David T. Zanatta

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.

Diversity, biogeography and conservation of freshwater mussels (Bivalvia: Unionida) in East and Southeast Asia

Recent research efforts have significantly advanced our knowledge on Asian freshwater mussel (Bivalvia: Unionida) diversity and distribution. Here we provide a modern consensus of the diversity, biogeography and conservation of Unionida in the region comprising East and Southeast Asia (excluding Wallacea) and Asian Russia. A data review confirmed the presence of 228 native and 3 non-native Unionida (98% Unionidae, 2% Margaritiferidae), rendering the region a global hotspot of freshwater mussel diversity. Species richness was highest in China (particularly Yangtze basin) in absolute numbers and Cambodia when correcting for country area, and decreased gradually towards the south and steeply towards the north and east. Six of the seven unionid subfamilies are native to the region, with species richness peaking in Southeast Asia for Rectidentinae, Gonideinae, Parreysiinae and Modellnaiinae, China for Anodontinae and Unioninae, and Asian Russia for Margaritiferidae. Conservation status and data collected after 1980 were not available for 61 and 24% of species, respectively. Dams, deforestation and pollution are likely the major threats to mussels in the region, though data in this respect are scarce. The Philippines, Laos, Indonesia, Myanmar and Malaysia are among the countries with the poorest data availability and urgently require research.

Phylogeography and genetic variability of the freshwater mussels (Bivalvia: Unionidae) Ellipse, Venustaconcha ellipsiformis (Conrad 1836), and Bleeding Tooth, V. pleasii (Marsh 1891)

Abstract: Following the retreat of the last Pleistocene glaciers ∼10,000 years before present, aquatic organisms re-colonized previously uninhabitable regions from various glacial refuges. Glaciations had major impacts shaping patterns of genetic diversity and population structure for organisms throughout North America. Knowledge of genetic population structure is critical for successful conservation programs involving an increasingly threatened freshwater fauna. Due to variations in life history and ecology, species-specific planning may be the most effective method for preserving rare or threatened species. The Ellipse mussel (Venustaconcha ellipsiformis) and its congener the Bleeding Tooth mussel (V. pleasii) are species of conservation concern through much of their respective ranges in the Midwestern United States. The Ellipse is found in small to medium rivers from the northern Ozark highlands north to the Upper Mississippi River drainage and into tributaries of Lake Michigan and Lake Huron. Mitochondrial DNA from the COI and ND1 regions was amplified to assess the genetic diversity and structure of these species. Phylogenetic analyses confirmed that V. ellipsiformis and V. pleasii are distinct species. Little variation was recovered in the Ellipse with a single common haplotype dominating throughout its range. For Ellipse, only limited genetic differentiation was found among the geographic regions sampled, with consistently significant differentiation only found between populations in the Illinois River drainage and populations in the northern Ozarks. The general low to moderate genetic structure among various geographically distant Ellipse populations suggests this species dispersed rapidly from unglaciated refugia with little time for genetic isolation to occur. The data suggest that V. ellipsiformis populations should be treated as three separate management units: northern Ozark highlands, Upper Mississippi River drainage, and the Illinois River/ Great Lakes drainages.

Comparative analysis of riverscape genetic structure in rare, threatened and common freshwater mussels

Freshwater mussels (Bivalvia: Unionoida) are highly imperiled with many species on the verge of local extirpation or global extinction. This study investigates patterns of genetic structure and diversity in six species of freshwater mussels in the central Great Lakes region of Ontario, Canada. These species vary in their conservation status (endangered to not considered at risk), life history strategy, and dispersal capabilities. Evidence of historical genetic connectivity within rivers was ubiquitous across species and may reflect dispersal abilities of host fish. There was little to no signature of recent disturbance events or bottlenecks, even in endangered species, likely as a function of mussel longevity and historical population sizes (i.e., insufficient time for genetic drift to be detectable). Genetic structure was largely at the watershed scale suggesting that population augmentation via translocation within rivers may be a useful conservation tool if needed, while minimizing genetic risks to recipient sites. Recent interest in population augmentation via translocation and propagation may rely on these results to inform management of unionids in the Great Lakes region.

Competitive Replacement of Invasive Congeners May Relax Impact on Native Species: Interactions among Zebra, Quagga, and Native Unionid Mussels

Determining when and where the ecological impacts of invasive species will be most detrimental and whether the effects of multiple invaders will be superadditive, or subadditive, is critical for developing global management priorities to protect native species in advance of future invasions. Over the past century, the decline of freshwater bivalves of the family Unionidae has been greatly accelerated by the invasion of Dreissena. The purpose of this study was to evaluate the current infestation rates of unionids by zebra (Dreissena polymorpha) and quagga (D. rostriformis bugensis) mussels in the lower Great Lakes region 25 years after they nearly extirpated native unionids. In 2011–2012, we collected infestation data for over 4000 unionids from 26 species at 198 nearshore sites in lakes Erie, Ontario, and St. Clair, the Detroit River, and inland Michigan lakes and compared those results to studies from the early 1990s. We found that the frequency of unionid infestation by Dreissena recently declined, and the number of dreissenids attached to unionids in the lower Great Lakes has fallen almost ten-fold since the early 1990s. We also found that the rate of infestation depends on the dominant Dreissena species in the lake: zebra mussels infested unionids much more often and in greater numbers. Consequently, the proportion of infested unionids, as well as the number and weight of attached dreissenids were lower in waterbodies dominated by quagga mussels. This is the first large-scale systematic study that revealed how minor differences between two taxonomically and functionally related invaders may have large consequences for native communities they invade.

Distribution of Native Mussel (Unionidae) Assemblages in Coastal Areas of Lake Erie, Lake St. Clair, and Connecting Channels, Twenty-Five Years After a Dreissenid Invasion

Abstract Over the past 25 years, unionid mussels in the Laurentian Great Lakes of North America have been adversely impacted by invasive dreissenid mussels, which directly (e.g., by attachment to unionid shells) and indirectly (e.g., by competing for food) cause mortality. Despite the invasion, unionids have survived in several areas in the presence of dreissenid mussels. We investigated current spatial patterns in these native mussel refuges based on surveys for unionid mussels across 48 sampling locations (141 sites) in 2011 and 2012, and documented species abundance and diversity in coastal areas of lakes St. Clair and Erie. The highest-quality assemblages of native mussels (densities, richness, and diversity) appear to be concentrated in the St. Clair delta, where abundance continues to decline, as well as in in Thompson Bay of Presque Isle in Lake Erie and in just a few coastal wetlands and drowned river-mouths in the western basin of Lake Erie. The discovery of several new refuge areas suggests that unionids have a broader distribution within the region than previously thought.

Insular lake island biogeography: using lake metrics to predict diversity in littoral zone mollusk communities

Abstract.  Island biogeography theory can be used to explain patterns of species richness on various types of habitat islands, including freshwater lake systems. Mollusk production in these systems also has been linked to various water-chemistry variables, such as pH, alkalinity, hardness, and specific conductance. We examined how mollusk diversity patterns were related to geographical and limnological factors in insular lakes of the Beaver and Manitou Archipelagos in Lake Michigan (Laurentian Great Lakes), USA. The strongest correlations observed were with shoreline development (r  =  0.80), specific conductance (r  =  0.87), and pH (r  =  0.87). Principal components analysis revealed that isolation by distance and PO43− concentration also may have affected species richness and abundance. Shoreline length was a better predictor of species richness than surface area, but both measures of habitat size were unable to account for much of the variation in species richness. The data suggest that shoreline length and development represent available habitat area more accurately than lake area for primarily littoral-dwelling mollusks. The relatively weak correlations observed with lake area and isolation from Lake Michigan suggest that application of island biogeography theory to predict mollusk species richness using only lake surface area and isolation by distance is limited for freshwater mollusks.

The first Margaritiferidae male (M-type) mitogenome: mitochondrial gene order as a potential character for determining higher-order phylogeny within Unionida (Bivalvia)

This work was partially supported by the Mohamed bin Zayed Species Conservation Fund under project ‘Biodiversity and conservation of the critically endangered freshwater mussels in Morocco: ecogeographic, genetic and physiological information’ (Reference 15256799), by the IUCN SOS Save Our Species fund under project ‘Breeding the most endangered bivalve on Earth: Margaritifera marocana’ (Ref. 2015B-015) and by the Portuguese Foundation for Science and Technology (FCT) under grants SFRH/BPD/70654/ 2010 (M.M.F.) and SFRH/BPD/108445/2015 (E.F.)

Isolation and characterization of microsatellite loci in the freshwater mussel Lasmigona costata (Bivalvia: Unionoida)

Eleven microsatellite loci for the freshwater mussel Lasmigona costata were isolated and characterized. Genetic screening of individuals from four rivers in southern Ontario confirmed that all loci were highly polymorphic. These loci should prove useful in a range of studies from fine- and coarse-scale population structure and gene flow to reproductive success of individuals.

Mitochondrial DNA Structure of Pyganodon grandis (Bivalvia: Unionidae) from the Lake Erie Watershed and Selected Locations in its Northern Distribution

Abstract: The distribution of Pyganodon grandis (Say, 1829) and the entire community of unionid freshwater mussels within the Laurentian Great Lakes became greatly reduced following invasion of dreissenid mussels. While some populations remain, how much gene flow still occurs is not known, nor has the level of population structure been examined within a large lake subsequent to dreissenid infestation. Pyganodon grandis is a common and relatively abundant lacustrine species that utilizes diverse host fish, and, therefore, it may disperse as much as or more than any other unionid species in the region. To test for population structure, we examined a fragment of the maternal mtDNA COI gene from 300 individuals encompassing shallow areas from Lake Eries western and central basins, Sandusky Bay, Lake St. Clair, and the upper Niagara River. Another 94 individuals from the upper Great Lakes and upper Mississippi River watersheds were added to the analysis. A total of 34 different haplotypes were found for P. grandis in the Lake Erie watershed, but just one was common and composed > 80% of all individuals. No other haplotype exceeded a frequency of 2% and most were found only once. Just thirteen haplotypes were found west of Lake Erie, and only the common haplotype and one other were shared with the Lake Erie watershed. However, structure in haplotype frequencies and the presence of one very different clade were limited to samples abutting the Red River of the North. Thus recent population declines in Lake Erie appear not to have significantly impacted levels of genetic variation.