Intraspecific density mediates sex-change in the territorial patellacean limpet Lottia gigantea

The effects of intraspecific density and agonistic interactions on sex-change were studied in the territorial limpet Lottia gigantea. In a one-year field experiment (1982–1983) on San Nicolas Island off the southern California coast, USA, male limpets transplanted to large enclosures changed sex more frequently than those transplanted to small enclosures (9 of 13 vs 1 of 10; p=0.013), indicating that intraspecific density can profoundly influence the probability of sex change. Large limpets were more likely to change sex than small ones. Observations of gender-age distributions as well as field behavior suggested that each limpet's territorial status prior to the experiment may have been an important component of this size effect, although other interpretations including an effect of age are possible. Pooling the results with those of two previous studies confirmed that sex-change is enhanced by low density. This enhancement was observed among the largest members of a local population in the first year of each experiment, while among the smaller members the enhancement was delayed until the second or third year. Low density may be a correlate of high mortality, and therefore an adaptive cue for an earlier age of sex change. Dominant territorial status correlates with an individual's size, and therefore egg-producing capacity, relative to its neighbors, and thus may also be a good cue for the initiation of sex-change.     

Ecological impacts on the limpet Lottia gigantea populations: human pressure over a broad scale on island and mainland intertidal zones

Here long-term monitoring data taken at 33 sites in southern and central California coast and islands were used to evaluate the size structure of the large intertidal limpet, Lottia gigantea in restricted-access and in easily accessible intertidal zones that encompass a wide range of ecological variables. Using multi-dimensional analysis of population size structures, we found that sites on islands and strictly protected mainland sites have significantly larger median limpet sizes and a greater range of limpet sizes than unprotected mainland sites, while no pattern occurs in latitudinal or regional comparison of sites. Although intertidal predators such as oystercatchers were not the primary focus of the monitoring efforts, extensive natural history notes taken during sampling visits support the argument that predation was not a primary cause for the size structure differences. Finally, substratum differences were determined not to have biased the observation of larger limpets in protected sites. In regard to human interactions with limpets, we conclude that the degree of enforcement against poaching is the better predictor of limpet size structure than proximity to population centers or visitation to intertidal sites.     

Population structure,northern range limit,and recruitment variation in the intertidal limpet Lottia scabra

The northern range limit of the intertidal limpet Lottia scabra is Cape Arago, Oregon (43°N), where adult survival is excellent, the population is small (<300), and recruitment is low; the range limit may be set by limited recruitment. Between June 2012 and March 2013, 25 sites from the middle of the species range (33°N) to Cape Arago were sampled and population size frequency distributions, densities, and nearest neighbor distances were compared to the amount of rocky and sandy shore and kelp bed size. North and south of 37°N, the densities of new recruits averaged 22 and 86 m^?2, respectively. This shift was associated with the range limit of Macrocystis pyrifera kelp beds; we hypothesize that slower currents in M. pyrifera beds may limit larval dispersal leading to higher recruitment. North and south of 40°N, adult density averaged <1 and 458 m^?2, respectively, with the species absent from many sites to the north. This shift was associated with a sharp drop in the amount of rocky shoreline and an increase in uninhabitable sandy shore. Near the northern range limit, >80 % of the individuals were solitary and may be unable to spawn successfully. Recruitment at Cape Arago was infrequent and likely due to self-recruitment. This study suggests that the range limit was set by the absence of M. pyrifera and too little rocky shore leading to high larval wastage, low settlement, low population densities, and, due to an Allee effect, very small effective population sizes.     

Recruitment in the intertidal limpet Lottia digitalis (Patellogastropoda: Lottiidae) may be driven by settlement cues associated with adult habitat

The ribbed limpet, Lottia digitalis, is found high in rocky intertidal habitat throughout its geographic range. In order to identify likely natural settlement locations for larvae of this species, laboratory-reared larvae were settled onto substrata collected from within and near an adult L. digitalis habitat. Of larvae exposed to rock chiseled from within high-intertidal adult habitat, 31.0% and 23.3% underwent metamorphosis during two separate experiments. Similarly, an unidentified filamentous green alga that was isolated from this rock induced metamorphosis in 26.6% and 8.7% of larvae during additional experiments. In contrast, larvae did not metamorphose upon bare rocks or upon rocks encrusted with a crustose corraline alga (CCA) that were collected from lower intertidal zones, nor did they metamorphose upon the macroalgae Ulva sp., Enteromorpha contorta, Alaria marginata, or Polysiphonia sp. The presence of mucus from adult conspecifics during these experiments did not enhance metamorphosis onto rock taken from adult habitat, but it did induce metamorphosis in an average of 13.5% and 7.0% of larvae introduced to the mid-intertidal bare rock and CCA substrata, respectively. Finally, 38.0% and 34.4% of larvae from two experiments underwent metamorphosis when exposed to the high-intertidal barnacle Pollicipes polymerus. These results suggest that larval settlement, rather than differential post-settlement mortality and/or migration, drives recruitment of L. digitalis in high-intertidal habitats.     

Mineralization of major lateral teeth in the radula of a deep-sea hydrothermal vent limpet (Gastropoda:Neolepetopsidae)

Radular teeth of a neolepetopsid patellogastropod limpet, Paralepetopsis ferrugivora, from a deep-sea hydrothermal vent site have similar elemental composition (O, Si, P, S, Cl, K and Fe) to radular teeth of the shallow-waters patellogastropod limpets. However, in contrast to shallow waters limpets, the fully mature teeth of P. ferrugivora do not show any crystalline phases. Amorphous silica was found in the cusp of the teeth and amorphous iron oxide in the junction zone and base of the teeth. Ferritin-rich vesicles were observed in cells adjacent to the junction zone of the early mature teeth, suggesting that these vesicles can mediate the delivery of iron to the tooth matrix. The similarity in the elemental composition between the hydrothermal limpet P. ferrugivora and shallow-waters patellogastropod limpets shows that the extreme hydrothermal environment did not alter the elemental composition of the radular teeth in the deep-sea species.Communicated by P. W. Sammarco, Chauvin     

Analyses of limpet defense and predator offense in the field

Between November 1982 and August 1984 diving observations of two intertidal limpets' defensive behaviours in response to two predatory species were made near the Seto Marine Biological Laboratory of Kyoto University, in Wakayama Prefecture, Japan, for over 800 h. The focus of the observations was a simple isolated rock, 0.9 m² in area with an inclination of 75°. The pulmonate homing limpet Siphonaria sirius responded by fleeing from its home in response to the whelk Thais clavigera and by calmping tightly to its home scar in response to the starfish Coscinasterias acutispina. Both behaviours were successful for avoiding predation. After a whelk moved far away, limpets returned to their homes. The patellid limpet Cellana toreuma showed mantle folding behaviour or fled for an average distance of 8 cm vertically upwards in response to the whelk and for an average distance of 21 cm vertically upwards in response to the starfish. The amount of time predators spent foraging increased in the low intertidal zone relative to the mid and high zones, and most predator attacks were observed during the limpets' resting periods (submersion in late afternoon or nighttime). The upward directional flight displayed by C. toreuma was related to the upward orientation of the limpets' heads when they are in a resting position. Half of the limpets observed fleeing downward away from a starfish, a movement elicited by a downward attack, received a second attack. These limpets were preyed upon at the second encounter 67% of the time. The upward fleeing behaviour of C. toreuma resulted in the shifting of its resting site higher up the study site where fewer attacks occurred and where the mortality rate was at its lowest. It is suggested that the homing behaviour of S. sirius and the upward fleeing behaviour of C. toreuma are mechanisms by means of which interspecific competition between limpets is reduced and coexistence on a small rock surface is maintained.     

Morphological and habitat divergence in the intertidal limpet Patelloida pygmaea

In the intertidal limpet Patelloida pygmaea, two distinctive morphs, the forms pygmaea and conulus, have been recorded. The former possesses a flat elongated shell, and the latter has an extremely high round shell. It has been observed in the field that pygmaea is found on oyster shells Crassostrea gigas. The form conulus uses an unusual substrate for attachment. It is found on the living shells of the intertidal gastropod Batillaria cumingi. Although conulus is normally found only on shells of Batillaria, it can also be found on oyster shells when pygmaea and Batillaria shells are not present in nature. An electrophoretic analysis of allozymes showed that these two forms are reproductively isolated from each other and coexist without gene exchange on the same mudflat. Laboratory experiments showed that pygmaea prefers oyster shells and conulus prefers Batillaria shells as substrates for attachment when both oyster and Batillaria shells are present. The form pygmaea did not attach to Batillaria shells, even when only Batillaria shells were available. However, conulus also attached to oyster shells when Batillaria shells were not available. The proportion of individuals of conulus that attached to oyster shells decreased significantly when pygmaea was attaching to the oyster shells. These results suggest that pygmaea is ecologically more specialized to living on oyster shells than conulus.     

Growth studies of the tropical intertidal limpet Acmaea antillarum

The tropical intertidal limpet Acmaea antillarum (Sowerby) was used in a series of field and aquarium growth studies, carried out in Venezuela. Both field and aquarium experiments demonstrated the formation of diurnal growth ridges and subdiurnal periodic growth striations on the shell surface. It was shown in aquarium experiments that the normal growth pattern was inhibited in constant darkness and that continous illumination stimulated the formation of extra growth ridges. Alterations of the experimental sequence of illumination influenced the formation of subdiurnal growth markings. This secondary growth pattern appears to be distinct from the basic system of diurnal ridge formation. Limpet shell lengths were related to estimated age based on diurnal growth ridge counts. It is probable that maximum shell size is attained in less than 1 year. Equations for allometric shell growth characteristics were calculated relative to shell length. Calculations for instantaneous relative growth rate were made from natural populations, experimental field populations and aquarium specimens. These were compared to show that the field and aquarium experiments demonstrated similar growth rates. The results of these observations and calculations are compared with other molluscan growth studies.     

Computational model for protein-mediated biomineralization of the diatom frustule

The mechanism of silicification from which the intricate cell walls of diatoms emerge, as well as the stereochemical relationship between the wall's organic casing and the siliceous materials within, continue to elude current technology. The present study further develops Hecky et al.'s standing model of the organicinorganic interface with semi-empirical computer simulations of a biosilicification pathway. Polycondensation reactions between silicic acid molecules and a hydroxyl-rich -sheet protein template results in a stereochemically-compatible chemisorbed tetrasiloxane ring. The 24-stage reaction pathway has an activation barrier of +15.4 kcal mol^-1 and results in a net stabilization of-28.0 kcal mol^-1. Spatial matching and favorable thermodynamics support the theory of protein-mediated biomineralization of the diatom.     

Ultrastructural examination of chamber morphogenesis and biomineralization in the planktonic foraminiferOrbulina universa

Pre-sphere, trochospiralOrbulina universa (d'Orbigny) were hand-collected between June and September, 1982 to 1984, from surface waters of the Pacific Ocean ca. 2 km off Santa Catalina Island, California, USA. The formation of a spherical chamber by this planktonic foraminifer was studied with light and electron microscopy. Chamber morphogenesis is preceded by the secretion of a cytoplasmic layer rich in mitochondria. The layer expands away from the pre-existing foraminiferal shell surface in a spherical pattern. Full cytoplasm expansion is followed by the secretion of an organic matrix (OM) approximately 200 m above the original shell surface. Cytoplasm, mitochondria and/or vesicles may play a role in OM secretion. Calcification and chamber thickening, new spine growth and pore development are documented and continue for a period of 1–7 d. Approximately 24 h prior to gamete release, the foraminiferal spines are resorbed and a veneer of calcite is deposited on the shell surface. An extensive intracellular organelle unique to foraminifera, the fibrillar system, is examined and is hypothesized to play a role in the biomineralization process. The taxonomic and functional significance of theO. universa spherical chamber is discussed with respect to other foraminiferal species.     

Genetic differentiation independent of intertidal gradients in the pulmonate limpet Siphonaria kurracheensis

The intertidal limpet Siphonaria kurracheensis (Reeve, 1856) has a bimodal vertical distribution of abundance on rocky shores at Rottnest Island, Western Australia. An electrophoretic study of 5 polymorphic enzymes revealed no consistent genetic differences between adults high and low on the shore. Contrasting with this absence of a detectable genetic response to the steep environmental gradients in the intertidal zone, there were genetic differences among low-shore adults from different sites, and between adults and recruits. This genetic differentiation could be due to either localized selection or temporal variation in the genetic makeup of recruits.Communicated by G. F. Humphrey, Sydney     

Biochemical and energy changes during embryogenesis in the rock scallopCrassadoma gigantea

The biochemical composition of eggs spawned from rock scallopsCrassadoma gigantea (Gray) collected from Clayoquot Sound, Vancouver Island (British Columbia, Canada) in the winter of 1987 and the summer of 1988, differed significantly only in lipid and soluble-ash contents. Major macronutrients were catabolized simultaneously and linearly with time of embryogenesis. Total egg energy expended during development was 11.8 kJ g^–1 derived 46.7, 9.8 and 43.5%, from lipid, carbohydrate, and protein, respectively. Glucose in the egg was the dominant source of carbohydrate energy. Deposition of shell was linear with time of embryogenesis and the formation of 44.8% dry wt of shell in the early larval stage, referred to as the D-larva, consumed 64.4% of the total energy expended. Energy required for shell formation was 17.55 kJ g^–1. The RNA:DNA ratio declined exponentially from 18.6 in the egg to 2.21 in the D-larva, which was consistent with that of adult bivalves. Many changes in fatty acid composition were linear with time of embryogenesis, and the percentage ofn3- andn6-higher unsaturated fatty acids to total polyethylenic acids exhibited significant declining and increasing trends, respectively. The linear rate of catabolism of eicosapentaenoic acid, 20:5n3, and the constant level of docosahexaenoic acid, 22:6n3, illustrated an energy and a structural role, respectively, for these dominant acids in the embryonic development of the rock scallop.     

Comparison of allozyme and mitochondrial DNA spatial differentiation in the limpet Patella vulgata

Allozyme and restriction enzyme analysis of mtDNA was used to study variation in samples from British populations of the marine limpet Patella vulgata in two regions. South Wales and Northeast England. Allozyme analysis revealed significant differences in allele frequencies among samples. However F _ST (population differentiation) values were no higher between than within regions, indicating that genetic heterogeneity was localised and not related to geographic separation. For mtDNA, samples from South Wales exhibited higher haplotype diversity values than samples from Northeast England. In addition there were substantial differences in the haplotype distribution between regions. The value of , the haploid analogoue of F _ST , was low within regions (=0.09) but high between regions (=0.44). The estimated difference in migration rate for allozymes and mtDNA exceed the neutral expectation, unless it is assumed that there are influential differences in the magnitude of female and male gametic dispersal.     

Temporal genetic variation in populations of the limpet Cellana grata from Hong Kong shores

Variations in the relative contributions of gene flow and spatial and temporal variation in recruitment are considered the major determinants of population genetic structure in marine organisms. Such variation can be assessed through repeated measures of the genetic structure of a species over time. To test the relative importance of these two phenomena, temporal variation in genetic composition was measured in the limpet Cellana grata, among four annual cohorts over 10 years at four rocky shores in Hong Kong. A total of 408 limpets, comprising individuals from 1998, 1999, 2006 and 2007 cohorts were screened for genetic variation using five microsatellite loci. Minor but significant genetic differentiation was detected among samples from the 1998/1999 collection (F _ST = 0.0023), but there was no significant differentiation among the 2006/2007 collection (F _ST = 0.0008). Partitioning of genetic variation among shores was also significant in 1998/1999 but not in the 2006/2007 collection, although there was no correlation between genetic and geographic distances. There was no significant difference between collections made in 1998/1999 and 2006/2007. This lack of clear structure implies a high level of gene flow, but differentiation with time may be the result of stochastic recruitment variation among shores. Estimates of effective population size were not high (599, 95% C.L. 352–11397), suggesting the potential susceptibility of the populations to genetic drift, although a significant bottleneck effect was not detected. These findings indicate that genetic structuring between populations of C. grata in space and time may result from spatio-temporal variation in recruitment, but the potential development of biologically significant differentiation is suppressed by a lack of consistency in recruitment variability and high connectivity among shores.     

Life-history features of the marine intertidal limpet Notoacmea scutum (Gastropoda) in central California

Growth of individually marked specimens of Notoacmea scutum (Rathke) was followed for 15 months (April, 1978 to June, 1979) at a field site in central California, USA. Growth rates were highly seasonal, being highest from late spring through early summer and lowest during winter. Growth rate also varied significantly with intertidal height: limpets lower in the intertidal zone grew faster. Both relationships may have been related to the relative abundance of food or to the amount of time available for foraging. Recently settled limpets, which were present throughout the year, grew to approximately 17 mm in length by the end of their first year; by then, they had also reached the size at which mature gonads were consistently found (16 mm). Limpets were almost 26 mm long by the end of the second year. Substantial mortality occurred throughout the year, but it was particularly severe during winter, when a large portion of the reproductive population was lost. This pronounced winter mortality was probably not caused by invertebrate predators such as seastars. Most limpets at the study site were less than 2 yr old.     

The Wahlund effect and the geographical scale of variation in the intertidal limpet Siphonaria sp.

Samples of Siphonaria sp. were collected between 1978 and 1982 from sites covering its known geographic range, from Kalbarri, Western Australia to Port Robe, South Australia. Geographic variation of 7 polymorphic enzymes was examined in this intertidal pulmonate limpet, and was found to be consistently small, indicating a large-scale influence of gene flow due to planktonic dispersal. Despite this large-scale uniformity, there is fine-scale genetic patchiness, which is repeated, rather than accumulated, on the larger scale. Throughout its geographic range, Siphonaria sp. shows deficits of heterozygotes for all 7 loci. The consistency among loci indicates that the causes of the deficits are populational, rather than locus-specific. A Wahlund effect, the departure from Hardy-Weinberg equilibrium due to mixing of individuals from groups with different allelic frequencies, is the simplest explanation of such deficits. The limited geographic variation of allelic frequencies, however, is grossly inadequate to produce these deficits through a Wahlund effect. Similarly, temporal variation in allelic frequencies in recruits does not explain the deficits. The largest contributor to a Wahlund effect appears to be binomial sampling variance among small local breeding groups. Thus, mixing of larvae on a scale of metres, rather than among geographical areas, apparently produces the deficits of heterozygotes.     

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 a complex archipelago on genetic subdivision of the intertidal limpet Siphonaria kurracheensis

Allozyme variation in the intertidal limpet Siphonaria kurracheensis was examined in 11 populations from the Houtman Abrolhos Islands, Western Australia, and four from the adjacent mainland, to test if the effects of these islands on genetic subdivision should include species with high dispersal. Consistent with extensive planktonic dispersal, genetic subdivision was low, with an average standardized variance in allelic frequencies (F_ST) of 0.010 over 400 km along the mainland, and 0.009 over 70 km in the Abrolhos Islands. Nevertheless, subdivision was statistically significant at the smallest scale examined (about 10 km), showing a pattern of local heterogeneity and large-scale homogeneity, which is common in planktonic dispersers. Among the island populations, heterozygosity was positively correlated with a multivariate index of exposure. The level of heterozygosity at the most exposed island sites is equivalent to that at the (also exposed) mainland sites, whereas it is lower in the most sheltered island sites. Although this indicates that some island populations are less well connected to the major pool of larvae, the overall effect of the archipelago on genetic subdivision is no greater than occurs on the mainland coast. This is contrary to findings in previously studied species with less potential for dispersal, suggesting that the local impediments to dispersal are selective in their effects, and are unlikely to be broadly important for genetic divergence in widely dispersing species.     

Assessment of factors affecting heart rate of the limpet Patella vulgata on the natural shore

 Heart rate variations of a population of the limpet Patella vulgata were monitored in the natural environment (Lough Hyne, southern Ireland) by non-invasive, optoelectronic recording. The heart rates of 145 limpets of different sizes, living on vertical and horizontal substrata, were measured both in air and water at different environmental temperatures, while the animals were inactive on their home scars. The heart rates of emersed, inactive limpets were positively related to air temperature and negatively related to limpet size. These relationships were similar for limpets on vertical and horizontal substrates. In contrast, no significant relationship between heart rate and temperature was found in submerged limpets, probably due to the narrow thermal range of the water during the study period. During submersion, a significant negative relationship between heart rate and size was evident for limpets on vertical surfaces but not for limpets on horizontal surfaces. In general, submerged limpets had a higher heart rate, 1.16 times that of limpets exposed to air. Moreover, the heart rates of nine animals were recorded while they were moving and while inactive on their home scars. Active limpets had a faster heart rate, 1.6 times that of limpets resting on their home scars. The dependence of heart rate on environmental temperature, size, respiratory medium and activity, as observed in limpets on the shore, agrees well with laboratory data and with previous findings of the correlation of oxygen consumption with the same factors. Such in situ measurements may, therefore, prove useful in attempts to determine natural levels of energy expenditure in models on the behaviour of foraging molluscs. Received: 5 September 1999 / Accepted: 17 April 2000