Laboratory culture of the larvae of Conus textile Linné (Gastropoda: Toxoglossa)

The larvae of the Indo-Pacific gastropod Conns textile Linné were reared in the laboratory from hatching through metamorphosis. Larvae fed a mixed phytoplankton culture of Isochrysis galbana and Phaeodactylum tricornutum grew at a rate of 0.06 mm/day and began metamorphosing 16 days after hatching. Unfed control cultures yielded no metamorphically competent larvae. Laboratory-reared larvae metamorphosed spontaneously on the walls of the fïberglass rearing tanks when their average shell length was 1.5 mm. Measurements made on field-collected Conns textile juveniles indicate that the larvae metamorphose at the same size in the laboratory as they do in nature.Rates of larval shell length increase and dry weight increase paralleled each other until metamorphosis. At this point, shell growth slowed while dry weight increased suddenly. It is suggested that this weight increase reflects calcification and strengthening of the fragile larval shell upon entering the benthic environment.     

Functional morphogenesis from embryos to adults: Late development shapes trophic niche in coral reef damselfishes

The damselfishes are one of the dominant coral reef fish lineages. Their ecological diversification has involved repeated transitions between pelagic feeding using fast bites and benthic feeding using forceful bites. A highly‐integrative approach that combined gene expression assays, shape analyses, and high‐speed video analyses was used to examine the development of trophic morphology in embryonic, larval, juvenile, and adult damselfishes. The anatomical characters that distinguish pelagic‐feeding and benthic‐feeding species do not appear until after larval development. Neither patterns of embryonic jaw morphogenesis, larval skull shapes nor larval bite mechanics significantly distinguished damselfishes from different adult trophic guilds. Analyses of skull shape and feeding performance identified two important transitions in the trophic development of a single species (the orange clownfish; Amphiprion percula): (a) a pronounced transformation in feeding mechanics during metamorphosis; and (b) more protracted cranial remodeling over the course of juvenile development. The results of this study indicate that changes in postlarval morphogenesis have played an important role in damselfish evolution. This is likely to be true for other fish lineages, particularly if they consist of marine species, the majority of which have planktonic larvae with different functional requirements for feeding in comparison to their adult forms.     

The influence of temperature on growth rate and length of larval life of the gastropod, Crepidula plana Say

The relationship between rate of larval development and the potential to prolong larval life was examined for larvae of the marine prosobranch gastropod Crepidula plana Say. Larvae were maintained in clean glass dishes at constant temperatures ranging from 12–29°C and fed either Isochrysis galbana Parke (ISO) or a Tahitian strain of Isochrysis species (T-ISO). Under all conditions, larvae grew at constant rates, as determined by measurements of shell length and tissue biomass. Most larvae eventually underwent spontaneous metamorphosis. Regardless of temperature, faster growth was associated with a shorter planktonic stage prior to spontaneous metamorphosis. Within an experiment, higher temperatures generally accelerated growth rates and reduced the number of days from hatching to spontaneous metamorphosis. However, growth rates were independent of temperature for larvae fed ISO at 25 and 29°C and for larvae fed T-ISO at 20 and 25°C. Where growth rates were unaffected by temperature, time to spontaneous metamorphosis was similarly unaffected. Maximum durations of larval life at a given temperature were shorter for larvae of Crepidula plana than for those of the congener C. fornicata (L.), although both species grew at comparable rates. Interpretations of the ecological significance of these interspecific differences in delay capabilities will require additional data on adult distributions and larval dispersal patterns in the field.     

The initiation of metamorphosis as an ancient polyphenic trait and its role in metazoan life-cycle evolution

Comparative genomics of representative basal metazoans leaves little doubt that the most recent common ancestor to all modern metazoans was morphogenetically complex. Here, we support this interpretation by demonstrating that the demosponge Amphimedon queenslandica has a biphasic pelagobenthic life cycle resembling that present in a wide range of bilaterians and anthozoan cnidarians. The A. queenslandica life cycle includes a compulsory planktonic larval phase that can end only once the larva develops competence to respond to benthic signals that induce settlement and metamorphosis. The temporal onset of competence varies between individuals as revealed by idiosyncratic responses to inductive cues. Thus, the biphasic life cycle with a dispersing larval phase of variable length appears to be a metazoan synapomorphy and may be viewed as an ancestral polyphenic trait. Larvae of a particular age that are subjected to an inductive cue either maintain the larval form or metamorphose into the post-larval/juvenile form. Variance in the development of competence dictates that only a subset of a larval cohort will settle and undergo metamorphosis at a given time, which in turn leads to variation in dispersal distance and in location of settlement. Population divergence and allopatric speciation are likely outcomes of this conserved developmental polyphenic trait.     

Differences in heat shock protein 70 expression during larval and early spat development in the Eastern oyster, Crassostrea virginica (Gmelin, 1791)

For a variety of species, changes in the expression of heat shock proteins (HSP) have been linked to key developmental changes, i.e., gametogenesis, embryogenesis, and metamorphosis. Many marine invertebrates are known to have a biphasic life cycle where pelagic larvae go through settlement and metamorphosis as they transition to the benthic life stage. A series of experiments were run to examine the expression of heat shock protein 70 (HSP 70) during larval and early spat (initial benthic phase) development in the Eastern oyster, Crassostrea virginica. In addition, the impact of thermal stress on HSP 70 expression during these early stages was studied. C. virginica larvae and spat expressed three HSP 70 isoforms, two constitutive, HSC 77 and HSC 72, and one inducible, HSP 69. We found differences in the expression of both the constitutive and inducible forms of HSP 70 among larval and early juvenile stages and in response to thermal stress. Low expression of HSP 69 during early larval and spat development may be associated with the susceptibility of these stages to environmental stress. Although developmental regulation of HSP 70 expression has been widely recognized, changes in its expression during settlement and metamorphosis of marine invertebrates are still unknown. The results of the current study demonstrated a reduction of HSP 70 expression during settlement and metamorphosis in the Eastern oyster, C. virginica.     

Changes in biomass and chemical composition during lecithotrophic larval development of the southern king crab, Lithodes santolla (Molina)

Changes in biomass and elemental composition (dry mass, W; carbon, C; nitrogen, N; hydrogen, H) were studied in the laboratory during complete larval and early juvenile development of the southern king crab, Lithodes santolla (Molina), formerly known as Lithodes antarcticus (Jacquinot). At 6±0.5 °C, total larval development from hatching to metamorphosis lasted about 10 weeks, comprising three demersal zoeal stages and a benthic megalopa, with mean stage durations of 4, 7, 11 and 47 days, respectively. No differences in development duration or mortality were observed in larvae either fed with Artemia sp. nauplii or unfed, indicating that all larval stages of L. santolla are lecithotrophic. First feeding and growth were consistently observed immediately after metamorphosis to the first juvenile crab stage. Regardless of the presence or absence of food, W, C, N and H decreased throughout larval development. Also the C:N mass ratio decreased significantly, from 7.7 at hatching to 4.1 at metamorphosis, indicating that a large initial lipid store remaining from the egg yolk was gradually utilized as an internal energy source, while proteins played a minor role as a metabolic substrate. In total, 56-58% of the initial quantities of C and H present at hatching, and 20% of N were lost during nonfeeding larval development to metamorphosis. Nine to ten percent of the initially present C, N and H were lost with larval exuviae, half of these losses occurring in the three zoeal stages combined and another half in the megalopa stage alone. Metabolic biomass degradation accounted for losses of about 47-50% in C and H but for only 10% in N. Hence, most of the losses in C and H reflected metabolic energy consumption (primarily lipid degradation), while about half of the losses in N and two thirds of those in W were due to larval exuviation. Complete independence from food throughout larval development is based on an enhanced maternal energy investment per offspring and on energy-saving mechanisms such as low larval locomotory activity and low exuvial losses. These traits are interpreted as bioenergetic adaptations to food-limited conditions in Subantarctic regions, where a pronounced seasonality of day length limits the period of primary production, while low temperatures enforce a long duration of pelagic development.     

Linking life history traits in successive phases of a complex life cycle: effects of larval biomass on early juvenile development in an estuarine crab, Chasmagnathus granulata

In marine benthic invertebrates with complex life cycles, recruitment success, juvenile survival, and growth may be affected by variation in both maternal factors and environmental conditions prevailing during preceding embryonic or larval development. In an estuarine crab, Chasmagnathus granulata, previous investigations have shown that initial larval biomass is positively correlated with the biomass of recently extruded eggs, and it depends also on the salinity experienced during embryogenesis. Biomass at hatching has consequences for the subsequent larval development which, in this species, comprises two alternative developmental pathways with four or five zoeal instars (short or long pathway) and a megalopa. Larvae hatching with a lower than average biomass tend to develop through the long pathway and metamorphose to megalopae with higher biomass. In the present study, we show experimentally that the long pathway produces also significantly larger juveniles (crab size measured as carapace width, biomass as dry mass, carbon and nitrogen contents). Compared with juveniles originating from the short pathway, those from the long pathway showed in successive instars longer moulting cycles and larger carapace width, but lower size increments at ecdysis. In consequence, differences in size or biomass of long pathway vs short pathway crabs tended to disappear in later instars (after stage V). Furthermore, we tested in juveniles the tolerance of starvation at three salinities (5‰, 15‰, 32‰). Tolerance of starvation was significantly higher in juveniles originating from the long pathway, indicating higher energy reserves. While salinity played only a minor role for survival, it exerted significant effects on the time of moulting to the second juvenile instar, regardless of the preceding developmental pathway. The biomass of first juveniles obtained from the short pathway showed a significant positive correlation with the biomass of the freshly hatched zoea I, but not in those from the long pathway. In conclusion, the fitness of juvenile C. granulata is linked with previous developmental processes and environmental conditions during the embryonic and larval phase. Hence, a better understanding and prediction of the recruitment success of marine benthic invertebrates with a complex life cycle may require more comprehensive life‐history investigations.     

Reproduction and development of the limpet Limalepeta lima (Dall, 1918) (Gastropoda: Lepetidae) from Peter the Great Bay, Sea of Japan

Reproduction and larval development of the limpet Limalepeta lima (Dall, 1918) were studied under laboratory conditions for the first time. L. lima breeds in early July; it exhibits external fertilization and the pelagic lecithotrophic type of development. Larvae, juvenile, and adult specimens have different shell sculptures. Development from fertilization to settling and metamorphosis continues for 4–5 days at a water temperature of 16°C.     

Effects of egg size reduction and larval feeding on juvenile quality for a species with facultative-feeding development

In free-spawning marine invertebrates, larval development typically proceeds by one of two modes: planktotrophy (obligate larval feeding) from small eggs or lecithotrophy (obligate non-feeding) from relatively large eggs. In a rare third developmental mode, facultative planktotrophy, larvae can feed, but do not require particulate food to complete metamorphosis. Facultative planktotrophy is thought to be an intermediate condition that results from an evolutionary increase in energy content in the small eggs of a planktotrophic ancestor. We tested whether an experimental reduction in egg size is sufficient to restore obligate planktotrophy from facultative planktotrophy and whether the two sources of larval nutrition (feeding and energy in the egg) differentially influence larval survival and juvenile quality. We predicted, based on its large egg size, that a reduction in egg size in the echinoid echinoderm Clypeaster rosaceus would affect juvenile size but not time to metamorphosis. We reduced the effective size of whole (W) zygotes by separating blastomeres at the two- or four-cell stages to create half- (H) or quarter-size (Q) “zygotes” and reared larvae to metamorphosis, both with and without particulate food. Larvae metamorphosed at approximately the same time regardless of food or egg size treatment. In contrast, juveniles that developed from W zygotes were significantly larger, had higher organic content and had longer and more numerous spines than juveniles from H or Q zygotes. Larvae from W, H and Q zygotes were able to reach metamorphosis without feeding, suggesting that the evolution of facultative planktotrophy in C. rosaceus was accompanied by more than a simple increase in egg size. In addition, our results suggest that resources lost by halving egg size have a larger effect on larval survival and juvenile quality than those lost by withholding particulate food.     

Carry‐over Effects of Size at Metamorphosis in Red‐eyed Treefrogs: Higher Survival but Slower Growth of Larger Metamorphs

Most animals have complex life histories, composed of a series of ecologically distinct stages, and the transitions between stages are often plastic. Anurans are models for research on complex life cycles. Many species exhibit plastic timing of and size at metamorphosis, due to both environmental constraints on larval growth and development and adaptive plastic responses to environmental variation. Models predicting optimal timing of metamorphosis balance cost/benefit ratios across stages, assuming that size affects growth and mortality rates in each stage. Much research has documented such effects in the larval period, but we lack an equal understanding of juvenile growth and mortality. Here, we examine how variation in size at metamorphosis in the Neotropical red‐eyed treefrog, Agalychnis callidryas, affects post‐metamorphic growth, foraging, and behavior in the lab as well as growth and survival in the field. Surprisingly, many individuals lost mass for weeks after metamorphosis. In the lab, larger metamorphs lost more mass following metamorphosis, ate similar amounts, had lower food conversion efficiencies, and grew more slowly after mass loss ceased than did smaller ones. In field cages larger metamorphs were more likely to survive than smaller ones; just one froglet died in the lab. Our data suggest that size‐specific differences in physiology and behavior influence these trends. Comparing across species and studies, large size at metamorphosis generally confers higher survival; size effects on growth rates vary substantially among species, in both magnitude and direction, but may be stronger in the tropics.     

Variations in larval growth and metabolism of an estuarine shrimp Palaemonetes pugio during toxicosis by an insect growth regulator

1. Exposure of the estuarine shrimp, Palaemonetes pugio, to a juvenile hormone analogue (⩾8 μg methoprene 1⁻¹) throughout larval development inhibited successful completion of metamorphosis.2. Methoprene exposure retarded growth in early larval stages and postlarvae, but enhanced growth in premetamorphic larvae.3. Respiration rates of early larvae were elevated by methoprene exposure, but not so older larvae or post larvae.4. Lower net growth efficiency (K₂ values) in methoprene-exposed early larvae suggests that increased metabolic demands reduced assimilated energy available for growth.5. Modifications in O:N ratios of premetamorphic larvae and postlarvae suggest that methoprene altered substrate utilization patterns during metamorphosis.     

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.     

Dynamic expression of ancient and novel molluscan shell genes during ecological transitions

Background  

The Mollusca constitute one of the most morphologically and ecologically diverse metazoan phyla, occupying a wide range of marine, terrestrial and freshwater habitats. The evolutionary success of the molluscs can in part be attributed to the evolvability of the external shell. Typically, the shell first forms during embryonic and larval development, changing dramatically in shape, colour and mineralogical composition as development and maturation proceeds. Major developmental transitions in shell morphology often correlate with ecological transitions (e.g. from a planktonic to benthic existence at metamorphosis). While the genes involved in molluscan biomineralisation are beginning to be identified, there is little understanding of how these are developmentally regulated, or if the same genes are operational at different stages of the mollusc's life.     

Linking larval history to juvenile demography in the bicolor damselfish Stegastes partitus (Perciformes: Pomacentridae)

Otolith-based reconstructions of daily larval growth increments were used to examine the effect of variation in larval growth on size and age at settlement and post-settlement growth, survival and habitat preferences of juvenile bicolor damselfish (Stegastes partitus Poey). During August 1992 and 1994, newly settled S. partitus were collected from Montastraea coral heads and Porites rubble piles in Tague Bay, St. Croix, U.S. Virgin Islands (17 degrees 45'N, 64 degres 42' W). Daily lapillar otolith increments from each fish were counted and measured with Optimas image analysis software. S. partitus pelagic larval duration was 23.7 d in 1992 (n = 70) and 24.6 d in 1994 (n = 38) and larval age at settlement averaged 13.0 mm total length both years. Analysis of daily otolith increments demonstrated that variation in larval growth rates and size and age at settlement had no detectable effect on post-settlement survivorship but that larger larvae showed a preference for Montastraea coral at settlement. Late larval and early juvenile growth rates showed a significant positive relationship indicating that growth patterns established during the planktonic stage can span metamorphosis and continue into the benthic juvenile phase. Larval growth rates during the first two weeks post-hatching also had a strong effect on age to developmental competence (ability to undergo metamorphosis) in both 1992 and 1994 with the fastest growing larvae being 8 d younger and 0.8 mm smaller at settlement than the slowest growing larvae. These differential growth rates in early stage larvae established trajectories toward larval developmental competence and may prove important in biogeographical studies of larval dispersal.     

RELATIONSHIPS BETWEEN SHELL SHAPE, WATER RESERVES, SURVIVAL AND GROWTH OF HIGHSHORE LITTORINIDS UNDER EXPERIMENTAL CONDITIONS IN NEW SOUTH WALES, AUSTRALIA

The shell morphologies of the highshore littorinids, Littorinaunifasciata Gray and Nodilittorina pyramidalis (Quoy & Gaimard)have previously been shown to vary at a variety of spatial scales,including among replicate sites at the same height, from heightto height and from shore to shore. In this study, the relationshipsbetween morphology of the shell, the reserves of water heldwithin the shell, the size of the foot and survival on differentshores and rates of growth in different habitats were examinedfor L. unifasciata and, to a lesser extent, N. pyramidalis.Reserves of water were not consistently related to size or shapeof the shell, but did increase as relative weight of shell increased.This may be due to the relatively smaller body providing moreinternal volume for extra-corporeal water. Water reserves andthe amount of free water held in the shell were also not relatedto loss of water or survival during extended periods of emersion.Although the shape of the shell on sheltered and exposed shoreswas correlated with size of the foot, with the snails on anexposed shore having larger apertures and feet than those ona sheltered shore, transplant experiments did not show differentialmortality between morphs from the different shores. All translocatedand transplanted snails disappeared from the exposed shore ata greater rate than from the sheltered shore, but this was probablydue to the snails dispersing out of the experimental areas ratherthan due to mortality. Therefore, many of the large-scale modelsthat have previously been used to describe patterns of shellshape in intertidal gastropods do not appear to be importantin these highshore littorinids. Finally, field experiments ongrowth of juvenile L. unifasciata indicated that rate of growth,largely governed by opportunity to feed rather than type andquantity of food, is the most likely explanation for the small-and large-scale patterns of shell shape that have been previouslydescribed in this species. (Received 22 October 1996; accepted 19 February 1997)     

Myogenesis in Aplysia californica (Cooper, 1863) (Mollusca,Gastropoda, Opisthobranchia) with special focus on muscular remodeling during metamorphosis

To date only few comparative approaches tried to reconstruct the ontogeny of the musculature in invertebrates. This may be due to the difficulties involved in reconstructing three dimensionally arranged muscle systems by means of classical histological techniques combined with light or transmission electron microscopy. Within the scope of the present study we investigated the myogenesis of premetamorphic, metamorphic, and juvenile developmental stages of the anaspidean opisthobranch Aplysia californica using fluorescence F‐actin‐labeling in conjunction with modern confocal laser scanning microscopy. We categorized muscles with respect to their differentiation and degeneration and found three true larval muscles that differentiate during the embryonic and veliger phase and degenerate during or slightly after metamorphosis. These are the larval retractor, the accessory larval retractor, and the metapodial retractor muscle. While the pedal retractor muscle, some transversal mantle fibers and major portions of the cephalopedal musculature are continued and elaborated during juvenile and adult life, the buccal musculature and the anterior retractor muscle constitute juvenile/adult muscles which differentiate during or after metamorphosis. The metapodial retractor muscle has never been reported for any other gastropod taxon. Our findings indicate that the late veliger larva of A. californica shares some common traits with veligers of other gastropods, such as a larval retractor muscle. However, the postmetamorphic stages exhibit only few congruencies with other gastropod taxa investigated to date, which is probably due to common larval but different adult life styles within gastropods. Accordingly, this study provides further evidence for morphological plasticity in gastropod myogenesis and stresses the importance of ontogenetic approaches to understand adult conditions and life history patterns. J. Morphol., 2008. © 2007 Wiley‐Liss, Inc.     

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.