Scale-dependence in geographic variation in a freshwater gastropod across the Palearctic

ABSTRACT

The reality of spatial clinal variation in morphological traits of freshwater pulmonate snails (Gastropoda: Pulmonata) has repeatedly been questioned or totally discounted. There is a lack of sound statistical evidence in the articles hitherto published on this subject supporting these claims. Here, by means of different analytical methods (analysis of spatial autocorrelation, linear regression analysis, canonical correlation analysis and others), we demonstrate that shell variation in the dwarf pond snail, Galba truncatula, is patterned in space throughout the northern and central Palearctic, with latitudinally-oriented clines in body size and in some shell proportions. Shell size in G. truncatula decreases with latitude and temperature, representing a special case of converse Bergmann cline. However, the temperature itself is hardly the main driver of shell size variation. It is argued that the shorter growing seasons at high latitudes may represent a better explanation for the observed trend. Shell proportions in the dwarf pond snails vary weakly at the macrogeographic scale, being spatially patterned at lower (mesogeographic) scales around 1200–1500?km. In general, spatial variation in G. truncatula shell size is decoupled from variation in shell shape, demonstrating clear scale-dependence similar to that found in different species of terrestrial (non-aquatic) pulmonate snails.     

Evolution of cell-to-cell communication and the structural brain organization

The review considers key issues of historical development of the nervous system, including evolution of the brain intercellular contacts and neurotransmitter systems. Special attention is given to the structural-functional organization of the central nervous system in a freshwater pulmonate gastropod, Lymnaea stagnalis.     

Metabolic rate depression in a marine pulmonate snail: pre-adaptation for a terrestrial existence?

Summary Terrestrial and freshwater pulmonate snails exhibit a marked depression of aerobic metabolism during estivation. This is an adaptation for existence in periodically harsh environments and, though marine gastropods may undergo anaerobic metabolism, they have not been shown to adaptively depress aerobic metabolic rate. We compared the metabolic response to progressive aerial exposure of two intertidal gastropod limpets, a prosobranch and a pulmonate. The prosobranch Patella granularis maintained a constant heart rate until shortly before death. In contrast, the pulmonate Siphonaria oculus underwent facultative depression of heart rate, accompanied by a decline in oxygen consumption. Both heart rate and oxygen consumption returned to normal levels on reimmersion in water. Metabolic rate depression is energy conserving, and may account for the ability of S. oculus to extend higher up the shore than P. granularis, into areas where food availability is low. S. oculus is a primitive, marine pulmonate, periodically subject to harsh conditions, and its capacity for metabolic rate depression may represent a pre-adaptation for life on land.     

Pleural-buccal interneurons in the pteropod mollusc Clione limacina

Paired, Phe-Met-Arg-Phe-NH₂-ergic pleural-to-buccal projecting neurons of the pleural ganglia were suggested to be responsible for feeding arrest associated with defensive withdrawal in freshwater and terrestrial pulmonate molluscs. In the present study, the pleural-to-buccal projecting cells were, for the first time, identified in a representative opisthobranch, the carnivorous marine pteropod Clione limacina. Two symmetric neurons of its pleural ganglia were found to be similar to the pulmonate pleural-to-buccal projecting neurons in the number of neurons, positions of their cell bodies in the central nervous system, a unique, indirect route of their axon, electrotonic coupling of the left and right cells, and expression of Phe-Met-Arg-Phe-NH₂-like immunoreactivity and inhibitory action on neurons participating in the motor program for feeding. In their turn, pleural-to-buccal projecting neurons receive excitatory inputs from the protractor interneurons involved in the feeding rhythm generation. Also, it was demonstrated that the pleural-to-buccal projecting cells activity positively correlates with spontaneous and induced acceleration of the locomotor rhythm. Accordingly, stimulation of the cerebral command neuron for locomotion, cell CPA1, excited pleural-to-buccal projecting neurons. We conclude that the neuronal network underlying feeding behavior in both pulmonate and opisthobranch molluscs is similarly linked to defensive behavior by pleural Phe-Met-Arg-Phe-NH₂-ergic neurons, thus indicating evolutionary conservation of these pleural-buccal projections. Accepted: 22 June 1999     

Biology of Latia neritoides Gray 1850 (Gastropoda,Pulmonata, Basommatophora): the Only Light-producing Freshwater Snail in the World

This report on the freshwater pulmonate basommatophoran Latia neritoides of the North Island of New Zealand is based on field and laboratory studies. It deals with aspects of the habitat, describes biological adaptations of organs and organ systems in Latia, reviews the chemical basis of bioluminescence in this species, discusses the possible roles of light production in Latia, and addresses zoogeographic and phylogenetic questions.     

Dragonfly predators influence biomass and density of pond snails

Studies in lakes show that fish and crayfish predators play an important role in determining the abundance of freshwater snails. In contrast, there are few studies of snails and their predators in shallow ponds and marshes. Ponds often lack fish and crayfish but have abundant insect populations. Here we present the results of field surveys, laboratory foraging trials, and an outdoor mesocosm experiment, testing the hypothesis that insects are important predators of pulmonate snails. In laboratory foraging trials, conducted with ten species of insects, most insect taxa consumed snails, and larval dragonflies were especially effective predators. The field surveys showed that dragonflies constitute the majority of the insect biomass in fishless ponds. More focused foraging trials evaluated the ability of the dragonflies Anax junius and Pantala hymenaea to prey upon different sizes and species of pulmonate snails (Helisoma trivolvis, Physa acuta, and Stagnicola elodes). Anax junius consumed all three species up to the maximum size tested. Pantala hymenaea consumed snails with a shell height of 3 mm and smaller, but did not kill larger snails. P. acuta were more vulnerable to predators than were H. trivolvis or S. elodes. In the mesocosm experiment, conducted with predator treatments of A. junius, P. hymenaea, and the hemipteran Belostoma flumineum, insect predators had a pronounced negative effect on snail biomass and density. A. junius and B. flumineum reduced biomass and density to a similar degree, and both reduced biomass more than did P. hymenaea. Predators did not have a strong effect on species composition. A model suggested that A. junius and P. hymenaea have the largest effects on snail biomass in the field. Given that both pulmonate snails and dragonfly nymphs are widespread and abundant in marshes and ponds, snail assemblages in these water bodies are likely regulated in large part by odonate predation.     

Food selection by freshwater snails in the Gezira irrigation canals,Sudan

Stomach content analysis was carried out on samples of the freshwater snail species Biomphalaria pfeifferi, Bulinus truncatus, Bulinus forskalii (Pulmonata, Planorbidae), Lymnaea natalensis (Pulmonata, Lymnaeidae), Melanoides tuberculata, Cleopatra bulimoides (Prosobranchia, Thiaridae) and Lanistes carinatus (Prosobranchia, Ampullariidae) from different irrigation canals in Sudan. In order to evaluate overlap in diet selection among these species, sites with two or more of the above-mentioned species present were selected. For some species food choice was examined in relation to size groupings. In addition, samples of Marisa cornuarietis (Prosobranchia, Ampullariidae) from small ponds in Sudan, samples of Biomphalaria pfeifferi and Helisoma duryi (Pulmonata, Planorbidae) from drainage canals in an irrigation scheme in northern Tanzania, and samples of H. duryi from fish ponds in the coastal area of Kenya were also analysed. The results indicate a great similarity in the food choice of these species, especially among the pulmonate species. All species feed on fine detritus, epiphytic algae and decaying macrophytes. No fresh fragments of aquatic macrophytes were found and animal remains were found only on a few occasions. However, the stomach contents of the ampullarid species were characterized by large fragments of dead macrophyte tissue, while the composition of the finer particles showed a great resemblance to that of the pulmonate species. The diet of the thiarid species is essentially the same as that of the pulmonate species, although in one site Cleopatra bulimoides showed a greater preference for green algae. Apart from the avoidance of blue-green algae, there was little evidence of selection of certain algal components of the Aufwuchs for the pulmonate species. Detritus constitutes the major component of the stomach content of all these snail species.     

The role of shell strength in selective foraging by crayfish for gastropod prey

1. Four gastropods common in Wisconsin lakes, Amnicola limosa, Gyraulus parvus, Physella gyrina and Helisoma anceps, were exposed to predation by three crayfish congeners, Orconectes rusticus, O. propinquus and O. virilis in the laboratory to determine prey preference. 2. There were no differences in prey choice among the crayfish congeners, but there were clear differences in electivity for the different snail prey. 3. Crayfish had higher electivities for the thin-shelled, plano-spiral pulmonate Gyraulus parvus, despite its lower abundance in samples, than the thicker-shelled prosobranch Amnicola limosa. Electivity for another plano-spiral pulmonate, Helisoma anceps, was low, evidently because of its relatively thick shell and larger size. Amnicola limosa and the thin-shelled pulmonate Physella gyrina (present at roughly the same relative abundance as Gyraulus parvus) were neither selected nor avoided. 4. Crayfish electivity appears to be a function of the resistance of shells to chipping by crayfish mandibles. Although different species are preferred, this is similar to the previously described selection of thin-shelled species by sunfish.     

Possible functions of Dpp in gastropod shell formation and shell coiling

We examined dpp expression patterns in the pulmonate snail Lymnaea stagnalis and analyzed the functions of dpp using the Dpp signal inhibitor dorsomorphin in order to understand developmental mechanisms and evolution of shell formation in gastropods. The dpp gene is expressed in the right half of the circular area around the shell gland at the trochophore stage and at the right-hand side of the mantle at the veliger stage in the dextral snails. Two types of shell malformations were observed when the Dpp signals were inhibited by dorsomorphin. When the embryos were treated with dorsomorphin at the 2-cell and blastula stages before the shell gland is formed, the juvenile shells grew imperfectly and were not mineralized. On the other hand, when treated at the trochophore and veliger stage after the shell gland formation, juvenile shells grew to show a cone-like form rather than a normal coiled form. These results indicated that dpp plays important roles in the formation and coiling of the shell in this gastropod species.     

Physiologic and environmental factors influencing the calcium-to-tissue ratio in populations of three species of freshwater pulmonate snails

Summary A study of three species of freshwater pulmonate snails, Physa gyrina (11 populations), Physa integra (17 populations), and Helisoma anceps (18 populations) was carried out from 1973 to 1976, primarily in Michigan.The ratio of whole animal calcium content to tissue dry weight (Ca: tissue ratio) changes with age, but these changes are largely restricted to early growth and do not significantly affect individuals over 40 mg total dry weight, regardless of species.Parasitization by larval trematodes was found to have no significant effect on the Ca: tissue ratio in the populations examined regardless of species.Ca: tissue ratio of P. gyrina did not vary greatly between populations and showed a narrow range over a wide range of environmental calcium concentrations. Shell mass in P. gyrina is therefore either physiologically regulated in all populations (at a species specific constant level) or interpopulation variation is minimized by moderately high levels of gene flow between populations.There was no relationship between Ca: tissue ratio and environmental calcium for either P. integra or H. anceps over a wide range of snail and environmental calcium values. In both of the foregoing species, shell calcium content varied greatly between populations. This variation did not conform to any apparent geographic cline.In 7 of the population sites studied, P. integra and H. anceps coexist, and when these sites are listed from highest to lowest Ca: tissue ratios, the rank orders for the two species are nearly identical. This suggests that there is some environmental factor (possibly trophic conditions) at these localities that influences shell mass.In 8 other species of pulmonates briefly examined, differences in Ca: tissue ratio between populations of the same species were often as great as or greater than differences between species.While the patterns of shell mass and environmental calcium for these species are not unlike those previously reported, the proposed causal factors for these patterns are clearly distinct from those suggested for other freshwater pulmonates.     

Y-axis orientation in the South American freshwater snail species Chilina patagonica (Gastropoda: Chilinidae)

Y-axis orientation, a movement perpendicular to the shore or coastline, enables aquatic animals to stay in a preferred zone in generally unstable habitats. Such behaviour is a widespread phenomenon in many freshwater and intertidal animal taxa. In the present study, an arena approach was used to test the orientation response of pulmonate freshwater snails. Using this experimental design, Y-axis orientation was shown for the first time in a freshwater snail species, the riverine Chilina patagonica. Some cues, potentially mediating Y-axis orientation, appeared to play no role in the shown orientation behaviour, such as chemical, gravity and humidity cues or a sun compass. Magnetic cues, however, could not be excluded. Since no significant differences in orientation were detected between different size classes in C. patagonica, orientation behaviour may not vary substantially throughout the snail's life history. In contrast to C. patagonica, no consistent orientation response was seen in the related lacustrine species Chilina llanquihuensis. The adaptation of C. patagonica to exhibit orientation along the Y-axis may be driven by the avoidance of high velocities in deeper water.     

The effects of calcium in mediating the inducible morphological defenses of a freshwater snail,Physa acuta

Predation risk is known to induce numerous, often adaptive, plastic changes in the morphology, life history, and behavior of prey. However, little is known about how abiotic factors such as environmental nutrient availability affect these responses. In this experiment, a freshwater pulmonate snail (Physa acuta) was used to determine how predator-induced shell morphology was affected by the availability of an abiotic nutrient important for shell growth (calcium). Each snail was reared individually in a factorial experiment consisting of two predator treatments (chemical cues from crayfish present or absent) and three calcium concentrations (20, 45, or 70 mg/L). Calcium induced larger, heavier, and thicker shells, while predator cues induced heavier and thicker shells. Importantly, the magnitude of the predator effect on shell thickness (i.e., the inducible defense) increased with additional calcium availability. Our results demonstrate the importance of nutrient availability in mediating and limiting the amount of adaptive predator-induced plasticity.     

Volatility in the effective size of a freshwater gastropod population

Despite the utility of gastropod models for the study of evolutionary processes of great generality and importance, their effective population size has rarely been estimated in the field. Here, we report allele frequency variance at three allozyme‐encoding loci monitored over 7 years in a population of the invasive freshwater pulmonate snail Physa acuta (Draparnaud 1805), estimating effective population size with both single‐sample and two‐sample approaches. Estimated N_e declined from effectively infinite in 2009 to approximately 40–50 in 2012 and then rose back to infinity in 2015, corresponding to a striking fluctuation in the apparent census size of the population. Such volatility in N_e may reflect cryptic population subdivision.     

An experimental investigation of interactions in snail-macrophyte-epiphyte systems

Summary An experimental investigation under field conditions of enclosures containing freshwater pulmonate snails, the macrophyteCeratophyllum demersum and epiphytes, produced evidence of beneficial interactions.Ceratophyllum growth, measured in terms of stem length, numbers of leaf-nodes and growing tips and leaf survival was significantly enhanced in the presence of snails. This effect was attributed to the increased availability of plant nutrients of snail origin, such as phosphates and ammonia, as well as to the snails' action as “cleaning symbionts” in reducing the density of bacterial and algal epiphyton potentially deleterious to macrophytes. Principal component analysis revealed both seasonal and treatment effects of snail grazing on algal epiphyton. Small adnate algal species (e.g.Cocconeis placentula) survived grazing and benefited from the removal of larger, competitor, species. Snail densities increased in all treatments, despite high (86%) juvenile mortality. It is concluded that freshwater pulmonate snails are strong interactors in lentic habitats, enhancing the growth ofCeratophyllum and producing characterisic epiphyte communities. This benefits not only the snails, but also the plants and epiphytes that are associated with them. Thus the interactions between these component parts of the community can be considered as mutualistic.     

The Heritability of Shell Morphometrics in the Freshwater Pulmonate Gastropod Physa

The cosmopolitan freshwater pulmonate snail Physa acuta hybridizes readily with Physa carolinae in the laboratory, although their F1 progeny are sterile. The two species differ qualitatively in shell shape, the former bearing a more globose shell and the latter more fusiform. We performed a hybridization experiment, measuring a set of 14 traditional (linear) and landmark-based shell morphological variables on even-aged parents and their offspring from both hybrids and purebred control lines. Parent-offspring regression yielded a strikingly high heritability estimate for score on the first relative warp axis, h² = 0.819 ± 0.073, a result that would seem to confirm the value of geometric morphometrics as a tool for retrieving evolutionary relationships from gastropod shell form. Score on the second relative warp axis was also significantly heritable (h² = 0.312 ± 0.123), although more moderate, as were scores on second principal components extracted from traditional measurements (correlation h² = 0.308 ± 0.069, covariance h² = 0.314 ± 0.050). Although score on the first relative warp axis was significantly correlated with centroid size (p < 0.001), scores on none of the three second axes were so correlated. This result suggests that second axis score might prove especially useful for estimating genetic divergence among mixed-age populations of gastropods sampled from the field.     

Correspondence analysis of shell morphology in the African freshwater snail Biomphalaria pfeifferi (Kraus 1848) (Pulmonata: Gastropoda)

A correspondence analysis of shell measurements taken from 521 widely dispersed specimens of the African aquatic pulmonate snail Biomphalaria pfeifferi suggests the existence of eight morphological groups. These groups appear to relate to either ecophysiological factors or to factors associated with the stability of the freshwater system rather than to aspects of geographic distribution and genetic isolation.     

Osmotic Balance in a Marine Pulmonate,Amphibola crenata

The pulmonate mud‐snail Amphibola crenata is an osmoconformer in 25%‐125% sea water, its haemolymph being slightly hyperosmotic and hyperionic to the medium. It maintains its haemolymph markedly hyperosmotic in media below 25% sea water and in freshwater, in which it survives for a week or longer. On exposure to dilute or concentrated media, water which enters or leaves the tissues preferentially enters or leaves the cells. Regulation of cell volume towards initial values is accomplished within 5 days. Measurements of changes in cell volume, and of distribution of tissue water between the intracellular and extracellular compartments, in snails moved from 100% sea water into dilute or concentrated media, and in snails moved back to 100% sea water, indicate that mechanisms of cell volume regulation are minimal in ca 60–65% sea water. Changes in the concentration of tissue free amino acids are in accord with current theories of mechanisms of isosmotic intracellular regulation. The results are discussed in the light of the taxonomic, evolutionary and ecological status of Amphibola as a shore‐living, primitive, marine representative of a predominantly terrestrial and freshwater group of gastropod molluscs.     

Evidence of predation in Early Cretaceous unionoid bivalves from freshwater sediments in the Cameros Basin,Spain

Here, we present evidence of possible vertebrate predation on freshwater bivalves from the Lower Cretaceous strata of the Cameros Basin (Spain). The described collection contains the largest number of vertebrate‐inflicted shell injuries in freshwater bivalve shells yet reported in the Mesozoic continental record. Several types of shell damage on fossil shells of Protopleurobema numantina (Bivalvia: Unionoida) are described and their respective modes of formation interpreted in the context of morphological attributes of the shell injuries and the inferred tooth morphology of predators that could have inflicted such injuries. Detailed study of these bite marks shows similarities with the well‐documented injuries in the shells of marine molluscs, namely ammonoids, that have likewise been attributed to reptilian predators. The most parsimonious interpretation suggests crocodiles as the vertebrates interacting with the bivalves in the Cameros Basin. □Barremian–Aptian; bite marks; freshwater bivalves; predation; reptile; Unionoida.     

Macro-invertebrate predators of freshwater pulmonate snails in Africa,with particular reference to Appasus grassei (Heteroptera) and Procambarus clarkii (Decapoda)

A range of African and alien macro-invertebrates has been reported preying on freshwater pulmonate snails, including those that serve as intermediate hosts for bloodflukes of the genus Schistosoma. Predation by five molluscivorous taxa is reviewed here: indigenous leeches (Glossiphoniidae), marsh fly larvae (Sciomyzidae), waterbugs (Belostomatidae), crabs (Potamonautidae) and invasive crayfish (Astacidae). Common features are a lack of prey specificity but clear prey-size specificity. Attention is drawn to the ability of invasive snail species (Physidae and Lymnaeidae) to avoid predation by several of these taxa. Evidence suggests that only the alien invasive crayfish Procambarus clarkii has potential as a snail biocontrol agent, but that its use should not be encouraged.     

Tuning in to multiple predators: conflicting demands for shell morphology in a freshwater snail

1. We examined the response to chemical cues from fish and crayfish, two predators with contrasting feeding modes, and their single and combined effect on shell morphology in the freshwater snail Radix balthica. 2. Snails were subjected to four treatments: tench (Tinca tinca), signal crayfish (Pacifastacus leniusculus), a combination of tench and signal crayfish and no predators (control). Shell shape, crushing resistance and shell thickness were quantified. We also analysed whether shape or shell thickness contributes most to crushing resistance. 3. Chemical cues from the fish induced a rounder shell shape in R. balthica, a thicker shell and a higher crushing resistance, whereas crayfish chemical cues had no effect on shell morphology, shell thickness or crushing resistance. Shell shape contributed more to crushing resistance than shell thickness. 4. The combined predator treatment showed an intermediate response between the fish and crayfish treatments. Shell roundness was reduced compared with the fish treatment, but the reduced crushing resistance that comes with a less rounded shell was compensated by an increased investment in extra shell material, exceeding that of the fish treatment. 5. Our study extends previous studies of multipredator effects on phenotypically plastic freshwater snails by showing that the snails are able to fine‐tune different elements of morphology to counter predator‐specific foraging modes.