Life history of Littorina scutulata and L. plena, sibling gastropod species with planktotrophic larvae

Abstract. The intertidal, sibling species Littorina scutulata and L. plena (Gastropoda, Proso‐branchia) are sympatric throughout most of their ranges along the Pacific coast of North America. Both species release disc‐shaped, planktonic egg capsules from which planktotrophic veliger larvae hatch. Here I review existing data and present new observations on these species' life history, including age at first reproduction, spawning season, maximum fecundity rates, capsule morphology, egg size and number, pre‐hatching development, larval growth at three food concentrations, potential settlement cues, planktonic period, and protoconch size. Previous classification of egg capsule morphologies used to distinguish the species is inaccurate; instead, capsules can be categorized into three types of which each species may produce two. Females of L. scutulata produced capsules with either two rims of unequal diameter or one rim, while females of L. plena produced capsules with one rim or two rims of nearly equal diameter. Females of each species spawned sporadically from early spring to early fall in Puget Sound. Larvae of L. plena hatched one day earlier than those of L. scutulata, and both species grew fastest in the laboratory at intermediate food concentrations. Larvae metamorphosed in the presence of a variety of materials collected from their adult habitat, including conspecific adults, algae, rocks, and barnacle tests. This is the first report of planktotrophic larvae in this genus metamorphosing in the laboratory. The total planktonic period of 8 larvae of L. scutulata raised in the laboratory was 37–70 days, and a single larva of L. plena metamorphosed after 62 days. Protoconch diameter of shells collected from the field was 256–436 μm and did not differ significantly between the species. Previous allozyme and mitochondrial DNA work has suggested high levels of genetic variability in both species and greater genetic population structure in L. plena, despite the long spawning season and long‐lived larvae in both species. The interspecific life history differences described here appear insufficient to produce consistent differences in gene flow patterns.     

The biology of the Northeastern Pacific Turridae. V. Demersal development,synchronous settlement and other aspects of the larval biology of Oenopota levidensis

Summary

The larval development and metamorphosis of a turrid gastropod is described for the first time. This snail, Oenopota levidensis, is typical of the boreal genus Oenopota, which has over 150 described species. Development to a veliger occurs within a lenticular capsule in about 50 days. The capsules hatch to release veligers which swim for less than a week. The remainder of their planktotrophic larval period is spent demersally. Demersal veligers assumed one of two characteristic postures; they remain on the bottom with the velum either extended laterally or folded over the shell. These demersal veligers continue development and metamorphose after another 25 days. The majority of the veligers in the 55 cultures examined metamorphosed and settled within a 96-h period, even though their oviposition occurred over a 47-day period. Potential selective forces leading to this synchronous settlement are proposed.     

Veligers of an introduced bivalve,Limnoperna fortunei,are a new food resource that enhances growth of larval fish in the Paraná River (South America)

1. Larvae of ‘sábalo’, Prochilodus lineatus, whose adults represent over 60% of overall fish biomass in the Río de la Plata Catchment, have been observed to feed intensively on veligers of the exotic bivalve Limnoperna fortunei. 2. To assess the effects of this dietary shift on the growth of P. lineatus, 28‐day laboratory experiments were carried out feeding newly hatched P. lineatus larvae with three diets: zooplankton artificially enriched with L. fortunei veligers; natural zooplankton; and zooplankton artificially enriched with cladocerans and copepods. The average length, weight and gut contents of the fish larvae were assessed weekly and metabolic rates of fish larvae were measured. 3. Proportions of veligers in gut contents were always higher than those in the experimental diet: 100, 76 and 21% for veliger‐enriched, natural and low‐veliger diets, respectively. Larvae fed a veliger‐enriched diet grew to a significantly larger size than larvae fed the other two diets. In energetic balance comparisons using metabolic rates and prey energy content, all three diets were sufficient to support metabolism and growth. The greatest values of excess energy at the end of each week were in the veliger‐enriched experiments. 4. Feeding on veligers of L. fortunei significantly enhances the growth of P. lineatus larvae and supports the idea that this new and abundant resource is selectively preyed upon by P. lineatus during its larval stage. Higher growth rates may stem from the higher energy contents of veligers compared to crustaceans and/or from the lower energy costs of capturing slower prey.     

Effect of plasticity in hatching on duration as a precompetent swimming larva in the nudibranch Phestilla sibogae

Abstract. Plasticity in hatching can balance risks of benthic and pelagic development and thereby affect the extent of larval dispersal. Veligers of the nudibranch Phestilla sibogae hatched from their individual capsules if the encapsulated embryos were scattered from a torn gelatinous egg ribbon. Hatching occurred as early as day 4 at 23°–25°C. The early hatchlings lacked a propodium, swam, and were not yet competent to settle and metamorphose. Hatching may be induced by predation: crabs consumed egg ribbons, and a portunid crab, caught in the act of tearing an egg ribbon, scattered encapsulated embryos. Undisturbed egg masses hatched as late as 9–11 d at 23°–25°C, or as early as 8 d in a trial at 26°C. Late hatchlings had a well-developed propodium, and 20–100% metamorphosed within a day of exposure to the inducer from the nudibranch's coral prey. A few metamorphosed nudibranchs were found within hatching egg masses. Thus, the veligers can hatch so late that many are competent to metamorphose or so early that the obligate planktonic period can last 4 or more days. An attack by a predator means the benthic habitat is dangerous for the embryos, and swimming is presumably the safer option. In the absence of disturbance, the veligers hatch when ready or nearly ready to settle.     

Embryonic development of the sea butterfly Desmopterus papilio (Gastropoda: Thecosomata)

The embryonic development of the thecosome Desmopterus papilio is described for the first time. The mature individual produced a round-shaped egg mass containing ca. 200 fertilised eggs. First cleavage was observed 15 min after the release of the egg mass. Embryos showed typical molluscan spiral cleavage: macromeres produced the first and second quartets of micromeres in clockwise and counterclockwise directions, respectively. A trochophore larva hatched from the egg capsule 28 h after the release of the egg mass. Thereafter, the larva secreted a primary shell at the posterior part, developing into the veliger stage. These findings may be useful for future work on postembryonic development, especially on the loss of the veliger shell, in the genus Desmopterus which is the only group of thecosome species without a shell in the adult stage.     

Specific amplification of the 18S rRNA gene as a method to detect zebra mussel (Dreissena polymorpha) larvae in plankton samples

An important issue in the management of zebra mussel (Dreissena polymorpha) populations is early, rapid, and accurate detection of the planktonic larvae (veliger) of the zebra mussel. The goal of this study was to explore the feasibility of developing a molecular approach for the detection of zebra mussel larvae in diverse environments. In this study a Dreissena polymorpha-specific 18S ribosomal RNA gene targeted oligonucleotide primer (ZEB-715a) and Polymerase Chain Reaction (PCR) assay was developed and compared with cross-polarized microscopy as a means to detect zebra mussel veligers in plankton samples. The design of the zebra mussel-specific primer was facilitated by sequencing nearly the complete 18S rRNA gene from the zebra mussel and three other closely related freshwater Veneroids including the quagga mussel (D. bugensis), the dark false mussel (Mytilopsis leucophaeata), and the Asian freshwater clam (Corbicula fluminea). The specificity of the primer for the zebra mussel was empirically tested by using the primer as a direct probe in a blot hybridization format. A single veliger in a plankton sample could be detected by PCR using this approach. Veliger detection sensitivity using the PCR approach was estimated to be over 300 times more sensitive than cross-polarized light microscopy based techniques. Cross-polarized light microscopy and the PCR technique were used to identify the presence of zebra mussel larvae in plankton samples that were collected from a variety of natural and industrial water sources. Detection results (presence or absence) were generally consistent between the two methods. Although additional studies will be required before routine application of molecular based veliger detection technology is available, a long-term goal of this work is the application of molecular technology to the development of a field device for the routine detection and quantification of zebra mussel veligers.     

Egg capsules and larval development of Nassarius burchardi (Philippi, 1849) and Nassarius jonasii Dunker, 1846 and comparisons with other Nassariidae (Caenogastropoda)

Adult Nassarius burchardi and N. jonasii were maintained in a laboratory, allowed to spawn and their early life stages described. N. burchardi veligers hatched from bulliform, oval capsules and N. jonasii veligers hatched from circular capsules with axial ridges. The capsules are compared with those described for other Nassariidae. All eggs developed within the capsules and hatching occurred within six to eight days in the laboratory. The planktotrophic veligers developed in four to five weeks before settling and metamorphosing. The veligers of both species were of comparable size and morphology and spent similar times developing as other Nassarius species from temperate waters. The two species differ in protoconch microsculpture.     

GABA is an inhibitory neurotransmitter in the neural circuit regulating metamorphosis in a marine snail

The marine mud snail, Tritia (=Ilyanassa) obsoleta, displays a biphasic life cycle. During the initial phase of early development, embryos hatch from benthic egg capsules to become weakly swimming veliger larvae. In the second phase, adult T. obsoleta are facultative carnivores and major agents of community disturbance. Metamorphosis is the irreversible developmental event that links these two life history stages. When physiologically competent, larvae can respond to appropriate environmental cues by settling onto their mudflat habitat and transforming themselves into miniature adult snails. Two neurotransmitters—serotonin and nitric oxide—have opposing effects on the metamorphic process in this species. In multiple other species of gastropod and bivalve molluscs, a third neurotransmitter, the classically inhibitory compound γ‐aminobutyric acid (GABA), can induce settlement or metamorphosis upon external application to competent larvae. In this situation, GABA is presumed to mimic the action of ligands from the juvenile environment that bind to larval chemosensory receptors and activate the metamorphic pathway. Results of our experiments contradict this commonly reported action of GABA on molluscan larvae. External application of GABA to competent larvae of T. obsoleta elicited no response, but instead attenuated the action of serotonin (5‐HT), a metamorphic inducer. Our investigations into the responses of larval T. obsoleta to multiple GABAergic reagents support our hypothesis that GABA functions internally as a neurotransmitter in the pathway that controls the initiation of metamorphosis. Our results also suggest that GABA acts directly on or downstream from serotonergic neurons to regulate the metamorphosis‐inducing effects of this neurotransmitter. © 2018 Wiley Periodicals, Inc. Develop Neurobiol 78: 736–753, 2018     

Embryonic development of the false limpet Siphonaria lateralis from Atlantic Patagonia

Siphonariids are pulmonate gastropods inhabiting rocky intertidal habitats, and many studies have focused on these false limpets around the world. In the southern South Atlantic, studies on reproduction and development in species of Siphonaria are scarce. We studied the embryonic development and egg masses of Siphonaria lateralis at its northernmost distribution in Atlantic Patagonia. In S. lateralis, as in most species of Siphonaria, individuals spawn benthic egg masses that strongly attach to intertidal rocky substrata. A single spherical egg that measures ~120 µm develops inside the egg capsule of S. lateralis. Considering the relatively small egg size, and reports from previous studies, the developmental modality of S. lateralis might be expected to include a planktotrophic larval phase. However, we found that hatchlings emerged as 1‐mm crawling juveniles, probably owing to the presence of intracapsular fluid, which may provide the energetic requirements for direct development. The embryonic size changed little from the egg to veliger stages, and then increased rapidly until the hatchling stage. We compared development in S. lateralis with development in the sympatric Siphonaria lessonii, in which egg size was reported to be ~80 µm and hatching occurs as planktotrophic veliger larvae. In these two species, spawn and early intracapsular developmental modes are remarkably different; these differences represent contrasting ways to survive in the harsh and physically stressful intertidal Patagonian coasts.     

Temperature‐mediated trade‐offs and changes in life‐history integration in two slipper limpets (Gastropoda: Calyptraeidae) with planktotrophic development

Intraspecific variation in egg size and hatching size, and the genetic and environmental trade‐offs that contribute to variation, are the basis of the evolution of life histories. The present study examined both univariate and multivariate temperature‐mediated plasticity of life‐history traits, as well as temperature‐mediated trade‐offs in egg size and clutch size, in two planktotrophic species of marine slipper limpets, Crepidula. Previous work with two species of Crepidula with large eggs and lecithotrophic development has shown a significant effect of temperature on egg size and hatching size. To further examine the effect of temperature on egg size in Crepidula, the effects of temperature on egg size and hatching size, as well as the possible trade‐offs with other the life‐history features, were examined for two planktotrophic species: Crepidula incurva and Crepidula cf. marginalis. Field‐collected juveniles were raised at 23 or 28 °C and egg size, hatching size, capsules/brood, eggs/capsule, time to hatch, interbrood interval, and final body weight were recorded. Consistent with results for the lecithotrophic Crepidula, egg size and hatching size decreased with temperature in the planktotrophic species. The affects of maternal identity and individual brood account for more than half of the intraspecific variation in egg size and hatching size. Temperature also showed a significant effect on reproductive rate, with time to hatch and interbrood interval both decreasing with increasing temperature. However, temperature had contrasting effects on the number of offspring. Crepidula cf. marginalis has significantly more eggs/capsule and therefore more eggs per brood at 28 °C compared to 23 °C, although capsules/brood did not vary with temperature. Crepidula incurva, on the other hand, produced significantly more capsules/brood and more eggs per brood at the lower temperature, whereas the number of eggs/capsule did not vary with temperature. The phenotypic variance–covariance matrix of life‐history variables showed a greater response to temperature in C. incurva than in C. cf. marginalis, and temperature induced trade‐offs between offspring size and number differ between the species. These differences suggest that temperature changes as a result of seasonal upwelling along the coast of Panama will effect the reproduction and evolution of life histories of these two co‐occurring species differently. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ?? , ??–??.     

Effect of desalination on the littoral tecturid gastropods in early development

The effect of decreased salinity on the limpetsCollisella dorsuosa, C. versicolor, C. radiata, andNotoacmea concinna (Mollusca, Gastropoda) is studied at early stages of development. It is shown that, for normal development from fertilization to the veliger stage, the salinity must be not less than 22–24‰. A decrease in salinity depressed the behavior of larvae. At earlier stages, the larvae were less sensitive to changes in salinity than at later stages. At the same time, veligers were better able to adapt to changes in salinity than trochophores. The vertical water distribution of larvae depended on their age. Two days after fertilization, the larvae sank down to start a benthic life. It is proposed that the narrow tolerance range of littoral limpet larvae to changes in salinity is connected with the fact that they spend a relatively small part of their life in plankton.     

Veligers from the nudibranch <Emphasis Type="Italic">Dendronotus</Emphasis><Emphasis Type="Italic">frondosus</Emphasis> show shell growth and extended planktonic period in laboratory culture

The planktonic period of planktotrophic veliger larvae from the nudibranch Dendronotus frondosus was characterized by laboratory culture methods. Larvae in culture successfully metamorphosed at 73–86 days after hatching. These veligers have Type 2 (Thompson) larval shells that significantly increased in length over the first 7–14 days after hatching. Direct observations of the development of nudibranch larvae with Type 2 protoconchs are limited, and these data help clarify previous attempts to correlate shell type and growth with minimum planktonic periods. Although these are not absolute values for the planktonic period of D. frondosus larvae, these data show the potential for extended larval dispersal and may help explain reports of an extensive geographic range in north-temperate waters for this species.     

Seamount egg‐laying grounds of the deep‐water skate Bathyraja richardsoni

Highly localized concentrations of elasmobranch egg capsules of the deep‐water skate Bathyraja richardsoni were discovered during the first remotely operated vehicle (ROV) survey of the Hebrides Terrace Seamount in the Rockall Trough, north‐east Atlantic Ocean. Conductivity–temperature–depth profiling indicated that the eggs were bathed in a specific environmental niche of well‐oxygenated waters between 4·20 and 4·55° C, and salinity 34·95–35·06, on a coarse to fine‐grained sandy seabed on the seamount's eastern flank, whereas a second type of egg capsule (possibly belonging to the skate Dipturus sp.) was recorded exclusively amongst the reef‐building stony coral Solenosmilia variabilis. The depths of both egg‐laying habitats (1489–1580 m) provide a de facto refuge from fisheries mortality for younger life stages of these skates.     

Long-term effects of prey-availability, partnering and temperature on overall egg capsule output of 'New Zealand flatworms', Arthurdendyus triangulates

Arthurdendyus triangulatus is an invasive terrestrial flatworm that preys on earthworms. To assess A. triangulatus egg capsule production, flatworms were maintained in ventilated polypropylene tubs (7.5 L) kept in controlled environment (CE) chambers or outdoors in the ground. Controlled environment chambers were maintained at 8°C or 14°C, flatworms kept singly or paired within tubs and offered Eisenia fetida according to a weight equalling one‐eighth or one‐half of the mean flatworm weight, or left unfed. The tubs were a successful method for keeping flatworms, with some surviving for over one year. The greatest number of egg capsules produced by an individual A. triangulatus was nine over a 16 week period for a flatworm kept at 14°C and fed at the one‐half regime (0.56 egg capsules flatworm^‐1 week^‐1). Although the effects of treatments varied with CE chambers, there was some evidence from flatworms kept outdoors, that feeding affected egg capsule output, with those flatworms fed at the one‐half regime tending to produce more egg capsules (P= 0.057). Flatworms at the one‐eighth regime or that were unfed produced progressively lighter egg capsules and substantially declined in weight themselves. Nevertheless, even unfed flatworms continued to produce egg capsules for 18 weeks. The lightest egg capsule weighed 8 mg, whilst the heaviest was 180 mg. In the CE chambers at 14°C, there was evidence for two different reproductive/survival strategies. Some flatworms produced cumulatively more egg capsules the longer they survived, whereas others lived longer but produced fewer egg capsules. Flatworms kept without a partner still produced egg capsules up to 35 weeks later. Egg capsules contained a mean of 4.14 (CE chambers) or 4.62 (outdoors) juveniles, with a maximum of 11. Overall, juveniles were 45% of the weight of egg capsules, although larger egg capsules had more juveniles, which comprised a greater proportion of the egg capsule. The conversion of earthworm prey to egg capsule production was estimated at 13%.     

Prey selection by larvae of Prochilodus lineatus (Pisces: Curimatidae): indigenous zooplankton versus veligers of the introduced bivalve Limnoperna fortunei (Bivalvia: Mitilidae)

We studied experimentally the feeding selectivity of larvae of Prochilodus lineatus (Pisces), with particular emphasis on the role of veligers of the exotic bivalve Limnoperna fortunei. Three concentrations of veligers were offered to three developmental stages of P. lineatus. Veliger concentrations were: (1) higher than in the field (“enriched”, 0.09 ind. ml⁻¹), (2) unmodified from field conditions (“normal”, 0.06 ind. ml⁻¹), and (3) lower than in the field (“low”, 0.02 ind. ml⁻¹). Fish developmental stages were protolarvae (approx. 10 days old), mesolarvae (17 days), and metalarvae (25 days). Proportions (in terms of numbers and biomass) and selectivity values were calculated for each prey item evaluated: veligers, small cladocerans + nauplii, medium-sized cladocerans, copepodits, and large cladocerans + copepods. Protolarvae and mesolarvae consumed veligers almost exclusively (88–90%, both in numbers and in biomass) when offered prey enriched in veligers, whereas for metalarvae veligers represented only 16.0% of the food consumed. At lower veliger concentrations, only protolarvae preferred Limnoperna veligers, whereas older fishes switched gradually to crustacean plankton. We conclude that veligers are preferred by the early fish developmental stages, and we speculate that this may be because their slower swimming makes them easier to capture than planktonic crustaceans. However, as fish larvae grow larger, veligers become too small a prey for their energetic needs, and they switch to larger items like cladocerans and copepods. We anticipate that this new and abundant food resource has an important impact on the survival and growth of P. lineatus.     

Embryonic development in the Patagonian red snail Odontocymbiola magellanica (Neogastropoda: Volutidae): Morphology and biochemistry

Embryo morphology, feeding mechanism and changes in composition of the egg capsule content during development (intracapsular fluids and embryos) were studied in Odontocymbiola magellanica from newly spawned egg capsules to the pre-hatching juvenile stage. Changes in embryo morphology and behavior are presented, based on observations and micrographs of living specimens and scanning electron microscopy. The arrangement of velar cilia and athrocytes and shell gland location and development differed markedly from other studied caenogastropods. Embryo ingestion of intracapsular fluid was promoted by velar ciliary currents at least from the early veliger stage, while feeding by grazing on the inner membranous layer of the egg capsule was rarely observed until juveniles were about to hatch. The main growth of embryos occurred during the veliger stages. A significant nutritional investment in egg capsules, as compared with other South American volutids was observed. Nutrition from proteins seemed to predominate at the expense of a high molecular weight fraction (>220 kDa). Calcium concentration in the intracapsular fluid remained constant during development, but notably, the total intracapsular content (i.e., the amount contained in both fluid and embryos) increased 3-fold, which may be explained by extraction from the egg capsule magnesium-rich calcite cover, or alternatively, by uptake of calcium from the surrounding sea water. Ammonia, a major end-product of nitrogen metabolism in marine invertebrates, was present in both embryos and intracapsular fluid, from which it may easily diffuse to the surrounding sea water through the egg capsule wall. Our results on embryo morphology, development and biochemical changes provide useful comparative data for evolutionary and developmental studies in the Volutidae as well as in other caenogastropods.     

Effects of temperature, salinity, and air exposure on development of the estuarine pulmonate gastropod Amphibola crenata

The primitive pulmonate snail Amphibola crenata embeds embryos within a smooth mud collar on exposed estuarine mudflats in New Zealand. Development through hatching of free-swimming veliger larvae was monitored at 15 salinity and temperature combinations covering the range of 2-30 ppt salinity and 15-25 °C. The effect of exposure to air on developmental rate was also assessed. There were approximately 18,000 embryos in each egg collar. The total number of veligers released from standard-sized egg collar fragments varied with both temperature and salinity: embryonic survival was generally higher at 15 and 20 °C than at 25 °C; moreover, survival was generally highest at intermediate salinities, and greatly reduced at 2 ppt salinity regardless of temperature. Even at 2 ppt salinity, however, about one-third of embryos were able to develop successfully to hatching. Embryonic tolerance to low salinity was apparently a property of the embryos themselves, or of the surrounding egg capsules; there was no indication that the egg collars protected embryos from exposure to environmental stress. Mean hatching times ranged between 7 and 22 days, with reduced developmental rates both at lower temperature and lower salinity. At each salinity tested, developmental rate to hatching was similar at 20 and 25 °C. At 15 °C, time to hatching was approximately double that recorded at the two higher exposure temperatures. Exposing the egg collars to air for 6-9 h each day at 20 °C (20 ppt salinity) accelerated hatching by about 24 h, suggesting that developmental rate in this species is limited by the rates at which oxygen or wastes can diffuse into and from intact collars, respectively. Similarly, veligers from egg capsules that were artificially separated from egg collars at 20 °C developed faster than those within intact egg collars. The remarkable ability of embryos of A. crenata to hatch over such a wide range of temperatures and salinities, and to tolerate a considerable degree of exposure to air, explains the successful colonization of this species far up into New Zealand estuaries.