Larval ecology and morphology in fossil gastropods

The shell of marine gastropods conserves and reflects early ontogeny, including embryonic and larval stages, to a high degree when compared with other marine invertebrates. Planktotrophic larval development is indicated by a small embryonic shell (size is also related to systematic placement) with little yolk followed by a multiwhorled shell formed by a free‐swimming veliger larva. Basal gastropod clades (e.g. Vetigastropoda) lack planktotrophic larval development. The great majority of Late Palaeozoic and Mesozoic ‘derived’ marine gastropods (Neritimorpha, Caenogastropoda and Heterobranchia) with known protoconch had planktotrophic larval development. Dimensions of internal moulds of protoconchs suggest that planktotrophic larval development was largely absent in the Cambrian and evolved at the Cambrian–Ordovician transition, mainly due to increasing benthic predation. The evolution of planktotrophic larval development offered advantages and opportunities such as more effective dispersal, enhanced gene flow between populations and prevention of inbreeding. Early gastropod larval shells were openly coiled and weakly sculptured. During the Mid‐ and Late Palaeozoic, modern tightly coiled larval shells (commonly with strong sculpture) evolved due to increasing predation pressure in the plankton. The presence of numerous Late Palaeozoic and Triassic gastropod species with planktotrophic larval development suggests sufficient primary production although direct evidence for phytoplankton is scarce in this period. Contrary to previous suggestions, it seems unlikely that the end‐Permian mass extinction selected against species with planktotrophic larval development. The molluscan classes with highest species diversity (Gastropoda and Bivalvia) are those which may have planktotrophic larval development. Extremely high diversity in such groups as Caenogastropoda or eulamellibranch bivalves is the result of high phylogenetic activity and is associated with the presence of planktotrophic veliger larvae in many members of these groups, although causality has not been shown yet. A new gastropod species and genus, Anachronistella peterwagneri, is described from the Late Triassic Cassian Formation; it is the first known Triassic gastropod with an openly coiled larval shell.     

Swimming Speed of Larval Snail Does Not Correlate with Size and Ciliary Beat Frequency

Many marine invertebrates have planktonic larvae with cilia used for both propulsion and capturing of food particles. Hence, changes in ciliary activity have implications for larval nutrition and ability to navigate the water column, which in turn affect survival and dispersal. Using high-speed high-resolution microvideography, we examined the relationship between swimming speed, velar arrangements, and ciliary beat frequency of freely swimming veliger larvae of the gastropod Crepidula fornicata over the course of larval development. Average swimming speed was greatest 6 days post hatching, suggesting a reduction in swimming speed towards settlement. At a given age, veliger larvae have highly variable speeds (0.8–4 body lengths s⁻¹) that are independent of shell size. Contrary to the hypothesis that an increase in ciliary beat frequency increases work done, and therefore speed, there was no significant correlation between swimming speed and ciliary beat frequency. Instead, there are significant correlations between swimming speed and visible area of the velar lobe, and distance between centroids of velum and larval shell. These observations suggest an alternative hypothesis that, instead of modifying ciliary beat frequency, larval C. fornicata modify swimming through adjustment of velum extension or orientation. The ability to adjust velum position could influence particle capture efficiency and fluid disturbance and help promote survival in the plankton.     

Reproduction and larval development of the gastropod <Emphasis Type="Italic">Cryptonatica janthostoma</Emphasis> (Gastropoda: Naticidae)

The larval morphology of the gastropod Cryptonatica janthostoma inhabiting the Northwest Pacific was described for the first time. Hatched planktotrophic veligers of C. janthostoma had shells 250 μm in height with 0.8 whorls, a bilobate velum with a dark brown pigmentation band shaped along its edge, pair of eye spots, tentacles and statocysts. The surface of the embryonal shell (protoconch 1) was covered with fine granules extended at the dorsal side and rounded at lateral surfaces. Concentric crests and growth lines occurred on part of the shell of late free-swimming larvae (protoconch 2) The velum of the C. janthostoma larvae remained bilobate during the pelagic stage of development, whereas it was divided in 4 lobes during larval development in most of the other species of the Naticidae family. The veliger of C. janthostoma was similar to that of Natica montagu from Danish waters [16] by its shape, pigmentation, shell sculpture and velum structure.     

扁玉螺早期发育的实验观察

在实验室条件下人工孵化扁玉螺(Neverita didyma)的卵块,观察了其胚胎发育和幼虫发育过程.扁玉螺的早期发育属间接发生型,其胚胎发育包括卵裂期、囊胚期、原肠胚、膜内担轮幼虫、膜内面盘幼虫;幼虫发育包括面盘幼虫、后期面盘幼虫和匍匐幼虫;匍匐幼虫经变态后发育为稚螺.在水温25～26℃条件下,受精卵发育至膜内面盘幼虫约需38h,5～6d后面盘幼虫冲破卵膜而孵化.扁玉螺面盘幼虫的显著特点是具有1对眼点和1对平衡囊,面盘呈双叶状;后期面盘幼虫的面盘为4叶,呈蝴蝶状,足发达,幼虫既能浮游,又能爬行.后期面盘幼虫进一步生长发育,逐渐转入匍匐生活.     

Notes on the reproduction of high-Antarctic molluscs from the Weddell Sea

Summary The reproductive modes of 66 molluscan species from the Weddell Sea, Antarctica were investigated either by rearing of specimens in aquaria (Neomeniomorpha [Solenogastres], Polyplacophora and Gastropoda) or by studies of the larval shell (Bivalvia). The results show that not all marine invertebrates living in cold water environments produce large eggs, provide postspawning parental care or lack planktonic larvae (Thorson's rule), nor that brooding behaviour is always associated with small adult size. Several lecithotrophic (Solenogastres, Polyplacophora) and meroplanktonic, planktotrophic larvae (Gastropoda) were observed in aquaria. Investigations of the larval shell morphology indicate a planktotrophic or lecithotrophic larval stage in 27 Bivalvia species. With exception of two species of meroplanktonic gastropod larvae no developmental stages of benthic molluscs were ever found in plankton hauls in the Weddell Sea. This indicates that most larvae may live demersally. Brooding occurred in 1 Monoplacophora and 17 Bivalvia species. Intracapsular metamorphosis with very long embryonic development was observed in 15 Gastropoda species.     

Predation on bellerophontiform molluscs in the Palaeozoic

Shell repair assumed to result from failed predation is documented in 66 specimens of Ordovician-Carboniferous bellerophontiform tergomyan and gastropod molluscs to examine the relationship between the distribution and appearance of injuries, shell morphology and the internal anatomy of the molluscs, as well as the attack strategies of the presumed predators. Furthermore, the distribution of repaired injuries from failed attacks along the apertural margin as a reflection of the nature of the margin and emarginations is investigated. Bellerophontiform molluscs are ideal for this study because of their distinctive isostrophic morphology and the possibility to directly compare broad and narrow conchs with either deep or shallow medial emarginations. The results show that taxa with a deep medial emargination in the form of a slit have significantly more medial injuries than lateral ones. Near-equal frequencies of lateral and medial injuries in specimens with a shallow emargination (slit or sinus) suggest random distribution. Shell form (narrow or broad) does not exert overall control on the distribution of injuries except, perhaps, in some broad explanate shells with an insignificant medial emargination. While this suggests that it is the type of medial emargination that governs distribution of injuries in these forms, it is not clear if this is a result of passive selection due to structural geometry or preferential targeting by predators (i.e. site-specific mode of attack). Predation strategies on bellerophontiform molluscs thus seem to be dependent on the morphological features of the shells rather than their interpretation as tergomyan or gastropod.     

SHELL MICROSTRUCTURE OF GASTROPODS FROM LAKE TANGANYIKA,AFRICA: ADAPTATION,CONVERGENT EVOLUTION,AND ESCALATION

Gastropod shells from Lake Tanganyika, with their heavy calcification, coarse noded ribbing, spines, apertural lip thickening and repair scars, resemble marine shells more closely than they resemble other lacustrine shells. This convergence between Tanganyikan and marine gastropod shells, however, is not just superficial. Scanning electron microscope (SEM) studies reveal that the Tanganyikan shells are primarily layers of crossed-lamellar crystal architecture (that is, needle-like aragonite crystals arranged into laths that are packed into sheets such that the aragonite needles of adjacent laths are never parallel). The number of crossed-lamellar layers can vary from one to four between different Tanganyikan gastropod species. In species with two or more crossed-lamellar layers, the orientation of the lamellae is offset by approximately 90° between the different layers. The number of crossed-lamellar layers in the shell wall is positively correlated with shell strength and with predation resistance. Three and four crossed-lamellar layers in the shell wall evolved several times independently within the endemic thiarid gastropod radiation in Lake Tanganyika. Repeated origins of three and four crossed-lamellar layers suggest that they may be specific adaptations by Tanganyikan gastropods to strengthen their shells as a defense against shell-crushing predators.     

THE PLANKTONIC VELIGER OF AMPHIBOLA CRENATA (GMELIN)

Amphibola crenata (Gmelin) has a well-developed planktonic veligerstage which remains in the plankton for several weeks and feedsactively. It resembles an opisthobranch veliger with a sinistralshell and conspicuous black larval kidney. After metamorphosisthe pitch of the coil of the shell is altered so that the bodywhorl grows, over the larval whorls and produces a dextrallycoiled adult shell with an internal protoconch. (Received 1 July 1980;     

Eastward and Westward Dispersal Across the Tropical Atlantic Ocean of Larvae Belonging to the Genus Bursa (Prosobranchia,Mesogastropoda, Bursidae)

Larvae of the genus Bursa are commonly found in the South Equatorial Current and the Equatorial Undercurrent of the tropical Atlantic Ocean. Identification of Bursa veliger larvae in the plankton of such tropical waters is made possible by a comparison of larval shells with protoconchs of juvenile and well-preserved adult specimens. The relationship between the average current velocity and the estimated minimum duration of larval development of Bursa thomae suggests that there is sufficient time to account for successful trans-Atlantic transport of its veligers in either direction between West Africa and South America. The dispersal of veliger larvae explains the wide geographical distribution attained by the genus Bursa.     

Larval fishes and zooplankton in a cyclonic eddy in Hawaiian waters

A cold-core eddy occurred off the Kona coast of the island ofHawaii in July 1982. It remained in that area for {small tilde}70days, sufficient time for many reef fish species to completetheir planktonic larval phase. The deployment of eight currentdrogues in the eddy showed how entrainment of plankton fromthe reef and adjacent offshore waters can occur and that passivedrift can return drifters from the deep sea to shore. Larvalfishes may be swept past the island every 7–8 days ina weak eddy and 3.5–5 days in a strong eddy. Planktoncollections were made at night near the surface and at the samedepth as the current drogues. Zooplankton were most concentratedat the eddy center. Taxonomic analysis of the plankton showedthat the dominant animals were calanoid copepods, malacostracans,hyperud amphipods, gastropod and bivalve larvae and chaetognaths.The densities of zooplankton and larval fishes in the eddy werehigher than in the same area before the arrival of an eddy.Larval fishes were most abundant in the periphery and amongthese, midwater fish larvae (gonostomatids and myctophids) werethe most numerous. Other numerous fish larvae in the eddy includedscombrids, particularly Thunnus albacares. carangids and thereef fish, Abudefduf abdominalis is (Pomacentridae).     

MORPHOLOGY AND BEHAVIOR OF CRABS AND GASTROPODS FROM LAKE TANGANYIKA,AFRICA: IMPLICATIONS FOR LACUSTRINE PREDATOR-PREY COEVOLUTION

The shells of most lacustrine gastropods are typically small, weakly calcified, and modestly ornamented to unornamented. Similarly, most lacustrine crabs are usually small detritivores with weak chelae. A number of invertebrate taxa in Lake Tanganyika, however, deviate from these generalities. This study explores a predator-prey coevolution model as an explanation for the large, heavily calcified, and ornate gastropods and the robust, durophagous crabs of Lake Tanganyika. The endemic thiarid and viviparid gastropods from Lake Tanganyika have significantly thicker shells and higher frequencies of terminal apertural lip thickening than closely related cosmopolitan taxa from outside the lake. Tanganyikan gastropods also display considerably higher incidence of shell repair, following nonlethal shell damage, than cosmopolitan taxa of the same families. There is a strong positive correlation between gastropod apertural lip thickness and shell repair frequency among all the gastropod species analyzed. The endemic Tanganyikan potamonautid crab Platytelphusa armata (a molluscivore) possesses larger, more robust crushing chelae than other African potamonautid or potamonid crabs. In contrast with the cosmopolitan African crabs, the Tanganyikan crabs display molariform, rather than serrate dentition on their crushing chelipeds. In shell-crushing experiments, the Tanganyikan gastropod shells were an order of magnitude stronger than typical lacustrine gastropod shells, many well within the range of tropical marine gastropod shell strengths. Predation experiments with the endemic gastropods Spekia, Neothauma, Lavigeria spp., Paramelania spp. and the crab Platytelphusa armata showed that increased size, apertural lip thickness or shell sculpture reduced the successful predation rate of P. armata. Crabs with large chelae have a greater ratio of successful: unsuccessful attacks than crabs with small chelae. Among cases of successful predation, crabs with large chelae employed predation methods that required less time and energy (such as crushing the shell in the cheliped) than the methods employed by crabs with small chelae (such as peeling the shell from the aperture or the spire). The morphological, shell-crushing, and aquarium experiment data, considered in concert, provide strong support for the idea that the endemic gastropods and crabs of Lake Tanganyika have coevolved over the past 7 million years.     

The influence of turbidity on growth and survival of fish larvae: a numerical analysis

Growth and survival through the early larval phase probably limit the production potential of many commercially important fish stocks. Attempts to increase the production of these stocks by restocking of juveniles have generally failed. Here, we analyse how enhanced concentrations of phytoplankton and zooplankton affect the survival of fish larvae during their early life stages. The analysis is developed for larvae feeding on copepod eggs and nauplii, with fish and invertebrates as major predators. A model of feeding and growth of fish larvae is applied to assess the benefit of enhanced phytoplankton and zooplankton abundance. The analysis shows that the shading effect of higher phytoplankton concentration may reduce predation rates on fish larvae substantially. This `top-down' effect may be more important for the cohort survivorship than the `bottom-up' mechanism in situations when larval food is sufficiently abundant. However, while increased algal biomass will improve recruitment at high zooplankton concentration, it may also reduce recruitment at low zooplankton concentrations and shallow mixing depths. Both the larvae and their vertebrate predators are dependent on light to detect their prey, and the longer reactive distance of the predators make them more susceptible than the larvae to reduced light levels and increased turbidity. We discuss the implications of reduced predation and increased zooplankton abundance on recruitment and production of fish larvae, and point at environmental conditions where changing algal biomass is likely to affect recruitment success.     

Synchronous spawning in a recently established population of the zebra mussel,Dreissena polymorpha,in western Lake Erie,USA

Seasonal patterns of reproduction in a newly established population of Dreissena polymorpha are described for a site in the western basin of Lake Erie. Reproduction was monitored by histological examination of gonads, analysis of shell length-dry weight relationships, and following abundance of planktonic and settling larvae. Patterns of planktonic larval abundance and settling showed a distinct bimodal pattern in July and August, but conflicted with histological and length-dry weight data that showed spawning was a brief, highly synchronous event occurring in late August. Differences between histological data and abundance of larvae in the plankton can be explained as resulting from drift of larvae from disjunct populations of D. polymorpha which spawned earlier, into the study area. Veliger larvae were present in the plankton at low densities throughout the warm months before and after periods of peak abundances. The presence of these larvae can be explained by a combination of asynchronous spawning among local populations and postponed settlement by planktonic larvae.     

Usefulness of the opercular nucleus for inferring early development in neritimorph gastropods

The early ontogeny of gastropods (i.e., planktotrophic vs. nonplanktotrophic) may be inferable from the morphology of the protoconch in adult shells. The protoconch consists of both embryonic and larval shells in species with planktotrophic development; the embryonic shell forms in the intracapsular period and the succeeding larval shell gradually develops during the larval period. In nonplanktotrophic species, on the other hand, there is no additional growth of the larval shell and the protoconch consists exclusively of a relatively large embryonic shell formed prior to hatching. This "shell apex theory" has been applied to many species of shell-bearing gastropods, but biotic and abiotic erosion of the apex often prevents detailed examination of the protoconch and subsequent inferences about ontogeny. I examined the gastropod operculum to test its utility for predicting developmental mode, drawing on the Neritimorpha as model taxa. Most aquatic members of Neritimorpha were found to bear an operculum with a clearly demarcated nucleus; SEM observations reveal four types of nuclei, which correspond to different types of protoconch morphologies and observed ontogenies for the study species. The nucleus is secreted before metamorphosis, fits into the shell aperture of the larva, and reflects early ontogeny as morphology, as does the protoconch. Moreover, the apparently organic (rather than calcareous) composition of the nucleus makes it nearly invulnerable to erosion and very advantageous, compared to the protoconch, in this ecologically diverse group, whose habitats range from freshwater streams and mangrove swamps to rocky shores and deep-sea hydrothermal vents. The measurements of the nucleus are also valuable for taxonomic purposes, especially in the species identification of veliger larvae and juvenile snails. On the other hand, the opercular nuclei of the Caenogastropoda and Heterobranchia are often eroded away in adult individuals; even if present, the morphology of the nuclei does not seem to clearly reflect early ontogeny in those groups.     

Reproduction and larval development of the gastropod molluskTegula rustica in Peter the Great Bay, Sea of Japan

The reproduction and larval development of the prosobranch gastropod molluskTegula rustica were studied under laboratory conditions. In Vostok Bay (Peter the Great Bay), the reproduction of theTegula takes place in August, when the water temperature is 19–20°C. Under laboratory conditions, the spawning of females was stimulated by adding a sperm emulsion to a vessel containing adult females. We observed asynchronous and intermittent release of gametes. The egg cell is 190 μm in diameter. Fertilization is external, and the course of development includes a lecithotrophic pelagic larva. Complete development, from fertilization to metamorphosis, takes 7 days in a laboratory culture. The larvae settle when the shell size across the first whorl is 220–230 μm and the total shell whorl is about 90°. The shape of the veliger shell is elongated mitriform and the velum is rounded, made up of a single lobe. The sculpture of the protoconch is irregularly ribbed.     

Interactions between adult and larval bluegill sunfish: positive and negative effects

Adult fish may affect the growth and survival of conspecific larvae through a variety of pathways, including negative interactions via competition for shared limiting resources or via predation (i.e., cannibalism), and positive interactions due to the consumption of larval predators and via resource enhancement (i.e., presence of adults increases availability of larval prey). To examine the overall effect of adult bluegill sunfish (Lepomis macrochirus) on larval bluegill, we conducted a field experiment in which we manipulated adult densities and quantified larval growth and survival, prey abundance, invertebrate predator abundance, and cannibalism. The presence of adult bluegill had a negative effect on final larval mass. This response was consistent with competition for zooplankton prey. Adult bluegill reduced the abundance of large zooplankton (e.g., Chaoborus and Daphnia), which were the dominant prey of bluegill larvae in the absence of adults. Larvae in the no-adult treatment also had significantly more prey in their stomachs compared to larvae in the presence of adults. Larval survival was maximized at intermediate adult densities and the overall production of larvae peaked at intermediate adult densities. The higher larval survival at intermediate adult densities is attributed to a reduction in invertebrate predators in treatments with adult bluegill; invertebrate predators experienced an 80% reduction in the presence of adult fish. Decreased larval survival at the highest adult density was not due to resource limitation and may be due to cannibalism, which was not directly observed in our study, but has been observed in other studies.     

Infaunal or semi-infaunal bellerophont gastropods: analysis of Euphemites and functionally related taxa

Burrowing and plowing gastropods may have existed prior to the Mesozoic, contrary to the conservative tendency of categorizing Paleozoic archaeogastropods as herbivorous hardground dwellers. We propose that Euphemites and other bellerophontiform molluscs such as Praematuratroph and Beyrichidiscus make functional and paleoecological sense only if reconstructed with an internal shell adapted to an infaunal mode of life. Attributes diagnostic of a probable infaunal mode of life in fossil bellerophontiform molluscs include: (1) lack of apertural flare; (2) restricted aperture; (3) low rate of whorl expansion; (4) semi-radial aperture; (5) extensive secondary shell deposits; (6) absence of extensive collabral ornament; (7) dorsolateral or umbilical furrows; (8) color patterns indicative of mantle extension and retraction capabilities; (9) absence of shell breakage and repair; and (10) associated lithologies indicative of penetrable substrates such as mudstones. Niche diversity in the bellerophontacean molluscs was probably much greater than previously suspected. This is entirely consistent with their long geologic range. Most bellerophontaceans, particularly the Late Paleozoic forms, were probably either 'nestling' or semi-infaunal with the apertural margins enwrapped by mantle or mantle and foot. As such they may have been particularly susceptible to predation during the postulated Mesozoic increase in number of infaunal predators- a factor which may have been contributory to the bellerophontacean demise.     

The Paleozoic evolution of the gastropod larval shell: larval armor and tight coiling as a result of predation‐driven heterochronic character displacement

Early and middle Paleozoic gastropod protoconchs generally differ strongly from their corresponding adult morphologies, that is, most known protoconchs are smooth and openly coiled, whereas the majority of adult shells are ornamented and tightly coiled. In contrast, larval and adult shells of late Paleozoic gastropods with planktotrophic larval development (Caenogastropoda, Neritimorpha) commonly resemble each other in shape and principle ornamentation. This is surprising because habitat and mode of life of planktonic larvae and benthic adults differ strongly from each other. Generally, late Paleozoic to Recent protoconchs are tightly coiled. This modern type of larval shell resembles the adult shell morphology and was obviously predisplaced onto the larval stage during the middle Paleozoic. The oldest known planktonic‐armored (strongly ornamented) larval shells are known from the late Paleozoic. However, smooth larval shells are also common among the studied late Paleozoic gastropods. The appearance of larval armor at the beginning of the late Paleozoic could reflect an increase of predation pressure in the plankton. Although there are counter examples in which larval and adult shell morphology differ strongly from each other, there is statistical evidence for a heterochronic predisplacement of adult characters onto the larval stage. Larval and adult shells are built in the same way, by accretionary secretion at the mantle edge. It is likely that the same underlying gene expression is responsible for that. If so, similarities of larval and adult shell may be explained by gene sharing, whereas differences may be due to different (planktic vs. benthic life) epigenetic patterns.     

Qualitative assessment of the diet of European eel larvae in the Sargasso Sea resolved by DNA barcoding

European eels (Anguilla anguilla) undertake spawning migrations of more than 5000 km from continental Europe and North Africa to frontal zones in the Sargasso Sea. Subsequently, the larval offspring are advected by large-scale eastward ocean currents towards continental waters. However, the Sargasso Sea is oligotrophic, with generally low plankton biomass, and the feeding biology of eel larvae has so far remained a mystery, hampering understanding of this peculiar life history. DNA barcoding of gut contents of 61 genetically identified A. anguilla larvae caught in the Sargasso Sea showed that even the smallest larvae feed on a striking variety of plankton organisms, and that gelatinous zooplankton is of fundamental dietary importance. Hence, the specific plankton composition seems essential for eel larval feeding and growth, suggesting a linkage between eel survival and regional plankton productivity. These novel insights into the prey of Atlantic eels may furthermore facilitate eel larval rearing in aquaculture, which ultimately may replace the unsustainable use of wild-caught glass eels.