Adjustment of the components of energy balance in the gastropod Crepidula fornicata in response to thermal acclimation

Synchronous measurements were made of the routine rate of oxygen consumption and the clearance rate of Phaeodactylum tricornutum at different exposure temperatures by specimens of the suspension-feeding gastropod Crepidula fornicata which had been acclimated to temperatures between 10° and 25°C. The results show that the cost of activity (l O₂ consumed h^-1/ml seawater cleared h^-1) increases dramatically in individuals exposed to short-term increases of temperature up to 30°C, especially in limpets acclimated to 10°C. The process of thermal acclimation, however, results in two compensatory adjustments in energy expenditure and uptake which profoundly affect the energetics of water transport. Firstly, the routine oxygen consumption shows lateral translation of the rate-temperature curve which results in the maintenance of a relatively uniform energy expenditure despite an increase in acclimation temperature from 10° to 25°C. Secondly, because of the form of the rate-temperature curve for filtration by C. fornicata, lateral translation in response to warm acclimation results in an increase in the maximal clearance rate. Lateral translation of the rate-temperature curves for feeding rates and for oxygen consumption in response to thermal acclimation may thus be linked to maintain a balance between energy gain and expenditure. In this way, the greatly increased cost of activity which would occur with increase of temperature in the absence of acclimation is evaded. The minimal maintenance energy requirement, and hence the greatest scope for growth and reproduction, is then adjusted to coincide with temperatures prevailing in the environment.     

Behavioral defenses of Crepidula fornicata against attack by Urosalpinx cinerea

Two behavioral defenses of the slipper shell Crepidula fornicata (L.) against attack by the oyster drill Urosalpinx cinerea (Say) are described: (1) Jabbing: when an oyster drill approaches, the slipper shell lifts the edge of its shell, extends the head and, with the radula, pricks or rasps the foot of the predator, which instantly retracts into its shell; sometimes, after repeated approaches, the oyster drill moves away. (2) Pivoting: when an oyster drill mounts C. fornicata, the latter slowly and repeatedly rotates its shell in a horizontal plane at a constant rate and through a constant arc. If this action brings the predator's shell to bear against an obstacle, motion ceases and C. fornicata maintains the pressure until the oyster drill is dislodged. These aggressive tactics are adaptive defensive measures for a nearly sessile prey otherwise highly vulnerable to oysterdrill attack.     

The invasive gastropod Crepidula fornicata: reproduction and recruitment in the intertidal at its northernmost range in Wales, UK, and implications for its secondary spread

The establishment and spread of a non-native species in an introduced range depends to a large extent on the performance of the species under the prevailing environmental conditions. The spawning, larval and spatfall periods of the invasive gastropod Crepidula fornicata were monitored in the intertidal zone at its northernmost range in Wales, UK, between February 2010 and January 2011. The duration of the reproductive season was similar to that recorded from more southerly European populations. Spawning and larval release occurred throughout most of the year even at low seawater temperatures of <7 °C, but benthic recruitment was observed over a much shorter period at seawater temperatures >16 °C. Recruitment was low and likely controlled by post-settlement mortality. These observations suggest that C. fornicata’s northwards spread in Welsh waters will not be limited by seawater temperature negatively affecting reproduction, but by processes acting after larval release. These data show the importance of incorporating settlement and post-settlement processes into studies on recruitment success when aiming to predict the potential spread of a potentially harmful invader such as C. fornicata.     

Genetic structure in native and non-native populations of the direct-developing gastropod Crepidula convexa

In many marine invertebrate species, larval development plays an important role in population connectivity and gene flow: species with direct benthic development generally show more genetic structure than those with planktonic development. We used nuclear markers (microsatellites) to determine population genetic structure of the direct-developing snail Crepidula convexa (Gastropoda: Calyptraeidae) in seven populations with 15–85 individuals each within its native range of the northwest Atlantic and compared it to Crepidula fornicata, a congener with planktonic development. Our results are consistent with general expectations and previous work in these species with other markers: C. convexa had greater population structure and even at a regional scale shows significant isolation-by-distance, in contrast to C. fornicata. We also genotyped a single population of C. convexa introduced to the northeastern Pacific to investigate the prediction of reduced genetic diversity following introduction (founder effect). We did not find a reduction in genetic diversity, suggesting that this non-native population may be characterized by multiple introductions. This pattern is consistent with many other introduced populations of marine invertebrates, including C. fornicata.     

Reproduction of the invasive slipper limpet, Crepidula fornicata, in the Bay of Brest, France

The reproduction of Crepidula fornicata was studied in the Bay of Brest in order to characterise the first step of the reproductive cycle of this invasive species. The survey was carried out from 2000 to 2003 and different parameters were measured, namely, the percentage of the different sexual stages, the straight length of the shell and the percentage of brooding females using a survey of the embryonic development and the fecundity. The juvenile frequency increases generally from mid-June or mid-August, depending on the year. In 2001 and 2003, a first peak was observed as early as May, but it was followed by a rapid disappearance of the individuals. The sex-ratio female/male increased from 0.22 to 0.46 between 2001 and 2003. The sex change between intermediates and females took place mainly in summer and was well marked in 2001 and 2003. The survey of the embryonic development in the egg capsules brooded by the females provided an annual phenology of the laying and hatching processes. The laying period extends from February to September with three to four major periods of egg-laying per year and corresponding hatching periods about 1 month later. Each female lays two to four times per year on average. The first egg-laying concerned fewer females than subsequent ones, except in 2003, and exhibited a higher fecundity. The annual mean of the number of eggs for each stage was not significantly different, thus indicating no significant mortality rate during embryonic development. For the C. fornicata population in the Bay of Brest, several reproductive characteristics tend to highlight its invasive capacity: (1) a long reproductive period, (2) reproduction in a ‘multi-trials’ process equivalent to a spreading out of the risks and (3) a relatively high fecundity.     

Effects of various temperature cycles on the larval development of the gastropod molluscCrepidula fornicata

Veligers ofCrepidula fornicata (L.) were reared for 12 days at constant temperatures of 15°, 20°, 25°, 30° and 35°C, and at 5 C° daily cycles of equal periodicity (COEP) over the temperature ranges 15° to 20°C, 20° to 25°C, 25° to 30°C and 30° to 35°C. COEP consisted of equal periods (6 h) of maximum temperature, minimum temperature, and uniformly increasing and decreasing temperature each 24 h period. Survival was high and not influenced by cyclic or constant temperature from 15° to 30°C. At 35°C and COEP 30° to 35°C, all larvae died before Day 6. Shell growth rate increased markedly over the range 15° to 25°C, and growth rates at cyclic temperatures in this range were intermediate between growth rates at the corresponding constant temperatures. Larvae reared at COEP 15° to 20°C and COEP 30° to 35°C had discontinuities in their shells due to inhibition of shell secretion during the adverse part of each temperature cycle. Groups ofc. fornicata veligers were exposed for 2 days to daily temperature cycles of equal and unequal periodicity in the critical 30° to 35°C range. [Cycles of unequal periodicity (COUP) consisted of unequal periods (varying between 3 and 15 h) of maximum and minimum temperature and uniformly increasing and decreasing temperature each 24 h period.] These veligers showed shell growth although their body tissue declined, as indicated by decreasing carbon content per larva. Least shell growth and most body tissue loss occurred in those cycles with the longest exposure to higher temperature. Larvae exposed for arious days to the mildest 30° to 35°C COUP (15 h at 30°C, 3 h increasing temperature, 3 h at 35°C and 3 h decreasing temperature) recovered and resumed normal growth when transferred to constant 30°C, but their growth was retarded in proportion to the number of days in the temperature cycle. Rates of shell growth of veligers in temperature cycles show an immediate effect of environmental temperature, while changes in carbon content per larva better reflect the effects of temperature on general metabolism and survival.     

Osmotic and ionic concentration of the egg capsule fluid of Crepidula fornicata in relation to embryonic development

Osmotic pressure and major ions (Cl⁻, Na⁺, Mg²⁺, Ca²⁺) of the egg capsule fluid in the slipper limpet Crepidula fornicata were investigated in relation to embryonic development. Calcium permeability of the capsule wall was studied at oviposition, by dipping freshly laid egg capsules in ⁴⁵Ca as a tracer. This study also determined total calcium content of the embryos at different developmental stages. Osmolarity and major ion concentrations in egg capsule fluid were higher than seawater at uncleaved and trochophore stages, and then dropped to the same level as sea water at veliger stage. Concentrations of Cl⁻ and Na⁺ were relatively high at oviposition, peaked at trochophore stage, and finally dropped close to concentrations of seawater at hatching. In contrast, concentrations of Mg²⁺ and Ca²⁺ decreased steadily during capsular development. Radiotracer permeability experiments in freshly laid egg capsules confirmed that the capsule wall is impermeable to this ion at that stage. However, because of the dissolution of the inner layer of the wall during the final part of capsular development, the wall becomes permeable to calcium and probably to the rest of the major ions studied.     

Temperature and pressure tolerance of larvae of Crepidula fornicata suggest thermal limitation of bathymetric range

The extant deep-sea fauna is thought to result from recolonisation of this environment by shallow-water organisms following climate-driven mass extinctions. Planktonic larval tolerance to high pressure is considered an important preadaptation for successful deep-sea invasion. In this study, the pressure and temperature tolerance of a species without any known confamilial deep-sea relative were assessed for the first time. Early- and late-veliger larvae of the shallow-water species Crepidula fornicata were subjected to a temperature/hydrostatic pressure regime from 5 to 25 °C and from 0.1 to 40 MPa. Although early and late veliger survived pressures equivalent to 2,000 m water depth or greater at all temperatures, decreased larval activity indicated significant sublethal temperature and pressure effects. Reduced larval activity of early veliger at low temperatures suggests that the bathymetric range of this species may be thermally constrained. A mechanistic model is proposed to explain the emerging pattern of ontogenetic shifts in pressure tolerance of shallow-water benthic invertebrates.     

Relationship between larval and juvenile growth rates in two marine gastropods,Crepidula plana and C. fornicata

Previous studies on various marine mollusc species have shown that both larval and juvenile growth rates are substantially heritable, but few workers have examined the extent to which larval and juvenile growth rates covary. We examined the relationship between larval and juvenile growth rates in seven laboratory experiments conducted between 1986 and 1993, using the prosobranch gastropods Crepidula plana Say and C. fornicata (L.). In most experiments larvae were reared individually, measured twice nondestructively to determine larval grwoth rate, allowed or stimulated (daily 5-h exposure to 20 mM excess K⁺ in seawater) to metamophose, and then measured at least twice after metamorphosis to determine juvenile growth rates. Generally, there was no significant (p >0.10) relationship between larval and juvenile growth rates, suggesting that in these two species selection can act independently on the two stages of development. A positive correlation (p=0.007) between larval and juvenile growth rates was observed for C. fornicata in one experiment, but only for offspring from females maturing the most rapidly in laboratory culture. Even for these larvae, however, variation in larval growth rate explained<2% of the variation in juvenile growth rate, so that larval and juvenile growth rates are at most only weakly associated in this species.     

Yolk utilization and hatching time in the Canadian lobster Homarus americanus

During the course of its embryonic development, the Canadian lobster Homarus americanus Milne-Edwards exhibits steady increases in water content (56.2 to 86.8%) and ash (5.8 to 21.2%), and a progressive decrease in energy content from 6636 to 4292 cal/g dry weight. Mean dry weight of a single egg is 965 g, equivalent to 6.4 cal; a freshly hatched egg. The lobster hatches about 1,500 larvae per night over a period of 4 to 5 days. Dry weight, ash and calorific contents of larvae hatched on different days show considerable variations. After larvae hatch on the first day, continuous salt absorption by eggs to hatch on subsequent days leads to a steady increase in ash content from 143 g/larva hatched on the first day to 255 g/larva hatched on the fourth day, and consequently, to an increase in dry weight from 854 to 956 g/larva. Metabolism of embryos (0.1 cal/day), which are yet to be hatched on subsequent days, depletes the calorific content per unit weight (from 4637 to 3837 cal/g dry weight) as well as per larva (from 3.98 to 3.67 cal).Dedicated to my colleague K.-H. Schumann (Biologische Anstalt Helgoland) who died on December 12, 1969 due to a diving accident.     

Yolk utilization and growth to yolk-sac absorption in summer flounder (Paralichthys dentatus) larvae at constant and cyclic temperatures

Rates of development, growth and yolk conversion efficiency were determined in larvae of the summer flounder Paralichtys dentatus at constant temperatures of 21°, 16°, 12° and 5°C and in temperature cycles of 21°–16°, 16°–11°, and 11°–5°C. In constant incubation temperatures, development rate increased with increasing temperature. Larvae reared in the cyclic temperature regimes exhibited development rates intermediate to those at the temperature extremes of the cycle. All larvae reared at 5°C and in the 11°–5°C cycle regime died prior to total yolk-sac absorption. Although development rates were temperature dependent, no significant differences in notochord length ash-free dry weight or yolk utilization efficiency were found at the time of total yolk-sac absorption. The similarity in growth and yolk utilization efficiency for larvae reared under these various temperature regimes suggests that the physiological mechanisms involved are able to compensate for temperature changes encountered in nature.Contribution No. 195 from EPA, Environmental Research Laboratory, Narragansett, Rhode Island 02882, USA     

Food limitation stimulates metamorphosis of competent larvae and alters postmetamorphic growth rate in the marine prosobranch gastropodCrepidula fornicata

The effects of food limitation on growth rates and survival of marine invertebrate larvae have been studied for many years. Far less is known about how food limitation during the larval stage influences length of larval life or postmetamorphic performance. This paper documents the effects of food limitation during larval development (1) on how long the larvae ofCrepidula fornicata (L.) can delay metamorphosis in the laboratory after they have become competent to metamorphose and (2) on postmetamorphic growth rate. To assess the magnitude of nutritional stress imposed by different food concentrations, we measured growth rates (as changes in shell length and ash-free dry weight) for larvae reared in either 0.45-m filtered seawater or at phytoplankton concentrations (Isoehrysis galbana, clone T-ISO) of 1 × l0³, 1 × 10⁴, or 1.8 × 10⁵ cells ml^–1. Larvae increased both shell length and biomass at 1 × 10⁴ cells ml^–1, although significantly more slowly than at the highest food concentration. Larvae did not significantly increase (p > 0.10) mean shell length in filtered seawater or at a phytoplankton concentration of only 1 × 10³ cells ml^–1, and in fact lost weight under these conditions. To assess the influence of food limitation on the ability of competent individuals to postpone metamorphosis, larvae were first reared to metamorphic competence on a high food concentration ofI. galbana (1.8 × 10⁵ cells ml^–1). When at least 80% of subsampled larvae were competent to metamorphose, as assessed by the numbers of indlviduals metamorphosing in response to elevated K⁺ concentration in seawater, remaining larvae were transferred either to 0.45-m filtered seawater or to suspensions of reduced phytoplankton concentration (1 × 10³, 1 × 10⁴, or 5 × 10⁴ cells ml^–1), or were maintained at 1.8 × 10⁵ cells ml^–1. All larvae were monitored daily for metamorphosis. Individuals that metamorphosed in each food treatment were transferred to high ration conditions (1.8 × 10⁵ tells ml^–1) for four additional days to monitor postmetamorphic growth. Competent larvae responded to all food-limiting conditions by metamorphosing precociously, typically 1 wk or more before larvae metamorphosed when maintained at the highest food ration. Surprisingly, juveniles reared at full ration grew more slowly if they had spent 2 or 3 d under food-limiting conditions as competent larvae. The data show that a rapid decline in phytoplankton concentration during the larval development ofC. fornicata stimulates metamorphosis, foreshortening the larval dispersal period, and may also reduce the ability of postmetamorphic individuals to grow rapidly even when food concentrations increase.     

Age-and sex-dependent patterns of aggregation in the tropical gastropod Strombus luhuanus

The spatial dispersion of the tropical coral sand-dwelling mesogastropod Strombus luhuanus Linné, 1758 was studied at several sites in two localities (Australian Great Barrier Reef and southern Papua New Guinea), from September 1980 to February 1983. S. luhuanus usually occurred in local aggregations, many of which were relatively dense with discrete boundaries: Four types of aggregation are described: mixed age-class, juvenile, mating, and clusters. The former two are termed colonies, because they persisted over time and exhibited some coordinated movements. Mixed age-class colonies contain individuals of all ages, but within them the different ageclasses are frequently spatially segregated from each other. This was sometimes due to the younger age-classes' preference for shallower areas, but also occurred in areas of constant depth. Juvenile colonies are relatively smaller in area but higher in density, and are dominated by a single size-class. Mating aggregations are concentrations of copulating individuals, in which competition between males for access to females occurs. Clusters are concentrations of inactive individuals (juvenile and adult) piled together in close contact. All types of aggregation were concentrated in only a part of what appeared to be the suitable habitat. Most aggregations' boundaries shifted over time within the habitat. We conclude that intraspecific attraction must be an important factor which maintains the spatial structure of all aggregations, although habitat specificity sets the larger area in which they move. Processes which may underlie this pattern, and some of its implications, are discussed.     

Encapsulated development of the marine prosobranch gastropod Nucella lapillus

Nucella (=Thais) lapillus (L.) develops to the juvenile stage within an egg capsule. This study was undertaken to investigate nutritive and bacteriostatic properties of the intracapsular fluid for this species. Capsules were collected intertidally at Nahant, Massachusetts, USA, in the summers of 1982 and 1983. The average capsule contained only 1.1 l of intracapsular fluid per embryo. A statistically significant correlation was observed between capsule height and number of developing embryos contained therein, although the number of embryos per capsule was more closely related to capsule volume. Total dry weight of encapsulated, shelled embryos increased exponentially as a function of shell length. However, weight increases may be entirely due to shell calcification; the average dry tissue weight of shelled embryos was significantly below that for pre-shelled individuals, suggesting a net loss of biomass during development. Aliquots of intracapsular fluid failed to inhibit the growth of the 13 bacterial strains tested. Despite the above results, pre-shelled embryos generally survived only several days following their premature removal from egg capsules at 12°C. Shelled veligers were reared outside of the capsules with no apparent ill effects. An explanation for these survivorship results is elusive.     

Evaluation of the significance of metal-binding proteins in the gastropod Littorina littorea

Measurements of metals in Littorina littorea from clean and contaminated sites in Great Britain confirmed that body concentrations of Ag, Cd and Hg vary according to environmental contamination, while the essential elements Cu and Zn are regulated. Investigation of the cytosolic distribution of metals in L. littorea, using Sephadex G-75 gel-permeation chromatography, revealed important distinctions in the partitioning of elements. In contrast to Ag and Hg, which were mainly associated with high molecular weight ligands, Cd was bound predominantly to an intermediate molecular weight, soluble protein (CdBP-I, apparent mol. wt=20 000). However, although the main function of CdBP-I, both in clean as well as contaminated individuals, was sequestration of Cd, significant quantities of other non-essential metals (Ag, Hg) were similarly bound. Laboratory experiments confirmed the role of CdBP-I in complexing cadmium, and also revealed the induction of a second cadmium-binding protein (CdBP-II) in response to high cadmium levels. The apparent molecular weight (10 000), absorbance characteristics and high (inducible)-SH content of CdBP-II suggest similarities with metallothionein. A dose-related increase in the-SH content of very low molecular weight (>3 000) fractions was also observed in cadmium-exposed L. littorea, although no cadmium was associated with these ligands. A detoxifying role is tentatively proposed for the metal-binding proteins CdBP-I and II in L. littorea. However, some spillover of cadmium to the high molecular weight protein pool was observed in individuals exposed to cadmium in the field and laboratory. The use of L. littorea in biochemical assays of environmental contamination is discussed.     

Life history of the temperate subtidal gastropod Umbonium costatum

The life history and reproductive biology of the trochid sand snail Umbonium costatum (Kiener) were investigated on a subtidal sandy shore in Hakodate Bay, Japan between 1988 and 1991. Female U. costatum mature at 1 yr of age (shell diameter-11 mm), reproduce twice (in June-July and September-October) in successive years, grow to a maximum size (shell diameter=22 mm) at age 8 yr, increase annual fecundity with age from 2000 (age 1 yr) to 37000 (age 8 yr), and show a maximum monthly gonad somatic index of 8% which is constant among ages. In comparison to a previously studied life history of a tropical Umbonium vestiatium, temperate U. costatum shows more sustained growth and a longer life span after maturation. This could be explained by: (1) the optimal size model concerned with resource investment, in gametes (Sebens 1987); and by (2) bet hedging to compensate large variability in larval success at high latitudes. These two hypotheses are not mutually exclusive, but both are based on season-related extremes of environment at high latitudes where the period suitable for reproduction is short.     

Energy budget of the predatory marine gastropod Polinices duplicatus

Based on direct monitoring of feeding and growth under field conditions and frequent measurements of respiration and energy content in the laboratory, annual energy budgets were derived for Polinices duplicatus feeding on Mya arenaria at Barnstable Harbor, Massachusetts. The gross growth efficiency (P_g/C) of P. duplicatus was high (35%) and varied inversely with snail size. The proportion of ingested energy expended on respiration (R/C) was modest (44%) and varied directly with snail size and inversely with temperature. The energetic efficiencies of P. duplicatus agreed with the few results available for othe predatory molluscs and differed from most results available for herbivorous and detritivorous molluscs.     

Yolk hormones and sexual conflict over parental investment in the pied flycatcher

Female birds might be able to manipulate the parental effort of their male partner through elevated transfer of hormones to the eggs, since these hormones affect many chick traits that males might use as cues for adjusting the level of their investment. We experimentally studied whether female pied flycatchers Ficedula hypoleuca could manipulate male investment via yolk androgens. There is much more variation in yolk androgen levels between females than within clutches, and in order to change the androgen levels of the eggs, we swapped whole clutches between nests. To estimate the androgen levels of the clutch, we measured the androgen content of a single egg per clutch. Females did not succeed in manipulating male effort using yolk androgens, since there was no relationship between the division of parental care within a pair and either original or foster egg androgen levels. One of these relationships should have occurred if females were manipulating males. The proportion of feeding visits by the male was higher when the male was old (55%) than when he was young (45%) and females laid eggs with higher androgen levels when mated with a young male. Young males did not exhibit any responses to yolk androgen levels either, which indicates that females cannot exploit their effort more than that of old males. We suggest that females may allocate yolk androgens to adjust the growth trajectories of the chicks to poor growing conditions when mated with young males that are poor providers or occupying a poor territory.     

Two modes of development in the morphospecies Crepidula dilatata (Gastropoda: Calyptraeidae) from Southern Chile

In Chinquihue Bay, a sheltered locality in Southern Chile, female Crepidula dilatata Lamarck brood egg masses which differ in intracapsular development. In some, all eggs develop and are hatched as free veliger larvae (indirect development). In others, only some of the eggs develop and hatch as young adults (direct development), the rest being consumed as nurse eggs. Two possible interpretations are considered: intrapopulation variation of developmental pattern in a species, and the coexistence of two sibling species. Stages of the intracapsular development are described and illustrated. Fecundity varies according to size of the female. For females brooding eggs with indirect development it is estimated at between 3840 and 85575 embryos per spawn; for females with eggs undergoing direct development, embryo production per egg mass is estimated at between 70 and 812. A comparison is made between females brooding the two kinds of egg masses. Minor differences exist in adult coloration, shape of egg capsules, egg diameters, spawning season and their abundance and distribution in the intertidal. Brooding females with eggs displaying indirect development are significantly larger than those with eggs of direct development. The latter females form chains subtidally but not intertidally as do females bearing eggs with indirect development. On these females with pelagic larvae, chains frequently include sedentary males which reach large sizes. On basal females with direct development, chains contain mostly other females, suggesting that matings are temporary and by errant males. These results are compared with existing information in the literature for other species both in this genus and in other marine invertebrates. It is concluded that two sympatric sibling species with different modes of development are present in the morphospecies C. dilatata Lamarck in Southern Chile.Devoted to Dr. E.F. Kilian, Zoologisches Institut der Universität Gießen, FRG.