Indigenous microflora and opportunistic pathogens of the freshwater zebra mussel, Dreissena polymorpha

Freshwater fouling invertebrate zebra mussels (Dreissena polymorpha) harbor a diverse population of microorganisms in the Great Lakes of North America. Among the indigenous microorganisms, selective species are opportunistic pathogens to zebra mussels. Pathogenicity to zebra mussels by opportunistic bacteria isolated from the mussels was investigated in this study. Among the more than 30 bacteria isolated from temperature-stressed mussels, Aeromonas media, A. veronii, A. salmonicida subsp. salmonicida, and Shewanella putrefaciens are virulent pathogens to juvenile zebra mussels. Inoculation of a bacterial concentration of A. media, A. salmonicida subsp. salmonicida and S. putrefaciens at 10⁷ cells per zebra mussel resulted in 100% mortality within 5 days, and only 64.9% for A. veronii. In contrast, mortality was less than 12.3% following inoculation of a sterile phosphate buffer solution as a control. In addition, mortality was dependent on the size of the pathogen population used in inoculation and the incubation temperature, indicating the close relationship between the bacterial population and subsequent death. On the mussel tissue, a dense microbial population was evident from the moribund mussels viewed with Scanning Electron Microscope (SEM). Opportunistic bacteria invaded and destroyed the D. polymorpha tissue after 7 days of incubation when the bacterial inoculation was larger than 10⁵ per zebra mussel. Our results suggest that mussels are reservoirs of opportunistic pathogenic microorganisms to aquatic organisms and humans and a better understanding of the microbial ecology of the mussels will provide insights to the possible health hazards from these microorganisms.     

Bioprocessing of polluted suspended matter from the water column by the zebra mussel (Dreissena polymorpha Pallas)

Measurements of pseudofaeces production of Dreissena polymorpha were carried out with the aim of developing a biological filter at the freshwater inlet of Lake Volkerak-Zoommeer, the Netherlands. Bioprocessing of polluted suspended matter by suspended cultures of D. polymorpha occurs by filtration and sedimentation of the suspended matter as pseudofaeces. The measurements were conducted under semi-natural conditions.Pseudofaeces production was mainly determined by the dry matter content of the water; the relation is linear. Temperature was of much less importance. This agrees with earlier investigations of the filtration rate of D. polymorpha. Even at the lowest temperature measured during the experiments (6.4 °C) no large decrease in activity was observed. The relation of pseudofaeces production with shell length was sigmoid in shape, in accordance with measurements of the filtration rate.The pseudofaeces produced was slightly more polluted than suspended matter, partly due to a finer grainsize. D. polymorpha from Lake IJsselmeer exposed for 217 days at the intended location of the filter showed bioaccumulation of toxicants, especially organic pollutants and Polycyclic Aromatic Hydrocarbons (up to 10-fold accumulation). The required number of D. polymorpha in the biological filter to treat the waterflow of 14 m³ s^–1 entering Lake Volkerak-Zoommeer is 1.24 * 10⁹. The purification efficiency of the filter, the reduction of the amount of toxicants, partly depends on the binding properties of the toxicants and is highest for those strongly bound to suspended matter.     

The filtration rate of the zebra mussel Dreissena polymorpha used for water quality assessment in Dutch rivers

The effects of contaminated river water on the filtration rate of zebra mussels from a clean reference site were studied. After a 48-h exposure period to filtered water from the rivers Rhine, Meuse and Amstel (The Netherlands), the filtration rate was measured. It was demonstrated that water from contaminated locations inhibited the filtration rate. Inhibition was higher during low water levels in the rivers Rhine and Meuse than during high water levels, suggesting that contaminants are diluted during high water levels. It is concluded that the shortterm filtration assay with D. polymorpha can be used for assessing water quality.     

The annual reproductive cycle of the freshwater mussel Dreissena polymorpha Pallas in lakes

Summary The annual development of the gonads of Dreissena polymorpha was studied at three sampling sites in two lakes over 3 and 1 1/2 years, respectively. A resting stage occurred after the last spawning in summer/autumn. Oogenesis (accompanied by multiplying segmentation of the oogonia and early growth processes of its oocytes) restarted in specimens at least 1 year old at low temperatures (below 10° C) during winter and early spring. At one location (Fühlinger See) the onset of the spawning season was correlated with an increase of water temperatures above 12° C. At 2 m depth, two main spawning periods in May and August were normally recognized, the first at temperatures of 12–16° C, the second at 16–21° C. It was clearly demonstrated for the first time in Dreissena polymorpha that the oocytes became mature in successive cohorts within one gonad. A female mussel may spawn several times during the reproductive season. At 9 m depth, the onset of spawning also started at about 12° C; this occurred in late summer, with two spawning periods within 1 month at a temperature range of 12–16° C. At another location (Heider Bergsee) the size of the gonads and the oocytes was reduced during April of both years studied, when food supply was low simultaneously with rapidly rising water temperatures in this shallow lake. There was no spawning period during spring. The major spawning period was delayed until July (temperatures 19–22°C). This shows (1) the synchronizing influence of low winter temperatures on the annual reproductive cycle and (2) a temperature threshold of at least 12° C for the start of the spawning processes. The results are discussed with regard to the geographical limits of further spread of Dreissena polymorpha.     

Synchronous spawning in a recently established population of the zebra mussel,Dreissena polymorpha,in western Lake Erie,USA

Seasonal patterns of reproduction in a newly established population of Dreissena polymorpha are described for a site in the western basin of Lake Erie. Reproduction was monitored by histological examination of gonads, analysis of shell length-dry weight relationships, and following abundance of planktonic and settling larvae. Patterns of planktonic larval abundance and settling showed a distinct bimodal pattern in July and August, but conflicted with histological and length-dry weight data that showed spawning was a brief, highly synchronous event occurring in late August. Differences between histological data and abundance of larvae in the plankton can be explained as resulting from drift of larvae from disjunct populations of D. polymorpha which spawned earlier, into the study area. Veliger larvae were present in the plankton at low densities throughout the warm months before and after periods of peak abundances. The presence of these larvae can be explained by a combination of asynchronous spawning among local populations and postponed settlement by planktonic larvae.     

Size-selective predation by roach (Rutilus rutilus) on zebra mussel (Dreissena polymorpha): field stuides

Summary Studies of predation by roach (Rutilus rutilus) on zebra mussel (Dreissena polymorpha) in a large, eutrophic lake showed that there was a clearly marked size threshold ( 160 mm SL) above which roach began to feed on mussels. Roach preying on various sizes of mussels selected them in proportions different from their abundance and accessibility in the habitat. The mean size of mussels ingested by roach of 220 mm and larger, which fed predominantly on Dreissena, closely followed the pattern expected for a constant ratio of mean prey size to mean predator mouth size = 0.59. To explain the size selection we applied an optimal foraging approach, based on the ability of different-sized fish to crush (cost) mussels of different sizes, and hence crushing resistance, and energy contents (benefit). We found that fish smaller than 160 mm, which showed no inclination to eat Dreissena, would only be able to take small mussels with a very high cost/benefit ratio. The real switch to Dreissena would be expected in fish of 230–240 mm that could take most of their prey from highly profitable, numerous, and easily accessible size classes while keeping the mean prey size at the optimal level relative to mean predator mouth size.     

Invasive zebra mussel colonisation of invasive crayfish: a case study

We investigated the interaction between two invasive invertebrate species in a shallow Central European flooded sandpit: the epibiosis of Ponto-Caspian zebra mussels Dreissena polymorpha on the American crayfish Orconectes limosus. Between 2004 and 2005, we followed the seasonal variation in number and size of the mussels attached to crayfish bodies, and microhabitats preferred by mussels. The proportion of crayfish colonised by mussels varied seasonally: in spring and early summer it was consistently over 75%, afterwards it dropped temporarily due to loss of bivalves during the crayfish moult, and later increased again due to re-colonisation by often relatively large juvenile mussels. Three different pathways of mussel settlement on crayfish hosts are likely: (1) primary settlement of free-swimming pediveliger larvae; (2) secondary settlement of plantigrade mussels and juveniles; (3) active re-attachment of grown mussels from the substrate to crayfish. This epibiosis was promoted by lack of suitable substrates at the studied locality. Electronic supplementary material The online version of this article (doi: ) contains supplementary material, which is available to authorized users.     

Particle transport in the zebra mussel, Dreissena polymorpha (Pallas)

The capture, transport, and sorting of particles by the gills and labial palps of the freshwater mussel Dreissena polymorpha were examined by endoscopy and video image analysis. More specifically, the morphology of the feeding organs in living zebra mussels was described; the mode and speeds of particle transport on the feeding organs was measured; and the sites of particle selection in the pallial cavity were identified. Particle velocities (outer demibranch lamellae, 90 microm s(-1); inner demibranch lamellae, 129 microm s(-1); marginal food groove of inner demibranchs, 156 microm s(-1); dorsal ciliated tracts, 152 microm s(-1)), as well as the movement of particles on the ctenidia and labial palps of D. polymorpha, are consistent with mucociliary, rather than hydrodynamic, transport. Particles can be sorted on the ctenidia of zebra mussels, resulting in a two-layer transport at the marginal food groove of the inner demibranch. That is: preferred particles are transported inside the marginal groove proper, whereas particles destined for rejection are carried superficially in a string of mucus. Sorting also occurs at the ventral margin of the outer demibranch; desirable particles are retained on the outer demibranch, whereas unacceptable particles are transferred to the inner demibranch and ultimately excluded from ingestion. We suggest that the structure of homorhabdic ctenidia does not preclude particle sorting, and that some ecosystem modifications attributed to zebra mussels may ultimately be due to ctenidial sorting mechanisms.     

The zebra mussel (Dreissena polymorpha), a new pest in North America: reproductive mechanisms as possible targets of control strategies

Summary

The zebra mussel (Dreissena polymorpha) has spread rapidly in temperate fresh waters of North America since its introduction into the Great Lakes in 1985 or 1986. It attaches to hard substrates, forming layers, occluding water intakes, encrusting and killing native mussels, filtering algae in competition with other planktivores, and possibly interfering with fish spawning. It reproduces prolifically, suggesting that an approach to its control may be by controlling its reproduction. Previous literature suggests that spawning in bivalves is regulated by both environmental and internal chemical cues. A suggested sequence is that phytoplankton chemicals initially trigger spawning; chemicals associated with gametes provide a species-specific pheromonal positive feedback for spawning; and the response to environmental chemicals is mediated internally by serotonin (5-HT). The role of 5-HT in zebra mussels is under investigation. Both males and females can be induced to spawn by either injection or external application of 5-HT. The response can also be activated by 8-hydroxy-2-(di-n-propylamino)-tetralin, an agonist at 5-HT_1A receptors. HPLC analysis has detected 5-HT as the major biogenic amine in both male and female gonads. 5-HT immunocytochemistry demonstrates nerves containing serotonergic fibers innervating gonads of both males and females, with prominent varicosities surrounding the follicles in both sexes. A role of 5-HT in mediating spawning responses in zebra mussels is thus strongly supported. These studies have shown that reproductive behavior of zebra mussels can be modified by outside chemicals, a property that may be exploited for purposes of control.     

Influence of food size and food quantity on the feeding of the mussel Dreissena polymorpha

Summary In common with many other suspension feeders, the freshwater mussel Dreissena polymorpha has a maximum filtration rate at low food concentrations and a maximum ingestion rate at high food concentrations. These high rates, which reflect the potential maximum food uptake of the animal, are called the filtration capacity and the ingestion capacity respectively. The ingestion capacity was attained without forming pseudofaeces with Chlamydomonas reinhardii as food. The incipient limiting level could be calculated as the quotient of these two values. A decrease of the filtration rate at high food concentrations was correlated with changes in pumping activity, which showed more frequent interruptions, or a lower level of water transport. Dreissena can filter out particles of diameter greater than 0.7 m from the water. Retention reaches a plateau at about 5 m particle diameter. Scanning electron micrographs of the arrangement of the cilia on the gill filaments are given.     

Ecotoxicity of lead to the zebra musselDreissena Polymorpha,Pallas

The effect of lead on the filtration rate of the zebra musselDreissena polymorpha was investigated, together with the accumulation of Pb in the soft tissues of the mussels. The NOEC-filtration was 116 g.l^–1 (0,56 mol.l^–1) and the EC₅₀-filtration was 370 g.l^–1 (1.79 mol.l^–1). The NOEC-accumulation was the concentration found in the control water (1.4g.l^–1). These experiments show that the EC₅₀-filtration for Pb is similar to that for Cd, higher than that for Cu and lower than that for Zn. The water quality criteria for lead allow 25 g Pb.l^–1 in surface water. This will not cause short-term effects. Long-term effects may, however, occur, since an accumulation of Pb as low as 16 g.l^–1 was recorded in this study.     

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.     

Activation of spawning in zebra mussels by algae-, cryptomonad-, and gamete-associated factors

In zebra mussels (Dreissena polymorpha) simultaneous release of gametes and peaks in larval densities at particular locations suggest that spawning is triggered by synchronizing stimuli. Furthermore, spawning tends to occur only after an adequate environmental temperature is reached. To test the hypothesis that phytoplankton and gamete-associated chemicals initiate spawning in zebra mussels and that the responsiveness to such chemicals is affected by ambient temperature, the spawning response of zebra mussels to extracts from algae, a cryptomonad, and a cyanobacterium and to water associated with released gametes was assayed in animals acclimated to 12 ^C and 17 ^C. For animals held at 12 ^C, only serotonin, a known activator of bivalve spawning used as a positive control, stimulated spawning. However, for animals acclimated to 17 ^C, extracts made from a diatom (Phaeodactylum), a brown alga (Fucus), and a cryptomonad (Rhodomonas) stimulated spawning in both sexes; extracts from green algae (Platymonas and Dunaliella) and a cyanobacterium (Oscillatoria) did not cause spawning. Water associated with either released sperm or eggs elicited spawning in both females and males. Positive controls, stimulated with serotonin, spawned at a high (>90%) rate, whereas no negative control spawned. Thus, phytoplankton chemicals and gamete-associated factors may have a role in synchronizing spawning in zebra mussels once adequate ambient temperature is reached.     

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.     

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.     

Zebra mussels (Dreissena polymorpha): a new perspective for water quality management

In the evaluation of the role of lake restoration programmesin situ measurements of the filtration rate of the freshwater musselDreissena polymorpha have been performed in Lake Wolderwijd, The Netherlands. The filtration rate mainly depends on the suspended matter content of the water, and shows an inverse exponential relationship with this factor. The filtration activity is temperature indifferent between approx. 5 and 20 °C. At low temperatures the filtration rate drops abruptly, at high temperatures gradual inhibition occurs. The filtration rate shows a sigmoidal relation with the length of the mussel. The largestD. polymorpha have a diminished filtration rate compared to animals of smaller size. This might be a degenerative feature of the oldest mussels. In Lake Wolderwijd a population density of 675 per m² is required to compensate phytoplankton growth by grazing. Manipulation of the size of the population can be executed by adding suitable substrates for the mussel.     

The byssus of the zebra mussel (Dreissena polymorpha): spatial variations in protein composition

The notorious biofouling organism Dreissena polymorpha (the zebra mussel) attaches to a variety of surfaces using a byssus, a series of protein threads that connect the animal to adhesive plaques secreted onto hard substrata. Here, the use of matrix-assisted laser desorption ionization time-of-flight mass spectrometry (MALDI-TOF MS) to characterize the composition of different regions of the byssus is reported. All parts of the byssus show mass peaks corresponding to small proteins in the range of 3.7–7 kDa, with distinctive differences between different regions. Indeed, spectra from thread and plaques are almost completely non-overlapping. In addition, several peaks were identified that are unique to the interfacial region of the plaque, and therefore likely represent specialized adhesive proteins. These results indicate a high level of control over the distribution of proteins, presumably with different functions, in the byssus of this freshwater species.     

Modelling the local dynamics of the zebra mussel (Dreissena polymorpha)

1. The bivalve Dreissena polymorpha has invaded many freshwater ecosystems worldwide in recent decades. Because of their high fecundity and ability to settle on almost any solid substratum, zebra mussels usually outcompete the resident species and cause severe damage to waterworks. Time series of D. polymorpha densities display a variety of dynamical patterns, including very irregular behaviours. Unfortunately, there is a lack of mathematical modelling that could explain these patterns. 2. Here, we propose a very simple discrete‐time population model with age structure and density dependence that can generate realistic dynamics. Most of the model parameters can be derived from existing data on D. polymorpha. Some of them are quite variable: with respect to these we perform a sensitivity analysis of the model behaviour and verify that non‐equilibrial regimes (either periodic or chaotic) are the rule rather than the exception. 3. Even in circumstances where the model dynamics are aperiodic it is possible to predict total density peaks from previous peaks. This turns out to be true also in the presence of environmental stochasticity. 4. Using the stochastic model we explore the effects of age‐selective predation. Quite surprisingly, larger removal rates of adults do not always result in smaller population densities and mussel biomasses. Moreover, non‐selective predation can result in skewed size‐frequency distributions which, therefore, are not necessarily the footprint of predators’ preference for larger or smaller zebra mussels.     

Changes in the distribution and abundance of Dreissena polymorpha within lakes through time

Dreissena polymorpha population densities and biomass were followed in three Belarusian lakes with different trophic status over a 12-year period subsequent to initial colonization. In all three lakes zebra mussel population densities did not change once they reached a maximum. Application of the Ramcharan et al. [1992. Canadian Journal of Fisheries and Aquatic Sciences 49: 2611–2620] model for predicting population dynamics of zebra mussels was accurate for two of the three lakes studied. Population density appears to depend on the time since initial colonization, relative abundance of substrate available for colonization, lake morphometry and trophic type. Zebra mussel distribution within lakes was highly patchy, but the degree of dispersion decreased over time after initial colonization, which may be a result of saturation of suitable substrates by zebra mussels as populations increase and reach carrying capacity. In lakes where submerged macrophytes are the dominant substrate for zebra mussel attachment, populations may be less stable than in lakes with a variety of substrates, which will have a more balanced age distribution, and be less impacted by year to year variation in recruitment. Dreissena polymorpha usually reach maximum population density 7–12 years after initial introduction. However, the timing of initial introduction is often very difficult to determine. Both European and North American data suggest that zebra mussels reach maximum density in about 2–3 years after populations are large enough to be detected.     

The effect of food availability on byssogenesis by the zebra mussel (Dreissena polymorpha Pallas)

The effect of varying algal availability on byssal thread productionby re–attaching zebra mussels (Dreissena polymorpha) wasquantified. The byssal apparatus was severed and mussels allowedto re–attach to a hard substratum for a 21 day periodduring which they were fed at algal concentrations of 0.0, 0.1,0.5, 1.0 or 2.0 mg C l^-1. Byssal thread production was quantifiedby counting the number of new attachment plaques present eachday. Results showed that starved mussels continued to partition organiccarbon towards thread production but the resultant byssal masswas compromised, containing fewer threads than those producedby fed mussels. The daily average byssal thread production bymussels fed at 2.0 mg C l^-1 was greater than that of starved musselsand the final mean dry soft tissue weight higher. At algal Cconcentrations below maintenance requirements byssal threadproduction was elevated compared to starved mussels, but therewas no concurrent increase in soft tissue. This suggests thatbelow maintenance levels assimilated carbon was solely partitionedtowards byssus production and stored reserves may have beenutilized. The ratio of organic carbon contained in the byssusto that in the soft tissues remained relatively constant acrossall feeding levels. This suggests that the carbon content ofthe byssus is a constant function of that of the soft tissuemass. These results may explain seasonal variation in attachmentstrength of numerous byssate species and seasonal vertical migrationsby D. polymorpha. Present Address-Queen Mary & Westfield College, Dept of Biology,University of London, Mile End Road, London E1 4NS, UK (Received 16 March 1998; accepted 30 September 1998)