Arthur E. Bogan

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.

A synoptical classification of the Bivalvia (Mollusca)

Preface This classification summarizes the suprageneric taxonomy of the Bivalvia for the upcoming revision of the Bivalvia volumes of the Treatise on Invertebrate Paleontology, Part N.

Freshwater bivalve (Unioniformes) diversity, systematics, and evolution: status and future directions

Abstract Freshwater bivalves of the order Unioniformes represent the largest bivalve radiation in freshwater. The unioniform radiation is unique in the class Bivalvia because it has an obligate parasitic larval stage on the gills or fins of fish; it is divided into 6 families, 181 genera, and ∼800 species. These families are distributed across 6 of the 7 continents and represent the most endangered group of freshwater animals alive today. North American unioniform bivalves have been the subject of study and illustration since Martin Lister, 1686, and over the past 320 y, significant gains have been made in our understanding of the evolutionary history and systematics of these animals. Here, the current state of unioniform systematics and evolution is summarized, and suggestions for future research themes are proposed. Advancement in the areas of systematics and evolutionary relationships within the Unioniformes will require a resurgence of survey work and reevaluation of all taxa, especially outside of North America and Western Europe. This work will require collection of animals for shell morphology, comparative anatomy, and molecular analyses. Along with reexamination of described taxa, a renewed emphasis on the natural history, host-fish relationships, ecology, and physiology of these animals is needed. Traditional conchological and anatomical characters should be reevaluated, new character suites should be added, and new morphometric methods should be applied. The fossil record of freshwater bivalves should be carefully reviewed, and phylogenetic hypotheses including fossil taxa must be developed. We will have to expand our set of molecular tools to include or develop additional markers, such as single-copy nuclear genes and microsatellites. Examination of double uniparental inheritance of mitochondrial deoxyribonucleic acid (DNA) is providing new insights into the evolution of this order. Mitochondrial gene order differs among genera but is still to be explored. Expansion of our understanding of the evolutionary relationships and history of unioniform bivalves will provide a solid foundation to study the zoogeography of these rather sessile, obligate freshwater organisms. The unique natural history of unioniform bivalves provides a fertile area for testing and developing evolutionary theories, and, as our understanding of the systematics of these animals improves, a better understanding of the evolution of this expansive radiation in freshwater will develop.

Comparative Mitochondrial Genomics of Freshwater Mussels (Bivalvia: Unionoida) With Doubly Uniparental Inheritance of mtDNA: Gender-Specific Open Reading Frames and Putative Origins of Replication

Doubly uniparental inheritance (DUI) of mitochondrial DNA in marine mussels (Mytiloida), freshwater mussels (Unionoida), and marine clams (Veneroida) is the only known exception to the general rule of strict maternal transmission of mtDNA in animals. DUI is characterized by the presence of gender-associated mitochondrial DNA lineages that are inherited through males (male-transmitted or M types) or females (female-transmitted or F types), respectively. This unusual system constitutes an excellent model for studying basic aspects of mitochondrial DNA inheritance and the evolution of mtDNA genomes in general. Here we compare published mitochondrial genomes of unionoid bivalve species with DUI, with an emphasis on characterizing unassigned regions, to identify regions of the F and M mtDNA genomes that could (i) play a role in replication or transcription of the mtDNA molecule and/or (ii) determine whether a genome will be transmitted via the female or the male gamete. Our results reveal the presence of one F-specific and one M-specific open reading frames (ORFs), and we hypothesize that they play a role in the transmission and/or gender-specific adaptive functions of the M and F mtDNA genomes in unionoid bivalves. Three major unassigned regions shared among all F and M unionoid genomes have also been identified, and our results indicate that (i) two of them are potential heavy-strand control regions (OH) for regulating replication and/or transcription and that (ii) multiple and potentially bidirectional light-strand origins of replication (OL) are present in unionoid F and M mitochondrial genomes. We propose that unassigned regions are the most promising candidate sequences in which to find regulatory and/or gender-specific sequences that could determine whether a mitochondrial genome will be maternally or paternally transmitted.

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...

On becoming cemented: evolutionary relationships among the genera in the freshwater bivalve family Etheriidae (Bivalvia: Unionoida)

Abstract A robust phylogeny for the Unionoida is emerging and presumed relationships of some major clades are being questioned. The Etheriidae or freshwater oysters has been a distinct family for over 160 years and currently contains three cemented genera: Acostaea (Columbia, South America), Pseudomulleria (India) and Etheria (Africa and Madagascar). Starobogatov (1970, Nauka, 1–372), Mansur and da Silva (1990, Amazoniana, 11(2), 147–166) and Bonetto (1997, Biociências, 5, 113–142) present conflicting testable hypotheses regarding the evolution of these taxa. Using cytochrome c oxidase subunit I DNA sequences the evolutionary relationships of these three genera has been examined, by comparing them to representatives of 30 other unionoid taxa from around the world. These analyses place Acostaea and Etheria within the Mycetopodidae while Pseudomulleria falls within the Unionidae. A monophyletic Etheriidae, composed of cemented freshwater bivalves, is not supported by the present analyses. Furthermore, the analyses indicate that cementation in the Unionida has evolved at least twice.

A Phylogenetic Perspective on the Evolution of Morphological and Reproductive Characteristics in the Unionoida

Unionoid bivalves have a long history of classification and reclassification. Pre-Darwin classifications were deductive and artificial, reflecting character selection and weighting. More recent classifications, which should be natural and inductive to reflect phylogeny, reveal a diversity of methodologies and results.

Phylogeny of the most species-rich freshwater bivalve family (Bivalvia: Unionida: Unionidae): Defining modern subfamilies and tribes

Freshwater mussels of the order Unionida are key elements of freshwater habitats and are responsible for important ecological functions and services. Unfortunately, these bivalves are among the most threatened freshwater taxa in the world. However, conservation planning and management are hindered by taxonomic problems and a lack of detailed ecological data. This highlights the urgent need for advances in the areas of systematics and evolutionary relationships within the Unionida. This study presents the most comprehensive phylogeny to date of the larger Unionida family, i.e., the Unionidae. The phylogeny is based on a combined dataset of 1032bp (COI+28S) of 70 species in 46 genera, with 7 of this genera being sequenced for the first time. The resulting phylogeny divided the Unionidae into 6 supported subfamilies and 18 tribes, three of which are here named for the first time (i.e., Chamberlainiini nomen novum, Cristariini nomen novum and Lanceolariini nomen novum). Molecular analyses were complemented by investigations of selected morphological, anatomical and behavioral characters used in traditional phylogenetic studies. No single morphological, anatomical or behavioral character was diagnostic at the subfamily level and few were useful at the tribe level. However, within subfamilies, many tribes can be recognized based on a subset of these characters. The geographical distribution of each of the subfamilies and tribes is also presented. The present study provides important advances in the systematics of these extraordinary taxa with implications for future ecological and conservation studies.

Palaeoheterodont Phylogeny, Character Evolution, Diversity and Phylogenetic Classification: A Reflection on Methods of Analysis

ABSTRACT Graf and Cummings (2006), hereafter referred to simply as “G & C”, provided phylogenetic analyses of a three-partition data set in order to (1) examine the higher level evolutionary relationships within the Palaeoheterodonta, (2) estimate the history of character state change, and (3) develop a phylogenetic classification for the group. However, portions of the available COI DNA sequence data, for multiple terminals, were omitted from G & Cs phylogenetic analyses, and no attempt was made to explicitly account for the documented saturation in the COI data partition. In order to evaluate the effects of these omissions, we performed Bayesian inference (BI) as well as maximum parsimony (MP) analyses on G & Cs combined evidence (CE) matrix that included all of the ingroup COI sequences contained in G & C, plus the omitted outgroup COI sequences. We conclude that G & Cs COI DNA sequence omissions, when combined with MP analyses not accounting for COI saturation, negatively affected the topologies of the best trees obtained from phylogenetic analyses of the CE matrix. This conclusion questions the utility of G & Cs inferences regarding palaeoheterodont bivalve character evolution as well as the taxonomic classification drawn from its preferred topology. For example, counter to G & Cs inferences, our BI and “transformed COI” MP analyses determined that unionoid oyster conchology has evolved multiple times, and all of our phylogenetic analyses indicate that the Etheriidae (sensu G & C) is not monophyletic. However, it should be noted that, to date, no phylogenetic analysis of this data set has robustly estimated all basal nodes within the Unionoida. Therefore, any inferences regarding unionoid bivalve character evolution, diversity and classification drawn from these topologies should be considered weakly supported.

Factors driving changes in freshwater mussel (Bivalvia, Unionida) diversity and distribution in Peninsular Malaysia.

Freshwater mussels (Bivalvia, Unionida) fulfil important ecosystem functions and are one of the most threatened freshwater taxa globally. Knowledge of freshwater mussel diversity, distribution and ecology in Peninsular Malaysia is extremely poor, and the conservation status of half of the species presumed to occur in the region has yet to be assessed. We conducted the first comprehensive assessment of Peninsular Malaysias freshwater mussels based on species presence/absence and environmental data collected from 155 sites spanning all major river catchments and diverse habitat types. Through an integrative morphological-molecular approach we recognised nine native and one widespread non-native species, i.e. Sinanodonta woodiana. Two species, i.e. Pilsbryoconcha compressa and Pseudodon cambodjensis, had not been previously recorded from Malaysia, which is likely a result of morphological misidentifications of historical records. Due to their restriction to single river catchments and declining distributions, Hyriopsis bialata, possibly endemic to Peninsular Malaysia, Ensidens ingallsianus, possibly already extinct in the peninsula, and Rectidens sumatrensis, particularly require conservation attention. Equally, the Pahang, the Perak and the north-western river catchments are of particular conservation value due to the presence of a globally unique freshwater mussel fauna. Statistical relationships of 15 water quality parameters and mussel presence/absence identified acidification and nutrient pollution (eutrophication) as the most important anthropogenic factors threatening freshwater mussel diversity in Peninsular Malaysia. These factors can be linked to atmospheric pollution, deforestation, oil-palm plantations and a lack of functioning waste water treatment, and could be mitigated by establishing riparian buffers and improving waste water treatment for rivers running through agricultural and residential land.