Genetic variability and phylogeography of the invasive zebra mussel, Dreissena polymorpha (Pallas)

The zebra mussel, Dreissena polymorpha (Pallas), a bivalve species originally native to the Black and Caspian seas, has invaded Ireland in the last decade. Five microsatellite loci were used to investigate genetic diversity and population structure in 10 populations across Europe (Ireland, UK, the Netherlands and Romania) and the Great Lakes (Lake Ontario and Lake St Clair). Levels of allelic diversity and mean expected heterozygosity were high for all populations (mean number of alleles/locus and H(E) were 10-15.2 and 0.79-0.89, respectively). High levels of polymorphism observed in Irish populations suggest that the Irish founder population(s) were large and/or several introductions took place after foundation. Significant deficits of heterozygotes were recorded for all populations, and null alleles were the most probable factor contributing to these deficits. Pairwise comparisons using Fisher exact tests and F(ST) values revealed little genetic differentiation between Irish populations. The UK sample was not significantly differentiated from the Irish samples, most probably reflecting an English origin for Irish zebra mussels. No significant differentiation was detected between the two Great Lakes populations. Our data support a northwest rather than a central or east European source for North American zebra mussels.     

Trinucleotide microsatellite loci for the zebra mussel Dreissena polymorpha,an invasive species in Europe and North America

The high mutation rate at microsatellite loci can supply important demographic information on founder events and range expansion in an invasive species such as the zebra mussel Dreissena polymorpha, following its initial introduction. In order to facilitate studies into the colonization patterns of this species in new habitats in Europe and North America, five trinucleotide microsatellite loci were isolated from a partial DNA library. Allelic diversity at all described loci was high, ranging from 20 to 35 alleles per locus. Homologous loci were not amplified in a second related invasive species, Dreisenna bugensis, using the primers developed here.     

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.     

Mortality of zebra mussel, Dreissena polymorpha, veligers during downstream transport

1. Streams flowing from lakes which contain zebra mussels, Dreissena polymorpha , provide apparently suitable habitats for mussel colonization and downstream range expansion, yet most such streams contain few adult mussels. We postulated that mussel veligers experience high mortality during dispersal via downstream transport. They tested this hypothesis in Christiana Creek, a lake-outlet stream in south-western Michigan, U.S.A., in which adult mussel density declined exponentially with distance downstream.
2. A staining technique using neutral red was developed and tested to distinguish quickly live and dead veligers. Live and dead veligers were distinguishable after an exposure of fresh samples to 13.3 mg L⁻⁻¹ of neutral red for 3 h.
3. Neutral red was used to determine the proportion of live veligers in samples taken longitudinally along Christiana Creek. The proportion of live veligers (mean ± SE) declined from 90 ± 3% at the lake outlet to 40 ± 8% 18 km downstream.
4. Veligers appear to be highly susceptible to damage by physical forces (e.g. shear), and therefore, mortality in turbulent streams could be an important mechanism limiting zebra mussel dispersal to downstream reaches. Predictions of zebra mussel spread and population growth should consider lake-stream linkages and high mortality in running waters.     

Serotonergic mechanisms mediating spawning and oocyte maturation in the zebra mussel,Dreissena polymorpha

Summary

The zebra mussel, Dreissena polymorpha, is a freshwater biofouling bivalve unintentionally introduced in the 1980s into North America from Europe. Oocyte maturation (germinal vesicle breakdown, GVBD) and spawning of the zebra mussel can be triggered with serotonin (5-hydroxytryptamine, 5-HT). In pharmacological experiments to characterize the receptor mediating spawning, the serotonin receptor agonists 8-OH-DPAT, TFMPP, and 1-(1-naphthyl)piperazine were effective at stimulating spawning; whereas, 2-methylserotonin and alpha-methylserotonin had no effect. In experiments with antagonists of serotonin receptors ketanserin and propranolol had no effect; mianserin, NAN-190, and cyproheptadine had partial inhibitory effects; and methiothepin was a very effective antagonist. Metergoline had mixed agonist/antagonist properties. Ergotamine was the most effective activator of spawning in females. Compared to serotonergic receptors in other organisms, the receptors that activate spawning in zebra mussels resemble 5HTlym, 5HTdro2 and human 5HT1Dβ, which are receptors that may act both by inhibiting adenylyl cyclase and by activating phospholipase C. In zebra mussels, 5-HT and 8-OH-DPAT activate GVBD in gonad fragments, a process also initiated by manual dissection of gonad fragments. GVBD can be inhibited by pre-treatment of ovaries with forskolin and theophylline, suggesting an inhibitory role for cyclic AMP. The Ca²⁺ ionophore A23187 can trigger GVBD and polar body formation. Thus, oocyte maturation in zebra mussels may be initiated via serotonergic receptors simultaneously inhibiting adenylyl cyclase and activating Ca²⁺ mechanisms.     

Long-term demography of a zebra mussel (Dreissena polymorpha) population

1. We used long‐term data and a simulation model to investigate temporal fluctuations in zebra mussel populations, which govern the ecological and economic impacts of this pest species. 2. The size of the zebra mussel (Dreissena polymorpha) population in the Hudson River estuary fluctuated approximately 11‐fold across a 13‐year period, following a cycle with a 2–4 year period. 3. This cycling was caused by low recruitment during years of high adult population size, rapid somatic growth of settled animals, and adult survivorship of 50% per year. 4. Adult growth and body condition were weakly correlated with phytoplankton biomass. 5. The habitat distribution of the Hudson's population changed over the 13‐year period, with an increasing proportion of the population spreading onto soft sediments over time. The character of soft‐sediment habitats in the Hudson changed because of large amounts (mean = 34 g DM m^?2) of empty zebra mussel shells now in the sediments. 6. Simulation models show that zebra mussel populations can show a range of long‐term trajectories, depending on the balance between adult space limitation, larval food limitation, and disturbance. 7. Effective understanding and management of the effects of zebra mussels and other alien species depend on understanding of their long‐term demography, which may vary across ecosystems.     

美国大陆外来入侵物种斑马纹贻贝(Dreissena polymorpha)潜在生境预测模型

防止外来生物入侵造成危害的重要手段是阻止可能造成入侵的物种进入适合其生存的地区.论文以1864个美国外来入侵物种斑马纹贻贝定点发生数据和开放式基础地理信息数据库Daymet的34个环境变量为主要信息源,采用逻辑斯蒂回归(LR)、分类与回归树模型(CART)、基于规则的遗传算法(GARP)、最大熵法(Maxent)4种途径,建立美国大陆部分潜在生境预测模型,从接受者运行特征曲线下面积(AUC)、Pearson相关系数、Kappa值3个方面来检验模型预测精度,在此基础上分析斑马纹贻贝的空间分布规律及其环境影响因素.研究结果表明:在3个评价指标中,4个生态位模型预测精度均达到优良水平,其中Maxent在物种现实生境模拟、主要生态环境因子筛选、环境因子对物种生境影响的定量描述方面都表现出了优越的性能;距水源距离、海拔高度、降水频率、太阳辐射是影响物种空间分布的主要环境因子.论文提出的研究方法对中国外来入侵物种生境预测具有较强的借鉴意义,研究结果对中国海洋外来入侵物种沙筛贝的预测与防治,具有一定的指导作用.     

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.     

Genetic variability and phylogeographical patterns of a nonindigenous species invasion: a comparison of exotic vs. native zebra and quagga mussel populations

There have been few investigations of the number of founding sources and amount of genetic variability that lead to a successful nonindigenous species invasion, although genetic diversity is believed to play a central role. In the present study, population genetic structure, diversity and divergence patterns were analysed for the zebra mussel Dreissena polymorpha [n=280 samples and 63 putative randomly amplified polymorphic DNA (RAPDs) gene loci] and the quagga mussel D. bugensis (n=136 and 52 loci) from 10 nonindigenous North American and six Eurasian sampling sites, representing their present‐day ranges. Results showed that exotic populations of zebra and quagga mussels had surprisingly high genetic variability, similar to those in the Eurasian populations, suggesting large numbers of founding individuals and consistent with the hypothesis of multiple colonizations. Patterns of genetic relationships indicate that the North American populations of D. polymorpha likely were founded by multiple source populations from north‐western and northcentral Europe, but not from southcentral or eastern Europe. Sampling areas within North America also were significantly divergent, having levels of gene flow and migration about twice those separating long‐established Eurasian populations. Samples of D. bugensis in Lakes Erie and Ontario were significantly different, with the former being more closely related to a native population from the Dnieper River, Ukraine. No evidence for a founder effect was discerned for either species.     

Effects of zebra mussel attachment on the foraging behaviour of a larval dragonfly,Macromia illinoiensis

1. Larvae of Macromia illinoiensis Walsh are often colonised by the zebra mussel, Dreissena polymorpha Pallas, a recent invader to North America. To determine how mussel attachment affects an individual's foraging behaviour, we quantified capture of Hexagenia limbata Hexes mayfly prey and the distance moved by newly‐molted final instars before and after an individual's colonisation with zebra mussels. 2. In night trials, larvae sprawled above the sand, and caught more mayflies than individuals in daytime trials, but the estimated distance travelled did not differ. When resting under a layer of sand with only its eyes exposed during the day, an individual could capture a mayfly prey using a sit‐and‐wait ambush strategy. When sprawled above the sand, some larvae caught prey that rested on their legs. 3. When mussel‐free, individuals captured more prey than they did when carrying zebra mussels, although mussel attachment per se did not affect the estimated distance that a larva moved. 4. During day trials, but not night ones, the increasing mussel load of colonised individuals decreased prey capture and the distance moved in an apparent step‐wise function. Although the number of mussels carried did not differ, night foragers carried a heavier load. Independent of time of the day, the distance an individual travelled when mussel‐free was predictive of the number of prey it caught when colonised, suggesting that the greater general activity of some individuals helped mitigate negative effects that mussel attachment had on prey capture. 5. Our results add to a growing number of negative effects of zebra mussel colonisation on sprawling and hiding dragonfly larvae. Although the impact of these costs on dragonfly populations remains to be determined, a decrease in this guild of predators whose life cycle spans aquatic and terrestrial habitats might have cascading effects across ecosystems.     

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.     

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.     

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.     

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.     

Predicting the impacts of an introduced species from its invasion history: an empirical approach applied to zebra mussel invasions

1. Quantitative models of impact are lacking for the vast majority of known invasive species, particularly in aquatic ecosystems. Consequently, managers lack predictive tools to help them prioritise invasion threats and decide where they can most effectively allocate limited resources. Predictive tools would also enhance the accuracy of water quality assessments, so that impacts caused by an invader are not erroneously attributed to other anthropogenic stressors. 2. The invasion history of a species is a valuable guide for predicting the consequences of its introduction into a new environment. Regression analysis of data from multiple invaded sites can generate empirical models of impact, as is shown here for the zebra mussel Dreissena polymorpha. Dreissena's impacts on benthic invertebrate abundance and diversity follow predictable patterns that are robust across a range of habitat types and geographic regions. Similar empirical models could be developed for other invaders with a documented invasion history. 3. Because an invader's impact is correlated with its abundance, a surrogate model may be generated (when impact data are unavailable) by relating the invader's abundance to environmental variables. Such a model could help anticipate which habitats will be most affected by invasion. Lack of precision should not be a deterrent to developing predictive models where none exist. Crude predictions can be refined as additional data become available. Empirical modelling is a highly informative and inexpensive, but underused, approach in the management of aquatic invasive species.     

Biological control of the zebra mussel Dreissena polymorpha and the snail Biomphalaria glabrata, using Gramicidin S and D and molluscicidal strains of Bacillus

Applications of Final Whole Culture (FWC) or primary powder material from strains of each of four Bacillus species (B. alvei, B. brevis, B. circulans, B. laterosporus) used singly, as well as the antibiotics Gramicidin S (GS) and Gramicidin D (GD) used singly, were found to be molluscicidal against several life cycle stages of the zebra mussel Dreissena polymorpha. Combinations of the bacterial material with either GS or GD were either additive (for GS) or antagonistic (for GD). The smaller the life cycle stage of the animal, the more sensitive it was to either the bacterial or antibiotic agent. The veliger stage was particularly sensitive to each agent, with the molluscicidal effect being more rapid in the veliger (5 h) than in the adult (6 days). The molluscicidal effects of these agents (at 1–100 μ g ml⁻¹) against the veliger stages of the zebra mussel were comparable to the activity of B. thuringiensis and B. sphaericus against their target organisms. These agents used singly were also active against small adult Biomphalaria glabrata, the snail vector of schistosomiasis (eg at tenths of μ g ml⁻¹ of GS). Received 09 July 1996/ Accepted in revised form 06 November 1996     

Variation in growth rates of the zebra mussel, Dreissena polymorpha, within Lake Wawasee

1. Field experiments conducted in Lake Wawasee in 1995 and 1996 measured the response of shell growth of Dreissena polymorpha to environmental gradients.
2. Shell growth decreased with initial shell length in four mussel size classes ranging between 8 and 22 mm, and decreased with depth, with mussels in shallow water (<4 m) having growth rates nearly twice those of mussels in deeper water (4–7 m).
3. Growth occurred early in the spring–summer period (May–June) with relatively little shell added later in the summer (July–September), and varied significantly among sites within Lake Wawasee, but not between the 2 years of this study.
4. Rank order of sites was consistent for both years implying that environmental conditions responsible for variation in shell growth were stable within Lake Wawasee.
5. Cage design did not have a significant effect on mussel shell growth nor did the distance of growth cages above the bottom (0.5–0.75 m above the bottom versus directly on the bottom).
6. This study demonstrates the sensitivity of adult mussel growth to subtle variation in environmental conditions occurring within and among lakes, with potential consequences for mussel population dynamics and community structure and function.     

Zebra mussels (Dreissena polymorpha) in Ireland, AFLP-fingerprinting and boat traffic both indicate an origin from Britain

1. The zebra mussel (Dreissena polymorpha) is an aquatic nuisance species that invaded Ireland around 1994. We studied the invasion of the zebra mussel combining field surveys and genetic studies, to determine the origin of invasion and the vector of introduction. 2. Field surveys showed that live zebra mussels, attached to the hulls of pleasure boats, were transported from Britain to Ireland. These boats were lifted from British waters onto trailers, transported to Ireland by ferry and lifted into Irish waters within a day. Length‐frequency distributions of dead and living mussels on one vessel imported 3 months earlier revealed a traumatic occurrence caused by the overland, air‐exposed transportation. Results show that a large number of individuals survived after re‐immersion in Irish waters and continued to grow. 3. Zebra mussels from populations in Ireland, Great Britain, the Netherlands, France and North America, were analysed using amplified fragment length polymorphisms (AFLP)‐fingerprinting to determine the origin of the Irish invasion. Phylogenetic analysis revealed that Irish and British mussels clustered closely together, suggesting an introduction from Britain. 4. Ireland remained un‐invaded by the zebra mussel for more than 150 year. The introduction of the zebra mussel to Ireland occurred following the abolition of value added tax in January 1993 on imported second‐hand boats from the European Union (UK and continental Europe). This, together with a favourable monetary exchange rate at that time, may have increased the risk of invasion of the zebra mussel.