Further twists in gastropod shell evolution

The manner in which a gastropod shell coils has long intrigued laypersons and scientists alike. In evolutionary biology, gastropod shells are among the best-studied palaeontological and neontological objects. A gastropod shell generally exhibits logarithmic spiral growth, right-handedness and coils tightly around a single axis. Atypical shell-coiling patterns (e.g. sinistroid growth, uncoiled whorls and multiple coiling axes), however, continue to be uncovered in nature. Here, we report another coiling strategy that is not only puzzling from an evolutionary perspective, but also hitherto unknown among shelled gastropods. The terrestrial gastropod Opisthostoma vermiculum sp. nov. generates a shell with: (i) four discernable coiling axes, (ii) body whorls that thrice detach and twice reattach to preceding whorls without any reference support, and (iii) detached whorls that coil around three secondary axes in addition to their primary teleoconch axis. As the coiling strategies of individuals were found to be generally consistent throughout, this species appears to possess an unorthodox but rigorously defined set of developmental instructions. Although the evolutionary origins of O. vermiculum and its shell's functional significance can be elucidated only once fossil intermediates and live individuals are found, its bewildering morphology suggests that we still lack an understanding of relationships between form and function in certain taxonomic groups.     

The effects of gastropod shell availability and habitat characteristics on shell utilization by the intertidal hermit crab Pagurus longicarpus Say

The shell utilization patterns of two intertidal populations of the hermit crab, Pagurus longicarpus Say, were studied. The populations differed with respect to the physical characteristics of their habitats and the availability of empty gastropod shells. The first population was in an estuary connected to Narragansett Bay. This population had few, if any. empty shells available in the area. The second population was in a rock-cobble area directly on Block Island Sound. There were large numbers of empty gastropod shells available for this population. The consistently high gastropod mortality on this shore appears to be caused by the animals being washed up on the beach, where they die due to desiccation.Data from samples collected from June to November of both 1974 and 1975 showed that there were distinct differences in the shell utilization patterns of the two populations. A greater proportion of the animals collected from the estuary population inhabited damaged shells and/or shells with symbionts compared to the individuals from the population with large numbers of empty shells available.The results of shell selection experiments indicated that individuals from both populations inhabited less than preferred shells. The population with large numbers of empty shells available was qualitatively shell-limited because of the effect of physical factors on the morphology of the gastropod species of that area. In addition, the shell selection experiments showed that individuals from the two areas had significantly different shell preferences. This result may be explained by the effects of the environment on the growth rates of the hermit crabs and/or as an indication that shell preferences may vary in response to the physical factors of a given habitat.     

Shell structure of two polar pelagic molluscs, Arctic Limacina helicina and Antarctic Limacina helicina antarctica forma antarctica

The purpose of this study was to investigate shell growth performance in two thin-shelled pelagic gastropods from cold seawater habitats. The shells of Arctic Limacina helicina and Antarctic Limacina helicina antarctica forma antarctica are very thin, approximately 2–9 μm for shells of 0.5–6 mm in diameter. Many axial ribbed growth lines were observed on the surface of the shell of both Limacina species. Distinct axial ribs were observed on the outermost whorl, while weak or no rib-like structures were observed on the inner whorls in the larger shell of L. helicina antarctica forma antarctica. For L. helicina, no ribs were observed on small individuals with three whorls, while larger individuals had distinct ribs on the outer whorls. Shell microstructure was examined in both species. There is an inner crossed-lamellar and extremely thin outer prismatic layer in small individuals of both species, and a distinct thick inner prismatic layer was observed beneath the crossed-lamellar layer in large Antarctic individuals. Various orientations of the crossed-lamellar structure were observed in one individual. Shell structure appeared to be different between the Antarctic and Arctic species and among shells of different size.     

Symbiosis of sea anemones and hermit crabs: different resource utilization patterns in the Aegean Sea

The small-scale distribution and resource utilization patterns of hermit crabs living in symbiosis with sea anemones were investigated in the Aegean Sea. Four hermit crab species, occupying shells of nine gastropod species, were found in symbiosis with the sea anemone Calliactis parasitica. Shell resource utilization patterns varied among hermit crabs, with Dardanus species utilizing a wide variety of shells. The size structure of hermit crab populations also affected shell resource utilization, with small-sized individuals inhabiting a larger variety of shells. Sea anemone utilization patterns varied both among hermit crab species and among residence shells, with larger crabs and shells hosting an increased abundance and biomass of C. parasitica. The examined biometric relationships suggested that small-sized crabs carry, proportionally to their weight, heavier shells and increased anemone biomass than larger ones. Exceptions to the above patterns are related either to local resource availability or to other environmental factors.     

Ecological relations between hermit crabs and their shell-supplying gastropods: Constrained consumers

Hermit crabs are critically dependent upon gastropod shells for their survival and reproductive fitness. While anecdotal reports have suggested that hermit crabs may be capable of removing live gastropods from their shells to access the essential shell resource, no systematic experiments have been conducted to investigate this possibility. This paper reports experiments on both marine (Pagurus bernhardus) and terrestrial (Coenobita compressus) hermit crabs in which crabs were paired in the laboratory with the gastropods whose shells they inhabit in the field. Pairings included both shelled and naked crabs and spanned the full range of the gastropod life cycle. Neither marine nor terrestrial hermit crabs were successful at removing live gastropods from their shells. Furthermore, only a small fraction of the crabs (5.7%) were capable of accessing shells in which the gastropod had been killed in advance, with its body left intact inside the shell. Finally, although hermit crabs readily entered empty shells positioned on the surface, few crabs (14.3%) were able to access empty shells that were buried just centimeters beneath them. These results suggest that hermit crabs are constrained consumers, with the shells they seek only being accessible during a narrow time window, which begins following natural gastropod death and bodily decomposition and which typically ends when the gastropod's remnant shell has been buried by tidal forces. Further experiments are needed on more species of hermit crabs as well as fine-grained measurements of (i) the mechanical force required to pull a gastropod body from its shell and (ii) the maximum corresponding force that can be generated by different hermit crab species' chelipeds.     

Larval and juvenile gastropods from a Carboniferous black shale: palaeoecology and implications for the evolution of the Gastropoda

A horizon in the late Visean Ruddle Shale from Arkansas contains the oldest well-preserved gastropod protoconchs known from the Americas. The gastropod fauna consists of a diverse larval shell assemblage and a low diversity assemblage of juvenile gastropods that probably had a benthic life habit. Gastropod larval shells are always isolated, i.e. the gastropods did not complete their life cycle (no metamorphosis) and were unable to become benthic. This was caused by unfavorable environmental conditions on the soft muddy bottom that was probably due to anaerobic to exaerobic conditions. The absence or scarcity of bioturbation caused by invertebrate detritus or sediment feeders in both shale and concretions (formed before compaction) favored preservation of the delicate larval shells. The lack or scarcity of infauna and bioturbation as well as the low diversity of the presumed benthos supports an interpretation of a quasi-anaerobic to exaerobic benthic environment. The superbly preserved larval shells demonstrate that there are more caenogastropod clades present in the late Palaeozoic than suggested previously. Some larval shell types have an openly coiled first whorl followed by a planktotrophic larval shell; openly coiled initial whorls are unknown from modern caenogastropods. The vetigastropods have a smooth protoconch of two whorls clearly demarked from the following whorls - a pattern unknown in modern vetigastropods which have a protoconch of less than one whorl and build no larval shell during their planktonic stage. This could indicate a link between Palaeozoic vetigastropods and the caenogastropods.     

Finite element analysis of a double membrane tube (DMS-tube) and its implication for gastropod shell morphology

Molluscan shells, including those of Gastropoda, are formed by accretionary growth at the mantle edge. The mantle is a thin membrane of skirt-like shape, which extends minutely beyond the aperture, and its edge adds a shell increment to the aperture margin so that each increment copies a configuration of the mantle edge at that time. Thus, regulation of shell morphogeny is almost equivalent to the factors which control the mantle form at the moment of shell growth. Form of the mantle skirt is considered to be kept in a state of balance between the force of its internal stress and forces acting on it such as fluid pressure or muscle contraction. The expansion behavior of the mantle skirt has been numerically analyzed by using an elastic model (DMS-tube), which represents the fundamental structure of the mantle tissue as a double membrane structure with internal springs (DMS). Four characteristic expansion patterns of the DMS-tube have been detected: (1) general outward expansion; (2) developing a ridge-like fold on an initial longitudinal protrusion of the tube edge; (3) drastic shift of the expanded state from a uniformly curved to an elliptical shape in outline, owing to the existence of a fixed boundary condition on the tube wall; and (4) constricted protrusion on the open region of the shell wall surrounding the DMS-tube. These results have the potential for answering the following questions relating to the morphogenesis of gastropod shells. How does the mantle skirt usually make contact with the inner surface of the shell wall so as to ensure continuous accretion of shell materials to the aperture margin? What is the cause of spiral ridges? Why do open coiling or minimally overlapping shells have generally circular apertures, while shells with apertures overlapped by whorls have non-uniformly curved apertural lips? What is the cause of long closed spines and why do they always appear on spiral ridges?     

Gastropod shells: A dynamic resource that helps shape benthic community structure

Empty gastropod shells are an important resource for many animals in shallow benthic marine communities. Shells provide shelter for hermit crabs, octopuses, and fishes, provide attachment substratum for hermit crab symbionts, and directly or indirectly modify hermit crab predation. Creation of an empty shell due to predation of one gastropod on another and acquisition of that shell by a hermit crab are two key events in the subsequent use of that shell. Shells of different gastropod species and the species of hermit crab acquiring them affect the symbiont complement that attaches to the shell, which in turn may affect future shell use by other symbionts. Certain shell types worn by the hermit crab, Pagurus pollicaris Say, are positively associated with the symbiotic sea anemone, Calliactis tricolor (Lesueur), which protects the hermit crab from predation by the crab, Calappa flammea (Herbst), and possibly from the octopus, Octopus joubini Robson. Shells of other species of gastropods are resistant to being crushed by the spiny lobster, Panulirusargus (Latreille). The inter-and intraspecific interactions centered on the gastropod shell are termed a “habitat web.” The potential of the shell to limit the size and distribution of animal populations demonstrates how this resource helps shape community structure.     

Gastropod shells: A potentially limiting resource for hermit crabs

The availability of gastropod shells to hermit crabs in the Newport River Estuary, Beaufort, N.C. has been assessed by determining the numbers of usuable shells occurring in characteristic subtidal habitats and by measuring shell size adequacy. The proportion of useable shells occupied by hermit crabs ranged from 58–99 % and many of the shells not used by hermit crabs were judged unavailable because they were occupied by sipunculids or only uncovered by the dredge. The shell adequacy index (shell size occupied/shell size preferred) was significantly below 1.0 for the largest species (Pagurus pollicaris Say) in the one location where sufficient numbers were collected and for the next largest species (P. longicarpus Say) in three of the four locations where it was collected. The shell size adequacy index for the smallest species (P. annulipes Stimpson) did not differ significantly from 1.0 in either of the two locations in which it was found. These observations suggest that the availability of gastropod shells plays a significant rôle in limiting the abundance of at least the larger hermit crabs.     

Appearance of morphological novelty in a hybrid zone between two species of land snail

On the small oceanic island of Chichijima, two endemic species of land snails, Mandarina mandarina and M. chichijimana, have discrete distributions separated by a hybrid zone. This study investigates the potential of hybridization as a source of morphological novelty in these snails. Mandarina mandarina possesses a shell with a higher whorl expansion rate and a smaller protoconch than M. chichijimana, relative to shell size. The number of whorls and shell size of M. mandarina do not differ from those of M. chichijimana, because the effect of higher expansion rate on number of whorls and size of the former is compensated for by its smaller protoconch. The whorl expansion rate and protoconch diameter of the individuals from the hybrid populations are intermediate or typical of either of the two species, and their average values show clinal changes along the hybrid zone. However, the hybrid populations include exceptionally high shells with many whorls and flat shells with few whorls, which are never found in the pure populations of either species. In addition, gradual increases in variance in shell height and number of whorls were found from the edges to the center of the hybrid zone. A combination of low expansion rate (typical of M. chichijimana) and a small protoconch (typical of M. mandarina) produces a shell with an extremely large number of whorls because of the geometry of shell coiling. However, the combination of high expansion rate and a large protoconch produces a shell with an extremely small number of whorls. Because of the correlation between the number of whorls and shell height, shells with an exceptional number of whorls possess an extraordinarily high or flat spire. Hybrids can inherit a mosaic of characters that, as they play out during growth, lead to novel adult morphologies. These findings emphasize the importance of hybridization as a source of morphological variation and evolutionary novelty in land snails.     

Reproduction and larval development of the gastropod <Emphasis Type="Italic">Cryptonatica janthostoma</Emphasis> (Gastropoda: Naticidae)

The larval morphology of the gastropod Cryptonatica janthostoma inhabiting the Northwest Pacific was described for the first time. Hatched planktotrophic veligers of C. janthostoma had shells 250 μm in height with 0.8 whorls, a bilobate velum with a dark brown pigmentation band shaped along its edge, pair of eye spots, tentacles and statocysts. The surface of the embryonal shell (protoconch 1) was covered with fine granules extended at the dorsal side and rounded at lateral surfaces. Concentric crests and growth lines occurred on part of the shell of late free-swimming larvae (protoconch 2) The velum of the C. janthostoma larvae remained bilobate during the pelagic stage of development, whereas it was divided in 4 lobes during larval development in most of the other species of the Naticidae family. The veliger of C. janthostoma was similar to that of Natica montagu from Danish waters [16] by its shape, pigmentation, shell sculpture and velum structure.     

Interference and exploitation components in interespecific competition between sympatric intertidal hermit crabs

This study was designed to evaluate the effect of interference and exploitation competition in shell partitioning between two hermit crab species (Pagurus criniticornis and Clibanarius antillensis). Field samples revealed that shells of the gastropod Cerithium atratum were the main resource used by both hermit crab species and that Pagurus used eroded or damaged shells in higher frequency than Clibanarius. The exploitative ability of each species was compared between species in the laboratory using dead gastropod (Cerithium) baits to simulate predation events and signalize newly available shells to hermit crabs. Pagurus reached the baits more rapidly than Clibanarius, but this higher exploitative ability did not explain shell utilization patterns in nature. Another experiment evaluated the dominance hierarchy between these two hermit crab species and revealed that Clibanarius was able to outcompete Pagurus for higher quality shells in agonistic encounters. This higher interference competitive ability of Clibanarius in relation to Pagurus may explain field observations. Nevertheless, Pagurus may be responsible to enhance shell availability to other hermit crab species that have lower ability to find and use newly available shells. Differently, the poorer condition of shells used by Pagurus, the higher ability of this species to attend gastropod predation events and its higher consumption rate by shell-breaking crabs (Menippe nodifrons) may increase its predation risks, thus revealing the disadvantages of such an exploitative competitive strategy for hermit crabs.     

Land hermit crab (Coenobita clypeatus) densities and patterns of gastropod shell use on small Bahamian islands

Aim To examine patterns of abundance, density, size and shell use in land hermit crabs, Coenobita clypeatus (Herbst), occurring on three groups of small islands, and to determine how these variables change among islands. Location Small islands in the Central Exuma Cays and near Great Exuma, Bahamas. Methods Land hermit crabs were captured in baited pitfall traps and were separately attracted to baits. A mark–recapture technique was used in conjunction with some pitfall traps monitored for three consecutive days. The size of each crab and the type of adopted gastropod shell were recorded, along with physical island variables such as total island area, vegetated area, island perimeter, elevation and distance to the nearest mainland island. Results Relative abundances, densities and sizes of crabs differed significantly among the three island groups. Densities of land hermit crabs were as high as 46 m⁻² of vegetated island area. In simple and multiple linear regressions, the only variable that was a significant predictor of the abundance of hermit crabs was the perimeter to area ratio of the island. Patterns of gastropod shell use varied significantly among the island groups, and the vast majority of adopted shells originated from gastropod species that inhabit the high intertidal and supratidal shorelines of the islands. Main conclusions Although densities of land hermit crabs varied, they were relatively high on many islands, and land hermit crabs may play an important role in these insular food webs. Patterns of shell use may be strongly restricted by island geomorphology: irregular shorelines provide relatively more habitat for the gastropod species that account for the majority of adopted shells and the steep sides of the islands prevent the accumulation of marine gastropod shells. The size of adult hermit crabs appears to be limited by the relatively small gastropod shells available, while the abundance of hermit crabs may be limited by the number of shells available.     

Shell preference and utilization patterns in littoral hermit crabs of the bay of Panama

Shell utilization patterns of three sympatric hermit crab species from the Bay of Panama are examined. Shell preferences, as shown by laboratory choice experiments and the selective use of empty shells experimentally added to hermit crab populations, are shown to be important determinants of shell utilization under natural conditions.Factors which influence the types and sizes of shells occupied by hermit crabs in separate populations include: (1) the presence and relative abundance of different gastropod species; (2) the specific shell preferences of different hermit crab species; and (3) the presence and relative abundance of sympatric hermit crab competitors for the limited supply of empty shells. Since the size and type of shell occupied by a hermit crab influences its growth rate and reproductive output, these factors appear to have a direct effect on hermit crab fitness and the demographic structure of separate hermit crab populations.     

Do predatory drill holes influence the transport and deposition of gastropod shells?

Predatory gastropod drill holes are an abundant and easily identifiable signal of predation in ancient and modern molluscan shell assemblages. Many workers have used drill holes to interpret patterns of predation intensity and success in fossil assemblages. These studies are predicated on the assumption that the relative abundances of drilled and undrilled shells in an assemblage accurately reflect those of the community from which the shells were originally derived. The underlying assumption is that drilled and undrilled shells are transported into shell accumulations in the same manner. If this assumption is false, shell accumulations do not represent taphonomically unbiased samples, but rather preferentially sorted deposits from which conclusions about drilling predation cannot be made. To test the hypothesis that drilled and undrilled gastropod shells transport at different flow velocities, multiple transport trials were conducted on two morphologically distinct taxa, Olivella biplicata and Euspira lewisii. Individual specimens were placed in a recirculating flume tank and observed from rest (in stable orientation) until they were transported downstream. During each trial, flow velocity was slowly and incrementally increased, so as to avoid pulses of acceleration, until shells began to move downstream. Drilled and undrilled specimens of both taxa demonstrate statistically significant correlations between shell mass and average transport velocity. Similarly sized drilled and undrilled specimens of both taxa do not exhibit significant differences in transport velocity. These results indicate that predatory drill holes do not change the hydrodynamic properties of gastropod shells. Therefore, gastropod shell assemblages are not likely to be affected by differential transport and sorting of drilled and undrilled shells.     

Shell alterations in the limpet Bostrycapulus odites: A bioindicator of harbour pollution and mine residuals

Molluscs are commonly used as bioindicators because of their abundance, low motility and the information their shells record. Although in harbour areas gastropod shell deposition would be affected at an endocrinal level, which may increase their vulnerability, studies on the shell of gastropods are scarce. Bostrycapulus odites is a limpet species that possess those characteristics as well as a wide distribution. Limpets were collected in 2001 and 2011, in a channel polluted by both, harbour activities and leaching mine residuals, to compare to a 2011 sample from an unpolluted area within San Antonio Bay. The sensitivity to pollution of this species and the possibility of it use to detect changes in the environmental situation of an area in a 10 years period were investigated. Soft body wet weight and shell morphological variables were measured while shells were also analyzed through scanning electron microscopy and energy dispersive spectroscopy for microstructure and elemental composition, respectively. Maximum likelihood ratio test showed shells from the polluted channel were thicker as well as the same shells presented microstructure malformations and changes in elemental composition (lower Ca and O levels, higher C and Fe levels). The present results indicate that B. odites can be considered a useful bioindicator species to study these kinds of pollution and the potential processes implicated in shell alterations are discussed.     

Ontogenic tracks and evolutionary vestiges in morphospace

Strombid shells were used to exemplify how to construct ontogenic tracks and evolutionary vestiges in morphological space (morphospace). Parameters in a mathematical model of shell form were used to construct morphospaces. Ontogenic information was mapped into these morphospaces to form 'tracks' Ontogenic tracks showed that the predominant trend of morphological evolution of strombid species consisted of an increase of vertical dimensions of whorls (apertures). Integrating information extracted from cladograms with ontogenic tracks in morphospace, 'evolutionary vestiges' were determined and used to infer and reconstruct ancestral shell forms.     

Shell shape affects movement patterns and microhabitat distribution in the hermit crabs Calcinus elegans, C. laevimanus and C. latens

This study examined the influence of shell shape on the distribution and movement patterns of three species of Hawaiian hermit crabs: Calcinus elegans, C. laevimanus, and C. latens. Field surveys showed strong differences in shell use depending on habitat. Individuals of C.elegans and C. latens were more frequently in unusual shapes of shells (the cowrie Cypraea caputserpentis and the variable worm shell Serpulorbis variabilis) when in tide pools and in more standard gastropod shells, such as the dog whelk Nassarius papillosus, when found in the subtidal. In addition, for both C.elegans and C. latens in tide pools, most crabs in unusual shaped shells were out on top of rocks, whereas most crabs in shells that were standard shapes were under rocks.In the laboratory, individuals of C.elegans and C. laevimanus in unusual shells initiated more shell exchanges and when given empty shells crabs readily occupied the standard shaped shells, but crabs did not move into the unusual shaped shells. Mark-recapture experiments in the field showed that C. elegans in standard shaped shells moved out of tide pools and stayed longer when placed on subtidal coral heads, whereas crabs in unusual shaped shells stayed in tide pools and did not stay on subtidal coral heads (in part due to predation). Laboratory tests showed that C. elegans in unusual shaped shells were more readily dislodged by surge than crabs in standard shaped shells. Thus, the difference in movement patterns in preferred vs. unpreferred shell shapes is an important factor influencing the microhabitat distribution of these hermit crabs.     

Export of non-native gastropod shells to a coastal lagoon: Alteration of habitat structure has negligible effects on infauna

Alteration of physical habitat structure is a fundamental mechanism by which invaders produce ecosystem level effects. We assessed whether, along the east coast of Australia, the impacts of the non-native gastropod Maoricolpus roseus on soft-sediment habitats extend beyond the range of live populations as a result of shell export following death of animals. Sampling over an 18 month period revealed that M. roseus shells were temporally persistent in surface sediments of a coastal lagoon devoid of live populations of the gastropod. The well-preserved shells, of which 92% were entire, did not accumulate above a maximal density of 260 m^− 2 due to periodic burial. Manipulation of M. roseus shell densities indicated that at densities (140 m^− 2) presently experienced within surface sediments of the lagoon, the structure provided by the shells was weakly facilitative of some invertebrate species. Further increasing shell densities to the possible future scenario of 280 m^− 2, which may occur under continued expansion of nearby live populations did not, however, strengthen positive effects. To the contrary, plots with higher densities of M. roseus shells contained similar invertebrate assemblages to control plots, without shells. Consistent with the negligible effects of M. roseus shells on infauna, the foraging efficiency of the generalist predator, Carcinus maenas, and the naticid gastropod, Polinices sordidus, were not affected by addition of shells. Surprisingly, even an extreme scenario of 1600 m^− 2 did not affect their predation. Thus, in this dynamic coastal lagoon, that experiences considerable sediment movement and environmental variability, the structure introduced by import of non-native shells is unimportant in structuring soft-sediment communities. Whether this unrecognised aspect of molluscan invasions impacts the ecology of more stable coastal environments remains unclear and warrants further consideration.