Impact of Dreissena fouling on the physiological condition of native and invasive bivalves: interspecific and temporal variations

The impact of Dreissena fouling on unionids has hardly been studied in Europe, despite the fact that in some ecosystems (e.g. Lake Balaton, Hungary) infestations of several hundreds to a thousand individuals per unionid have been observed. At present, the zebra mussel Dreissena polymorpha is a dominant species in Lake Balaton and in the last decade three other invasive bivalves were introduced, potentially increasing the pressure on native unionid survival. We examined whether the fouling of dreissenids (zebra and quagga (D. rostriformis bugensis) mussels) has a negative impact on native (Anodonta anatina, Unio pictorum and U. tumidus) and invasive (Corbicula fluminea and Sinanodonta woodiana) bivalves and whether there are any interspecific and temporal variations in fouling intensity and physiological condition measured by standard condition index and glycogen content. A significant negative impact was detected on native unionids only in July and September (no impact was detected in May), when the fouling rate was high. For invasive species, a significant negative impact was detected on S. woodiana with a high level of dressenid infestation; whereas no significant impact was detected on C. fluminea. Overall, this study confirms that Dreissena may threaten unionid species including the invasive S. woodiana, although high interspecific and temporal variations were observed. This situation should be taken into account in future ecological and conservational assessments because species respond differently to Dreissena fouling and effects seem to be more pronounced in late summer/early autumn. In addition, this study provides the first evidence that the invasive C. fluminea appear to be less vulnerable to dressenid fouling.     

Scale-dependent associations between native freshwater mussels and invasive Corbicula

In North America there is conflicting evidence concerning whether the invasive Asian clam, Corbicula fluminea, and native mussels (Unionidae), can successfully co-exist. One reason underlying disparate conclusions may be the different spatial scales at which data have been collected. We compared the distribution and abundance of native unionid mussels and Corbicula at two spatial scales, stream reaches and 0.25 m² patches, within one biogeographic region, the Ouachita Highlands, of the south central U.S. We found that Corbicula abundance was negatively related to native mussel abundance at small spatial scales. While Corbicula densities varied widely in patches without native mussels, and in patches where mussels occurred at low abundance, Corbicula density was never high in patches where mussels were dense. We hypothesize that the likelihood of successful Corbicula invasion decreases with increasing abundance of adult native mussels. Several mechanisms may potentially drive this pattern including lack of space for Corbicula to colonize, physical displacement by actively burrowing mussels, and locally reduced food resources in patches where native mussels are feeding. In addition, Corbicula may be unable to withstand environmental bottlenecks as readily as unionids. When patch-scale density and biomass information were pooled to represent entire stream reaches, the negative relationship between native mussels and Corbicula was no longer as apparent, and there was not a significant relationship between native mussels and Corbicula. These results point to the importance of appropriate sample scale in examining potential associations between species.     

Shell decay rates of native and alien freshwater bivalves and implications for habitat engineering

1. Spent shells of bivalves can provide habitat for other organisms, as well as playing important roles in biogeochemical cycles. The amount of spent shell material that will accumulate at a site depends on rates of both shell production and decay, although the latter is rarely considered. 2. We measured the instantaneous decay rates of four species of freshwater bivalves across a range of sites in south‐eastern New York, and found that rates varied by more than 500‐fold across sites and species. 3. Differences in decay rates were related to water chemistry (Ca, pH, dissolved inorganic C), the presence of a current, and the size of the bivalve shell. 4. Combining these decay rates with estimates of shell production derived from the literature, we conclude that the Unionidae, Corbicula, and Dreissena are all capable of producing large accumulations (>10 kg dry mass m⁻²) of spent shells, while members of the Sphaeriidae probably rarely will produce such large accumulations. 5. Hence the replacement of native unionid bivalves by the alien Corbicula and Dreissena may have little effect on standing stocks of spent shells, unless the aliens invade sites where unionids are scarce or absent.     

Do Zebra Mussels Grow Faster on Live Unionids than on Inanimate Substrate? A Study with Field Enclosures

The zebra mussel Dreissena polymorpha has invaded numerous freshwaters in Europe and North America and can foul many types of solid substrates, including unionid bivalves. In field experiments we compared growth rates of dreissenids on live specimens of the freshwater bivalve Anodonta cygnea to growth rates of dreissenids on stones. Dreissena density in the study lake was about 1000 m^–2 in most places, Anodonta density approximately 1 m^–2 and about 50% of the Anodonta were infested with 10–30 Dreissena . In summer/autumn small dreissenids generally grew faster on live Anodonta than on stones. Similar trends were observed for spring, but differences of growth increments between dreissenids on live Anodonta and stones were usually not significant. Dreissenids settled down or moved towards the ingestion/egestion siphons of Anodonta and ingestion siphons of dreissenids were directed towards siphons of Anodonta . These results suggest that dreissenids can use the food provided by the filter current of the large Anodonta . (© 2006 WILEY‐VCH Verlag GmbH & Co. KGaA, Weinheim)     

Can suspension feeding by bivalves regulate phytoplankton biomass in Lake Waccamaw, North Carolina?

Suspension feeding by bivalves has been hypothesized to control phytoplankton biomass in shallow aquatic ecosystems. Lake Waccamaw, North Carolina, USA is a shallow lake with a diverse bivalve assemblage and low to moderate phytoplankton biomass levels. Filtration and ingestion rates of two relatively abundant species in the lake, the endemic unionid, Elliptio waccamawensis, and an introduced species, Corbicula fluminea, were measured in experiments using natural phytoplankton for durations of 1 to 6 days. Measured filtration and ingestion rates averaged 1.78 and 1.121 ind.^–1 d^–1, much too low to control phytoplankton at the observed phytoplankton biomass levels and growth rates. Measured ingestion rates averaged 4.80 and 1.50 µg chlorophyll a ind.^–1 d^–1, too low to support individuals of either species. The abundance of benthic microalgae in Lake Waccamaw reaches 200 mg chlorophyll a m^–2 in the littoral zone and averages almost an order of magnitude higher than depth-integrated phytoplankton chlorophyll a. Total microalgal biomass in the lake is therefore not controlled by suspension feeding by bivalves.     

Potential effects on zooplankton from species shifts in planktivorous mussels: a field experiment in the St Lawrence River

1. Suspension feeding by bivalves exceeds that by other planktivores in many North American rivers, and food webs may be altered substantially by differences in feeding patterns between native unionid mussels and invading dreissenid mussels. 2. We conducted an experiment comparing zooplanktivory by one unionid and two dreissenid species that addressed several primary questions. Is benthic planktivory important in this river? Has this linkage been altered substantially by dreissenids? Do the two dreissenid species differ in planktivory, and is this ecologically important if quagga mussels extend their geographical range? 3. Our 12‐day experiment consisted of controls (no mussels) and treatments with unionid (Elliptio complanata), quagga (Dreissena bugensis) or zebra (D. polymorpha) mussels in 3500‐L, 80‐μm mesh enclosures placed in a slackwater area of the St Lawrence River. 4. The density of the most abundant calanoid copepod Eurytemora affinis increased in the presence of dreissenids, probably as an indirect food web response. By day 12, a cumulative effect was shown by the most overwhelmingly abundant rotifer, Polyarthra, whose density declined dramatically in dreissenid enclosures compared with control and unionid enclosures. Rotifer densities in unionid enclosures were not different from controls, nor were dreissenid treatments different from each other. The effects on rotifers were probably from predation, as Chl‐a did not vary among treatments. 5. We conclude that benthic‐pelagic coupling via planktivory is important in slackwater areas. Dreissenids have strengthened this linkage, but range extension of quaggas should not appreciably alter effects produced by a similar biomass of zebra mussels.     

Distribution, abundance, and roles of freshwater clams (Bivalvia, Unionidae) in the freshwater tidal Hudson River

1. An extensive series of PONAR grabs was used to determine the distribution and abundance of unionid clams in the freshwater tidal Hudson River. 2. The five species of unionids collected were distributed very unevenly within the river. Mean river-wide density and biomass of unionids were 8.0m^?2 and 6.2 g DM m^?2 (shell-free)., respectively. 3. The environmental variables that we measured (water depth, distance from shore, sediment granulometry and organic content, presence or absence of macrophytes, and the chlorophyll a and particulate organic matter content of the water) explained little of the variation in abundance of unionids. 4. The distributions of the various species of clams did not differ significantly with respect to the environmental variables measured. 5. We estimate that unionids filter a significant amount of water (0.14m³ m^?2 day^?1, on average) in the Hudson River estuary, roughly equivalent in magnitude to downstream flushing. 6. We project that unionids will serve as a major substratum for the settlement of the zebra mussel (Dreissena polymorpha), which is now invading the estuary. We emphasize that unionids may play important non-trophic roles in large river ecosystems.     

Habitat characteristics contributing to local occupancy and habitat use in rock pool <Emphasis Type="Italic">Daphnia</Emphasis> metapopulations

The effects of invasive macrophytes, water level fluctuations and predation on freshwater unionids Pyganodon grandis and Utterbackia imbecillis were studied in three small impoundments in Northeastern Texas in 2003–2005. Mussel density was sampled with quadrats. Mortality, associated with the water level fluctuations and predation, was estimated by collecting dead shells on the shore at about two month intervals. In two ponds, horizontal distribution of unionids was limited by dense beds of invasive and noxious macrophytes (mainly Eurasian watermilfoil Myriophyllum spicatum and American lotus Nelumbo lutea): mussel densities were significantly lower in these macrophyte beds (P < 0.001). In the third pond with the lowest density of macrophytes (stonewort Chara sp.), unionids were distributed more evenly, and the average unionid biomass was the highest among all ponds studied. Vertical distribution of unionids in all ponds was likely limited by low oxygen at depth >2 m. The total amount of shells found on the shore per year varied from 0.1% to 28% of the total population in the pond and was negatively correlated with water level (r = −0.72 to −0.81, P < 0.005). Mammalian predators consumed up to 19% of the total unionid population and predation was facilitated by water level fluctuations. Handling editor: K. Martens     

Mechanisms and impact of differential fouling of the zebra mussel Dreissena polymorpha on different unionid bivalves

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The functional role of burrowing bivalves in freshwater ecosystems

1. Freshwater systems are losing biodiversity at a rapid rate, yet we know little about the functional role of most of this biodiversity. The ecosystem roles of freshwater burrowing bivalves have been particularly understudied. Here we summarize what is known about the functional role of burrowing bivalves in the orders Unionoida and Veneroida in lakes and streams globally. 2. Bivalves filter phytoplankton, bacteria and particulate organic matter from the water column. Corbicula and sphaeriids also remove organic matter from the sediment by deposit feeding, as may some unionids. Filtration rate varies with bivalve species and size, temperature, particle size and concentration, and flow regime. 3. Bivalves affect nutrient dynamics in freshwater systems, through excretion as well as biodeposition of faeces and pseudofaeces. Excretion rates are both size and species dependent, are influenced by reproductive stage, and vary greatly with temperature and food availability. 4. Bioturbation of sediments through bivalve movements increases sediment water and oxygen content and releases nutrients from the sediment to the water column. The physical presence of bivalve shells creates habitat for epiphytic and epizoic organisms, and stabilizes sediment and provides refugia for benthic fauna. Biodeposition of faeces and pseudofaeces can alter the composition of benthic communities. 5. There is conflicting evidence concerning the role of resource limitation in structuring bivalve communities. Control by bivalves of primary production is most likely when their biomass is large relative to the water volume and where hydrologic residence time is long. Future studies should consider exactly what bivalves feed upon, whether feeding varies seasonally and with habitat, and whether significant overlap in diet occurs. In particular, we need a clearer picture of the importance of suspension versus deposit feeding and the potential advantages and tradeoffs between these two feeding modes. 6. In North America, native burrowing bivalves (Unionidae) are declining at a catastrophic rate. This significant loss of benthic biomass, coupled with the invasion of an exotic burrowing bivalve (Corbicula), may result in large alterations of ecosystem processes and functions.     

Zebra Mussel Infestation of Unionid Bivalves (Unionidae) in North America

SYNOPSIS. In 1989, zebra mussels received national attentionin North America when they reached densities exceeding 750,000/m2in a water withdrawal facility along the shore of western LakeErie of the Laurentian Great Lakes. Although water withdrawalproblems caused by zebra mussels have been of immediate concern,ecological impacts attributed to mussels are likely to be themore important long-term issue for surface waters in North America.To date, the epizoic colonization (i.e., infestation) of unionidbivalve mollusks by zebra mussels has caused the most directand severe ecological impact. Infestation of and resulting impactscaused by zebra mussels on unionids in the Great Lakes beganin 1988. By 1990, mortality of unionids was occurring at somelocations; by 1991, extant populations of unionids in westernLake Erie were nearly extirpated; by 1992, unionid populationsin the southern half of Lake St. Clair were extirpated; by 1993,unionids in widely separated geographic areas of the Great Lakesand the Mississippi River showed high mortality due to musselinfestation. All infested unionid species in the Great Lakes(23) have become infested and exhibited mortality within twoto four years after heavy infestation began. Data indicate thatmean zebra mussel densities >5,000–6,000/m² and infestationintensities >100-200/unionid in the presence of heavy zebramussel recruitment results in near total mortality of unionids.At present, all unionid species in rivers, streams, and akesthat sympatrically occur with zebra mussels have been infestedand, in many locations, negatively impacted by zebra mussels.We do not know the potential consequences of infestation onthe 297 unionid species found in North America, but believezebra mussels pose an immediate threat to the abundance anddiversity of unionids.     

High abundance of an invasive species gives it an outsized ecological role

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Decline of unionid mussels enhances hybridisation of native and introduced bitterling fish species through competition for breeding substrate

1. Bitterling fishes (Subfamily: Acheilognathinae) spawn in the gills of living freshwater mussels and obligately depend on the mussels for reproduction. On the Matsuyama Plain, Japan, populations of unionid mussels—Pronodularia japanensis, Nodularia douglasiae, and Sinanodonta lauta—have decreased rapidly over the past 30 years. Simultaneously, the population of a native bitterling fish, Tanakia lanceolata, which depends on the three unionids as a breeding substrate, has decreased. Furthermore, a congeneric bitterling, Tanakia limbata, has been artificially introduced, and hybridisation and genetic introgression occur between them. Here, we hypothesised that decline of the unionids has enhanced this invasive hybridisation through competition for the breeding substrate.
2. Three study sites were set in three streams on the Matsuyama Plain. We collected adult bitterling fishes (native T. lanceolata, introduced T. limbata, and foreign Rhodeus ocellatus ocellatus) once a week from April to October 2013 to measure their densities in streams and to examine seasonal differences in female ovipositor length, which elongates in the breeding season. Simultaneously, we set quadrats and captured unionids and measured environmental conditions. Each unionid individual was kept separately in its own aquarium to collect ejected bitterling eggs/larvae. Tanakia eggs and larvae were genotyped using six microsatellite markers and the mitochondrial cytochrome b gene.
3. Introduced T. limbata was more abundant, had a longer breeding period, and produced more juveniles than native T. lanceolata. Hybrids between the two species occurred at all sites, and in total 101 of the 837 juveniles genotyped were hybrids. The density of P. japanensis was low, at most 0.42 individuals/m². Nodularia douglasiae and S. lauta have nearly or totally disappeared from these sites. Hybrid clutches of Tanakia species occurred more frequently where the local density of P. japanensis was low. Mussels were apparently overused and used simultaneously by three species of bitterlings.
4. Decline of freshwater unionid populations has enhanced hybridisation of native and invasive bitterling fishes through increasing competition for breeding substrate. We showed that rapid decline of host mussel species and introduction of an invasive congener have interacted to cause a rapid decline of native bitterling fish.
5. Degradation of habitat and the introduction of invasive species interact to cause a cascade of extinctions in native species. In our study, obligate parasite species are threatened because the host species are disappearing, which means there is a serious threat of coextinction.

     

Cholinesterases from the marine mussels Mytilus galloprovincialis Lmk. and M. edulis L. and from the freshwater bivalve Corbicula fluminea Müller

In order to improve the molecular basis for the use of bivalve cholinesterases as a reliable biomarker for aquatic pollution, the polymorphism and characterization of these enzymes in Mytilus edulis, Mytilus galloprovincialis and Corbicula fluminea were investigated. All results are consistent with the presence of only one pharmacological form of cholinesterase in each species. The molecular masses were 180 kDa for the two marine mussels and 240 kDa for C. fluminea. The cholinesterases are anchored to the membrane by a glycosyl inositol phosphate like the G^a form (type I) described in vertebrates. Surprisingly, these cholinesterases were poorly inhibited by organophosphorous compounds compared to enzymes from other sources. This suggests that these bivalves could be used as a biomarker for acute rather than chronic contaminations by anticholinesterase insecticides.     

An indirect effect of biological invasions: the effect of zebra mussel fouling on parasitisation of unionid mussels by bitterling fish

Invasive species represent a major threat with both direct and indirect effects on natural ecosystems, including effects on established and coevolved relationships. In a series of experiments, we examined how the interaction between two native species, a unionid mussel (Unio pictorum) and the European bitterling (Rhodeus amarus), a fish that parasitises unionids, was affected by the non-native zebra mussel (Dreissena polymorpha). The zebra mussel fouls hard substrates, including shells of living unionids, and its presence is often associated with a decrease in population density of native unionid mussels. Bitterling lay their eggs into live unionids and the embryos develop inside their gills. Using a range of zebra mussel densities, we demonstrated that zebra mussel fouling had a negative effect on the number of bitterling eggs inside the mussel host, with abundances of 5–10 zebra mussels (shell size 15–25 mm) per unionid critical for bitterling ability to utilise the host. In a further experiment, we found that bitterling did not discriminate between unfouled unionids and those fouled with five zebra mussels. Most ovipositions into fouled hosts, however, were unsuccessful as eggs failed to reach the unionid gills. We discuss implications of such unsuccessful ovipositions for bitterling recruitment and population dynamics.     

贝类壳-体质量比和静水沉降特性的相关性

软体动物贝壳表型是适应性进化的结果,为探究贝壳形态特性与软体动物随水流扩散功能的相关性,实验选取9种具代表性的腹足纲和双壳纲贝类作为研究对象,研究了其成体的壳-体质量比与静水沉降特性及二者的相关性。结果表明：体质量的变异系数（C.V.=1.11）大于壳长（C.V.=0.67）、壳宽（C.V.=0.54）的变异系数;壳-体质量比具较强的种属特异性,种内变异系数小（C.V.=0.20）,而种间差异极显著（P < 0.01）。受试贝类的平均壳-体质量比为0.32±0.13,陆生贝类的壳-体质量比显著小于水生贝类（P < 0.01）,壳-体质量比最大的河蚬（0.54±0.06）是最小的非洲大蜗牛（0.17±0.04）的3倍,福寿螺的壳-体质量比为0.50±0.06。双壳类和螺类的沉降行为差异明显,只有中华园田螺、铜锈环棱螺和河蚬不能在静水中漂浮;沉降速度最大的河蚬（（24.99±4.22）cm/s）是最小的椭圆萝卜螺（（4.13±0.96）cm/s）的6倍,入侵种非洲大蜗牛（（18.30±3.64）cm/s）和福寿螺（（21.77±5.23）cm/s）与土著种铜锈环棱螺（（19.48±3.14）cm/s）和中华园田螺（（21.44±3.92）cm/s）在沉降速度上无显著差异（P < 0.01）。成体贝类的壳-体质量比与沉降速度（R²=0.28）、沉降加速度（R²=0.39）之间存在一定的相关性。在此基础上,贝类沉降特性随生活史变化的研究将进一步揭示贝类进化与种群扩散中的生态水力学作用。     

Secondary production of introduced Asiatic clam,Corbicula fluminea,in a central Arizona canal

Asiatic clam, Corbicula fluminea, is often a serious pest where introduced and established outside its native range. This includes many canals of the southwestern U.S.A. Because of its potential role in organic matter processing, nutrient dynamics, and sedimentation, the clam is an important component of the benthic community and of the aquatic ecosystems which it inhabits. To better understand the ecology of Corbicula in canals, secondary production and life history of an introduced population of clams in a small, earthen canal in the Phoenix metropolitan area, central Arizona, were studied over a 12-month period in 1981–1982. Clams had a monthly mean density of 2 255 m^–2, single annual spawning, 2 year life span, and overlapping cohorts. Annual secondary production (size-frequency method) was 25.62 g DM m^–2 and cohort production (composite Allen curve) was 29.32 g DM m^–2, with turnover ratios of 2.70 and 5.81, respectively. These are among the highest known single-species estimates for molluscs, and illustrate the importance of clams in these unique southwestern aquatic systems.     

Invasive mollusc faunas of the River Thames exemplify biostratigraphical characterization of the Anthropocene

Profound changes to the species configuration of ecosystems globally during the 19th to 21st centuries, resulting from the introduction of neobiota, have produced a distinctive palaeontological signature in sedimentary deposits, here exemplified by those of the River Thames. Coring near Teddington Lock (ca. 4.3 m above sea level, ca. 89 km upstream from the mouth of the Thames estuary) yielded dense assemblages of shells of the invasive Asian clam Corbicula fluminea (recently invaded in 2004) and the zebra mussel Dreissena polymorpha (invaded 1824), which together accounted for 96% of individuals sampled. Population densities of C. fluminea of over 6000 individuals per m² were maintained for a depth of 1 m indicating that the Asian clam is an important biostratigraphical marker in the Thames for sedimentary deposits accumulating since 2004. The first modern European occurrence of C. fluminea was in Portugal in 1980. In 1987, the first occurrence of C. fluminea on the northern coast of South America was observed in the Caripe River, Venezuela. The non-native range of D. polymorpha was restricted to continental Europe for over 200 years until it appeared in the Great Lakes, USA, in 1986 having been transported in ballast water. Within three years, it reached populations of over 750,000 individuals per m² and it is presently recorded in 35 states. Therefore, the pan-Atlantic range expansion of D. polymorpha, coupled with the recent invasion history of C. fluminea in Venezuela and Portugal, identifies a biostratigraphical interval in sedimentary deposits forming from the early 1980s that can be correlated between Europe and the Americas.     

The zebra mussel (<Emphasis Type="Italic">Dreissena polymorpha</Emphasis>) impacts European bitterling (<Emphasis Type="Italic">Rhodeus amarus</Emphasis>) load in a host freshwater mussel (<Emphasis Type="Italic">Unio pictorum</Emphasis>)

The European bitterling, Rhodeus amarus, is a non-indigenous fish species in British fresh waters. It lays its eggs in unionid mussels which themselves are vulnerable to fouling by the non-indigenous zebra mussel, Dreissena polymorpha. Observations from an unmanipulated natural system showed that only 27% of zebra mussel-fouled Unio pictorum hosted bitterling, while 47% of unfouled U. pictorum hosted bitterling. We conducted a field experiment in the River Great Ouse catchment, Cambridgeshire, England in May–June 2007 and 2008 to quantify the impact of zebra mussels on bitterling load in host mussels. Zebra mussel-fouled unionids were significantly less likely to host bitterling than unfouled unionids. The number of unionids hosting bitterling did not differ significantly whether the zebra mussels fouling the unionid were alive or dead. Bitterling appeared to discriminate against zebra mussel-fouled unionids less as the 2007 breeding season advanced, potentially because preferred unfouled unionids had a higher bitterling load, and were therefore relatively lower quality hosts than at the start of the breeding season.     

Morphological and molecular differentiation of invasive freshwater species of the genus Corbicula (Bivalvia, corbiculidea) suggest the presence of three taxa in French rivers

Asiatic Clams are common in brackish and fresh water in Asia, and they were introduced into North America in 1924 and have now spread throughout the continent. During the last two decades they have been reported in Europe, but the number of species here is uncertain. Populations of Corbicula from France and the Netherlands were analysed morphologically and genetically to quantify the degree of species and/or population differentiation. The morphological and genetic data, based on allozymes and mitochondrial sequences, were in full agreement. They indicate that there are two distinct species, identified as C. fluminalis and C. fluminea, in the two countries. Analyses of the mitochondrial COI gene revealed an unexpected divergent population of Corbicula in the Rhône. All these individuals were morphologically identified as C. fluminea, but had a COI sequence different from the two previous species. This population may, therefore, be a more ancient population, or a distinct species introduced via a different colonization route.