality and quantity, as well as temperature, are all factors that are expected to affect rates of development, and are likely to be affected by expected climatic change. We tested the effect of a mixed diet versus a single-food diet on metamorphic competence in the emerging model species Crepidula fornicata. We then compared our results with other published studies on this species that examined time to metamorphic competence across a range of food concentrations and rearing temperatures. Ours was the only study to test the effects of single food versus a mixed diet on metamorphic competence for this species. Diet composition did not affect metamorphic competence or survivorship. Comparing results across studies, we found that the shortest time to metamorphic competence was typically found when the food availability per larva was the greatest, independent of rearing temperature. Unfortunately, some published studies did not include important metadata needed for comparison with other studies; these data included larval rearing density, food density, frequency of feeding, and rearing temperature. Mortality rates were not always reported and when reported were often measured in different ways, preventing comparison. Such metadata are essential for comparisons among studies as well as among taxa, and for the determination of generalizable patterns and evolutionary trends. Increased reporting of all such metadata is essential if we are to use scientific studies performed to their fullest potential. [ABSTRACT FROM AUTHOR]

Adelphophagy occurs when encapsulated embryos complete development by feeding on their developing siblings, which are known as nutritive embryos. Nutritive embryos are found in a variety of animal groups, and are especially common in some groups of marine invertebrates. Although they have evolved numerous times independently in the calyptraeid gastropods, adelphophagic development with nutritive embryos has not been described in detail. Using light microscopy and time-lapse imaging of laboratory-reared embryos, we describe the development of Crepidula navicella, a direct developer with nutritive embryos that cleave and gastrulate. Early stages of nutritive and viable embryos do not show any obvious morphological differences, but do show asynchrony in early cleavage among embryos from the same capsule. We discovered that two classes of nutritive embryos are produced; gastrula-like nutritive embryos, which arrest after gastrulation, and post-gastrula-like nutritive embryos that are more variable in morphology, and show evidence of minor differentiation.This study provides a framework for future research on the developmental and molecular mechanisms of nutritive embryo development of C. navicella, which will allow us to address the role of nutritive embryos in the origins of developmental polyphenisms. Careful description of the developmental sequence is necessary before adaptive hypotheses can be addressed, and comparisons with other taxa can be made. Understanding the different ways that embryos and their development are disrupted to produce nutritive embryos will provide important insights into the normal process of development. [ABSTRACT FROM AUTHOR]

In sex-changing animals with internal fertilization, gregarious behavior may increase mating opportunities and the frequency of multiple paternity, thus increasing maternal reproductive success. Crepidula convexa is a direct-developing protandrous gastropod characterized by only modest gregarious behavior compared with previously studied members of the genus: females are frequently found isolated. Using 6 microsatellite markers, we analyzed paternity profiles in 10 broods (25 embryos per mother). The number of assigned fathers varied among families from 1 to 4 fathers per brood. Interestingly, polyandry was not detected in solitary females but only in females grouped with conspecific individuals. Overall, we found an average of 1.8 fathers per brood, but this increased to 2.6 fathers per brood when considering only the nonisolated females. Among 18 unambiguously identified fathers, only 5 were collected in our samples, suggesting substantial male mobility. Comparison with previous paternity analyses in Crepidula fornicata and Crepidula coquimbensis revealed that polyandry appears as a common trait of these sex-changing gastropods despite their different grouping behaviors and life histories. As expected, the level of polyandry was nevertheless lower in the modestly gregarious C. convexa. [ABSTRACT FROM AUTHOR]

In this work we studied bioerosion and encrustation on dead shells of the shallow benthic clam Venus antiqua from Patagonia Argentina with the aim of understanding biotic interactions (live/live interaction) and postmortem encrustation (live/dead interaction). In this regard, drill hole analysis and epibiont distribution in shells from modern death assemblages were performed. Additionally, we analyzed crushing traces in the shells of the drilling gastropod Trophon geversianus, which were caused by another predator. The analysis of drill hole placement and epibiont distribution on V. antiqua shells show drill holes (75%) and the epibiont Crepidula spp. (70.91%) more concentrated in the upper sector of the valve, which might be explained by the vertical position and a semi-infaunal mode of life in this clam. Nevertheless, the presence of drill holes in the lower sector of the valve indicates that clams spent part of the time reclining on the sediment. There is also evidence that clams with Crepidula spp. as commensals are less frequently attacked by drilling gastropods. Besides, a high percentage of articulated clams (30.97%) show signs of attack by drilling gastropods, but incomplete drill holes (7.67%) also suggest failed attempts, resulting in a minimum of 23.30% of successful predation. These incomplete drill holes may suggest failed attempts due to another predator attack upon the snails consuming the clams thus interrupting the feeding activity: more than 60% of marks of crushing in T. geversianus shells could have been produced by other predators, such as crabs. The postmortem encrustation on V. antiqua shells (35%) was mainly produced by calcareous polychaetes, preferably located on the inner side of the valve indicating that the empty shells of V. antiqua served as cryptic environment before they become exposed on the beach. Finally our data show that drilling frequency is very low in Pleistocene assemblages, suggesting changes in burial depth dynamics of this suspension feeder. [ABSTRACT FROM AUTHOR]