Biological Control of Pest Non-Marine Molluscs: A Pacific Perspective on Risks to Non-Target Organisms.

Classic biological control of pest non-marine molluscs has a long history of disastrous outcomes, and despite claims to the contrary, few advances have been made to ensure that contemporary biocontrol efforts targeting molluscs are safe and effective. For more than half a century, malacologists have warned of the dangers in applying practices developed in the field of insect biological control, where biocontrol agents are often highly host-specific, to the use of generalist predators and parasites against non-marine mollusc pests. Unfortunately, many of the lessons that should have been learned from these failed biocontrol programs have not been rigorously applied to contemporary efforts. Here, we briefly review the failures of past non-marine mollusc biocontrol efforts in the Pacific islands and their adverse environmental impacts that continue to reverberate across ecosystems. We highlight the fact that none of these past programs has ever been demonstrated to be effective against targeted species, and at least two (the snails Euglandina spp. and the flatworm Platydemus manokwari) are implicated in the extinction of hundreds of snail species endemic to Pacific islands. We also highlight other recent efforts, including the proposed use of sarcophagid flies and nematodes in the genus Phasmarhabditis, that clearly illustrate the false claims that past bad practices are not being repeated. We are not making the claim that biocontrol programs can never be safe and effective. Instead, we hope that in highlighting the need for robust controls, clear and measurable definitions of success, and a broader understanding of ecosystem level interactions within a rigorous scientific framework are all necessary before claims of success can be made by biocontrol advocates. Without such amendments to contemporary biocontrol programs, it will be impossible to avoid repeating the failures of non-marine mollusc biocontrol programs to date.

Overlooked but not forgotten: the first new extant species of Hawaiian land snail described in 60 years, Auriculella gagneorum sp. nov. (Achatinellidae, Auriculellinae).

Recent surveys of Oahu's Waianae Mountains uncovered a small, previously undescribed species of Auriculella that is conchologically similar to the three members of the A. perpusilla group all of which are endemic to the Koolau Mountain Range. However, sequence data demonstrate that the perpusilla group is not monophyletic. Moreover, the new species is not closely related to A. perpusilla or A. perversa, the only extant members of the group, but instead is sister to A. tenella, a species from the high spired A. castanea group. A neotype is designated for A. auricula, the type species of Auriculella; all members of the conchologically similar perpusilla group are anatomically redescribed; and lectotypes designated for A. minuta, A. perversa, and A. tenella. The new species is described and compared to the type of the genus, members of the perpusilla group, and the genetically similar species A. tenella.

First evidence of introgressive hybridization of apple snails (Pomacea spp.) in their native range.

Genetic variation facilitates both natural range expansions and anthropogenic invasions. Contrary to expectations, hybridization does not always impact negatively on biodiversity. Increasing evidence indicates advantageous roles for introgressive hybridization in maintaining standing genetic variation. Hypothesizing that hybridization may contribute to the evolutionary and invasive success of a diverse group of freshwater snails (Ampullariidae, commonly known as apple snails), we estimated the frequency of hybridization between two globally invasive species of Pomacea, Pomacea canaliculata (Lamarck, 1822) and P. maculata Perry, 1810, in their native range. While previous work in Asia has uncovered the occurrence of extensive hybridization, we provide the first phylogenetic evidence of a high degree of hybridization (30%) between these species in Uruguay and Brazil. Hybrids carried both heterozygous and homozygous combinations of elongation factor 1-α (EF1α) nuclear alleles in both mating directions, indicating that hybridization has occurred over multiple generations and likely preceded introductions outside the native range. Among the five sites in Brazil previously documented as containing only P. maculata, one far northern population (Careiro Castanho), which is thousands of kilometres from the northern range of P. canaliculata, unexpectedly contained hybrids. This may be the result of human-facilitated introductions. Together with recent work from Asia, our investigations in the native range of apple snails support a reframing of historical perspectives of hybridization as a driver of extinction and diversity loss towards a modern paradigm where hybridization may promote diversification and contribute to the survival of evolutionary lineages such as molluscs.

Signatures of Divergence, Invasiveness, and Terrestrialization Revealed by Four Apple Snail Genomes.

The family Ampullariidae includes both aquatic and amphibious apple snails. They are an emerging model for evolutionary studies due to the high diversity, ancient history, and wide geographical distribution. Insight into drivers of ampullariid evolution is hampered, however, by the lack of genomic resources. Here, we report the genomes of four ampullariids spanning the Old World (Lanistes nyassanus) and New World (Pomacea canaliculata, P. maculata, and Marisa cornuarietis) clades. The ampullariid genomes have conserved ancient bilaterial karyotype features and a novel Hox gene cluster rearrangement, making them valuable in comparative genomic studies. They have expanded gene families related to environmental sensing and cellulose digestion, which may have facilitated some ampullarids to become notorious invasive pests. In the amphibious Pomacea, novel acquisition of an egg neurotoxin and a protein for making the calcareous eggshell may have been key adaptations enabling their transition from underwater to terrestrial egg deposition.

Modelling the distribution in Hawaii of Angiostrongylus cantonensis (rat lungworm) in its gastropod hosts.

Angiostrongylus cantonensis (rat lungworm), a parasitic nematode, is expanding its distribution. Human infection, known as angiostrongyliasis, may manifest as eosinophilic meningitis, an emerging infectious disease. The range and incidence of this disease are expanding throughout the tropics and subtropics. Recently, the Hawaiian Islands have experienced an increase in reported cases. This study addresses factors affecting the parasite's distribution and projects its potential future distribution, using Hawaii as a model for its global expansion. Specimens of 37 snail species from the Hawaiian Islands were screened for the parasite using PCR. It was present on five of the six largest islands. The data were used to generate habitat suitability models for A. cantonensis, based on temperature and precipitation, to predict its potential further spread within the archipelago. The best current climate model predicted suitable habitat on all islands, with greater suitability in regions with higher precipitation and temperatures. Projections under climate change (to 2100) indicated increased suitability in regions with estimated increased precipitation and temperatures, suitable habitat occurring increasingly at higher elevations. Analogously, climate change could facilitate the spread of A. cantonensis from its current tropical/subtropical range into more temperate regions of the world, as is beginning to be seen in the continental USA.

Invisible apple snail invasions: importance of continued vigilance and rigorous taxonomic assessments.

BACKGROUND: Due to the similarities of overall shell morphology among apple snail species and considerable variability within species, substantial taxonomic confusion has plagued the accurate identification of Pomacea species. Many invasive apple snails have been mistakenly identified as P. canaliculata since their introduction to Asia around 1980. In 2008, three other introduced species in addition to P. canaliculata were recognized. In 2013, a fifth, previously unrecognized lineage was reported from China, indicating that despite the taxonomic clarity brought by previous work, continued surveys and taxonomic research are necessary to prevent additional introductions and continued spread, as well as to develop effective management strategies. RESULTS: Phylogenetic analysis of mitochondrial COI sequences confirmed the presence of a widespread unidentified Pomacea lineage in China. All sequences from samples of this newly documented lineage were recovered in a monophyletic clade delineated from closely related species; however, different DNA barcoding methods yielded inconsistent species boundaries. Additionally, nuclear EF1α sequences indicated incomplete lineage sorting or recent hybridization of the unidentified lineage with the other two established species. CONCLUSION: Barcoding is a valuable tool for species discovery, and a powerful approach for delineating introduced species. However, determining the identity of the newly discovered invasive lineage in China will require an integrated taxonomic approach incorporating individuals from the native range, and examination of natural history collections at museums around the world. To manage and prevent additional spread of already established species, and to stop the introduction of new taxa, continued monitoring and rigorous taxonomic assessments must be undertaken. © 2018 Society of Chemical Industry.

Biodiversity and Extinction of Hawaiian Land Snails: How Many Are Left Now and What Must We Do To Conserve Them-A Reply to.

Pacific islands, with their incredible biodiversity, are our finest natural laboratories for evolutionary, ecological, and cultural studies. Nowhere, in relation to land area, does land snail diversity reach that of the Pacific islands, with more than 6000 species, most of which are single island endemics. Unfortunately, land snails are the most imperiled group with the most recorded extinctions since the 1500s, and Pacific island snails make up the majority of those extinctions. In 1990, Dr. Alan Solem, a well renowned malacologist, with expertise in Pacific island land snails, posthumously published a plea to save the remaining Hawaiian land snails before they vanish forever. Now, more than 25 years later, we have finally begun to make inroads into answering the questions "How many Hawaiian land snails remain?" and "What will we need to save them?". Here we provide a belated reply to Solem (1990) and address these questions about Hawaiian land snails. We conclude by building on the actions suggested by Solem and that we feel are still needed to realize his hope of conserving Hawaii's remaining land snails specifically, but also our hope of conserving invertebrates more broadly.

Correction: Diverse Gastropod Hosts of Angiostrongylus cantonensis, the Rat Lungworm, Globally and with a Focus on the Hawaiian Islands.

[This corrects the article DOI: 10.1371/journal.pone.0094969.].

Extinction in a hyperdiverse endemic Hawaiian land snail family and implications for the underestimation of invertebrate extinction.

The International Union for Conservation of Nature (IUCN) Red List includes 832 species listed as extinct since 1600, a minuscule fraction of total biodiversity. This extinction rate is of the same order of magnitude as the background rate and has been used to downplay the biodiversity crisis. Invertebrates comprise 99% of biodiversity, yet the status of a negligible number has been assessed. We assessed extinction in the Hawaiian land snail family Amastridae (325 species, IUCN lists 33 as extinct). We did not use the stringent IUCN criteria, by which most invertebrates would be considered data deficient, but a more realistic approach comparing historical collections with modern surveys and expert knowledge. Of the 325 Amastridae species, 43 were originally described as fossil or subfossil and were assumed to be extinct. Of the remaining 282, we evaluated 88 as extinct and 15 as extant and determined that 179 species had insufficient evidence of extinction (though most are probably extinct). Results of statistical assessment of extinction probabilities were consistent with our expert evaluations of levels of extinction. Modeling various extinction scenarios yielded extinction rates of 0.4-14.0% of the amastrid fauna per decade. The true rate of amastrid extinction has not been constant; generally, it has increased over time. We estimated a realistic average extinction rate as approximately 5%/decade since the first half of the nineteenth century. In general, oceanic island biotas are especially susceptible to extinction and global rate generalizations do not reflect this. Our approach could be used for other invertebrates, especially those with restricted ranges (e.g., islands), and such an approach may be the only way to evaluate invertebrates rapidly enough to keep up with ongoing extinction.

Diverse gastropod hosts of Angiostrongylus cantonensis, the rat lungworm, globally and with a focus on the Hawaiian Islands.

Eosinophilic meningitis caused by the parasitic nematode Angiostrongylus cantonensis is an emerging infectious disease with recent outbreaks primarily in tropical and subtropical locations around the world, including Hawaii. Humans contract the disease primarily through ingestion of infected gastropods, the intermediate hosts of Angiostrongylus cantonensis. Effective prevention of the disease and control of the spread of the parasite require a thorough understanding of the parasite's hosts, including their distributions, as well as the human and environmental factors that contribute to transmission. The aim of this study was to screen a large cross section of gastropod species throughout the main Hawaiian Islands to determine which act as hosts of Angiostrongylus cantonensis and to assess the parasite loads in these species. Molecular screening of 7 native and 30 non-native gastropod species revealed the presence of the parasite in 16 species (2 native, 14 non-native). Four of the species tested are newly recorded hosts, two species introduced to Hawaii (Oxychilus alliarius, Cyclotropis sp.) and two native species (Philonesia sp., Tornatellides sp.). Those species testing positive were from a wide diversity of heterobranch taxa as well as two distantly related caenogastropod taxa. Review of the global literature showed that many gastropod species from 34 additional families can also act as hosts. There was a wide range of parasite loads among and within species, with an estimated maximum of 2.8 million larvae in one individual of Laevicaulis alte. This knowledge of the intermediate host range of Angiostrongylus cantonensis and the range of parasite loads will permit more focused efforts to detect, monitor and control the most important hosts, thereby improving disease prevention in Hawaii as well as globally.

Effects of washing produce contaminated with the snail and slug hosts of Angiostrongylus cantonensis with three common household solutions.

The emerging infectious disease angiostrongyliasis (rat lungworm disease) is caused by ingesting snails and slugs infected by the nematode Angiostrongylus cantonensis. The definitive hosts of A. cantonensis are rats and the obligatory intermediate hosts are slugs and snails. Many cases result from accidentally ingesting infected snails or slugs on produce (eg, lettuce). This study assessed three readily available household products as washing solutions for removing snails and slugs from produce (romaine lettuce) to lower the probability of accidentally ingesting them. The solutions were acetic acid (vinegar), sodium hypochlorite (bleach), and sodium chloride (domestic salt). Snail and slug species known to be intermediate hosts and that are common in the Hawaiian Islands were used in the experiments: the alien snail Succinea tenella, the alien semi-slug Parmarion martensi, and the alien slugs Veronicella cubensis and Deroceras laeve. None of the products was any more effective than washing and rinsing with tap water alone. Most snails and slugs were removed after treatment but some remained on the lettuce even after washing and rinsing the produce. Only washing, rinsing, and then rinsing each leaf individually resulted in complete removal of all snails and slugs. The study did not address removal of any remaining slime left by the snails and slugs, nor did it address killing of worms.

Extreme population subdivision in the crown conch (Melongena corona): historical and contemporary influences.

Organisms with crawl-away larvae are thought to experience highly restricted gene flow. Here, we assess the pattern and magnitude of population subdivision of the direct developing snails in the Melongena corona complex and assess the validity of species and subspecies designations in the genus. A total of 516 individuals from 15 locations were assayed at 8 microsatellite loci. Levels of genetic diversity were moderate and typical of gastropods. There were from 8 to 28 alleles per locus and the average observed per sample heterozygosity ranged from 0.16 to 0.79. Levels of genetic divergence were generally large with all sample pairwise F(ST) values statistically significant and ranging from 0.011 to 0.438 and Jost's D(EST) ranging from 0.028 to 0.731. A Bayesian analysis identified 7 clusters of, usually adjoining, samples. The population subdivision is likely derived from a complex mixture of life-history attributes, frequent short-distance dispersal via swimming larvae, rare short- and long-distance dispersal of rafting larvae and eggs, and a patchwork of adjacent and adjoining habitats. As with a previous study, the current taxonomy is not supported by the genetic results and the complex can be considered as M. corona, a single, albeit clearly geographically genetically structured, species.

The identity, distribution, and impacts of non-native apple snails in the continental United States.

BACKGROUND: Since the mid 1990s populations of non-native apple snails (Ampullariidae) have been discovered with increasing frequency in the continental United States. Given the dramatic effects that introduced apple snails have had on both natural habitats and agricultural areas in Southeast Asia, their introduction to the mainland U.S. is cause for concern. We combine phylogenetic analyses of mtDNA sequences with examination of introduced populations and museum collections to clarify the identities, introduced distributions, geographical origins, and introduction histories of apple snails. RESULTS: Based on sampling to date, we conclude there are five species of non-native apple snails in the continental U.S. Most significantly, we recognize three species within what has been called the channeled apple snail: Pomacea canaliculata (California and Arizona), Pomacea insularum, (Florida, Texas, and Georgia) and Pomacea haustrum (Florida). The first established populations of P. haustrum were discovered in the late 1970s in Palm Beach County Florida, and have not spread appreciably in 30 years. In contrast, populations of P. insularum were established in Texas by 1989, in Florida by the mid to late 1990s, and in Georgia by 2005, and this species continues to spread rapidly. Most introduced P. insularum haplotypes are a close match to haplotypes from the Río Uruguay near Buenos Aires, indicating cold tolerance, with the potential to spread from Florida, Georgia, and Texas through Louisiana, Alabama, Mississippi, and South Carolina. Pomacea canaliculata populations were first discovered in California in 1997. Haplotypes of introduced P. canaliculata match native-range haplotypes from near Buenos Aires, Argentina, also indicating cold tolerance and the potential to establish farther north. CONCLUSION: The term "channeled apple snail" is descriptive of a morphology found in many apple snail species. It does not identify a single species or a monophyletic group. Clarifying species identifications permits a more accurate assessment of introduction histories and distributions, and provides a very different picture of the tempo and pattern of invasions than was inferred when the three species with channeled sutures were considered one. Matching introduced and native-range haplotypes suggests the potential for range expansion, with implications for native aquatic ecosystems and species, agriculture, and human health.