Length‐specific growth rates in freshwater mussels (Bivalvia: Unionidae): extreme longevity or generalized growth cessation?

1. North American lacustrine freshwater mussels (Bivalvia: Unionidae) are one of the world's most imperilled groups of organisms. Knowledge of their age structure and longevity is needed for the understanding and management of mussels. Current methods for age estimation in freshwater mussels are insufficient and may have resulted in an erroneous view of the ages of lacustrine freshwater mussels.
2. We collected growth data through mark-recapture in Minnesota and Rhode Island, U.S.A., examining four lentic populations of three of the most common species of freshwater mussels, Elliptio complanata , Lampsilis siliquoidea , and Pyganodon grandis . Using an inversion of the von Bertalanffy growth equation, we estimated age at length from length-specific growth relationships.
3. In some populations, lacustrine mussels may be much older than previously predicted. Ages predicted from actual growth rates suggest that individuals in some populations frequently reach ages in excess of a century, placing unionid mussels among the Earth's longest-lived animals. Alternatively, if growth has only recently slowed in these populations, generalized growth cessation may be occurring over a broad distributional range of some common North American lacustrine mussels.     

Population genetics and phylogeography of freshwater mussels in North America, Elliptio dilatata and Actinonaias ligamentina (Bivalvia: Unionidae)

Extrinsic and intrinsic forces combined shape the population structure of every species differently. Freshwater mussels are obligate parasites to a host fish during a juvenile stage (glochidia). Elliptio dilatata (ED) and Actinonaias ligamentina (AL) are co-occurring freshwater mussel taxa with similar North American distribution and share some potential host fish. Using mitochondrial DNA, we determined the genotypes of 190 + individuals from collection sites in at least two tributaries in the Lake Erie and Ohio River watersheds, along with the Ouachita and Strawberry rivers in the southeast. Both species had followed a stepping-stone model of dispersal, with greater pairwise genetic structure among collection sites of ED. Also, phylogeographical analysis for ED found significant geographical structuring of haplotype diversity. Overall, within-population variation increased significantly from north to south, with low genetic diversity in the Strawberry River. We calculated significant among-population structure for both species (ED: Phi(ST) = 0.62, P < 0.001; AL: Phi(ST) = 0.16, P < 0.001). Genetic analysis identified the Ouachita River as an area of significant reproductive isolation for both species. Results for AL indicated dispersal into northern areas from two genetically distinct glacial refugia, where results for ED indicated dispersal followed by low gene flow in northern areas. The conservation strategies for mussels that co-occur in the same 'bed' could be species specific. Species such as ED have management units on the population scale, where AL has a more homogeneous genetic structure across its range.     

Reach- and catchment-scale determinants of the distribution of freshwater mussels (Bivalvia: Unionidae) in south-eastern Michigan, U.S.A.

1. We investigated the diversity and distribution of freshwater mussels at 40 sites in an agricultural catchment, the River Raisin in south‐eastern Michigan, to relate mussel assemblages and individual taxa to reach and catchment‐scale variables. Unionids were surveyed by timed searches in 100‐m reaches, and in‐stream and riparian habitat were quantified as well as flow, water chemistry and channel morphology. Land use/cover and surficial geology were determined for site subcatchments and riparian buffers. 2. Some 21 mussel species were found overall; richness ranged from 0 to 12 living species per site. From the upper to middle to lower catchment, the number of individuals, number of species, Shannon–Weaver diversity and relative abundance of intolerant unionids all declined significantly. 3. Four groupings based on overall mussel diversity and abundance were significantly related to reach‐scale habitat variables. The richest mussel assemblages were associated with sites with higher overall habitat quality, greater flow stability, less fine substratum, and lower specific conductance. 4. Stepwise multiple regressions revealed that the distribution and abundance of the total mussel assemblage, as well as the most common species, could be predicted from a combination of reach‐ and catchment‐scale variables (R² = 0.63 for total mussels, R² = 0.51–0.86 for individual species). 5. Flow stability, substratum composition and overall reach habitat quality were the most commonly identified reach‐scale variables, and measures of surficial geology were the most effective catchment‐scale variables. The spatial pattern of geology is likely to be responsible for the diversity gradient from the upper to the lower catchment. 6. Prior studies, attempting to explain mussel distributions from local habitat features alone, have found relatively weak relationships. By employing a combination of reach‐ and catchment‐scale habitat variables, this study was able to account for a substantial amount of the spatial variability in mussel distributions.     

Molecular genetics of peripheral populations of Nova Scotian Unionidae (Mollusca: Bivalvia)

Peripheral populations of eight species of freshwater bivalves (Unionidae.) extending their geographic ranges into Nova Scotia, Canada, were examined electrophoretically to determine both the extent of genetic variability within such populations, and whether the hypothesized pathway of colonization across the Isthmus of Chignecto is reflected in patterns of genetic resemblance among these populations. The Nova Scotian species examined could be separated into two groups based on levels of observed heterozygosity and levels of variability in allele frequencies. The first group is characterized by low levels of heterozygosity and polymorphism compared with north-eastern American populations, and in the case of one species, Elliptio complanala, considerable variability in allele frequencies among populations occurring in similar habitats in different drainages. Populations of E. complanata from Nova Scotia can be differentiated from conspecific populations on the southern Atlantic Slope by possession of fast alleles at two loci. Multivariate analyses define subgroups within populations of E. complanata consistent with hypothesis that the species invaded Nova Scotia by way of the Isthmus of Chignecto, and then split into two groups, one of which colonized Cape Breton to the north and the other of which colonized southern areas of the Province. The second group of Nova Scotian species is characterized by little reduction in heterozygosity and polymorphism compared with values observed among north-eastern American conspecifics or congeners, little variability in allele frequencies from population to population, and little evidence to suggest that these species were dependent on the land bridge to invade the Province. The type of dispersal is hypothesized to be responsible, in part, for these differences: larvae of species in the first group rely on a parasitic attachment to fish with territorial habits limited to fresh water, and are thus likely to invade new drainages separated by salt water by chance, in small numbers, and in stepping-stone fashion. Species in the second group parasitize anadromous or saltwater tolerant hosts, are likely to be introduced into new habitats in greater numbers and/or receive greater amounts of gene flow subsequent to colonization, and seem less dependent on land-bridges to colonize new habitats.     

Comparison of oxygen consumption in freshwater mussels (Unionidae) from different habitats during declining dissolved oxygen concentration

The rate of oxygen consumption (OC) of 9 species of freshwater mussels was measured under declining dissolved oxygen (DO) concentrations. The effects of temperature for some species also was investigated. The pattern of the OC vs. DO curve for each species was used in a hyperbolic model to compare abilities to regulate OC under low oxygen conditions. At 24.5 °C, Pyganodon grandis (from lakes), Amblema plicata and Quadrula pustulosa (from mud or sand in large rivers), Elliptio complanata (from pool areas in rivers), and Elliptio fisheriana and Elliptio lanceolata (from bank margins of rivers) were better able to maintain OC under low DO than were Villosa iris and Villosa constricta (which inhabit riffles) and Pleurobema cordatum (found in rivers with moderate flow). Villosa iris was especially sensitive to low oxygen conditions. The ability to maintain normal OC at low DO was improved considerably at 16.5 °C for V. iris, P. grandis and E. complanata. It is concluded that oxygen regulation ability appears to be related to the degree of hypoxia a species normally experiences in its habitat type, and it is enhanced at low temperature. The measurement of OC vs. DO may be a useful technique for estimating DO water quality criteria for endangered species because it is noninvasive.     

Unravelling the systematics of Nodularia (Bivalvia,Unionidae) species from eastern Russia

Conservation efforts have been hindered by data deficient conservation status assessments, especially due to taxonomic problems. This is especially true for many eastern Russian species of freshwater mussels, where distinct classification systems have complicated their delimitation and identification. Nodularia is a widespread eastern Asian freshwater mussel genus, present from Vietnam in the south to the Magadan region in eastern Russia in the north. The number of recognized species in the genus Nodularia in eastern Russia has been inflated over the last several decades due to the use of a typological species concept, the so-called 'Comparatory Method'. This method uses a single diagnostic character for species delimitation, i.e., the arc of maximal convexity of the shell's outline. Using this classification system, 10 species were recognized for far eastern Russia under the genus Nodularia Conrad, 1853, divided into three subgenera: Nodularia s. str., Amurunio and Magadaninaia. Since it is not supported by any other classification methods, the current comparatory classification is rejected by many Russian and international scientists, who only recognize a single species for that region, i.e., Nodularia douglasiae. Therefore, the aim of the present study is to clarify the taxonomy and systematics of the Nodularia genus in far eastern Russia and adjacent territories, using a multiple dataset approach that combines distribution with detailed conchological and anatomical analyses with morphometry and COI barcoding molecular techniques. All analyses performed in this study support the existence of a single Nodularia species in eastern Russia, i.e., N. douglasiae.     

Global diversity of freshwater mussels (Mollusca, Bivalvia) in freshwater

The term freshwater bivalve is very inclusive and not very informative. There are representatives of at least 19 families that have at least one representative living in freshwater. This suggests at least 14 different invasions of freshwater. At least nine families have small to large radiations in the freshwater environment: Corbiculidae, Sphaeriidae, Dreissenidae, and the unioniforme families: Hyriidae, Margaritiferidae, Unionidae, Etheriidae, Iridinidae, and Mycetopodidae. The unioniforme families contain at least 180 genera and about 800 species. This order is characterized by the unique parasitic larval stage on the gills, fins or the body of a particular host fish. This order of freshwater bivalves is suffering a very high rate of extinction, with about 37 species considered presumed extinct in North America alone. The level of endangerment and extinction facing these animals is primarily the result of habitat destruction or modification. Guest editors: E. V. Balian, C. Lévêque, H. Segers & K. Martens Freshwater Animal Diversity Assessment     

Estimating the biomass of freshwater mussels (Bivalvia: Unionidae) from shell dimensions

Packs of autumn-shed maple leaves were placed at coal ash effluent-exposed and reference sites in streams on December 5, 1977 and removed after 27 and 96 days. Leaf surface area (cm²/leaf) and disc weight (ash-free dry wt/15 mm disc) were greater at the effluent-exposed site than at the reference site after 96 days (p < .001). ATP content of leaves from the reference stream quadrupled between 27 and 96 days while ATP content of effluent-exposed leaves remained low. Macroinvertebrates colonized the leaf packs in the reference site but were not found on or in effluent-exposed packs. We concluded that leaf processing beyond the leaching of soluble organics did not occur in the effluent-exposed packs owing to reduced colonization and decomposition by fungi. Since stream invertebrates prefer decomposed leaf material and animals grow faster on leaves colonized by microbes, the ash effuent appears to indirectly affect macroinvertebrates by interfering with leaf decomposition and thus reducing the quality of their food.     

Molecular phylogenetic analysis of tropical freshwater mussels (Mollusca: Bivalvia: Unionoida) resolves the position of Coelatura and supports a monophyletic Unionidae

In previous molecular phylogenetic analyses of the freshwater mussel family Unionidae (Bivalvia: Unionoida), the Afrotropical genus Coelatura had been recovered in various positions, generally indicating a paraphyletic Unionidae. However that result was typically poorly supported and in conflict with morphology-based analyses. We set out to test the phylogenetic position of Coelatura by sampling tropical lineages omitted from previous studies. Forty-one partial 28S nuclear rDNA and partial COI mtDNA sequences (1130 total aligned nucleotides) were analyzed separately and in combination under both maximum parsimony and likelihood, as well as Bayesian inference. There was significant phylogenetic incongruence between the character sets (partition homogeneity test, p < 0.01), but a novel heuristic for comparing bootstrap values among character sets analyzed separately and in combination illustrated that the observed conflict was due to homoplasy rather than separate gene histories. Phylogenetic analyses robustly supported a monophyletic Unionidae, with Coelatura recovered as part of a well-supported Africa–India clade (= Parreysiinae). The implications of this result are discussed in the context of Afrotropical freshwater mussel evolution and the classification of the family Unionidae.     

Population genetics of the freshwater mussel, <Emphasis Type="Italic">Amblema plicata</Emphasis> (Say 1817) (Bivalvia: Unionidae): Evidence of high dispersal and post-glacial colonization

Over 70% of North American freshwater mussel species (families Unionidae and Margaritiferidae) are listed as threatened or endangered. Knowledge of the genetic structure of target species is essential for the development of effective conservation plans. Because Ambelma plicata is a common species, its population genetic structure is likely to be relatively intact, making it a logical model species for investigations of freshwater mussel population genetics. Using mtDNA and allozymes, we determined the genotypes of 170+ individuals in each of three distinct drainages: Lake Erie, Ohio River, and the Lower Mississippi River. Overall, within-population variation increased significantly from north to south, with unique haplotypes and allele frequencies in the Kiamichi River (Lower Mississippi River drainage). Genetic diversity was relatively low in the Strawberry River (Lower Mississippi River drainage), and in the Lake Erie drainage. We calculated significant among-population structure using both molecular markers (A.p. Φ_st = 0.15, θ_st = 0.12). Using a hierarchical approach, we found low genetic structure among rivers and drainages separated by large geographic distances, indicating high effective population size and/or highly vagile fish hosts for this species. Genetic structure in the Lake Erie drainage was similar to that in the Ohio River, and indicates that northern populations were founded from at least two glacial refugia following the Pleistocene. Conservation of genetic diversity in Amblema plicata and other mussel species with similar genetic structure should focus on protection of a number of individual populations, especially those in southern rivers.     

Thermal sensitivity of metabolic enzymes in subarctic and temperate freshwater mussels (Bivalvia: Unionoida)

Temperature has a major impact on the physiological processes of freshwater invertebrates. Despite the endangered status of many freshwater mussel species and the potential effect of global warming on North America’s northern aquatic habitats, thermal sensitivity of the metabolic apparatus of freshwater bivalves has received little attention. By examining the thermal sensitivity of 10 key metabolic enzymes and in situ growth rates of latitudinally separated populations (temperate and subarctic) of two closely-related Pyganodon species from northeastern North America, we provide the first insights into thermal sensitivity of key enzymes of energy and reactive oxygen species metabolism in relation to habitat localization and growth performance. The subarctic population of Pyganodon grandis displayed higher in situ growth rates than the temperate population of Pyganodon fragilis. The subarctic population of P. grandis had a lower mitochondrial capacity as expressed by citrate synthase and cytochrome c oxidase but displayed similar electron transport system (ETS) and higher isocitrate dehydrogenase capacities. Our results suggest that higher growth performance of the subarctic population of P. grandis is not associated with higher aerobic capacity. The high thermal sensitivity of mitochondrial enzymes in subarctic population of P. grandis might rather reflect enhanced stenothermy. The higher electron transport system/cytochrome c oxidase ratio for the subarctic P. grandis species than P. fragilis might affect mitochondrial regulation or reactive oxygen species production. Antioxidant enzymes displayed lower Q₁₀s suggesting thermal independence of antioxidant capacity.     

Isolation and characterization of microsatellite loci in Alasmidonta heterodon (Bivalvia: Unionidae)

We developed 13 species‐specific microsatellite markers for the federally endangered Atlantic slope unionid Alasmidonta heterodon. Four to 18 alleles per locus were observed among 30 individuals. Observed heterozygosity throughout the loci ranged from 26.9 to 86.2% and averaged 63.6%. Estimates of individual pairwise genetic distances indicated that levels of genetic diversity among loci were sufficient to produce unique multilocus genotypes for all animals surveyed. Randomization tests showed that genotypes for this collection were consistent with Hardy–Weinberg expectations, and no significant linkage disequilibrium was observed between loci. These loci therefore appear suitable for population surveys, kinship assessment and other such applications.     

Sediment particles as a cause of nacre staining in the freshwater mussel,Amblema plicata (Say) (Bivalvia: Unionidae)

Brown stains sometimes appear in the inner shell layers (nacre) of freshwater mussels. An electron microprobe was used to analyze the stained nacre of the unionid Amblema plicata (Say, 1817) from selected localities on the Mississippi River in the vicinity of LaCrosse and Prairie du Chien, Wisconsin.Several elements such as Na, Mg, Al, Si, P, S, Cl, K, and Fe are more highly concentrated in stained than in unstained nacre. Concentrations of these elements relative to Ca were found to vary significantly among the localities from which the specimens were obtained. Ratios have significantly higher variances downstream of the confluence of the Yellow and Mississippi Rivers, downstream of a barge fleeting area, near the town of Marquette, Iowa, near the site of sewage effluent for Prairie du Chien, Wisconsin and downstream of a scrap metal yard near LaCrosse, Wisconsin in contrast to control localities.Suspended silt, the result of runoff and river activity (barge traffic, dredging, pleasure boating) may be the stimulus for stain formation. Clay minerals adsorb accessory elements and in turbid water are trapped within the pallial space of A. plicata. The mussel secretes an organic-rich, periostracum-like layer over the entrapped sediment, and later reverts to prismatic and finally nacreous shell deposition. Some of the elements found in the stain could directly disturb Ca metabolism by competing with Ca for binding sites in shell aragonite.     

Sexual selection and simultaneous hermaphroditism among the Unionidae (Bivalvia: Mollusca)

Simultaneous hermaphroditism is an infrequent mode of reproduction among bivalves of the family Unionidae: only five of the 220 North American species are simultaneous hermaphrodites. However, hermaphroditic individuals of otherwise predominantly dioecious species have been encountered in 30 of I01 species examined. These hermaphroditic individuals as well as simultaneous hermaphrodites can exhibit considerable variability in the ratio of spermatogenic: oogenic tissue within the gonad, and the purposes of this paper are to determine the underlying causes of both this variability and the occurrence of occasional hermaphroditic individuals among dioecious species. Results indicate that the ratio of male: female gonodal tissue of a simultaneous hermaphrodite is bimodally distributed, and several hypotheses to account for this observation are presented. It is proposed that populations occurring in different habitats and under conditions of different individual density are subject to fundamentally different sexual selection pressures acting on ratios of allocation to male and female gametes. Occasional hermaphroditism among otherwise predominantly dioecious species was in this study associated with infection of the gonads by digenean trematodes. A model of sexual determination among unionids presented in this paper proposes that sex is determined by genetically controlled hormone levels: occasional hermaphrodites result from alterations in these hormone levels caused by developmental errors and trematodal infections which mimic the results of such errors. Predictions of this model are consistent with observed levels of variability in male: females gonadal tissue among occasional hermaphrodites.     

Population size and structure of three mussel species (Bivalvia: Unionidae) in a northeastern German river with special regard to influences of environmental factors

Unionid mussels are of great ecological importance in running and standing waters, however their populations declined continually during the 20th century. In order to collect more data on the situation of these mussels in running waters, the populations of Anodonta anatina, Anodonta cygnea, and Unio tumidus (Unionidae) were investigated in the northeastern German river Ryck from 1996 to 1998. At three sampling stations along the river, the mussel stocks as well as sediment and water properties were analyzed. In this river abundances of up to 138.7 indiv./m² were detected. The average population densities varied from 10.9 to 34.9 indiv./m². More critically however, the age structures showed significant signs of irregular reproductive success and overaging. Consequently, the mussel stocks are going to decline, and furthermore, U.tumidus should be listed as an endangered species in the Ryck river. Negative influences on bivalves can be expected from sporadically occurring low oxygen and high ion concentrations in the water. But after all, the conditions within the sediments seem to be decisive for the survival of juvenile mussels and thus for the age structure of the populations.     

通过RAPD分析揭示五种淡水无齿蚌（软体动物门：双壳类）的遗传多样性

Unionidae(Bivalvia)are distributed infreshwaters,and represent a significanttaxonof benthic community[1].In China,freshwater mussels are abundant resources[2].Since1949,substantial investigations onthe unionidfau-na had been undertakenin China[3—8].Withreference tooverseas research[9,10],a preliminary reorganization onthe Unionidae was performed accordingtosome classifica-tion characteristics such as shell shape,larvae character-istics,and breeding habit[11].Due tothe serious conver-gence o…     

Life history traits and abundance can predict local colonisation and extinction rates of freshwater mussels

1. A critical need in conservation biology is to determine which species are most vulnerable to extinction. Freshwater mussels (Bivalvia: Unionacea) are one of the most imperilled faunal groups globally. Freshwater mussel larvae are ectoparasites on fish and depend on the movement of their hosts to maintain connectivity among local populations in a metapopulation. 2. I calculated local colonisation and extinction rates for 16 mussel species from 14 local populations in the Red River drainage of Oklahoma and Texas, U.S. I used general linear models and AIC comparisons to determine which mussel life history traits best predicted local colonisation and extinction rates. 3. Traits related to larval dispersal ability (host infection mode, whether a mussel species was a host generalist or specialist) were the best predictors of local colonisation. 4. Traits related to local population size (regional abundance, time spent brooding) were the best predictors of local extinction. The group of fish species used as hosts by mussels also predicted local extinction and was probably related to habitat fragmentation and host dispersal abilities. 5. Overall, local extinction rates exceeded local colonisation rates, indicating that local populations are becoming increasingly isolated and suffering an ‘extinction debt’. This study demonstrates that analysis of species traits can be used to predict local colonisation and extinction patterns and provide insight into the long‐term persistence of populations.     

Geometrical and crystallographic constraints determine the self-organization of shell microstructures in Unionidae (Bivalvia: Mollusca)

Unionid shells are characterized by an outer aragonitic prismatic layer and an inner nacreous layer. The prisms of the outer shell layer are composed of single-crystal fibres radiating from spheruliths. During prism development, fibres progressively recline to the growth front. There is competition between prisms, leading to the selection of bigger, evenly sized prisms. A new model explains this competition process between prisms, using fibres as elementary units of competition. Scanning electron microscopy and X-ray texture analysis show that, during prism growth, fibres become progressively orientated with their three crystallographic axes aligned, which results from geometric constraints and space limitations. Interestingly transition to the nacreous layer does not occur until a high degree of orientation of fibres is attained. There is no selection of crystal orientation in the nacreous layer and, as a result, the preferential orientation of crystals deteriorates. Deterioration of crystal orientation is most probably due to accumulation of errors as the epitaxial growth is suppressed by thick or continuous organic coats on some nacre crystals. In conclusion, the microstructural arrangement of the unionid shell is, to a large extent, self-organized with the main constraints being crystallographic and geometrical laws.     

Population genetic structure, gene flow and sex-biased dispersal in frillneck lizards (Chlamydosaurus kingii)

By using both mitochondrial and nuclear multiloci markers, we explored population genetic structure, gene flow and sex-specific dispersal of frillneck lizards ( Chlamydosaurus kingii ) sampled at three locations, separated by 10 to 50 km, in a homogenous savannah woodland in tropical Australia. Apart from a recombinant lizard, the mitochondrial analyses revealed two nonoverlapping haplotypes/populations, while the nuclear markers showed that the frillneck lizards represented three separate clusters/populations. Due to the small population size of the mtDNA, fixation may occur via founder effects and/or drift. We therefore suggest that either of these two processes, or a combination of the two, are the most likely causes of the discordant results obtained from the mitochondrial and the nuclear markers. In contrast to the nonoverlapping mitochondrial haplotypes, in 12 out of 74 lizards, mixed nuclear genotypes were observed, hence revealing a limited nuclear gene flow. Although gene flow should ultimately result in a blending of the populations, we propose that the distinct nuclear population structure is maintained by frequent fires resulting in local bottlenecks, and concomitant spatial separation of the frillneck lizard populations. Limited mark–recapture data and the difference in distribution of the mitochondrial and nuclear markers suggest that the mixed nuclear genotypes were caused by juvenile male-biased dispersal.