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.     

Hatching plasticity in the tropical gastropod Nerita scabricosta

Hatching plasticity has been documented in diverse terrestrial and freshwater taxa, but in few marine invertebrates. Anecdotal observations over the last 80 years have suggested that intertidal neritid snails may produce encapsulated embryos able to significantly delay hatching. The cause for delays and the cues that trigger hatching are unknown, but temperature, salinity, and wave action have been suggested to play a role. We followed individual egg capsules of Nerita scabricosta in 16 tide pools to document the variation in natural time to hatching and to determine if large delays in hatching occur in the field. Hatching occurred after about 30 d and varied significantly among tide pools in the field. Average time to hatching in each pool was not correlated with presence of potential predators, temperature, salinity, or pool size. We also compared hatching time between egg capsules in the field to those kept in the laboratory at a constant temperature in motionless water, and to those kept in the laboratory with sudden daily water motion and temperature changes. There was no significant difference in the hatching rate between the two laboratory treatments, but capsules took, on average, twice as long to hatch in the laboratory as in the field. Observations of developing embryos showed that embryos in the field develop slowly and continuously until hatching, but embryos in the laboratory reach the hatching stage during the first month of development and remain in stasis after that. Instances of hatching plasticity in benthic marine invertebrates, like the one in N. scabricosta, could greatly enhance our ability to investigate the costs and benefits of benthic versus planktonic development, a long‐standing area of interest for invertebrate larval biologists.     

Heterochrony and the evolution of poecilogony: generating larval diversity

Poecilogony is the production of more than one type of young within a single species of marine invertebrate. We chose a poecilogonous polychaete to investigate potential differences in morphogenesis among offspring that are polymorphic in dispersal potentials (planktonic, benthic) and trophic modes (planktotrophy, adelphophagy). Differences in morphogenesis occur and are strongly influenced by maternal type. Females that provide extra-embryonic nutrition (as nurse eggs; type III females) also produce offspring with an accelerated onset of juvenile traits, relative to planktotrophic offspring of females that do not provide extra-embryonic nutrition (type I females). Thus, progeny of some females appear morphologically preadapted for a benthic lifestyle. Surprisingly, differences in phenotype among offspring do not parallel offspring ecotype, as offspring with early onset of juvenile traits (III) are ecologically bimodal. Some Type III offspring eat the nurse eggs (adelphophagy), have accelerated development, and hatch as benthic juveniles. In contrast, their siblings hatch as small, planktotrophic, dispersive larvae that are morphologically similar to their type III siblings, but ecologically similar to Type I planktotrophic larvae. We propose that poecilogony evolved through sequence heterochrony in morphogenesis with accelerated onset of juvenile traits in type III offspring. In addition, we suggest that heterochrony in life-history events (hatching, metamorphosis) also occurs, thereby generating offspring that are dimorphic in both phenotype and ecotype. Over time, selection acting on different levels of ontogeny (morphogenesis vs. dispersal) may balance this polymorphism and allow poecilogony to persist.     

A REVIEW OF LARVAL DEVELOPMENT IN THE INTERTIDAL LIMPET GENUS SIPHONARIA (GASTROPODA: PULMONATA)

A compilation of distributional and life-history data relatingto mode of larval development is presented for 26 species ofSiphonana, a genus of intertidal pulmonates. Most species depositgelatinous benthic egg masses with two species releasing pelagicegg masses. Fifteen species hatch as planktonic-developing larvae,nine hatch as direct-developing juveniles, and in a furthertwo larvae hatch with both the swimming velar apparatus (associatedwith plank-tonic development) and a crawling foot (associatedwith direct development). Data on mode of larval developmentare interpreted with respect to some adaptive models. Despiteimportant exceptions, there is support for adaptive models basedupon egg capsule size (direct developers hatch from larger eggcapsules) and intertidal distribution (direct developers generallyoccur higher on the shore than planktonic developers). Worldwide,planktonic developers are more widespread than direct-developingspecies, and individual planktonic species have a greater meanlatitudinal range. The evidence for adaptive models relatinglatitudinal distribution to developmental mode is equivocal.There appears to be no clear relationship between body sizeand developmental mode in the genus, although the smallest specieshas direct development and the largest has planktonic development.In most siphonariid subgenera, developmental mode appears tobe constant, but two subgenera contain a mixture of developmentaltypes (Received 1 November 1993; accepted 15 April 1994)     

Size-specific predation on marine invertebrate larvae

Predation on planktonic larval stages is frequently a major source of mortality for the offspring of benthic marine invertebrates. Mortality rate likely varies with larval size and developmental stage, but few experiments have measured how these factors affect predation rates. I used experimental reductions in egg size to test how variation in larval size affects the likelihood of predation during planktonic development. Blastomeres of the sand dollar Dendraster excentricus were separated at the two-cell stage to produce half-sized zygotes. Larvae resulting from this manipulation were tested for their susceptibility to predation relative to whole-sized siblings at four ages. Individuals from each size class were simultaneously presented as prey items to five predators (crab zoeae, crab megalopae, chaetognaths, solitary tunicates, and postlarval fish) in the laboratory. Four predators consumed significantly more half-sized larvae than whole-sized larvae, but one predator type (postlarval fish) consumed more whole-sized larvae. Predators that consumed more half-sized larvae also preferentially consumed younger larvae. In contrast, postlarval fish showed no significant prey preference based on larval age. These results suggest that assumptions of constant mortality rates during development should be modified to account for the effects of larval size and age.     

The effects of nurse eggs and sibling interactions on the larval development of the poecilogonous annelid Boccardia proboscidea (Spionidae)

In poecilogony, different types of larvae are produced within the same species. Previous studies have suggested maternal control of the production of larval types; however, it is not clear which factors or mechanisms generate contrasting developmental patterns among siblings. The spionid polychaete Boccardia proboscidea produces within the same capsule adelphophagic larvae that eat nurse eggs and siblings and complete all or most of their development inside the capsule (Type A larvae), and larvae with little growth until they hatch as planktotrophic larvae (Type B larvae). In this study, we manipulated capsule content to explore the factors determining larval type in B. proboscidea and the role of extra‐embryonic maternal nutrition and sib–sib interaction in the developmental fate of offspring. When early larval stages were grown individually in vitro, with nurse eggs as the only food source, some of them remained small, while others continue developing into larger pre‐competent larvae by feeding on nurse eggs. This suggests that larval types in B. proboscidea are determined very early in development and are not solely the product of sib–sib interaction inside the capsule. However, our data also suggest that hatching size variability within larval types of a clutch depends on nurse egg availability. Type B larvae grew normally to metamorphosis when phytoplankton was available, but suffered high rates of cannibalism by Type A larvae. These results are consistent with the hypothesis that individual larval fates are determined very early in development and that once their fate is determined, hatching size and intracapsular survival are affected by maternal food provisioning and sibling interaction.     

Oxygen, gills, and embryo behavior: mechanisms of adaptive plasticity in hatching.

Many species alter the timing of hatching in response to egg or larval predators, pathogens, or physical risks. This plasticity depends on separation between the onset of hatching competence and physiological limits to embryonic development. I present a framework based on heterokairy to categorize developmental mechanisms and identify traits contributing to and limiting hatching plasticity, then apply it to a case of predator-induced hatching. Red-eyed treefrogs have arboreal eggs, and tadpoles fall into ponds upon hatching. Egg and tadpole predators select for earlier and later hatching, respectively. Embryos hatch up to 30% early in predator attacks, and later if undisturbed. They maintain large external gills throughout the plastic hatching period, delaying gill regression while development otherwise continues. Rapid gill regression occurs upon hatching. Prolonged embryonic development depends on external gills; inducing gill regression causes hatching. External hypoxia retards development, kills eggs, and induces hatching. Nonetheless, embryos develop synchronously and without hatching prematurely across a broad range of perivitelline PO2, from 0.5-12.5 kPa. Embryos exploit spatial variation of PO2 within eggs by positioning gills against patches of air-exposed surface. Respiratory plasticity and oxygen-sensitive behavior appear critical for the hatching plasticity that balances a predation risk trade-off across life stages.     

Observations on development,larval growth and metamorphosis of four species of aplysiidae (gastropoda: Opisthobranchia) in laboratory culture

The development of simple, reliable techniques for the laboratory culture of aplysiid gastropods through their complete life cycle, has enabled us to study the larval biology, metamorphosis, and early juvenile development of these animals. Egg masses, duration of the embryonic phase, veligers, and larval growth and development are described for four species of Hawaiian Aplysiidae, namely, Aplysia dactylomela Rang, Aplysia Juliana Quoy and Gaimard, Dolabella auricularia (Lightfoot) and Stylocheilus longicauda (Quoy and Gaimard). Metamorphosis and early juvenile development of A. Juliana are described in detail with additional comments on these processes in the other three species. Length of the embryonic phase and size of the veliger at hatching are a function of the size of the uncleaved egg. All four species develop planktotrophically and have ≈ 30-day larval phases. In each species the larval phase includes a period of rapid shell growth to a species-specific size followed by a non-growth period during which other morphological developments occur to culminate in metamorphic competence. The larvae of each species metamorphose preferentially on a particular species of benthic algae. The events of metamorphosis require 2 to 4 days for completion and transform the planktonic filter-feeding larva into a benthic, radular-feeding juvenile. Postlarval development includes growth of the shell, parapodia, oral tentacles, rhinophores, anal siphon, and structures of the mantle cavity.     

Oxygen, gills, and embryo behavior: mechanisms of adaptive plasticity in hatching

Many species alter the timing of hatching in response to egg or larval predators, pathogens, or physical risks. This plasticity depends on separation between the onset of hatching competence and physiological limits to embryonic development. I present a framework based on heterokairy to categorize developmental mechanisms and identify traits contributing to and limiting hatching plasticity, then apply it to a case of predator-induced hatching. Red-eyed treefrogs have arboreal eggs, and tadpoles fall into ponds upon hatching. Egg and tadpole predators select for earlier and later hatching, respectively. Embryos hatch up to 30% early in predator attacks, and later if undisturbed. They maintain large external gills throughout the plastic hatching period, delaying gill regression while development otherwise continues. Rapid gill regression occurs upon hatching. Prolonged embryonic development depends on external gills; inducing gill regression causes hatching. External hypoxia retards development, kills eggs, and induces hatching. Nonetheless, embryos develop synchronously and without hatching prematurely across a broad range of perivitelline PO₂, from 0.5–12.5 kPa. Embryos exploit spatial variation of PO₂ within eggs by positioning gills against patches of air-exposed surface. Respiratory plasticity and oxygen-sensitive behavior appear critical for the hatching plasticity that balances a predation risk trade-off across life stages.     

Wasp predation and wasp-induced hatching of red-eyed treefrog eggs

Eggs often suffer high levels of predation and, compared with older animals, embryos have few options available for antipredator defence. None the less, hatchlings can escape from many predators to which eggs are vulnerable. I studied early hatching as an antipredator defence of red-eyed treefrog embryos, Agalychnis callidryas, in response to egg predation by social wasps (Polybia rejecta). Red-eyed treefrogs attach their eggs to vegetation overhanging water, where they are exposed to arboreal and aerial predators. Wasps attacked half the egg clutches and killed almost a quarter of the eggs I monitored at a natural breeding site in Panama. Hatching tadpoles fall into the water, where they face aquatic predators. As predicted from improved survival of older hatchlings with aquatic predators, most undisturbed eggs hatched relatively late. However, many younger embryos directly attacked by wasps hatched immediately. Embryos attacked by wasps hatched as much as a third younger than the peak undisturbed hatching age, and most hatching embryos escaped. Thus hatching is an effective defence against wasp predation, and plasticity in hatching stage allows embryos to balance risks from stage-specific egg and larval predators. Wasp-induced hatching is behaviourally similar to the snake-induced hatching previously described in A. callidryas, but occurs in fewer eggs at a time, congruent with the scale of the risk. Individual embryos hatch in response to wasps, which take single eggs, whereas whole clutches hatch in response to snakes, which consume entire clutches. Embryos of A. callidryas thus respond appropriately to graded variation in mortality risks. Copyright 2000 The Association for the Study of Animal Behaviour.     

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     

Consequences of induced hatching plasticity depend on predator community

Many prey species face trade-offs in the timing of life history switch points like hatching and metamorphosis. Costs associated with transitioning early depend on the biotic and abiotic conditions found in the subsequent life stage. The red-eyed treefrog, Agalychnis callidryas, faces risks from predators in multiple, successive life stages, and can hatch early in response to mortality threats at the egg stage. Here we tested how the consequences of life history plasticity, specifically early hatching in response to terrestrial egg predators, depend on the assemblage of aquatic larval predators. We predicted that diverse predator assemblages would impose lower total predation pressure than the most effective single predator species and might thereby reduce the costs of hatching early. We then conducted a mesocosm experiment where we crossed hatchling phenotype (early vs. normal hatching) with five larval-predator environments (no predators, either waterbugs, dragonflies, or mosquitofish singly, or all three predator species together). The consequences of hatching early varied across predator treatments, and tended to disappear through time in some predation treatments, notably the waterbug and diverse predator assemblages. We demonstrate that the fitness costs of life history plasticity in an early life stage depend critically on the predator community composition in the next stage.     

Glassfrog embryos hatch early after parental desertion

Both parental care and hatching plasticity can improve embryo survival. Research has found that parents can alter hatching time owing to a direct effect of care on embryogenesis or via forms of care that cue the hatching process. Because parental care alters conditions critical for offspring development, hatching plasticity could allow embryos to exploit variation in parental behaviour. However, this interaction of parental care and hatching plasticity remains largely unexplored. We tested the hypothesis that embryos hatch early to cope with paternal abandonment in the glassfrog Hyalinobatrachium fleischmanni (Centrolenidae). We conducted male-removal experiments in a wild population, and examined embryos'' response to conditions with and without fathers. Embryos hatched early when abandoned, but extended development in the egg stage when fathers continued care. Paternal care had no effect on developmental rate. Rather, hatching plasticity was due to embryos actively hatching at different developmental stages, probably in response to deteriorating conditions without fathers. Our experimental results are supported by a significant correlation between the natural timing of abandonment and hatching in an unmanipulated population. This study demonstrates that embryos can respond to conditions resulting from parental abandonment, and provides insights into how variation in care can affect selection on egg-stage adaptations.     

Patterns in the abundance,phenology, and hatching of the resting egg stage of the invasive zooplankter <Emphasis Type="Italic">Bythotrephes longimanus</Emphasis>: implications for establishment

To examine how dormancy contributes to the establishment and persistence of Bythotrephes longimanus, we investigated resting egg production and hatching in relation to the demography of the planktonic stage and environmental conditions in Island Lake Reservoir (USA). During a 3-year study, the largest contribution to the egg bank occurred in autumn and most eggs hatched in spring, but we also detected some resting egg production and hatching in summer. The difference between summer and late autumn densities of eggs in sediments averaged 47% (range 0–98%) for 18 sites throughout the reservoir, which was similar to experimental estimates of in situ hatching fraction of 67% for eggs in the spring and summer following their production. Based on emergence traps, neonates hatch in the field during May and June. We estimated mortality rates of 64% for resting eggs and embryos, and 59% for newly emerged neonates. Although hatching fraction saturated at the same level, eggs incubated offshore hatched later than those nearshore where water temperature was warmer and light was detectable at the sediment surface. Low dissolved oxygen concentration did not significantly reduce hatching fraction but resulted in some eggs that initiated development but failed to hatch. Collectively, our results demonstrate substantial annual turnover in the resting egg bank of B. longimanus and high mortality of resting eggs during recruitment from the egg to the first molt of the planktonic stage. These patterns suggest that propagule pressure in the form of resting eggs requires large numbers for establishment, and that considerable post-establishment resting egg production is necessary for inter-annual persistence.     

Pathways to fitness: carry‐over effects of late hatching and urbanisation on lifetime mating success

Life history theory and most empirical studies assume carry‐over effects of larval ­conditions to shape adult fitness through their impact on metamorphic traits (age and mass at metamorphosis). Yet, very few formal tests of this connection across metamorphosis exist, because this entails longitudinal studies from the egg stage and requires measuring fitness in (semi)natural conditions. In a longitudinal one‐year common‐garden rearing experiment consisting of an outdoor microcosm part for the larval stage and a large outdoor insectary part for the adult stage, we studied the effects of two factors related to time constraints in the larval stage (egg hatching period and urbanisation) on life history traits and lifetime mating success in the males of the damselfly Coenagrion puella. We reared early‐ and late‐hatched larvae from each of three rural and three urban populations from the egg stage throughout their adult life. Key findings were that both the hatching period and urbanisation shaped adult fitness, yet through different pathways. As expected, the more time‐constrained late‐hatched individuals accelerated their larval life history and this was associated with a lower lifetime mating success. A path analysis revealed this carry‐over effect was mediated by the changes in the two metamorphic traits (reduced age and lower mass at emergence). Notably, urban males had a 50% lower lifetime mating success, which was not mediated by age and mass at emergence, and possibly driven by their shorter lifespan. Our results point to long‐term carry‐over effects of the usually ignored natural variation in egg hatching dates, and further contribute to the limited evidence showing fitness costs of adjusting to an urban lifestyle.     

Inflated protoconchs and internally dissolved, coiled protoconchs of nudibranch larvae: different developmental trajectories achieve the same morphological result

Abstract. Light and scanning electron microscopy were used to examine protoconch form in eight species of planktotrophic heterobranch larvae, including four nudibranch species with a coiled (type 1) protoconch, two nudibranch species with an inflated (type 2) protoconch, and two cephalaspid species with a coiled protoconch. The coiled protoconchs of the cephalaspids and nudibranchs have a similar form at hatching, and shell growth up to metamorphic competence is hyperstrophic. Shell added to coiled protoconchs during the larval stage overgrows all but the left wall of the initial protoconch that exists at hatching. The entire protoconch of cephalaspids, including overgrown areas, is retained through metamorphosis. However, during later larval development in nudibranchs with a coiled protoconch, overgrown shell is completely removed by dissolution. As a result, regardless of whether nudibranch larvae hatch with an inflated or coiled protoconch type, the protoconch is a large, hollow cup at metamorphic competence. The protoconch of nudibranchs is shed at metamorphosis and absence of a post-metamorphic shell is correlated with absence of visceral coiling in this gastropod group. Internal dissolution of the coiled protoconch in nudibranchs allows the left digestive gland to uncoil prior to metamorphic shell loss. Retention of overgrown protoconch whorls in cephalaspids allows the attachment plaque of the pedal muscle to migrate onto the parietal lip of the post-metamorphic shell. Release from this constraint in nudibranchs, in which the larval pedal muscles and the entire protoconch are lost at metamorphosis, may have permitted internal protoconch dissolution and precocious uncoiling of the visceral mass, as well as evolutionary emergence of the inflated larval shell type.     

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, ?? , ??–??.     

Environmental context shapes immediate and cumulative costs of risk-induced early hatching

In animals with complex life cycles, fitness trade-offs across life stages determine the optimal time for transitions between stages. If these trade-offs vary predictably, adaptive plasticity in the timing of life history transitions may evolve. For instance, embryos of many species are capable of accelerating hatching to escape from egg predation and other hazards, but for plasticity in hatching timing to be selectively maintained, early hatching must also entail costs, probably in subsequent life stages. However the post-hatching environment, which influences this cost, is variable in nature. We assessed how two elements of the post-hatching environment, predator species and age structure created by hatching age plasticity, affect costs of hatching early in red-eyed treefrogs, Agalychnis callidryas. Red-eyed treefrog embryos were induced to hatch at the onset of hatching competence or near the peak of spontaneous hatching and exposed to one of three insect predators in single or mixed hatching-age treatments. Age structure created by hatching-age plasticity did not affect tadpole survivorship or growth; however, the consequences of hatching timing depended on predator species and foraging mode. Tadpoles that were induced to hatch early experienced initially higher mortality rates only with the more actively foraging predator. Nonetheless, mortality costs of accelerated hatching were apparent with all predators once we factored in the longer duration of exposure that early hatchlings experience in nature. This study suggests that extended exposure of young larvae to predators may be a general cost of early hatching, explaining why spontaneous hatching occurs later in life across variable environmental contexts.     

Reproduction and development in a vermetid gastropod, Vermetus triquetrus

Abstract. We report on a study of reproduction and development in the Mediterranean vermetid gastropod Vermetus triquetrus from the SE coast of Spain. It is a gonochoristic species. The egg capsules are attached to the inside of the shell, and females brood up to 22 capsules simultaneously (more often 4–10). The capsules hold 10–61 eggs or embryos; the uncleaved eggs are yolk-rich, with a mean diameter of 377.3 μm. A distinct polar lobe occurs during the first cleavage, and blastomere D has discernible qualities after the 4-cell stage. The formation of the mesentoblast 4d occurs at the transition from the 24-cell stage to the 25-cell stage. Gastrulation begins after the 36-cell stage. Internal yolk is the major source of nutrition for the encapsulated embryos, but some nurse eggs (∼ 12%) and some sibling larvae are also ingested by the developing embryos. Hatching occurs during the swimming/crawling pediveliger stage, and metamorphosis is completed outside the capsules soon after hatching. Hence, larval development in Vermetus triquetrus is lecithotrophic intracapsular, with a short free-swimming/crawling phase.     

Risks for larvae mediated by plasticity in hatching

Risks associated with benthic and planktonic development can be mediated by plasticity in hatching. The ability to delay hatching while awaiting favorable planktonic conditions, combined with the ability to accelerate hatching when encapsulated offspring are at risk, should be advantageous. We tested this predicted association of hatching plasticities with a barnacle. In the winter, broods of barnacles (Balanus glandula) reached hatching‐capable stages at widely varying times, but these broods hatched in the spring within about 2 weeks, consistent with a synchronizing environmental stimulus for hatching. In contrast, the same adults held subsequent broods (during later spring and summer) briefly. Either an environmental stimulus for hatching was not needed later in the season, or it was more frequently present. Dissections of brood lamellae that scattered smaller clumps of the encapsulated nauplii induced hatching. Crabs eating brooding adults had a similar effect: crabs broke the barnacles' tests, and many nauplii hatched. In contrast, when whelks ate barnacles, they left the barnacles' wall plates and opercula in place, and few nauplii were released. In some cases, numerous hatched nauplii were trapped within the test of the killed mother. At a field site with abundant whelks, many dead barnacles had opercular plates in place. Plasticity in hatching of broods adjusted risks for planktonic larvae against risks of death of the parent before release of embryos, but escape or death of brooded offspring depended on the kind of damage to the brooding mother and thus on the kind of predator. Although both predators killed brooding parents, subtle snails imposed a greater risk than crushing crabs.