Crawl-away Juveniles Research Articles

Non-native molluscan colonizers on deliberately placed shipwrecks in the Florida Keys, with description of a new species of potentially invasive worm-snail (Gastropoda: Vermetidae).

Artificial reefs created by deliberately sinking ships off the coast of the Florida Keys island chain are providing new habitat for marine invertebrates. This newly developing fouling community includes the previously reported invasive orange tube coral Tubastraea coccinea and the non-native giant foam oyster Hyotissa hyotis. New SCUBA-based surveys involving five shipwrecks spanning the upper, middle, and lower Florida Keys, show T. coccinea now also established in the lower Keys and H. hyotis likewise extending to new sites. Two additional mollusks found on the artificial reefs, the amathinid gastropod Cyclothyca pacei and gryphaeid oyster Hyotissa mcgintyi, the latter also common in the natural reef areas, are discussed as potentially non-native. A new species of sessile, suspension-feeding, worm-snail, Thylacodes vandyensis Bieler, Rawlings & Collins n. sp. (Vermetidae), is described from the wreck of the USNS Vandenberg off Key West and discussed as potentially invasive. This new species is compared morphologically and by DNA barcode markers to other known members of the genus, and may be a recent arrival from the Pacific Ocean. Thylacodes vandyensis is polychromatic, with individuals varying in both overall head-foot coloration and mantle margin color pattern. Females brood stalked egg capsules attached to their shell within the confines of their mantle cavity, and give rise to crawl-away juveniles. Such direct-developing species have the demonstrated capacity for colonizing habitats isolated far from their native ranges and establishing rapidly growing founder populations. Vermetid gastropods are common components of the marine fouling community in warm temperate and tropical waters and, as such, have been tagged as potentially invasive or with a high potential to be invasive in the Pacific Ocean. As vermetids can influence coral growth/composition in the Pacific and have been reported serving as intermediate hosts for blood flukes of loggerhead turtles, such new arrivals in the Florida Keys National Marine Sanctuary are of concern. Growing evidence indicates that artificial reefs can act as permanent way-stations for arriving non-natives, providing nurseries within which populations may grow in an environment with reduced competition compared to native habitats. Consequently, artificial reefs can act as sentinels for the appearance of new species. Ongoing monitoring of the developing molluscan fauna on the artificial reefs of the Florida Keys is necessary to recognize new invasions and identify potential eradication targets, thereby assuring the health of the nearby natural barrier reef.

Oviposition and Embryonic Development in the Volutid SnailAdelomelon ancilla

Intracapsular embryonic development is common in marine gastropods. In many species, embryos obtain nutrition during ontogeny by ingesting substances contained in the intracapsular fluid. South American volutids spawn egg capsules containing relatively few eggs, and development is entirely intracapsular, with young hatching as crawl-away juveniles. The spawning habits, egg capsules morphology and embryonic development of the South American volutid Adelomelon ancilla is described in this work. Egg capsules of A. ancilla (n = 42) contained 3.0 ± 1.4 (mean ± SD) embryos with a range of 1–6 eggs or embryos. The embryonic morphological changes and body spiralization occur simultaneously with embryo feeding. All embryos within a single egg capsule shared the same developmental stage. No evidence of cannibalism or intracapsular competition was found, suggesting that food is not a limiting resource as in other volutid species. Estimated intracapsular developmental time varied between five and six months (between 12–14°C). The long developmental time and low number of embryos inside the egg capsules, together with late reproductive maturity and longevity of adult individuals, reinforce the statement that the neogastropod Adelomelon ancilla is a fragile resource that must be conserved in Argentinean benthic communities.

Oviposition site influences dispersal potential in a marine bubble snail

For benthic marine invertebrates that deposit offspring inside protective capsules or gelatinous egg masses, small-scale variation in environmental parameters can affect offspring mortality, performance, timing of hatching and dispersal potential. Plasticity in hatching and dispersal potential have received less attention than egg mass mortality and juvenile performance, but there may be adaptive responses that balance the costs and benefits of benthic and pelagic development in specific contexts, such as escaping poor environments. Some species, such as the bubble snail Haminoea japonica, produce two offspring phenotypes at hatching that differ in dispersal potential. Here, I investigated whether the substrata that egg masses develop on can influence whether offspring tended to hatch as either phenotype. In the field, egg masses were more commonly deposited in association with filamentous algae and in laboratory experiments, free-swimming larvae settled and metamorphosed more readily on algae. When egg masses developed on the algae that induced settlement, there were more crawl-away juveniles than free-swimming larvae. Such a response has important consequences for dispersal potential, hence the deposition substratum may have an adaptive value because crawl-away juveniles can avoid a potentially risky planktonic period when settlement substratum is present, but larvae can disperse when a suitable settlement substratum is absent.

Thermal tolerance during early ontogeny in the common whelk Buccinum undatum (Linnaeus 1785): Bioenergetics, nurse egg partitioning and developmental success

Temperature is arguably the primary factor affecting development in ectotherms and, as a result, may be the driving force behind setting species' geographic limits. The shallow-water gastropod Buccinum undatum is distributed widely throughout the North Atlantic, with an overall annual thermal range of below zero to above 22°C. In UK waters this species is a winter spawner. Egg masses are laid and develop when sea temperatures are at their coolest (4 to 10°C) indicating future climate warming may have the potential to cause range shifts in this species. In order to examine the potential impacts of ocean warming, we investigate the effects of temperature on the early ontogeny of B. undatum across a thermal range of 0 to 22°C. Each egg mass consists of approximately 100 capsules, in which embryos undergo direct development. Successful development was observed at temperatures ranging from 6 to 18°C. Rates of development increased with temperature, but the proportion of each egg mass developing successfully decreased at the same time. With increasing temperature, the mean early veliger weight increased, but the number of early veligers developing per capsule decreased, suggesting a negative impact on the number of crawl-away juveniles produced per capsule. Elemental analysis showed both carbon (C) and nitrogen (N) to increase with temperature in early veligers but not in hatching juveniles, indicating greater energy reserves are accumulated during early ontogeny to compensate for the higher energetic demands of development at higher temperature. The developmental plasticity observed in B. undatum suggests this species to be capable of adapting to temperatures above those it currently experiences in nature. B. undatum may possess a thermal resilience to ocean warming at its current upper temperature distribution limit. This thermal resilience, however, may come at the cost of a reduced offspring number.

Spatial and temporal population genetic structure of four northeastern Pacific littorinid gastropods: the effect of mode of larval development on variation at one mitochondrial and two nuclear DNA markers

We investigated the effect of development mode on the spatial and temporal population genetic structure of four littorinid gastropod species. Snails were collected from the same three sites on the west coast of Vancouver Island, Canada in 1997 and again in 2007. DNA sequences were obtained for one mitochondrial gene, cytochrome b (Cyt b), and for up to two nuclear genes, heat shock cognate 70 (HSC70) and aminopeptidase N intron (APN54). We found that the mean level of genetic diversity and long-term effective population sizes (N(e)) were significantly greater for two species, Littorina scutulata and L. plena, that had a planktotrophic larval stage than for two species, Littorina sitkana and L. subrotundata, that laid benthic egg masses which hatched directly into crawl-away juveniles. Predictably, two poorly dispersing species, L. sitkana and L. subrotundata, showed significant spatial genetic structure at an 11- to 65-km geographical scale that was not observed in the two planktotrophic species. Conversely, the two planktotrophic species had more temporal genetic structure over a 10-year interval than did the two direct-developing species and showed highly significant temporal structure for spatially pooled samples. The greater temporal genetic variation of the two planktotrophic species may have been caused by their high fecundity, high larval dispersal, and low but spatially correlated early survivorship. The sweepstakes-like reproductive success of the planktotrophic species could allow a few related females to populate hundreds of kilometres of coastline and may explain their substantially larger temporal genetic variance but lower spatial genetic variance relative to the direct-developing species.

Life Cycle of a Bioluminescent Marine Ostracode, Vargula Annecohenae (Myodocopida: Cypridinidae)

Abstract We present the first complete description of a life cycle for a marine ostracode that uses bioluminescence for courtship. The life cycle of Vargula annecohenae consists of five juvenile instars separated by molts and an adult instar following the terminal molt. Body size is tightly conserved within each instar; therefore, most individuals can be reliably identified to instar by the length-to-height regression of carapace size. Sexual dimorphism becomes apparent in the penultimate A-I instar and remains evident through adulthood. Each juvenile instar of V. annecohenae lasts between 10 and 27 days, resulting in an estimated total juvenile development time of three months. Females have multiple broods and give birth to crawl-away juveniles following a 26 ± 1.6 day incubation period. Adults live up to 188 additional days, and thus V. annecohenae has a potential life span of up to nine months. This species is one of the large number of myodocopid ostracode species that use bioluminescence for courtshi...

Marine algal symbionts benefit benthic invertebrate embryos deposited in gelatinous egg masses

Algae colonize the gelatinous egg masses of marine invertebrates. This study demonstrates a symbiotic relationship between marine algae and the invertebrate embryos in gelatinous egg masses found in Indian River Lagoon, FL, USA. The benefits to the embryos in this association differ among host species investigated. The embryos of the polychaete Axiothella mucosa graze on the diatom assemblage in their egg masses and the fitness of the crawl-away juveniles is improved by this food source. The tenuous egg masses of the polychaete Arenicola cristata and the mollusk Haminoea succinea are negatively buoyant when spawned and become buoyant when symbiotic algae are present. In addition to increased dispersal of their lecithotrophic larvae, the potential of the egg masses of A. cristata and H. succinea to float may reduce predation on the embryos by benthic predators such as the gastropod Nassarius vibex. Photosynthetically derived oxygen from the algae may benefit the embryos of the opisthobranch Haminoea elegans by increasing oxygen supply when crawl-away juveniles emerge from the egg mass. However, when mostly earlier stage larvae are hatched from egg masses of H. elegans, the additional oxygen supplied by the algae does not provide a substantial advantage. Algae were absent in the gelatinous egg mass core of only one of the five species examined, Haminoea antillarum. H. antillarum has both a short embryonic development time and denser egg mass gel than the other four species tested. What is not understood is whether invertebrate egg masses are an opportunistic space for algae to colonize or whether only a few microalgal species can exploit the gelatinous substrate.

Comparative population genetic structure of marine gastropods ( Littorina spp.) with and without pelagic larval dispersal

Population genetic theory predicts that marine animal species with planktonic larvae will have less genetic structure than those with direct development. We compared the genetic structure of four species of littorinid snails – two with planktonic egg capsules that hatch as planktonic larvae and two with benthic egg masses that hatch as crawl-away juveniles. We used DNA sequencing and single stranded conformational polymorphism (SSCP) to assess sequence variation in a 480 bp fragment of the mitochondrial cytochrome b gene and then used an analysis of molecular variance (AMOVA) to estimate Φst for populations from the northeastern Pacific coast. One of the two direct-developing species, Littorina subrotundata, had a moderate amount of population structure (Φst=0.209) as expected but the other direct-developing species, L. sitkana, was nearly fixed for a single haplotype that made it impossible to precisely estimate Φst. One of the two planktonic-developing species, L. scutulata, did not show any significant population structure (Φst=0.004). In contrast to our expectations, the other planktonic-developing species, L. plena, showed some weak but statistically significant population structure (Φst=0.052). We discuss how differences in population genetic structure between species with the same type of development may reflect differences in their historical demography.

Vertical Changes in Density, Size Structure and Shell Shape of the Bivalve Lasaea Undulata Within Intertidal Mussel Beds

Vertical changes in density, size structure and shell shape of Lasaea undulata (Bivalvia: Galeommatoidea) inhabiting intertidal mussel beds were studied at Wakayama Prefecture, Japan. At the study site, where two mytilids Septifer virgatus and Hormomya mutabilis formed vertically contiguous mussel beds, Lasaea density decreased downshore within the S. virgatus bed of the upper and mid zones. Few individuals were found within the H. mutabilis bed of the lower zone. Multiple linear regression analysis revealed that shore height was the only factor which showed a significant, positive correlation with density. Size structure differed between the upper and lower parts of the S. virgatus bed, suggesting that reproductive periods or growth rates of L. undulata differed with shore height. Prodissoconch length and shell shape were also different among shore heights. Number, size and shell shape of juveniles brooded within parents indicated that this species releases its young as non-planktotrophic, crawl-away juveniles. There was no significant difference in density of recruits between artificial mussel clumps of S. virgatus and H. mutabilis within enclosure cages, and no specific association was detected between L. undulata and either of the two mussel species.

Larval and early post-larval development of the protobranch bivalve Solemya velum (Mollusca: Bivalvia)

Early development in the north-west Atlantic awning clam, Solemya velum (Solemyoida: Solemyidae) was examined by light and scanning electron microscopy. Embryonic and pericalymma larval stages, typical of protobranch bivalves, developed within individual adhesive gelatinous egg capsules and offspring emerged at hatching as benthic crawl-away juveniles. Fertilized eggs were light orange in colour, spherical, and had a yolk-mass diameter of approximately 190 μm. Entirely ciliated cylindrical pericalymma larvae, with a length and width of 318 μm and 208 μn, respectively, were obtained within 24 h. These larvae lacked an apical ciliary tuft, possessed nine rows of calymma cells, and actively rotated within the egg capsule. During metamorphosis, which occurred within 48 h of fertilization, the transitory larval ectoderm was entirely ingested. The prodissoconch measured roughly 320 μm in length by 215 μm in height. The foot and ciliated gill buds were well developed by four days after fertilization and subsequent growth contributed to the dissoconch or adult shell. Hatching began at 13 d after fertilization when the shell measured approximately 402 μm in length by 251 μm in height. Actively crawling and burrowing juveniles were cultured for six months after fertilization and an ontogenetic sequence of encapsulated and juvenile shell morphology was obtained for identification purposes. Current contradictory hypotheses regarding the phylogeny of marine bivalve develop-mental types are reviewed in light of new information on the Order Solemyoida.

Drifting and dispersal of small bivalves and gastropods with direct development

Quantitative evidence that several marine benthic invertebrates lacking a planktonic larval stage disperse as juveniles and small adults by drifting in the water column has been obtained using off-bottom intertidal collectors. These collectors were mimics of a habitat commonly used by small molluscs in intertidal seaweed communities: red turf algae. Taxa caught in collectors include three brooding bivalves [ Musculus sp., Lasaea sp., Transennella tantilla (Gould, 1853)] and small gastropods that produce benthic egg capsules and crawl-away juveniles ( Barleeia spp.). Dispersal is accomplished by juveniles—and even sexually mature adults in the case of small-sized species — drifting with water currents using mucous threads in at least some of the taxa found. Some of these molluscs have also been caught in off-bottom collectors placed away from the shore, in the middle of a bay. Findings indicate that, contrary to what is suggested by their mode of development, these invertebrates have alternative and likely effective dispersal mechanisms (at least at a local scale). It is probable that frequent drifting excursions in these taxa enhance rafting opportunities, which in turn may favor long distance dispersal. Large numbers of juveniles of several other species of molluscs whose life cycles include a planktonic larval stage were also caught in off-bottom collectors. These results, coupled with those from previous studies, show that postmetamorphic drifting is a common feature of the life history and ecology of many marine bivalves and gastropods, regardless of their mode of development.

Planktotrophic larval development is associated with a restricted geographic range in Lasaea, a genus of brooding, hermaphroditic bivalves

Members of the intertidal, near-cosmopolitan mollusc genus Lasaea brood their young either to a planktotrophic veliger or crawl-away juvenile stage of development. Developmental mode can be reliably inferred from brood masses and from prodissoconch structure. I have conducted a global developmental survey of this genus based mainly on examination of hundreds of museum lots. With one exception, Lasaea species with a planktotrophic larval development were restricted to the western Pacific. Congeners that lack planktotrophic larvae were found on all continents apart from Antarctica, and also on a large number of oceanic islands. These results indicate that (1) Lasaea “species” releasing crawl-away juveniles have a markedly greater collective geographic range than congeners with planktotrophic larvae; (2) pelagic larvae are not necessary for long-distance dispersal in this genus; (3) rafting has played a key role in the evolutionary success of the genus Lasaea; (4) cross-fertilizing Lasaea species with feeding larvae are less successful in utilizing chance rafting events to colonize new areas than are congeners lacking these traits.