Ellen E. Strong

The Global Decline of Nonmarine Mollusks

Abstract Invertebrate species represent more than 99% of animal diversity; however, they receive much less publicity and attract disproportionately minor research effort relative to vertebrates. Nonmarine mollusks (i.e., terrestrial and freshwater) are one of the most diverse and imperiled groups of animals, although not many people other than a few specialists who study the group seem to be aware of their plight. Nonmarine mollusks include a number of phylogenetically disparate lineages and species-rich assemblages that represent two molluscan classes, Bivalvia (clams and mussels) and Gastropoda (snails, slugs, and limpets). In this article we provide an overview of global nonmarine molluscan biodiversity and conservation status, including several case studies documenting the diversity and global decline of nonmarine mollusks. We conclude with a discussion of the roles that mollusks and malacologists should play in conservation, including research, conservation management strategies, and education and outreach.

Global diversity of gastropods (Gastropoda; Mollusca) in freshwater

The world’s gastropod fauna from continental waters comprises ∼4,000 valid described species and a minimum of 33–38 independent lineages of Recent Neritimorpha, Caenogastropoda and Heterobranchia (including the Pulmonata). The caenogastropod component dominates in terms of species richness and diversity of morphology, physiology, life and reproductive modes and has produced several highly speciose endemic radiations. Ancient oligotrophic lakes (e.g., Baikal, Ohrid, Tanganyika) are key hotspots of gastropod diversity; also noteworthy are a number of lower river basins (e.g., Congo, Mekong, Mobile Bay). But unlike many other invertebrates, small streams, springs and groundwater systems have produced the most speciose associations of freshwater gastropods. Despite their ecological importance in many aquatic ecosystems, understanding of even their systematics is discouragingly incomplete. The world’s freshwater gastropod fauna faces unprecedented threats from habitat loss and degradation and introduced fishes and other pests. Unsustainable use of ground water, landscape modification and stock damage are destroying many streams and springs in rural/pastoral areas, and pose the most significant threats to the large diversity of narrow range endemics in springs and ground water. Despite comprising only ∼5% of the world’s gastropod fauna, freshwater gastropods account for ∼20% of recorded mollusc extinctions. However, the status of the great majority of taxa is unknown, a situation that is exacerbated by a lack of experts and critical baseline data relating to distribution, abundance, basic life history, physiology, morphology and diet. Thus, the already considerable magnitude of extinction and high levels of threat indicated by the IUCN Red List of Threatened Species is certainly a significant underestimate.

Investigating the Bivalve Tree of Life – an exemplar-based approach combining molecular and novel morphological characters

Abstract. To re-evaluate the relationships of the major bivalve lineages, we amassed detailed morpho-anatomical, ultrastructural and molecular sequence data for a targeted selection of exemplar bivalves spanning the phylogenetic diversity of the class. We included molecular data for 103 bivalve species (up to five markers) and also analysed a subset of taxa with four additional nuclear protein-encoding genes. Novel as well as historically employed morphological characters were explored, and we systematically disassembled widely used descriptors such as gill and stomach ‘types’. Phylogenetic analyses, conducted using parsimony direct optimisation and probabilistic methods on static alignments (maximum likelihood and Bayesian inference) of the molecular data, both alone and in combination with morphological characters, offer a robust test of bivalve relationships. A calibrated phylogeny also provided insights into the tempo of bivalve evolution. Finally, an analysis of the informativeness of morphological characters showed that sperm ultrastructure characters are among the best morphological features to diagnose bivalve clades, followed by characters of the shell, including its microstructure. Our study found support for monophyly of most broadly recognised higher bivalve taxa, although support was not uniform for Protobranchia. However, monophyly of the bivalves with protobranchiate gills was the best-supported hypothesis with incremental morphological and/or molecular sequence data. Autobranchia, Pteriomorphia, Heteroconchia, Palaeoheterodonta, Archiheterodonta, Euheterodonta, Anomalodesmata and Imparidentia new clade ( = Euheterodonta excluding Anomalodesmata) were recovered across analyses, irrespective of data treatment or analytical framework. Another clade supported by our analyses but not formally recognised in the literature includes Palaeoheterodonta and Archiheterodonta, which emerged under multiple analytical conditions. The origin and diversification of each of these major clades is Cambrian or Ordovician, except for Archiheterodonta, which diverged from Palaeoheterodonta during the Cambrian, but diversified during the Mesozoic. Although the radiation of some lineages was shifted towards the Palaeozoic (Pteriomorphia, Anomalodesmata), or presented a gap between origin and diversification (Archiheterodonta, Unionida), Imparidentia showed steady diversification through the Palaeozoic and Mesozoic. Finally, a classification system with six major monophyletic lineages is proposed to comprise modern Bivalvia: Protobranchia, Pteriomorphia, Palaeoheterodonta, Archiheterodonta, Anomalodesmata and Imparidentia.

Conservation Status of Freshwater Gastropods of Canada and the United States

ABSTRACT This is the first American Fisheries Society conservation assessment of freshwater gastropods (snails) from Canada and the United States by the Gastropod Subcommittee (Endangered Species Committee). This review covers 703 species representing 16 families and 93 genera, of which 67 species are considered extinct, or possibly extinct, 278 are endangered, 102 are threatened, 73 are vulnerable, 157 are currently stable, and 26 species have uncertain taxonomic status. Of the entire fauna, 74% of gastropods are imperiled (vulnerable, threatened, endangered) or extinct, which exceeds imperilment levels in fishes (39%) and crayfishes (48%) but is similar to that of mussels (72%). Comparison of modern to background extinction rates reveals that gastropods have the highest modern extinction rate yet observed, 9,539 times greater than background rates. Gastropods are highly susceptible to habitat loss and degradation, particularly narrow endemics restricted to a single spring or short stream reaches. Compil...

Insights from an Integrated View of the Biology of Apple Snails (Caenogastropoda: Ampullariidae)

ABSTRACT Apple snails (Ampullariidae) are among the largest and most ecologically important freshwater snails. The introduction of multiple species has reinvigorated the field and spurred a burgeoning body of research since the early 1990s, particularly regarding two species introduced to Asian wetlands and elsewhere, where they have become serious agricultural pests. This review places these recent advances in the context of previous work, across diverse fields ranging from phylogenetics and biogeography through ecology and developmental biology, and the more applied areas of environmental health and human disease. The review does not deal with the role of ampullariids as pests, nor their control and management, as this has been substantially reviewed elsewhere. Despite this large and diverse body of research, significant gaps in knowledge of these important snails remain, particularly in a comparative framework. The great majority of the work to date concerns a single species, Pomacea canaliculata, which we see as having the potential to become a model organism in a wide range of fields. However, additional comparative data are essential for understanding this diverse and potentially informative group. With the rapid advances in genomic technologies, many questions, seemingly intractable two decades ago, can be addressed, and ampullariids will provide valuable insights to our understanding across diverse fields in integrative biology.

Rubyspira, New Genus and Two New Species of Bone-Eating Deep-Sea Snails With Ancient Habits

Rubyspira, a new genus of deep-sea snails (Gastropoda: Abyssochrysoidea) with two living species, derives its nutrition from decomposing whalebones. Molecular phylogenetic and morphological evidence places the new genus in an exclusively deep-sea assemblage that includes several close relatives previously known as fossils associated with Cretaceous cold seeps, plesiosaur bones, and Eocene whalebones. The ability to exploit a variety of marine reducing environments may have contributed to the evolutionary longevity of this gastropod lineage.

Identifying gastropod spawn from DNA barcodes: possible but not yet practicable.

Identifying life stages of species with complex life histories is problematic as species are often only known and/or described from a single stage. DNA barcoding has been touted as an important tool for linking life‐history stages of the same species. To test the current efficacy of DNA barcodes for identifying unknown mollusk life stages, 24 marine gastropod egg capsules were collected off the Philippines in deep water and sequenced for partial fragments of the COI, 16S and 12S mitochondrial genes. Two egg capsules of known shallow‐water Mediterranean species were used to calibrate the method. These sequences were compared to those available in GenBank and the Barcode of Life Database (BOLD). Using COI sequences alone, only a single Mediterranean egg capsule was identified to species, and a single Philippine egg capsule was identified tentatively to genus; all other COI sequences recovered matches between 76% and 90% with sequences from BOLD and GenBank. Similarity‐based identification using all three markers confirmed the Mediterranean specimens’ identifications. A phylogenetic approach was also implemented to confirm similarity‐based identifications and provide a higher‐taxonomic identification when species‐level identifications were not possible. Comparison of available GenBank sequences to the diversity curve of a well‐sampled coral reef habitat in New Caledonia highlights the poor taxonomic coverage achieved at present in existing genetic databases, emphasizing the need to develop DNA barcoding projects for megadiverse and often taxonomically challenging groups such as mollusks, to fully realize its potential as an identification and discovery tool.

A family-level Tree of Life for bivalves based on a Sanger-sequencing approach

The systematics of the molluscan class Bivalvia are explored using a 5-gene Sanger-based approach including the largest taxon sampling to date, encompassing 219 ingroup species spanning 93 (or 82%) of the 113 currently accepted bivalve families. This study was designed to populate the bivalve Tree of Life at the family level and to place many genera into a clear phylogenetic context, but also pointing to several major clades where taxonomic work is sorely needed. Despite not recovering monophyly of Bivalvia or Protobranchia-as in most previous Sanger-based approaches to bivalve phylogeny-our study provides increased resolution in many higher-level clades, and supports the monophyly of Autobranchia, Pteriomorphia, Heteroconchia, Palaeoheterodonta, Heterodonta, Archiheterodonta, Euheterodonta, Anomalodesmata, Imparidentia, and Neoheterodontei, in addition to many other lower clades. However, deep nodes within some of these clades, especially Pteriomorphia and Imparidentia, could not be resolved with confidence. In addition, many families are not supported, and several are supported as non-monophyletic, including Malletiidae, Nuculanidae, Yoldiidae, Malleidae, Pteriidae, Arcidae, Propeamussiidae, Iridinidae, Carditidae, Myochamidae, Lyonsiidae, Pandoridae, Montacutidae, Galeommatidae, Tellinidae, Semelidae, Psammobiidae, Donacidae, Mactridae, and Cyrenidae; Veneridae is paraphyletic with respect to Chamidae, although this result appears to be an artifact. The denser sampling however allowed testing specific placement of species, showing, for example, that the unusual Australian Plebidonax deltoides is not a member of Donacidae and instead nests within Psammobiidae, suggesting that major revision of Tellinoidea may be required. We also showed that Cleidothaerus is sister group to the cementing member of Myochamidae, suggesting that Cleidothaeridae may not be a valid family and that cementation in Cleidothaerus and Myochama may have had a single origin. These results highlight the need for an integrative approach including as many genera as possible, and that the monophyly and relationships of many families require detailed reassessment. NGS approaches may be able to resolve the most recalcitrant nodes in the near future.

Evidence for convergent evolution of brooding in a unique gastropod from Lake Tanganyika: anatomy and affinity of Tanganyicia rufofilosa (Caenogastropoda, Cerithioidea, Paludomidae)

Tanganyicia rufofilosa is an enigmatic gastropod endemic to Lake Tanganyika and unique among lake species in possessing a brood pouch within the head‐foot. However, the only existing anatomic studies of the species are incomplete. Hence, the affinity of this species to other Tanganyikan gastropods and the evolution of viviparity among limnic Cerithioidea are unclear. The anatomic redescription and reinterpretation of reproductive homologies presented here revealed several features from the midgut and kidney that are informative concerning the phylogeny of Lake Tanganyika gastropods. In addition, the complex reproductive anatomy of both sexes is described. A rare accessory gland is present in males that is hypothesized to function in spermatophore formation and to be homologous to the ‘penis’ of some cerithioideans, an otherwise predominantly aphallic group. The structurally unique brood pouch, restricted to the mesopodial portion of the foot, is described and demonstrated to be unknown among viviparous cerithioideans. In contrast to the view that the cerithioideans of Lake Tanganyika represent an endemic radiation of Thiaridae, based on these new data T. rufofilosa appears to be allied to the Paludomidae.

Using microwaves to prepare gastropods for DNA barcoding.

Extracting DNA from gastropods presents particular difficulties due to the capacity of the living animal to retract into the shell, resulting in poor penetration of the ethanol into the tissues. Because the shell is essential to establish the link between sequences and traditional taxonomic identity, cracking the shell to facilitate fixation is not ideal. Several methods are currently in routine use to overcome this difficulty, including chemical relaxation, drilling the shell and boiling. Most of these methods are time‐consuming, may be safety hazards and constitute a bottleneck in the preparation of large numbers of specimens in the field. We have experimented with a method traditionally used to clean shells that involves placing the living gastropods in a microwave (MW) oven; the electromagnetic radiation very quickly heats both the animal and the water trapped inside the shell, resulting in separation of the muscles that anchor the animal to the shell. Done properly, the body can be removed intact from the shell and the shell voucher is preserved undamaged. To test the method, the bodies of live‐collected specimens from two gastropod species were separated from their shell by microwaving and by anesthetizing/drilling. After identical extraction and PCR procedures, the gels showed no difference in DNA quantity or quality, and the resulting sequences are identical within species. The method was then implemented on a large scale during expeditions, resulting in higher percentage of DNA extraction success. The MWs are also effective for quickly and easily removing other molluscs from their shells, that is, bivalves and scaphopods. Workflows implementing the MW technique show a three‐ to fivefold increase in productivity compared with other methods.