Northern map turtles (Graptemys geographica) derive energy from the pelagic pathway through predation on zebra mussels (Dreissena polymorpha)

1. Zebra mussels ( Dreissena polymorpha ) derive their energy from the pelagic energy pathway by filtering plankton. Because zebra mussels occur in high densities in littoral habitats, they potentially constitute an important trophic link between littoral consumers and pelagic energy sources. Northern map turtles ( Graptemys geographica ) are widespread in North America and consume zebra mussels.
2. We used stable isotopes analyses to quantify the flow of energy from the pelagic pathway to northern map turtles and to infer the contribution of zebra mussels to map turtle biomass. We then built a bioenergetic model to estimate the annual intake of zebra mussels by northern map turtles in Lake Opinicon, Ontario, Canada.
3. Stable isotopes analyses indicated that zebra mussels constitute between 0% and 14% of the diet of males and between 4% and 36% of the diet of females. Assuming that zebra mussels account for all of the pelagic contribution, we estimated that map turtles consume 3200 kg of zebra mussels annually. Because female map turtles are much larger than males and consume more zebra mussels, they are responsible for 95% of the zebra mussel biomass ingested annually.
4. The pelagic pathway supports an important part of the standing crop biomass of map turtles in Lake Opinicon. We highlight the importance of freshwater turtles in lake ecosystems. Unravelling the trophic interactions mediated by freshwater turtles will lead to a more integrated picture of lake ecosystems.     

Impending extinctions of North American freshwater mussels (Unionoida) following the zebra mussel (Dreissena polymorpha) invasion

1. Freshwater mussels (Order Unionoida) are the most imperiled faunal group in North America; 60% of described species are considered endangered or threatened, and 12% are presumed extinct. Widespread habitat degradation (including pollution, siltation, river channelization and impoundment) has been the primary cause of extinction during this century, but a new stress was added in the last decade by the introduction of the Eurasian zebra mussel, Dreissena polymorpha , a biofouling organism that smothers the shells of other molluscs and competes with other suspension feeders for food. Since the early 1990s, it has been spreading throughout the Mississippi River basin, which contains the largest number of endemic freshwater mussels in the world. In this report, we use an exponential decay model based on data from other invaded habitats to predict the long-term impact of D. polymorpha on mussel species richness in the basin.
2. In North American lakes and rivers that support high densities (>3000 m⁻²) of D. polymorpha , native mussel populations are extirpated within 4–8 years following invasion. Significant local declines in native mussel populations in the Illinois and Ohio rivers, concomitant with the establishment of dense populations of D. polymorpha , suggest that induced mortality is occurring in the Mississippi River basin.
3. A comparison of species loss at various sites before and after invasion indicates that D. polymorpha has accelerated regional extinction rates of North American freshwater mussels by 10-fold. If this trend persists, the regional extinction rate for Mississippi basin species will be 12% per decade. Over 60 endemic mussels in the Mississippi River basin are threatened with global extinction by the combined impacts of the D. polymorpha invasion and environmental degradation.     

Filtering impacts of larval and sessile zebra mussels (Dreissena polymorpha) in western Lake Erie

Summary We assessed the feeding biology of veliger larvae of the introduced zebra mussel (Dreissena polymorpha Pallas) in laboratory experiments using inert microspheres as food analogues. Mean clearance rate on 2.87-m beads ranged between 247 and 420 L veliger^–1 day^–1. Clearance rate was unrelated to bead concentration up to 100 beads L^–1, but was positively correlated with veliger shell length. Clearance rates of Dreissena veligers are within the range of those reported for marine bivalve veligers of similar size and for herbivorous Great Lakes microzooplankton, but are orders of magnitude lower than those of settled, conspecific adults. The impact of settled zebra mussel grazing activities on phytoplankton stocks may be up to 1162 times greater than that exerted by veliger populations in western Lake Erie. Based on 1990 size-frequency distributions and associated literature-derived clearance rates, reef-associated Dreissena populations in western Lake Erie (mean depth 7 m) possess a tremendous potential to filter the water column (up to 132 m³ m^–2 day^–1) and redirect energy from pelagic to benthic foodwebs. Preliminary analyses indicate that chlorophyll a concentration is strongly depleted (<1 g L^–1) above Dreissena beds in western Lake Erie.     

Fouling of European freshwater bivalves (Unionidae) by the invasive zebra mussel (Dreissena polymorpha)

1. The zebra mussel (Dreissena polymorpha) is well known for its invasive success and its ecological and economic impacts. Of particular concern has been the regional extinction of North American freshwater mussels (Order Unionoida) on whose exposed shells the zebra mussels settle. Surprisingly, relatively little attention has been given to the fouling of European unionoids. 2. We investigated interspecific patterns in fouling at six United Kingdom localities between 1998 and 2008. To quantify the effect on two pan‐European unionoids (Anodonta anatina and Unio pictorum), we used two measures of physiological status: tissue mass : shell mass and tissue glycogen content. 3. The proportion of fouled mussels increased between 1998 and 2008, reflecting the recent, rapid increase in zebra mussels in the U.K. Anodonta anatina was consistently more heavily fouled than U. pictorum and had a greater surface area of shell exposed in the water column. 4. Fouled mussels had a lower physiological condition than unfouled mussels. Unlike tissue mass : shell mass ratio, tissue glycogen content was independent of mussel size, making it a particularly useful measure of condition. Unio pictorum showed a stronger decline in glycogen with increasing zebra mussel load, but had a broadly higher condition than A. anatina at the time of study (July). 5. Given the high conservation status and important ecological roles of unionoids, the increased spatial distribution and fouling rates by D. polymorpha in Europe should receive more attention.     

Coping with warmer, large rivers: a field experiment on potential range expansion of northern quagga mussels (Dreissena bugensis)

SUMMARY 1. Zebra mussels ( Dreissena polymorpha ) have established a much greater range in North America and Europe than quagga mussels ( D. bugensis ), which occupy a very similar niche.
2. We hypothesised that quaggas are physiologically capable of sustaining populations in warmer rivers currently occupied only by zebra mussels and that unidentified, non-physiological factors account for their more limited distribution.
3. Growth and survival of individually tagged mussels (976 D. bugensis from Lake Erie; 2625 D. polymorpha from Lake Erie and the Ohio River) were recorded monthly for up to 15 months in an outdoor stream mesocosm receiving unfiltered water from the Ohio River.
4. Extreme temperatures stressed both species; but in contrast to several previous laboratory studies, quaggas survived high temperatures better than zebra mussels. We suspect this was the result of species-specific differences in their ability to obtain, assimilate and/or catabolise food at high, sublethal temperatures.
5. A unimodal growth pattern was observed in both species, with the highest growth rates from late spring to early autumn.
6. Our survival and growth data suggest that quaggas are not physiologically limited from expanding southward.
7. While lacking definitive proof that dreissenid populations in rivers are ecologically sustainable without upstream lentic ecosystems and/or unintended human intervention, we suggest that complex river currents and upstream retentive and highly productive slackwater habitats in rivers may help sustain downstream populations of these meroplanktonic, dreissenid mussels.     

Field and laboratory studies of Ophryoglena sp. (Ciliata: Ophryoglenidae) infection in zebra mussels,Dreissena polymorpha (Bivalvia: Dreissenidae)

This study, conducted in the Dnieper-Bug Canal in Belarus, is the first to monitor the seasonal (June-November) dynamics of infection with the parasitic ciliate Ophryoglena sp. in a zebra mussel (Dreissena polymorpha) population. Mean population prevalence and intensity of infection varied, respectively, from 11 to 62% and from 0.9 to 24.1 ciliates/mussel. Mean prevalence was highly correlated with mussel length in mussels <20 mm (R(2)=0.97) and was lower in larger mussels. Mean infection intensity in mussels 1-25 mm long was similarly correlated with their size (R=0.98), reached a maximum in the 20-25 mm size-class, and then sharply decreased, thus providing evidence, albeit limited, that high intensity of infection might be lethal. Transinfection of zebra mussels by Ophryoglena sp. was achieved in the laboratory-a first for a protozoan parasite of D. polymorpha; from an initial complete lack of infection, mean prevalence and intensity rose, respectively, to 86.7% and 8.3 ciliates/mussel.     

Exploration of structure-antifouling relationships of capsaicin-like compounds that inhibit zebra mussel (Dreissena polymorpha) macrofouling

Abstract

Macrofouling of aquatic man-made structures by zebra mussels (Dreissena polymorpha) poses significant economic burdens on commercial freshwater shipping and facilities utilising raw water. The negative environmental impact of some current antifouling technologies has limited their use and prompted investigation of non-organometallic and non-oxidising antifoulants as possible environment-friendly alternatives. The plant-derived natural product capsaicin and 18 other compounds with one or more capsaicin-like structural features were tested for their potential to inhibit zebra mussel byssal attachment at a single high concentration of 30 μM. Of these, three compounds displaying the highest levels of attachment inhibition where selected for further concentration-response testing. This testing revealed that capsaicin (8-methyl-N-vanillyl-trans-6-nonenamide), N-vanillylnonanamide, and N-benzoylmonoethanolamine benzoate all inhibited byssal attachment with potency values (EC₅₀) in the micromolar range. None of these compounds were lethal to adult specimens of the water flea, Daphnia magna, at concentrations that inhibited mussel byssal attachment.     

In situ survival and growth of zebra mussels (Dreissena polymorpha) under chronic hypoxia in a stratified lake

Experiments and field surveys were conducted in Hargus Lake (Ohio, U.S.) to investigate the effect of lake stratification on the survival, growth and distribution of zebra mussels. During the lake stratification period, relatively stable temperature and dissolved oxygen (DO) gradients persisted across the water column, allowing us to examine the chronic effect of hypoxia on zebra mussels. Zebra mussels were incubated in cages and suspended at different depths in the water column at both pelagic (max. depth = 12 m) and littoral (max. depth = 3.5 m) sites from April 18 to September 28, 1994. No mussel survived to the end of the experiment in cages ≥ 5.5 m, whereas the highest survival rate (76%) occurred at 5 m depth where temperature and DO remained fairly stable for at least 3 months. The threshold oxygen level for survival was between 1.0–1.7 mg l^-1 when water temperature was at about 17–18 °C. While zebra mussels′ survival rate was not affected under the sublethal hypoxic conditions, their growth was greatly retarded by poor water quality. The field survey showed that the zebra mussels and macrophytes had about the same distribution and their biomasses were positively related. The percentage of mussels in aggregates increased towards their maximum distribution depth. The maximum distribution depth of the naturally occurring zebra mussels was only 2.8 m, whereas the adult mussels could survive the entire stratification period when being artificially placed on the 3.5 m bottom, and young mussels could colonize the 3.5 m bottom if solid substrates were provided. We conclude that lack of substrate, rather than hypoxia, was the limiting factor of zebra mussel distribution above 5 m depth in Hargus Lake. This revised version was published online in July 2006 with corrections to the Cover Date.     

The effect of seasonal variation in selective feeding by zebra mussels (Dreissena polymorpha) on phytoplankton community composition

1. To investigate the impact of zebra mussels ( Dreissena polymorpha ) on phytoplankton community composition, temporal variability in selective feeding by the mussels was determined from April to November 2005 in a natural lake using Delayed Fluorescence (DF) excitation spectroscopy.
2. Selective grazing by zebra mussels varied in relation to seasonal phytoplankton dynamics; mussels showed a consistent preference for cryptophytes and avoidance of chlorophytes and cyanobacteria. Diatoms, chrysophytes and dinoflagellates responded differentially to zebra mussel grazing depending on their size. Analysis of excreted products of the zebra mussels revealed that in addition to chlorophytes and cyanobacteria, phytoplankton >50  μ m and very small phytoplankton (≤7  μ m) were largely expelled in pseudofaeces.
3. The zebra mussel is a selective filter-feeder that alters its feeding behaviour in relation to phytoplankton composition to capture and ingest high quality phytoplankton, especially when phytoplankton occur in preferred size ranges. Flexibility of zebra mussel feeding behaviour and variation in susceptibility among phytoplankton groups to mussel ingestion indicate that invading zebra mussels could alter phytoplankton community composition of lakes and have important ecosystem consequences.     

Specific amplification of the 18S rRNA gene as a method to detect zebra mussel (Dreissena polymorpha) larvae in plankton samples

An important issue in the management of zebra mussel (Dreissena polymorpha) populations is early, rapid, and accurate detection of the planktonic larvae (veliger) of the zebra mussel. The goal of this study was to explore the feasibility of developing a molecular approach for the detection of zebra mussel larvae in diverse environments. In this study a Dreissena polymorpha-specific 18S ribosomal RNA gene targeted oligonucleotide primer (ZEB-715a) and Polymerase Chain Reaction (PCR) assay was developed and compared with cross-polarized microscopy as a means to detect zebra mussel veligers in plankton samples. The design of the zebra mussel-specific primer was facilitated by sequencing nearly the complete 18S rRNA gene from the zebra mussel and three other closely related freshwater Veneroids including the quagga mussel (D. bugensis), the dark false mussel (Mytilopsis leucophaeata), and the Asian freshwater clam (Corbicula fluminea). The specificity of the primer for the zebra mussel was empirically tested by using the primer as a direct probe in a blot hybridization format. A single veliger in a plankton sample could be detected by PCR using this approach. Veliger detection sensitivity using the PCR approach was estimated to be over 300 times more sensitive than cross-polarized light microscopy based techniques. Cross-polarized light microscopy and the PCR technique were used to identify the presence of zebra mussel larvae in plankton samples that were collected from a variety of natural and industrial water sources. Detection results (presence or absence) were generally consistent between the two methods. Although additional studies will be required before routine application of molecular based veliger detection technology is available, a long-term goal of this work is the application of molecular technology to the development of a field device for the routine detection and quantification of zebra mussel veligers.     

Amplified fragment length polymorphism (AFLP) analysis of the genetic structure of the zebra mussel, Dreissena polymorpha, in the Mississippi River

1. We predicted that zebra mussel, Dreissena polymorpha (Pallas), genetic structure in the Mississippi River would follow a model of invasive species genetics, which predicts low genetic structure among populations of recently established species. This prediction was upheld in our previous genetic study using allozymes, however, one locus yielded anomalous results. 2. We employed amplified fragment length polymorphism (AFLP) analysis as a neutral marker to assess the amount of genetic structure within and among populations, and as a test of expected population structure from both invasion genetic theory, and the results from our previous study. 3. There was greater spatial differentiation, as measured by F_st, observed using AFLP's than for allozymes (P < 0.001). There was no evidence that AFLP variation conformed to an isolation by distance model, and genetic relationships of populations, as measured by AFLP markers, were not similar to those detected in our allozyme survey. 4. The lack of concordance between these two genetic marker systems probably reflects their differential responses to drift, migration, and selection occurring during this rapid invasion. Strong population structure is counter to predictions that populations of invasive species will not be differentiated, as with observations based on allozyme markers. Therefore, newly established species may require genetic surveys using multiple marker systems to evaluate population structure.     

Effects of temperature and temperature acclimation on survival of zebra mussels (Dreissena polymorpha) and Asian clams (Corbicula fluminea) under extreme hypoxia

Following acclimation to 5°, 15° or 25°C for 14days, samples of 30 Dreissena polymorpha (zebra mussels) andCorbicula fluminea (Asian clams)were held in either aerated(control) or extremely hypoxic N₂ gassed water (PO2 <3%of full air saturation). Mortality was negligible in all aeratedcontrols. Mean hypoxiatolerance in D. polymorpha ranged from3–4 days at 25°C to 38–42days at 5°C. Hypoxiatolerance time of zebra mussels increased significantly withdecliningtest temperature (P < 0.001) and increasing acclimationtemperature (P < 0.001). Largerzebra mussels were more tolerantthan smaller individuals. Asian clams were 2–7 timesmoretolerant of hypoxia than zebra mussels, surviving a mean of11.8 and 35.1 days at25°C and 15°C, respectively, andwithout mortality for 84 days at 5°C, and werenot influencedby temperature acclimation. At 25°C, larger specimens ofAsian clams wereless tolerant of hypoxia than smaller individuals.Both species are amongst the least hypoxiatolerant freshwaterbivalve molluscs, reflecting their prevalence in well-oxygenatedshallowwater habitats. Prolonged exposure to extreme hypoxiamay provide an efficacious controlstrategy, particularly forD. polymorpha (Received 12 January 1998; accepted 30 September 1998)     

Development of a molecular diagnostic system to discriminate Dreissena polymorpha (zebra mussel) and Dreissena bugensis (quagga mussel)

A 3-primer PCR system was developed to discriminate invasive zebra (Dreissena polymorpha) and quagga (Dreissena bugensis) mussel. The system is based on: 1) universal primers that amplifies a region of the nuclear 28s rDNA gene from both species and 2) a species-specific primer complementary to either zebra or quagga mussel. The species-specific primers bind to sequences between the binding sites for the universal primers resulting in the amplification of two products from the target species and one product from the nontarget species. Therefore, nontarget products are positive amplification controls. The 3-primer system accurately discriminated zebra and quagga mussels from seven geographically distinct populations.     

Horizontal and Vertical Distribution of the Zebra Mussel (Dreissena polymorpha,Pallas) Larvae in the Modrac Reservoir,Bosnia and Herzegovina

In the Modrac Reservoir, loaded with coal separation suspended material, rapid development of the zebra mussel (Dreissena polymorpha) took place from at least 1987. It is probably the first distinguished “infection” for this part of Balkan Peninsula, caused by this organism. Horizontal and vertical distribution of this mussel, at 15 different reservoir profiles, had been investigated.     

Characterization of zebra mussel (Dreissena polymorpha) sperm motility: duration of movement, effects of cations, pH and gossypol

We have examined effects of time after activation, pH, sodium and potassium, and gossypol concentrations on sperm motility of zebra mussel (Dreissena polymorpha). Zebra mussel spermatozoa appeared to have remarkable viability in the fresh water in comparison with freshwater fish sperm. Duration of sperm motility in fresh water is possibly one of the longest among freshwater animals, since it was not significantly changed 3 h after incubation at room temperature (20 °C) or 24 h of incubation at ±0 °C. High osmotic pressure suppresses sperm motility and effects of sodium and potassium are similar. Spermatozoa were inactive at acid pH and became gradually motile when exposed to pH 6.0–9.0. Gossypol appeared to be a very potent spermicidal agent and inhibited motility. This compound also inhibited fertilization. We observed some differences in gossypol effects on spermatozoa between North American and European zebra mussels. These data on zebra mussel sperm biology may be useful for better handling of gametes under laboratory conditions.     

Selective grazing by adults and larvae of the zebra mussel (Dreissena polymorpha): application of flow cytometry to natural seston

1. Selective grazing of adults and larvae of the zebra mussel (Dreissena polymorpha) on phytoplankton and detritus from both laboratory cultures and natural seston was quantified using flow cytometry. 2. Mean clearance rate of adult zebra mussels was higher on a mixture of the green alga Scenedesmus and the cyanobacterium Microcystis than when Scenedesmus was offered as single food, suggesting selective feeding by the mussels. 3. Feeding on lake seston both adults and larvae showed a higher clearance rate on phytoplankton than on detritus particles, suggesting that zebra mussels select for phytoplankton. Furthermore, it was noted that adults preferred seston particles in the 0–1 and 30–100 μm size ranges. 4. In our study, zebra mussels did not discriminate against cyanobacteria, and our results indicate that they may even ingest them preferentially.     

Filtration and ingestion rates of Salpa fusiformis Cuvier (Tunicata : Thaliacea): Effects of size,individual weight and algal concentration

Filtration and ingestion rates of Salpa fusiformis Cuvier were determined while fed Phaeodactylumtricomutum Bohlin at concentrations of 2?64 × 10³ cells·ml^?1. Filtration and ingestion rates increase exponentially with increasing length and body protein. The relations between protein content and body length, and between filtration rate and weight are similar for blastozooids and oozooids. A capture efficiency of the order of 6–32% is calculated: Salpa fusiformis seems to have a low retention efficiency, but its very high filtration rate gives it pride of place amongst filter-feeders. Specific filtration rates are independent of weight; specific ingestion rates are independent of weight for blastozooids, but for oozooids they seem to diminish with increasing weight. The mean daily ration (μg C ingested · μg body C^?1) is 107% for a blastozooid and 117% for an oozooid. Specific filtration rates decrease exponentially as particle concentration rises, as for many other filter-feeders, and the specific ingestion rate follows an Ivlev relation.     

Distribution and aspects of population dynamics of the zebra mussel,Dreissena polymorpha (Pallas, 1771), in the lake IJsselmeer area (The Netherlands)

Summary The distribution, settling and growth of the zebra mussel, Dreissena polymorpha Pallas, in Lake IJsselmeer and Lake Markermeer in The Netherlands were studied from 1980 to 1985. In these lakes D. polymorpha is the most important food source for wintering diving ducks. The study was part of an investigation into the carrying capacity of the lakes for these birds.     

Seasonal changes in the respiratory electron transport system (ETS) and respiration of the zebra mussel,Dreissena polymorpha in Saginaw Bay,Lake Huron

Electron transport system activity (ETS) and respiration rates (R) of the zebra mussel, Dreissena polymorpha, were determined monthly from April to November over 2 years at two sites in Saginaw Bay, Lake Huron. The sites were located in the inner and outer bay and contrasted in food quantity and quality. ETS ranged from 2 to 40 g O₂ mg DW^–1 h^–1 over the study period. Both ETS and respiration were strongly related to temperature, and maximum values were found between June and August. ETS also peaked in June/July when assays were conducted at a constant temperature (25 °C), indicating other factors besides temperature affected metabolic activity. R:ETS ratios decreased with increased temperature at the inner bay site, but trends were minimal at the outer bay site. In late summer, blooms of the cyanophyte Microcystis occurred in the inner bay, likely depressing filtration rates, and leading to lower respiration rates relative to ETS. ETS activity was consistently higher in the outer bay and was likely a result of higher food quality. Despite these spatial differences, annual mean R:ETS ratios varied only from 0.04 to 0.09 at the two sites over the 2-year period. Based on these values, ETS may be useful as an indicator of long-term metabolic activity in annual energy budgets of D. polymorpha. However, food conditions differentially affect respiration relative to ETS, and variability in this ratio must be considered when interested in shorter time scales.     

Environmental conditions increase growth rates and mortality of zebra mussels (<Emphasis Type="Italic">Dreissena polymorpha</Emphasis>) along the southern invasion front in North America

Environmental conditions found along an invasion front can mediate spread dynamics of an invasive species. Conditions that affect survival and individual growth rates of founder propagules and the first young-of-year generation can have a profound effect on establishment dynamics. Responses of younger, more sensitive individuals to these novel conditions, in part, determine establishment success. The southern invasion front of zebra mussels in North America expanded into Texas in 2009. To determine mechanisms that could affect establishment of zebra mussel populations at low latitudes in North America, an in situ study was conducted in Lake Texoma, on the Texas-Oklahoma border. Survival and growth were measured of young-of-year juveniles at multiple sites within the reservoir. Age-specific mortality was significantly positively correlated with temperature at all sites and no mortality occurred when temperatures were <26 °C. Shell-length growth rates were the highest ever reported for lentic environments. A decrease in shell-length growth rates was associated with an increase in soft tissue mass, possibly resulting from flexible energy allocation from shell development to gametogenesis after maturation. Overall, survivorship and growth were related to water temperatures and chlorophyll-a concentrations. Warm waters found at lower latitudes along the invasion front could facilitate establishment of populations by increasing growth rates and decreasing time to maturity. However, due to extreme climate events (e.g. drought and flooding) and a strong temperature-mortality relationship, mortality likely will also be high beyond the southern invasion front, resulting in highly dynamic boom and bust cycles.