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.     

Grazing on toxic and non-toxic Microcystis aeruginosa PCC7820 by Unio douglasiae and Corbicula fluminea

To explore the potential grazing effects of mussels on Microcystis aeruginosa, a common bloom-forming phytoplankton, Unio douglasiae and Corbicula fluminea were fed with Scenedesmus obliquus, toxic and non-toxic strains of Microcystis aeruginosa as single food and as mixtures in the laboratory. When fed with single foods, U. douglasiae has similar clearance rates on the three algae populations, while C. fluminea has significantly lower clearance rate on toxic M. aeruginosa than those on the other two algae populations. When fed with mixture foods, both the mussels show significantly higher clearance rates than on single foods. The clearance rates of U. douglasiae on the different food mixtures are not significantly different, and C. fluminea has a significantly lower clearance rate on the toxic food mixtures than that on non-toxic food mixtures. Although the relative lower clearance rates of C. fluminea on toxic food, we may still deduce that both the mussels can exert grazing pressure on phytoplankton. The deduction is supported by the composition of the excretion products. The excretion products (faeces and pseudofaeces) of both mussels contained mainly S. obliquus. In both mixed-food treatments, the ratios of S. obliquus to M. aeruginosa in the excrete products are significantly higher than those in the foods. Therefore, it can be concluded that both mussels prefer M. aeruginosa to S. obliquus, and can cause grazing pressure on M. aeruginosa.     

Non-lethal predator effects on the feeding rate and prey selection of the exotic zebra mussel Dreissena polymorpha

Predators may induce changes in prey feeding that indirectly influence both the impact of prey on resource abundances and their interactions with other species in their community. We evaluated whether clearance and excretion (faeces plus pseudofaeces) of phytoplankton by zebra mussels were affected by the presence of predatory cues from roach, Rutilus rutilus, and signal crayfish, Pasifastacus leniusculus . We found that non-lethal effects of predators can alter zebra mussel clearance rate and thus the impact of zebra mussels on phytoplankton. Risk cues released by both predators had similar negative effects on clearance rate of zebra mussels and cascading positive indirect effects on phytoplankton resources. Predation risk had a stronger effect on zebra mussels' clearance rate of cyanobacteria and diatoms than cryptophytes and chrysophytes. The presence of predators did not significantly affect the rate at which zebra mussels expelled and excreted phytoplankton, although there was a tendency for more chlorophyll to be expelled and excreted in the presence of predators. Our results contribute to the growing evidence that predators indirectly affect resource dynamics and food web structure through their non-lethal effects on consumers. Our results suggest that exotic species such as zebra mussels can show behavioural responses to both native (e.g. roach) and exotic (e.g. crayfish) predators.     

Grazing on colonial and filamentous, toxic and non-toxic cyanobacteria by the zebra mussel Dreissena polymorpha

Colony forming and toxic cyanobacteria form a problem in surfacewaters of shallow lakes, both for recreation and wildlife. Zebramussels, Dreissena polymorpha, have been employed to help torestore shallow lakes in the Netherlands, dominated by cyanobacteria,to their former clear state. Zebra mussels have been presentin these lakes since they were created in the 19th century bythe excavation of peat and are usually not considered to bean invasive species. Most grazing experiments using Dreissenahave been performed with uni-cellular phytoplankton laboratorystrains and information on grazing of larger phytoplankton taxahardly exists. To gain more insight in to whether D. polymorphais indeed able to decrease cyanobacteria in the phytoplankton,we therefore performed grazing experiments with zebra musselsand two species of cyanobacteria, that greatly differ in shape:colony forming strains of Microcystis aeruginosa and the filamentousspecies Planktothrix agardhii. For both species a toxic anda non-toxic strain was selected. We found that zebra musselscleared toxic Planktothrix at a higher rate than non-toxic Planktothrix,toxic or non-toxic Microcystis. Clearance rates between theother strains were not significantly different. Both phytoplanktonspecies, regardless of toxicity, size and shape, were foundin equal amounts (based on chlorophyll concentrations) in theexcreted products of the mussels (pseudofaeces). The resultsshow that zebra mussels are capable of removing colonial andfilamentous cyanobacteria from the water, regardless of whetherthe cyanobacteria are toxic or not. This implies that the musselsmay be used as a biofilter for the removal of harmful cyanobacterialblooms in shallow (Dutch) lakes where the mussels are alreadypresent and not a nuisance. Providing more suitable substratefor zebra mussel attachment may lead to appropriate mussel densitiescapable of filtering large quantities of cyanobacteria.     

Influence of toxic and non-toxic phytoplankton on feeding and survival of Dreissena polymorpha (Pallas) larvae

Grazing and survival of larvae of the zebra mussel, Dreissena polymorpha, on a green alga and cyanobacteria were studied in laboratory experiments. Clearance rates of the larvae were determined for Chlamydomonas reinhardtii (green alga), two non-toxic and two toxic Microcystis aeruginosa strains (Cyanobacteria). Clearance rates of larvae on non-toxic Microcystis were significantly higher than on toxic Microcystis. The clearance rate on Chlamydomonas reinhardtii was in between the clearance rates on toxic and non-toxic Microcystis strains and not significantly different from them. Effects of toxicity of Microcystis on the survival of zebra mussel larvae was investigated in a short-term experiment. Survival of larvae fed toxic Microcystis was lower than that of larvae fed non-toxic Microcystis, but higher than that of starved larvae. This may imply that, for survival of zebra mussel larvae, it is better to have bad quality (toxic) food than no food.     

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.     

Experimental measurements of zebra mussel (Dreissena polymorpha) impacts on phytoplankton community composition

1 . To investigate direct effects of zebra mussel ( Dreissena polymorpha ) feeding activities on phytoplankton community composition, short‐term microcosm experiments were performed in natural water with complex phytoplankton communities. Both gross effects (without resuspension of mussel excretions) and net effects (with resuspension) were studied.
2. Gross clearance rates were not selective; essentially all taxa were removed at similar rates ranging from 24 to 63 mL mussel^–1 h^–1. Net clearance rates were highly selective; different plankton taxa were removed at very different rates, ranging from 12 to 83% of the gross rates, leading to consistent changes in the phytoplankton community composition. Thus, although zebra mussels can cause most phytoplankton to decline, there is considerable variation among taxa in either pre‐digestive selection or post‐digestive survival.
3. The direct, short‐term effects of zebra mussels on phytoplankton community composition are consistent with some of the major changes observed in the Hudson River since establishment of zebra mussels.
4. We show, with simple calculations, how zebra mussel filtration rate, its selective efficiency on various taxa, and phytoplankton growth rates interact to produce changes in the phytoplankton composition.     

Feedback between zebra mussel selective feeding and algal composition affects mussel condition: did the regime changer pay a price for its success?

1. We investigated the role of algal composition on pumping, clearance, assimilation, pseudofaeces and faeces production, feeding time budgets, and condition of zebra mussels from spring to autumn at two sites in Saginaw Bay (Lake Huron) and one site in western Lake Erie. Size‐fractioned chlorophyll was used to distinguish between feeding on small (<53 μm) and large (>53 μm) size fractions, and mussel feeding behaviour was quantified by video observations. 2. Mussel pumping, clearance and assimilation rates varied among sites, particularly during summer, when phytoplankton composition varied considerably among sites. Lowest values were seen at the inner‐bay site of Saginaw Bay, low to moderate values at the outer‐bay site of Saginaw Bay, and high values at the Lake Erie site. Clearance, pumping and assimilation rates were all highly positively correlated (R² = 0.76) with per cent contribution of flagellates to total algal biomass and negatively correlated with per cent of Microcystis aeruginosa (R² = 0.63). The negative effects on pumping rate (as determined by clearance rate on the <53 μm fraction) of Microcystis, which occurred in the >53 μm fraction, could be mitigated by the presence of flagellates in the <53 μm fraction. 3. Visual observations of mussel feeding showed evidence for poor seston quality during summer negatively affecting feeding rates. High faeces production during times of low assimilation rate was suggestive of poor assimilation efficiency and/or viable gut passage of grazing resistant algae. Long periods of time not filtering by the mussels during some Microcystis blooms and lack of production of a filtering current during one experiment were suggestive of intoxication from microcystin or other secondary compounds. 4. Clearance and feeding rates of the mussels in Saginaw Bay were high during spring and autumn and very low in summer, particularly at the inner‐bay site. Condition of the mussels (mass : length ratio) was highest in spring and lowest during summer. This seasonal variation probably reflected high food assimilation rate during autumn and spring and low assimilation rate and reproduction during summer. The condition of mussels throughout the year was higher at the outer‐bay than the inner‐bay site, reflecting better feeding conditions at the former. Mussel selective feeding may have been responsible for the poor quality of food at the inner bay site; therefore, we postulate that a regime shift in phytoplankton composition promoted by the mussels fed back into lowered condition of the mussels.     

Effects of the benthic suspension feeder Dreissena polymorpha on zooplankton in a large river

1. We conducted a series of in situ enclosure experiments to assess the impact of zebra mussels ( Dreissena polymorpha ) on the plankton of the Ohio River. Adult mussels were suspended in pelagic enclosures ('potamocorrals') at three densities (0, 1000, 2500 mussels per corral) and incubated for 6 days with daily plankton and physiochemical sampling.
2. The presence of adult zebra mussels was correlated with a shift in composition of the phytoplankton community and a severe reduction in some rotifers. The effects of zebra mussels on the larger zooplankton were taxon-dependent, but bacterial density showed no trend among treatments.
3. Zebra mussels may have significant negative impacts on zooplankton, which may in turn alter riverine food webs.     

Life history consequences for Daphnia pulex feeding on nutrient-limited phytoplankton

1. The growth and feeding of Daphnia pulex De Geer on different algal species was examined. The green algae Chlamydomonas reinhardtii Dangeard and Scenedesmus acutus Meyen, the diatom Synedra tenuissima Kützing, the cryptophyte Cryptomonas pyrenoidifera Geitler and the cyanobacterium Microcystis aeruginosa Kützing were cultured in non-limiting and in N- or P-limiting medium and used as food for D. pulex.
2. Growth limitations were reflected in the elemental and biochemical composition and the morphological characteristics of the algal resources.
3. The clearance rates of D. pulex feeding on nutrient-limited algae were reduced. This was not observed when nutrient-limited mutant Chlamydomonas cells without cell walls were used as food, indicating that the cell wall may play an important part.
4. In comparison with animals grown on nutrient-sufficient cells, nutrient-limited algae resulted in smaller body length, reduced brood sizes, reduced size at maturity, increased age at first reproduction and, consequently, in reduced Daphnia population growth rates.
5. Daphnia population growth rates ( r ) were negatively correlated with the C : P ratio and the carbohydrate content of the food. Moreover, significant correlations between r and clearance rates were found.
6. The observed differences in the grazing and the life history parameters of Daphnia feeding on non-limited and nutrient-limited algae may be the result of both reduced nutritional value and reduced digestibility of nutrient-limited algae.