Density fluctuations in populations (1982–1986) and biological observations ofPotamopyrgus Jenkinsi in two trophically differing lakes

The hydrobiid snailPotamopyrgus jenkinsi (E.A. Smith), characterized by parthenogenesis and ovovivipary, was quantitatively sampled monthly between June, 1982, and December, 1986, on sandy bottoms in the shallow zones of the meso-oligotrophic Lake Maarsseveen I and the eutrophic Lake Maarsseveen II. The snail demonstrated a very clumped distribution in both lakes. The mean numbers of juveniles and adults taken together fluctuated strongly. Organisms in Lake I showed relatively high densities (up to 25,000 per m²) in 1982, followed by a sudden drop to values approaching zero in December, 1982, with a subsequent rapid increase in densities, fluctuating between 2,000 and 200 per m². In Lake II, densities of snails fluctuated between 13,000 and 300 per m² with decreases in the spring of 1985 and 1986. The various types of decreases in the lakes are extensively discussed, but no explanation is presently available. The reduction in Lake I was of catastrophic proportions, but the speed of recovery of the population was remarkable.Floating was observed only in Lake I, and only during the occurrence of the highest densities on the sediment. Burrowing behaviour was very common, but strongly suppressed under an uninterrupted dark regime. A shift of temperature from 15 to 22°C had the same effect. A number of submerged macrophyte species from Lake I proved to attractP. jenkinsi in the absence of sandy substrate, though these plants were only covered by the snail during the period of the highest densities in 1982. Temperatures of 20°C or lower were well tolerated, unlike temperatures of 25 and 30°C. Growth was distinct at 10, 15 and 20°C. Keeled individuals were encountered in much higher numbers in Lake I than in Lake II.     

Male phenotypes in a female framework: Evidence for degeneration in sperm produced by male snails from asexual lineages

How changes in selective regimes affect trait evolution is an important open biological question. We take advantage of naturally occurring and repeated transitions from sexual to asexual reproduction in a New Zealand freshwater snail species, Potamopyrgus antipodarum, to address how evolution in an asexual context—including the potential for relaxed selection on male‐specific traits—influences sperm morphology. The occasional production of male offspring by the otherwise all‐female asexual P. antipodarum lineages affords a unique and powerful opportunity to assess the fate of sperm traits in a context where males are exceedingly rare. These comparisons revealed that the sperm produced by ‘asexual’ males are markedly distinct from sexual counterparts. We also found that the asexual male sperm harboured markedly higher phenotypic variation and was much more likely to be morphologically abnormal. Together, these data suggest that transitions to asexual reproduction might be irreversible, at least in part because male function is likely to be compromised. These results are also consistent with a scenario where relaxed selection and/or mutation accumulation in the absence of sex translates into rapid trait degeneration.     

A layover in Europe: Reconstructing the invasion route of asexual lineages of a New Zealand snail to North America

Non‐native invasive species are threatening ecosystems and biodiversity worldwide. High genetic variation is thought to be a critical factor for invasion success. Accordingly, the global invasion of a few clonal lineages of the gastropod Potamopyrgus antipodarum is thus both puzzling and has the potential to help illuminate why some invasions succeed while others fail. Here, we used SNP markers and a geographically broad sampling scheme (N = 1617) including native New Zealand populations and invasive North American and European populations to provide the first widescale population genetic assessment of the relationships between and among native and invasive P. antipodarum. We used a combination of traditional and Bayesian molecular analyses to demonstrate that New Zealand populations harbour very high diversity relative to the invasive populations and are the source of the two main European genetic lineages. One of these two European lineages was in turn the source of at least one of the two main North American genetic clusters of invasive P. antipodarum, located in Lake Ontario. The other widespread North American group had a more complex origin that included the other European lineage and two New Zealand clusters. Altogether, our analyses suggest that just a small handful of clonal lineages of P. antipodarum were responsible for invasion across continents. Our findings provide critical information for prevention of additional invasions and control of existing invasive populations and are of broader relevance towards understanding the establishment and evolution of asexual populations and the forces driving biological invasion.     

Pleistocene glaciation is implicated in the phylogeographical structure of Potamopyrgus antipodarum, a New Zealand snail

Pleistocene glaciation has been identified as an important factor shaping present-day patterns of phylogeographical structure in a diverse array of taxa. The purpose of this study was to use mitochondrial sequence data to address whether Pleistocene glaciation is also a major determinant of phylogeographical patterns in Potamopyrgus antipodarum, a freshwater snail native to New Zealand. We found that haplotypes were separated by no more than 3.7% sequence divergence, and major genetic divisions tended to occur on a north-south axis. These data fit the predictions of the hypothesis that isolation of P. antipodarum in glacial refugia at the northern and southern tip of the South Island of New Zealand during the Pleistocene glaciation underlies the present-day phylogeographical structure. Because sexual P. antipodarum occasionally produce asexual offspring, we also used these data to show that the appearance of asexuality is not phylogeographically constrained. This means that the maintenance of sex in P. antipodarum cannot be wholly due to limited contact between sexual and asexual lineages and must instead be linked to a selective advantage of sexual reproduction.     

Development,validation and comparison of LC–MS/MS and RIA methods for quantification of vertebrates-like sex-steroids in prosobranch molluscs

The role of vertebrate-like sex-steroids (testosterone, T, progesterone, P, and 17β-estradiol, E2) in molluscs is still debated, but they could represent potential biomarkers of endocrine disruption. A radioimmunoassay (RIA) and a liquid chromatography coupled to tandem mass spectrometry (LC–MS/MS) methods have been developed and compared to measure their levels in a gastropod snail Potamopyrgus antipodarum. Both methods showed a good reproducibility despite the complex matrix and the very low levels of vertebrate-like sex-steroids. Only T and P were detected using the LC–MS/MS method, while the RIA method reached lower detection limits and enabled the detection of all three steroids. Results indicated that T and P were mainly present as unconjugated forms. Both methods were compared in the analysis of snails exposed to waste water treatment plant effluents and led to the same conclusions concerning the modulation of steroids levels. Moreover, they both were in agreement concerning T measurements. On the other hand, LC–MS/MS appeared to be more suitable when analyzing P levels due to a low sensitivity of the RIA method. As E2 was not measured using the LC–MS/MS method because of a higher detection limit compared to the other steroids, the results obtained with the RIA method should be interpreted with caution. LC–MS/MS remains the gold standard for sex-steroid determinations, however a relevant and alternative method based on RIA was developed, requiring fewer organisms. RIA seems a promising method as a screening tool for experimental use, allowing comparison of sex-steroid levels in the mudsnail both in laboratory and in field experiments.     

Mitochondrial haplotypes and the New Zealand origin of clonal European Potamopyrgus, an invasive aquatic snail

The small aquatic snail Potamopyrgus antipodarum is an important invading species in Europe, Australia and North America. European populations are generally believed to derive from accidental introductions from New Zealand, probably dating back to the mid-19th century. We have employed mitochondrial DNA sequences to test the proposed New Zealand origin of European Potamopyrgus, and to learn more about its genealogical history. Using a 481-bp region of the 16S ribosomal RNA gene, we identified 17 distinct haplotypes among 65 snails from New Zealand. In marked contrast, only two haplotypes were found across all European samples, which cover a large geographical area. Importantly, these two haplotypes are shared with snails from the North Island of New Zealand. Due to sampling limitations we cannot rule out a South Island origin for one of the haplotypes, but our results clearly demonstrate the New Zealand origin of European populations. The marked divergence among the two European haplotypes implies the successful colonization by two distinct mitochondrial lineages, which is consistent with previous data based on nuclear markers.     

Consumption of toxic cyanobacteria by Potamopyrgus antipodarum (Gastropoda, Prosobranchia) and consequences on life traits and microcystin accumulation

Among the wide range of toxins produced by cyanobacterial blooms, microcystins (MCs) are the most common and are known to accumulate in aquatic organisms. Freshwater gastropods are grazers and likely to ingest toxic cyanobacteria, particularly Planktothrix agardhii, one of the most common species in the northern hemisphere. The study examines (i) the ingestion of toxic P. agardhii by the prosobranch Potamopyrgus antipodarum, (ii) the kinetics of MC accumulation and depuration in snail tissues during and post-exposure, and (iii) the impact of MCs on their life traits (survival, growth and fecundity). We showed that P. antipodarum ingested 71% of cyanobacteria available during the first 24 h in the presence or not of non-toxic food, and accumulated 1.3% of ingested MCs during the 5-week intoxication period. Elimination of MCs was total after 3 weeks of depuration. A decrease of growth and fecundity was observed during the intoxication period, but it was reversible after the end of exposure. Results are discussed in terms of variation of the response between prosobranch and pulmonate gastropods to toxic cyanobacteria exposure, and the negative impact of toxic cyanobacteria on natural communities of freshwater gastropods.     

Competitive interactions between two successful molluscan invaders of freshwaters: an experimental study

The New Zealand mud snail Potamopyrgus antipodarum (Hydrobiidae) and the pulmonate Physella acuta (Physidae) have invaded freshwaters in many parts of the world and become established. They co-exist in many streams, lakes and ponds in New Zealand, often at high densities. In the present study the effects of intraspecific- and interspecific interactions between the two species on growth and reproductive output were examined in laboratory mesocosms. In 30-day experiments, growth of Potamopyrgus antipodarum was lower in high density treatments than controls providing evidence for competition at higher densities of both snail species. No competitive effect was obtained for Physella acuta when controls were compared with high-density treatments, but growth was reduced at high densities of conspecifics. Numbers of juveniles released by Potamopyrgus antipodarum in 40 day trials declined at high snail densities and were lowest at high densities of conspecifics. Egg production by Physella acuta was also reduced at high snail densities. However, when the two species were kept together at equal densities (total snail density twice that of controls), egg production by Physella acuta was significantly higher than in all other treatments, suggesting facilitation by the congenor. Lastly, in a 10-day experiment, Physella acuta grew faster in water conditioned by Potamopyrgus antipodarum than in Physa-conditioned water, whereas Potamopyrgus antipodarum showed no growth response to Physella-conditioned water. Overall, our results indicate that growth and reproductive output of both snail species are influenced more by the density of conspecifics than the presence and density of the other species. The successful co-existence of the two species in New Zealand freshwaters therefore may be a reflection, at least in part, of few competitive interactions between them.     

Distribution of the invasive New Zealand mudsnail (Potamopyrgus antipodarum) in the Columbia River Estuary and its first recorded occurrence in the diet of juvenile Chinook salmon (Oncorhynchus tshawytscha)

Estuaries play an important role as nurseries and migration corridors for Chinook salmon and other fishes. The invasive New Zealand mudsnail, Potamopyrgus antipodarum (Gray, 1843), has been noted in the Columbia River Estuary and other estuaries in the western USA, yet no studies have addressed the estuarine impacts of this invader. Our data show P. antipodarum is currently found in five peripheral bays and many tributaries of the Columbia River Estuary, where it can constitute a major portion of the benthic invertebrate biomass and where it co-occurs with native amphipod species. We review the history of the P. antipodarum invasion in the Columbia River Estuary and discuss potential impacts on estuarine food webs. We also report the first occurrence of P. antipodarum in the diet of juvenile Chinook salmon from the Columbia River Estuary. Although present in Chinook diets at very low frequencies, our observations of P. antipodarum in Chinook gut contents may represent early stages of food web change due to the establishment of dense estuarine snail populations. Additional research is needed to determine the effects of P. antipodarum on benthic resources, native benthic invertebrates, and benthic predators. We encourage biologists working in western USA estuaries to be alert to the possibility of encountering P. antipodarum in benthic habitats and predator diets.

Adaptive phenotypic plasticity in a clonal invader

Organisms featuring wide trait variability and occurring in a wide range of habitats, such as the ovoviviparous New Zealand freshwater snail Potamopyrgus antipodarum, are ideal models to study adaptation. Since the mid‐19th century, P. antipodarum, characterized by extremely variable shell morphology, has successfully invaded aquatic areas on four continents. Because these obligately and wholly asexual invasive populations harbor low genetic diversity compared to mixed sexual/asexual populations in the native range, we hypothesized that (1) this phenotypic variation in the invasive range might be adaptive with respect to colonization of novel habitats, and (2) that at least some of the variation might be caused by phenotypic plasticity. We surveyed 425 snails from 21 localities across northwest Europe to attempt to disentangle genetic and environmental effects on shell morphology. We analyzed brood size as proxy for fitness and shell geometric morphometrics, while controlling for genetic background. Our survey revealed 10 SNP genotypes nested into two mtDNA haplotypes and indicated that mainly lineage drove variation in shell shape but not size. Physicochemical parameters affected both shell shape and size and the interaction of these traits with brood size. In particular, stronger stream flow rates were associated with larger shells. Our measurements of brood size suggested that relatively larger slender snails with relatively large apertures were better adapted to strong flow than counterparts with broader shells and relatively small apertures. In conclusion, the apparent potential to modify shell morphology plays likely a key role in the invasive success of P. antipodarum; the two main components of shell morphology, namely shape and size, being differentially controlled, the former mainly genetically and the latter predominantly by phenotypic plasticity.