Dreissena rostriformis bugensis (quagga mussel)
- Summary of Invasiveness
- Taxonomic Tree
- Notes on Taxonomy and Nomenclature
- Distribution Table
- History of Introduction and Spread
- Risk of Introduction
- Habitat List
- Biology and Ecology
- Water Tolerances
- Natural enemies
- Notes on Natural Enemies
- Means of Movement and Dispersal
- Pathway Causes
- Pathway Vectors
- Impact Summary
- Economic Impact
- Environmental Impact
- Threatened Species
- Social Impact
- Risk and Impact Factors
- Uses List
- Detection and Inspection
- Similarities to Other Species/Conditions
- Prevention and Control
- Gaps in Knowledge/Research Needs
- Links to Websites
- Distribution Maps
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PicturesTop of page
IdentityTop of page
Preferred Scientific Name
- Dreissena rostriformis bugensis Andrusov, 1897
Preferred Common Name
- quagga mussel
Other Scientific Names
- Dreissena bugensis Andrusov, 1897
Summary of InvasivenessTop of page
D. rostriformis bugensis is a bivalve mollusc originating from the estuarine region of the rivers Dnieper and Southern Bug. The expansion of its range in Europe began only after 1940 and likely was associated with construction of interbasin canals and creation of impoundments along the large European rivers (see Orlova et al., 2005). In the mid-1980s, D. rostriformis bugensis was introduced into North America, presumably through discharge of ballast water from transoceanic ships (Mills et al., 1994). The dreissenids, including D. rostriformis bugensis, are sessile filter-feeders capable of reaching extremely high densities. Due to these biological traits, Dreissena spp. can substantially affect the environment, food webs and biodiversity of the ecosystems they invade (e.g., Karatayev et al., 1997; 2002), and cause tremendous economic damage in raw water-using industries, potable water treatment plants, and electric power stations (Pimentel et al., 2005). This species was identified as the top ranking invasive species threat to the UK in a study of almost 600 non-native species (Roy et al., 2014); it was discovered for the first time in Surrey in October 2014.
Taxonomic TreeTop of page
- Domain: Eukaryota
- Kingdom: Metazoa
- Phylum: Mollusca
- Class: Bivalvia
- Subclass: Heterodonta
- Order: Veneroida
- Unknown: Dreissenoidea
- Family: Dreissenidae
- Genus: Dreissena
- Species: Dreissena rostriformis bugensis
Notes on Taxonomy and NomenclatureTop of page
The family Dreissenidae has been reclassified many times, resulting in substantial confusion of phylogenetic relationships between its representatives. Most previous revisions of the family were based on morphological characters (reviewed in Rosenberg and Ludyanskiy, 1994). However, some dreissenid species, particularly Dreissena rostriformis and its putative subspecies Dreissena bugensis, intergrade and overlap in morphology, making DNA sequencing techniques the only possible means to resolve these systematic problems. The first extensive genetic study to resolve the nomenclatural position of D. rostriformis and D. bugensis was conducted by Stepien et al. (2003). The sequencing of mitochondrial 16S ribosomal DNA and cytochrome b gene regions showed very little difference between D. rostriformis and D. bugensis, thus suggesting that they might either be subspecies or recently (about 300 000 years ago) diverged species. Nevertheless, Stepien et al. (2003) took into account that D. bugensis was recognized by many investigators as a separate species from D. rostriformis, and recommended to continue such recognition. Therriault et al. (2004) published results of similar study in which they used the fragments of 16S ribosomal RNA and cytochrome c oxidase subunit I (COI) as genetic markers. The latter authors also found very low sequence divergence between D. rostriformis and D. bugensis indicating that these taxa are likely to constitute a single species with two distinct ecological races (saline and freshwater, respectively). However, in contrast to the former study, Therriault et al. (2004) emphasized that D. rostriformis is an ancestral name, which, in compliance with established nomenclature rules, has priority for being used in taxonomic descriptions. Therefore, until new genetic data are available, D. bugensis should be treated as a subspecies of D. rostriformis.
DescriptionTop of page
The description provided below concerns only adults of D. rostriformis bugensis. Morphological characteristics of other stages of its life cycle are presented in sections “Reproductive biology” and “Similarities to other species”. See also Ackerman et al. (1994) and ZMIS (2002) for detailed description and illustrations related to the life cycle stages of dreissenid mussels.
External shell morphology
Adults have a triangular shell of up to about 40 mm in length (see pictures). The shell is rounded ventro-posteriorly and has a pronounced convex ventral surface with no acute ventrolateral ridge or carina. The dorsal shell margin is also rounded and often has a wing-like extension (May and Marsden, 1992; Pathy and Mackie, 1993). The valves in D. rostriformis bugensis are distinctly asymmetrical, i.e. anteriorly the right valve is curved along the mediventral line (Domm et al., 1993). The thickest and oldest portion of the shell, the umbo, is pointed and lies anteriorly.
D. rostriformis bugensis are sessile molluscs which attach themselves to hard surfaces with the help of byssal threads, sclerotized non-living extracorporeal cords with adhesive plaques at the ends. These threads jut out from the pedal gape located in the middle of the ventral shell portion. They may get pulled out when removing the mussel from the substrate and one should take this into account during taxonomic identification (ZMIS, 2002).
Shell colouration patterns in D. rostriformis bugensis range from brown-yellowish to completely black, including intermediate forms with stripes of different shape and size. A sometimes useful distinguishing characteristic of D. rostriformis bugensis is a white stripe or line going across the middle of the shell from the umbone toward the posterior end. There also may be a difference in colouration between the ventrolateral and dorsolateral sides of the shell (Pathy and Mackie, 1993). In the deep waters of Lake Erie, Dermott and Munawar (1993) had discovered a distinctive D. rostriformis bugensis morph named "profunda", which is strongly laterally compressed and is pale or all white in colour. The deepwater morphotype in Lake Michigan showed great variation in both siphon length and shell dimensions, which may reflect an ability to readily adapt to various habitat conditions (Nalepa et al., 2013). Further studies, however, found no genetic differences between the common D. rostriformis bugensis and its profundal morphotype (Baldwin et al., 1996; Stepien et al., 1999; 2003).
Internal shell morphology
The internal anterior portion of the shell in D. rostriformis bugensis is covered with a small shelf-like structure called the “myophore plate” or “septum”. This plate serves as a place for attachment of the anterior adductor and anterior pedal retractor muscles. Along the dorsal edges of the valves there are two elongated “scars”, the zones where the posterior adductor and posterior pedal-byssal retractor mussels attach. The valves are connected to each other via a ligament in their dorsal-anterior portion. The hinge teeth in D. rostriformis bugensis are vestigial (Pathy and Mackie, 1993).
DistributionTop of page
The quagga mussel, D. rostriformis bugensis, originates from the estuarine region of the rivers Southern Bug and Dnieper, Ukraine. The mussels began their range extension within Europe only after 1940, when the first reservoirs were constructed on the Dnieper River. Between the 1940s and 1990s, they had spread in the following main directions (reviewed in Mills et al., 1996; Orlova et al., 2004, 2005; Son, 2007):
- north along the cascades of reservoirs on the Dnieper River;
- east through the Don River system and then north along the reservoirs on the Volga River;
- northwest through the Dniester River.
Until 2005, the westernmost European records of D. rostriformis bugensis were from the Danube River within Romania (Micu and Telembici, 2004; Popa and Popa, 2006). In 2006, however, D. rostriformis bugensis was discovered as far westward of its native area as in Rhine River Delta, the Netherlands (Molloy et al., 2007), the Dutch Haringvliet (Schonenberg and Gittenberger, 2008) and also in the Main River, Germany (Van der Velde and Platvoet, 2007). The spread of D. rostriformis bugensis within mainland Europe was facilitated by creation of river impoundments, by construction of interbasin canals and by shipping (see Orlova et al., 2004; 2005). In October 2014, it was reported for the first time from the UK, in Wraysbury Reservoir and the Wraysbury River, near Egham, Surrey (BBC, 2014; NNSS, 2014).
In the mid-1980s, D. rostriformis bugensis was introduced into North America, presumably through discharge of ship ballast water (Mills et al., 1994). Currently, the mussels are confined mainly to the Great Lakes region, though recently their range has expanded to the west and south-west (USGS-NAS, 2008), where they are found in Arizona, California, Colorado, Nevada and Utah (Wong and Gerstenberger, 2011; Benson, 2012). A special issue of the journal Aquatic Invasions has been devoted to 'Quagga Mussels in the Western United States' (http://www.aquaticinvasions.net/2011/issue2.html).
Up to date information on distribution in North America can be found on the Zebra Mussel and Quagga Mussel Information Resource Page published by the US Geological Survey.
Distribution TableTop of page
The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.
|Continent/Country/Region||Distribution||Last Reported||Origin||First Reported||Invasive||Reference||Notes|
|Canada||Present||1992||Introduced||USGS-NAS, 2008||Soulanges Canal, St Lawrence River|
|-Ontario||Present||1999||Introduced||Invasive||USGS-NAS, 2008||St Lawrence River, Lake Ontario and Lake Erie|
|-Quebec||Present||Introduced||Invasive||Vanderploeg et al., 2002||St Lawrence River|
|USA||Present||2005||Introduced||USGS-NAS, 2008||Lake Superior in Duleth-Superior Harbour|
|-Arizona||Widespread||Introduced||Invasive||USGS-NAS, 2008; McMahon, 2011||Lakes Pleasant, Powell, Havasu, Mohave, Mead; Central Arizona Project Canal|
|-California||Present||Introduced||Invasive||USGS-NAS, 2008||San Vicente, Copper Basin and Dixon reservoirs, Lakes Otay, Havasu, Skinner, Mathews, Murray, Miramar, Sweetwater Reservoir; Hinds Pumping Station|
|-Colorado||Present||Introduced||Benson et al., 2012||Several lakes along the Colorado River and Pueblo Reservoir|
|-Illinois||Present||2003||Introduced||Invasive||USGS-NAS, 2008||Lake Michigan|
|-Indiana||Present||2003||Introduced||Invasive||USGS-NAS, 2008||Lake Michigan|
|-Iowa||Present, few occurrences||Introduced||Benson et al., 2012|
|-Kentucky||Present, few occurrences||Introduced||Benson et al., 2012|
|-Massachusetts||Present||1995||Introduced||USGS-NAS, 2008||Mississippi River|
|-Michigan||Present||Introduced||USGS-NAS, 2008||Lake Michigan (invasive), Lake Huron and Lake St Clair|
|-Minnesota||Present, few occurrences||Introduced||Benson et al., 2012|
|-Missouri||Present||1995||Introduced||Invasive||USGS-NAS, 2008||Mississippi River|
|-Nevada||Present||2007||USGS-NAS, 2008; McMahon, 2011; Wong and Gerstenberger, 2011||Colorado River, Lake Mead|
|-New York||Present||Introduced||Invasive||May and Marsden, 1992; Mills et al., 1996; USGS-NAS, 2008||Lake Erie, Erie Canal; Lake Ontario and several Finger Lakes; Niagara River; Port Colbourne; Cayuga Lake; Onondaga Lake outlet in Syracuse; Mohawk River; Great Lakes region and several inland waterbodies|
|-Ohio||Present||2002||Introduced||Invasive||USGS-NAS, 2008||Lake Erie|
|-Pennsylvania||Present||2007||Introduced||Invasive||USGS-NAS, 2008||Lake Erie; Dutch Springs Reservoir; Clover Creek Quarry|
|-Wisconsin||Present||2005||Introduced||Invasive||USGS-NAS, 2008||Lake Michigan, Lake Superior|
|Germany||Present||Introduced||Invasive||Velde and Platvoet, 2007||River Main, east of Wurzburg near Horblach|
|Hungary||Present||Introduced||Invasive||Bódis et al., 2011|
|Moldova||Present||2007||Introduced||Son, 2007||Moldavian part of the Dniester River|
|Netherlands||Present||2006||Introduced||Invasive||Molloy et al., 2007; Schonenberg and Gittenberger, 2008||Hollands Diep, Delta of the Rhine River near Willemstadt|
|Romania||Present||2005||Introduced||Invasive||Micu and Telembici, 2004; Popa and Popa OPLO, 2006||Danube River|
|Russian Federation||Present||Antonov, 1993; Antonov, 1996; Orlova et al., 1999; Antonov and Khokhlova, 2004; Lvova, 2004; Orlova et al., 2004; Scherbina GKh, 2005; Zhulidov et al., 2005; Zhulidov et al., 2006; Son, 2007|
|-Northern Russia||Present||Introduced||Invasive||Orlova et al., 2005||Basin of the Upper Volga River|
|-Southern Russia||Present||Introduced||Invasive||Orlova et al., 2005||Lower reaches of the rivers Volga, Don and Manych|
|UK||Present||Introduced||2014||Invasive||NNSS, 2014||First UK report. Wraysbury Reservoir and the Wraysbury River, a tributary of the River Colne, near Egham, Surrey|
|Ukraine||Present||Zhuravel, 1951; Kharchenko, 1995; Mills et al., 1996; Orlova et al., 2005; Silaeva and Protasov, 2005; Son, 2007|
History of Introduction and SpreadTop of page
D. rostriformis bugensis was first discovered in the Southern Bug River part of the Dnieper-Bug Liman near the Nikolaev City, Ukraine (Andrusov, 1890 in Mills et al., 1996). Although there was extensive ship traffic between the native area of D. rostriformis bugensis and other European regions, this mussel remained restricted to the Dnieper-Bug Liman and the lower parts of the Southern Bug and Ingulets rivers until the middle of the twentieth century. According to Orlova et al. (2005), a crucial factor in the range expansion of D. rostriformis bugensis was the creation of impoundments on large European rivers. These authors suggest that D. rostriformis bugensis is poorly adapted to colonize unaltered riverine ecosystems wheareas in large reservoirs it finds conditions similar to those of its native estuary. In correspondence with this hypothesis, the first observation of D. rostriformis bugensis outside its native area was reported in 1941, soon after construction of the first reservoir on the Dnieper River (Dnieper Reservoir). Between the 1950s and 1970s, D. rostriformis bugensis eventually moved upstream and colonised the whole cascade of reservoirs built on the Dnieper. By 1990-1992, the mussel had spread to the Pripyat River Delta, which is currently its northernmost range within the Dnieper River basin (Mills et al., 1996; Orlova et al., 2005).
In 1980, D. rostriformis bugensis was recorded for the first time east of its native area, i.e. in the lower stretch of the Don River in Russia, where it supposedly was delivered on the ship hulls or in ballast water. In 1996, it was found in the middle part of that river (Zhulidov et al., 2005). Construction of the Volga-Don Canal (1948-1952) and extensive ship traffic along it allowed mussels to penetrate into the next large Russian river – the Volga, which drains into the Caspian Sea. Until recently, the initial finding of D. rostriformis bugensis in the Volga River system was believed to have occurred in 1992 (Antonov, 1993; Orlova et al., 2004; 2005). However, Zhulidov et al. (2005) re-examined their own archived dreissenid specimens collected between 1979 and 1996 and revealed that D. rostriformis bugensis were present in the Volga River system near the Akhtyubinsk City as early as 1981. Between 1994 and 1997, the species was found in the Volga Delta and in the shallows of the Caspian Sea. In 1997, D. rostriformis bugensis was recorded in the upper part of the Volga River. By 2000, the mussels colonised seven of the nine large reservoirs of the Volga cascade (Orlova et al., 2004). Around 2001, D. rostriformis bugensis penetrated through the shipping canal from the Volga River into the Moscow River (Lvova, 2004).
The first record of D. rostriformis bugensis west of its native range was in 1988 from the Dniester Reservoir, Ukraine (Shevtsova, 2000), and by 2001 the mussel was already common in the lower part of this river, including the Dniester Estuary (Prof. T. A. Kharchenko, personal communication in Orlova et al., 2005). In 2005, D. rostriformis bugensis were observed also in the Moldavian part of the Dniester (Son, 2007). Further spread of D. rostriformis bugensis west of its native area was evidenced by two records from the Lower Danube River made in 2004 (Micu and Telembici, 2004) and 2005 (Popa and Popa, 2006) in Romania. The creation of irrigation and shipping canals and ship traffic are considered the main causes for D. rostriformis bugensis invasion into the Dniester and Danube Basins (Kharchenko, 1995; Son, 2007). The westernmost European populations of D. rostriformis bugensis were revealed in 2006 in the Rhine River Delta, the Netherlands (Molloy et al., 2007), and in 2007 in the Main River, Germany (Van der Velde and Platvoet, 2007). A later paper by Schonenberg and Gittenberger (2008) reports quagga mussel in the Dutch Haringvliet which is now recognised as the westernmost record of this species in Europe. Molloy et al. (2007) suspected that the source of the introduction of D. rostriformis bugensis into Western Europe was the Main-Danube Canal re-opened after reconstruction in 1992. As Van der Velde and Platvoet (2007) did not find D. rostriformis bugensis in the canal itself, it is likely that population of D. rostriformis bugensis in the Netherlands arose as a result of a single long-distance transfer of the propagules from the lower Danube River. After having been identified as the top ranking invasive species threatening to invade the UK (Roy et al., 2014) this mussel was found in Wraysbury Reservoir and the Wraysbury River, a tributary of the River Colne in the Thames catchment, near Egham, Surrey in October 2014.
In 1989, D. rostriformis bugensis was first discovered in North America, at Port Colborne in Lake Erie (Mills et al., 1996). The most likely vector for this introduction was via ballast water of transoceanic ships carrying the mussel’s larvae (Mills et al., 1994). The biochemical (Spidle et al., 1994) and genetic (May et al., 2006) comparative studies indicate that the Black Sea drainage was the most probable source of the North American population of D. rostriformis bugensis. By 1993, D. rostriformis bugensis was found in the Great Lakes from the central basin of Lake Erie to the St. Lawrence River at Quebec City (Mills et al., 1996). The first record of D. rostriformis bugensis outside the Great Lakes Basin was made in 1995 in the Mississippi River between St. Louis, Missouri and Atlon, Illinois (O’Neil, 1995). In 2005, the first mussels were sighted in Lake Superior (J Kelly, personal communication in Benson et al., 2008). By January 2007 the mussels were found in Lake Mead near Boulder City, Nevada (W Baldwin, personal communication in Benson et al., 2008), and in the lakes Havasu and Mohave on the California/Arizona border (R Aikens, personal communication in Benson et al., 2008). Late in 2007, D. rostriformis bugensis was found in six Californian reservoirs (D Norton, personal communication in Benson et al., 2008). The spread of D. rostriformis bugensis between water basins in the USA was facilitated by overland transportation of recreational boats (Benson et al., 2008), and the presence of many artificial waterways for drinking water and irrigation also exacerbates the spread of D. rostriformis bugensis veligers (Wong and Gerstenberger, 2011).
For a synthesis of data on the invasion history, distribution and relative abundances of D. bugensis see Zhulidov et al. (2010).
IntroductionsTop of page
|Introduced to||Introduced from||Year||Reason||Introduced by||Established in wild through||References||Notes|
|Natural reproduction||Continuous restocking|
|Germany||Romania||2000-2005||Interbasin transfers (pathway cause)||Yes||No||Velde and Platvoet (2007)|
|Moldova||Ukraine||1990-1995||Interconnected waterways (pathway cause)||Yes||No||Son (2007)|
|Netherlands||Romania||2000-2005||Interbasin transfers (pathway cause)||Yes||No||Molloy et al. (2007)|
|Romania||Ukraine||1995-2000||Interconnected waterways (pathway cause)||Yes||No||Micu and Telembici (2004); Popa and Popa OPLO (2006)|
|Russian Federation||Ukraine||1970-1980||Interbasin transfers (pathway cause)
Interconnected waterways (pathway cause)
|Yes||No||Zhulidov et al. (2005)|
|Ukraine||Ukraine||1940||Interconnected waterways (pathway cause)||Yes||No||Mills et al. (1996); Orlova et al. (2005)||Until 1940 is was confined to a restricted area of interconnected estuaries of the Dnieper and Southern Bug rivers, after 1940 it began to spread along the entire Ukranian part of the Dnieper River Basin|
|USA||Ukraine||1980-1985||Yes||No||Miller et al. (1994)||Intercontinental transfer|
Risk of IntroductionTop of page
There are two principal means for the spread of D. rostriformis bugensis (Orlova et al., 2005):
- natural downstream drift of planktonic larvae from an invaded upstream locality;
- human-mediated transfers.
HabitatTop of page
Habitat ListTop of page
|Irrigation channels||Present, no further details||Harmful (pest or invasive)|
|Lakes||Present, no further details||Harmful (pest or invasive)|
|Reservoirs||Principal habitat||Harmful (pest or invasive)|
|Rivers / streams||Present, no further details||Harmful (pest or invasive)|
|Inshore marine||Present, no further details||Natural|
Biology and EcologyTop of page
No karyological studies have been conducted on D. rostriformis bugensis. However, its close relative D. polymorpha has a karyotype with 2n=32, composed of 20 metacentric and 12 acrocentric chromosomes (Grishanin, 1990).
Allozyme electrophoresis revealed relatively high levels (9.7-14.5%) of genetic variability both in North American and European populations of D. rostriformis bugensis (see Table 1). The high level of allozyme genetic diversity found in D. rostriformis bugensis from North America (May and Marsden, 1992; Spidle et al., 1994) suggests that the founder population consisted of a large number of individuals and that there was no severe genetic bottleneck within that population. Much lower intraspecific diversity, however, was found in studies which used the mitochondrial cytochrome c oxidase subunit I gene (COI) (e.g., 0.65%; Baldwin et al., 1996). Such results are likely to be explained by lower rates of mutagenesis in these parts of genome (e.g., Stepien et al., 1999).
Genetic discrimination from other species
Several studies have been undertaken to develop reliable genetic markers allowing for the discrimination between dreissenids and other related molluscs at their various life cycle stages. In these works, the COI gene and mitochondrial 16S and 28S ribosomal DNA fragments were sequenced and then subjected to restriction enzyme analysis to find species-specific digestion profiles:
Table 1. Genetic markers developed for discrimination of D. rostriformis bugensis from other related molluscs
DNA used for sequencing
Enzyme used in restriction analysis
Length of diagnostic digestion fragments (base pairs)
710 bp fragment of the COI mitochondrial gene
Baldwin et al., 1996
710 bp fragment of the COI mitochondrial gene
Claxton et al., 1997
486 bp fragment of the mitochondrial 16S ribosomal DNA
Stepien et al., 1999
Nuclear 28S ribosomal DNA*
Therriault et al., 2004
Mitochondrial 16S ribosomal DNA *
Therriault et al., 2004
NOTE: * The size of the fragment is not specified in original paper.
Hybridization with other species
Hybrids between D. rostriformis bugensis and D. polymorpha were obtained in the laboratory by pooling gametes collected after exposure to serotonin. Nevertheless, the hybrid larvae did not survive to the settling stage (Nichols and Black, 1994), indicating that successful interspecific hybridization between these molluscs is unlikely to occur under natural conditions. Indeed, an extensive allozyme survey of D. polymorpha and D. rostriformis bugensis from Lake Ontario and Lake Erie revealed no hybrid individuals (Spidle et al., 1995). Species-specific sperm attraction (Miller et al., 1994) and the large genetic distance between D. rostriformis bugensis and D. polymorpha (May and Marsden, 1992; Spidle et al., 1994; Stepien et al., 1999; Therriault et al., 2004) also present significant barriers to hybridization.
The life cycle of dreissenids begins with external fertilization of gametes released into the water by dioecious individuals. The sperm cells of D. rostriformis bugensis are composed of three parts: 1) a head (acrosome + nucleus); 2) a slightly curved middle piece containing mitochondria and basal bodies, and 3) a flagellum. The mean size of sperm is about 4.6x1.2 μm (Walker et al., 1996). Ripe eggs of D. rostriformis bugensis are about 80 μm in diameter (Roe and MacIsaac, 1997). The number of eggs produced by a female D. rostriformis bugensis are believed to be as high as found in D. polymorpha, i.e. up to 960,000 per year (Keller et al., 2007).
Numerous field studies have shown that spawning in dreissenids usually does not start if water temperature is below 12°C, and that the mass release of gametes takes place in June-August (e.g., Walz, 1978; Sprung, 1987; Borcherding, 1991; Nichols, 1996; Karatayev et al., 1997). In deep part of Lake Erie, however, the spawned D. rostriformis bugensis females were recorded at temperatures as low as 4.8°C (Roe and MacIsaac, 1997). Synchronization of spawning is likely to be chemically mediated by serotonin (5-hydroxytryptamine) which is released by mussels into the water column (Ram et al., 1992; 1993). In Lake Mead, Nevada-Arizona, a histological analysis of the gonads of D. rostriformis bugensis showed that they are able to reproduce year-round, although the seasonal pattern of maturity indices were found to differ between the deepest and shallowest depths. Among different environmental variables, including water temperature, depth, water salinity, and dissolved oxygen, temperature was the only factor which showed a significant effect upon D. rostriformis bugensis reproduction (Ianniella 2009). Concentration of food is also a significant cue for the gametogenesis and spawning in D. rostriformis bugensis. For example, the gametogenic index of D. rostriformis bugensis from Lake Erie was demonstrated to strongly correlate with the content of chlorophyll a and protein in the water (Claxton and Mackie, 1998).
The time intervals required for development of D. rostriformis bugensis at subsequent stages of their life cycle have not been investigated in detail.
Planktonic and settling larvae
After the fertilization and embryological period (up to 2 days), a trochophore larva develops. This free-swimming ciliated larva gives rise to the next developmental stage called the veliger or shelled larva. Four basic types of veligers can be defined on the basis of hinge development, shell shape, shell size, and the presence or absence of a foot and velum, a ciliated larval organ of feeding and locomotion. Within 2-9 days post fertilization (dpf), the developing veligers secrete a shell with a straight hinge line. The straight-hinged or D-shelled larvae of D. rostriformis bugensis are rounded in appearance, with the shell height averaging 90% of the shell length. Within 7-9 dpf, the hinge line begins to curve and the shell umbo becomes distinct. In developed umbonal veligers of D. rostriformis bugensis, the right umbo is slightly more convex and extends further upward compared to the left umbo. The next type of veliger is the pediveliger. This stage is characterized by a clam-shaped body and appearance of the foot (and associated byssal apparatus) and gill filaments. The foot is used for swimming and for crawling on surfaces. Within 18-90 dpf, the pediveligers settle and secrete a byssal thread onto a suitable substrate. Once anchored, the pediveliger undergoes metamorphosis (within 3-5 days at 22°C) and becomes a postveliger or plantigrade mussel.The principal morphological changes that occur during metamorphosis are loss of the velum, full development of the gills and mouth, and secretion of the adult shell. The shell reorients its growth planes and transforms from a clam shape to an elongated mussel shape (Ackerman et al., 1994; Nichols and Black, 1994). The planktonic veligers of the invasive quagga mussel were present year round in Lake Mead (Arizona-Nevada), with high abundance from September to October (>20 veligers/l), whereas the percentage of pediveligers peaked from November to January (Gerestenberger et al., 2011).
In Lake Erie, Martel et al. (2003) found that veligers of D. rostriformis bugensis settle at a greater size offshore than in nearshore habitats. As suggested by the authors, this difference could have several, if not mutually exclusive, explanations:
- the larvae might grow faster in the offshore deep-water habitats;
- only faster growing larvae could survive the time period required to drift offshore and settle on substrates;
- larger larvae could have advantage under early postmetamorphic natural selection in hypolimnion;
- longer planktonic period or delay of metamorphosis might also result in greater larval size at settlement.
In Lake Mead, D. rostriformis bugensis veligers showed no preference to settlement on any of the six testing substrates (acrylonitrile butadiene styrene (ABS) plastic, high density polyethylene (HDPE) plastic, concrete underlayment board (CUB), aluminum, stainless steel and fiberglass were tested), but settlement was limited by depth, with greater settlement on substrates at depths of 6–28 m (Mueting et al., 2010). In another experiment in Lake Mead, Wong et al. (2012) reported that active settlement of veligers was recorded in all sampling events from January to December, with the highest settlement rate found from 20th October to 19th December (Wong et al., 2012).
Juvenile and adult mussels
When the siphons appear during metamorphosis, the mussel is considered to be a juvenile. Juveniles can crawl over substrates or sometimes return to the water column (Ackerman et al., 1994). However, they soon anchor themselves to a substrate and eventually become adult. The minimal size at which dreissenids become sexually mature varies significantly between populations, e.g. >5 mm (Nichols, 1996), 6 mm (Juhel et al., 2003), 9.4 mm (Walz, 1978). Commonly, the mussels reach this size in their first year.
Physiology and Phenology
Feeding and respiration
D. rostriformis bugensis is a filter-feeder which consumes food particles suspended in the water column (algae, bacteria, detritus, micro-zooplankton). Dreissenid mussels have a very complex and effective filtration apparatus (see detailed descriptions in Morton, 1969, 1971; Silverman, 1996a,b; Sprung and Rose, 1988). Water is pumped into the mantle cavity of a mussel through the inhalant siphon, which has many tentacles aiding in the rejection of too large, irritating or sharp particles. Smaller particles enter into the mantle cavity and are strained from the water through a network of cilia located on the surfaces of each of the four gill sheets. The cilia gradually sweep the particles anteriorly towards the two labial palps located on each side of the mouth. Cilia of the labial palps are able to sort the particles into edible and inedible. Particles of an appropriate size (usually 5-35 μm) and palatability are then moved into the mouth, whereas rejected particles are bound in mucus and moved to the edge of the mantle. The mucoid-bound particle pellets are called pseudofaeces or agglutinates. They are ejected from the mantle cavity through the excurrent siphon by rapid closing of the shell valves.
Ackerman (1999) showed that water velocity has a positive influence on clearance rate in D. rostriformis bugensis up to a value of 9 cm×s-1 (clearance rate is the volume of water passing through gills per unit time). Beyond this point, increasing velocity had an inhibitory effect on filtration. At optimal velocity, there was a strong positive correlation between the clearance rate and mussel size, e.g., individuals with the shell lengths of 11 and 32 mm filtered at mean rates of about 120 and 400 mL×mussel-1×h-1, respectively. Diggins (2001) revealed similar positive impact of mussel size, and found that filtration was most intensive during warm seasons of the year.
Filtration in dreissenids is coupled with respiration. Oxygen penetrates into the blood when water passes though the gills via small openings called “ostia” (Morton, 1969). In laboratory experiments, Summers et al. (1996) revealed that respiration rate in D. rostriformis bugensis declines with increasing water turbidity and increases at high temperatures. Smaller mussels demonstrated a higher respiration rate per unit weight than larger individuals. Smaller mussels also exhibited a greater drop in respiration when subjected to turbid water. Field observations conducted by Stoeckmann (2003) in Lake Erie indicate that respiration in D. rostriformis bugensis tracks the seasonal increase of temperature and reaches its highest values in July-August.
A detailed discussion of digestion in dreissenids and other bivalves can be found in Morton (1971, 1983). Having entered the mouth, food particles pass through the esophagus to the stomach where they undergo a mechanical and chemical digestion. The stomach of dreissenids is a thin-walled sac with a gelatinous rod-like body inside (“crystalline style”). This body contains starch-digesting enzymes that facilitate the chemical breakdown of the food particles. The rest of the stomach is composed of ciliated folds that also participate in processing food. Cilia carry well decomposed particles to the digestive diverticulum for subsequent intracellular digestion. Small particles are taken up by the cells of diverticulum into food vacuoles, whereas larger undigested particles and waste products are carried to the rectum and eventually expelled via the anus through the exhalant siphon.
The excretory system of dreissenids is composed of two kidneys located just under the pericardium. The hemolymph is filtered through the pericardial wall into the cavity of the pericardium and then passes into the kidneys. The excess water and waste metabolic products are carried out of the mussel through the exhalant siphon (see ZMIS, 2002). Conroy et al. (2005) found that rates of excretion of soluble nitrogen and phosphorus by D. rostriformis bugensis positively correlate with the size and individual weight of mussels.
Field data by MacIsaac (1994) and Stoeckmann (2003) indicate that smaller D. rostriformis bugensis grow at a lower rate than larger mussels. For instance, in an in situ experiment conducted by MacIsaac (1994), the mean growth rate in 15-mm D. rostriformis bugensis was 0.04 mm day-1, whereas in 5-mm mussels it was 0.12 mm day-1. Water temperature also positively affects the growth of D. rostriformis bugensis (MacIsaac, 1994; Baldwin et al., 2002), as does food quantity (Baldwin et al., 2002). Baldwin et al. (2002) found that growth depends also on the quality of food that mussels consume. When fed on a lake seston, D. rostriformis bugensis demonstrated an up to 0.78 day-1 mean instantaneous growth rate. However, in an experiment using Chlamydomonas as food, the mean instantaneous growth rate was up to 1.45 day-1. In general, D. rostriformis bugensis expends more energy in somatic growth than in reproduction (Stoeckmann, 2003), with the highest growth rates observed from late spring to early autumn (Thorp et al., 2002). In the sub-tropical Lake Mead, Nevada-Arizona, lowest growth rates of D. rostriformis bugensis were recorded from late summer to early autumn (Wong et al., 2012).
Highly prolific molluscs of the genus Dreissena can be considered typical r-strategists (e.g., McMahon, 2002). An increasing number of studies are now reporting displacement of D. polymorpha by D. rostriformis bugensis in co-invaded waterbodies of Europe (e.g., Tseyeb et al. 1966; Zhuravel 1967; Pligin 1984; Orlova et al. 2004, 2005; Zhulidov et al. 2004) and North America (e.g., Mills et al. 1999; Ricciardi and Whoriskey 2004; Haynes et al. 2005; Wilson et al. 2006) indicating that the latter species has a set of K-strategy traits allowing it to outcompete its ecologically similar congener. Such K-selection traits of D. rostriformis bugensis, in particular, include:
- a higher filtration rate (Diggins, 2001; Prianichnikova and Scherbina, 2005);
- a higher bioenergetic efficiency manifested as a low respiration rate accompanied with a higher growth rate (e.g., Mills et al. 1993, 1999; Baldwin et al., 2002; Stoeckmannn, 2003; Ricciardi and Whoriskey 2004);
- allocation of a greater portion of energy to growth than to reproduction (Stoeckmann, 2003; Conroy et al., 2005);
- spawning at a lower temperature (Roe and MacIsaac, 1997; Claxton and Mackie, 1998);
- settlement of the planktonic larvae at a larger size (Martel et al., 2001).
Dreissenid mussels, including Dreissena rostriformis bugensis, are filter-feeders that consume a wide range of particles suspended in the water column, i.e. algae, bacteria, detritus and, occasionally, micro-zooplankton. The most preferred foods, however, are diatom and cryptophyte algae, especially those that contain high concentrations of long-chained polyunsaturated fatty acids (Vanderploeg et al., 2002; Wacker and von Elert, 2003).
Dreissenid mussels modify the aquatic habitats via various mechanisms, including (see Karatayev et al., 1994; 2002):
- formation of complex three-dimensional structures composed of shells;
- production of faeces and pseudofaeces that are readily digestible for detritophagous animals;
- improvement of the oxygen regime via filtration activity.
As a result, large aggregations of dreissenids attract various aquatic organisms that gain a shelter and abundant food resources (e.g., Stewart et al., 1998; 1999; Bially and MacIsaac, 2000; Ward and Ricciardi, 2007).
Bially and MacIsaac (2000) reported that the most common taxa of invertebrates they found in mixed colonies of D. rostriformis bugensis and D. polymorpha in Lake Erie, North America were the amphipods Gammarus fasciatus and Chaetogammarus (=Echinogammarus) ischnus, cyclopoid copepods, ostracods, oligochaetes, chironomids, the hydrozoan Hydra, and the planarian worm Dugesia. Taxa found exclusively in the mussel’s colonies but not in adjacent soft sediments were Gammarus and Chaetogammarus, Hydra, Dugesia, Hirudinea (leeches), Zaitzevia (beetles), Hydropsychidae (caddis flies), Asselidae (isopods), and gastropods. The authors revealed strong positive relationships between the area of Dreissena colony and such parameters as invertebrate taxon richness and total invertebrate abundance. Dreissena aggregations appeared to support between 462% and 703% more taxa and between 202% and 335% more individuals than did adjacent sediments lacking mussels.
Similar taxa were found to be closely associated with D. rostriformis bugensis colonies in Europe. For example, in the Kanev Reservoir (Dnieper River Basin), Ukraine these taxa included the amphipods C. ischnus, Dikerogammarus villosus, Dikerogammarus haemobaphes, Chelicorophium curvispinum, the polychaete worm Hypania invalida, the gastropod Lithoglyphus naticoides, some chironomids, and oligochaetes (Pligin, 2005).
Besides invertebrates, Dreissena aggregations may also affect bacterial communities. Lohner et al. (2007) reported that overall bacterial activity and metabolic diversity in Lake Erie was enhanced by the presence of D. polymorpha and D. rostriformis bugensis clusters.
Despite generally positive effects of Dreissena on the taxonomical richness and abundance of benthic invertebrates and microorganisms, some species, e.g., unionid and sphaeriid clams and burrowing amphipods (Diporeia spp.), may decline in the presence of these mussels (see Karatayev et al., 2007; Ward and Ricciardi, 2007).
Water TolerancesTop of page
|Parameter||Minimum Value||Maximum Value||Typical Value||Status||Life Stage||Notes|
|Depth (m b.s.l.)||Optimum||130 tolerated, the maximum tolerated depth is given after Mills et al. (1993). The preferred depth for D. r. bugensis reported in literature is controversial|
|Dissolved oxygen (mg/l)||8||10||Optimum||1 tolerated|
|Hardness (mg/l of Calcium Carbonate)||68||Optimum||27 tolerated, the values of hardness were re-calculated from the calcium concentration data provided for D. r. bugensis by Jones and Ricciardi (2005)|
|Salinity (part per thousand)||0.00||0.02||Optimum||5 tolerated|
|Turbidity (JTU turbidity)||Optimum||Typical value of 80, tolerated turbidity indicated herein is the maximum turbidity value used in the experimental laboratory study by Summers et al. (1996)|
|Velocity (cm/h)||9||Optimum||0-19 tolerated, the values of velocity were taken from the experimental study on clearance rate in quagga mussels conducted by Ackerman (1999)|
|Water pH (pH)||7.3||9.6||Optimum|
|Water temperature (ºC temperature)||20||Optimum||Lower limit tolerated close to 0, upper limit 30|
Natural enemiesTop of page
|Natural enemy||Type||Life stages||Specificity||References||Biological control in||Biological control on|
|Aix sponsa||Predator||Adult||not specific||Petrie and Knapton, 1999|
|Anas americana||Predator||Adult||not specific||Petrie and Knapton, 1999|
|Anas crecca||Predator||Adult||not specific||Petrie and Knapton, 1999|
|Anas platyrhynchos||Predator||Adult||not specific||Petrie and Knapton, 1999|
|Anas rubripes||Predator||Adult||not specific||Petrie and Knapton, 1999|
|Anas strepera||Predator||Adult||not specific||Petrie and Knapton, 1999|
|Aythya affinis||Predator||Adult||not specific||Petrie and Knapton, 1999|
|Aythya americana||Predator||Adult||not specific||Petrie and Knapton, 1999|
|Aythya marila||Predator||Adult||not specific||Petrie and Knapton, 1999|
|Aythya valisineria||Predator||Adult||not specific||Petrie and Knapton, 1999|
|Bucephala albeola||Predator||Adult||not specific||Petrie and Knapton, 1999|
|Bucephala clangula||Predator||Adult||not specific||Petrie and Knapton, 1999|
|Bucephalus polymorphus||Parasite||Adult||to genus||Chernogorenko and Boshko, 1992|
|Caspiobdella fadejewi||Parasite||Adult||not specific||Popova and Biochino, 2001|
|Chaetogaster limnaei||Parasite||Adult||not specific||Conn et al., 1996|
|Cyprinus carpio||Predator||Adult||not specific||Ricciardi, 2001|
|Dorylaimus stagnalis||Adult||not specific||Popova and Biochino, 2001|
|Echinoparyphium recurvatum||Parasite||Adult||not specific||Tyutin and Scherbina, 2006|
|Ephydatia muelleri||Adult||not specific||Ricciardi et al., 1995|
|Erpobdella||Parasite||Adult||not specific||Tyutin and Scherbina, 2006|
|Eunapius||Adult||not specific||Ricciardi et al., 1995|
|Helobdella stagnalis||Parasite||Adult||not specific||Popova and Biochino, 2001|
|Mideopsis||Parasite||Adult||not specific||Tyutin and Scherbina, 2006|
|Neoacanthoparyphium||Parasite||Adult||not specific||Tyutin and Scherbina, 2006|
|Neogobius melanostomus||Predator||Adult||to genus||Ricciardi, 2001|
|Ophryoglena||Parasite||Adult||to genus||Tyutin and Scherbina, 2006|
|Paratanytarsus||Adult||not specific||Ricciardi, 1994|
|Proterorhinus marmoratus||Predator||Adult||not specific||Ricciardi, 2001|
|Trichodina||Adult||not specific||Tyutin and Scherbina, 2006|
|Unionicola||Parasite||Adult||not specific||Tyutin and Scherbina, 2006|
Notes on Natural EnemiesTop of page
In their comprehensive review of international literature on the natural enemies of Dreissena spp., Molloy et al. (1997) revealed 176 species of predators, 34 taxa of parasites and 10 species of space/food competitors. Most of these species were reported for D. polymorpha, whereas information on D. rostriformis bugensis is much scarcer. However, due to their very similar life histories and ecological properties, both dreissenid mussels can be expected to have similar natural enemies. Thus, a short extract from the review paper by Molloy et al. (1997) is provided below to give a general idea on taxa that negatively affect Dreissena:
Ten species in Europe and 5 species in North America have been field-documented as consuming planktonic Dreissena larvae, including Cyprinidae (7 species), Clupeidae (3 species), Osmeridae (2 species), Percidae (2 species), and Percichthyidae (1 species). Predation on attached mussels has been recorded for at least 38 species within 13 families, including 14 species within 10 families in North America and 27 species within 9 families in Europe. The most commonly reported predators of Dreissena in Europe are species of the family Cyprinidae, especially roach (Rutilus rutilus), silver bream (Blicca bjorkna), and bream (Abramis brama). The best-documented fish predators in North America are freshwater drum (Aplodinotus grunniens), round goby (Neogobius melanostomus) and redear sunfish (Lepomis microlophus) (Wong et al., 2013).
At least 36 species of birds, including 21 in Europe and 20 in North America, have been recorded to consume attached mussels. Five of them, i.e. tufted duck (Aythya fuligula), pochard (Aythya ferina), greater scaup (Aythya marila), lesser scaup (Aythya affinis), and goldeneye (Bucephala clangula), are the most well-documented avian predators of Dreissena.
Predatory calanoid copepods (e.g. Mesocyclops) have been reported to consume planktonic dreissenid larvae. Predation on attached Dreissena is known for the blue crab (Callinectes sapidus) and at least 6 crayfish species.
Other predators reported to attack larval or attached Dreissena include coelenterates, turtles, rodents and leeches.
More than 40 taxa are known to date to be associated with the mantle cavity and/or visceral mass of D. polymorpha (Molloy et al., 1997; Karatayev et al., 2000; Mastitsky, 2004; Mastitsky and Gagarin, 2004; Mastitsky and Samoilenko, 2005). The endosymbionts of D. rostriformis bugensis are not so diverse though this may be a reflection of less research work made on D. rostriformis bugensis.
Most of the organisms that occur within dreissenids, e.g. nematodes, chironomid larvae, and oligochaetes, are likely to inadvertently penetrate into the mantle cavity by being sucked in through the inhalant siphon of a mussel (e.g. Mastitsky and Gagarin, 2004; Mastitsky and Samoilenko, 2005). Some species, however, are true parasites able to cause negative impact on Dreissena. The most severe parasitic disease is likely to be caused by the trematode Bucephalus polymorphus, which can substantially destruct the gonads of a mussel host (Molloy et al., 1997; Laruelle et al., 2002). However, this and other trematodes parasitizing dreissenids cannot be used for biological control as they pose a risk for non-target species, i.e. fish and waterfowl that serve as hosts to adult stages of parasites (Molloy, 1998).
Evidence suggests that D. rostriformis bugensis is less susceptible to infections by parasites and commensals than its congener, D. polymorpha. For example, a 2-year study of the dynamics of infection by the ciliate Conchophthirus acuminatus in dreissenids from the Dnieper River, Ukraine has demonstrated a much lower infection rate in D. rostriformis bugensis than in D. polymorpha (Karatayev et al., 2000). Similarly, 4 taxa of pathogenic helminths were found in D. polymorpha from the Rybinsk Reservoir (Volga River Basin), Russia, while no helminth infection was registered in sympatric D. rostriformis bugensis (Tyutin, 2005).
Attachment to a suitable hard substrate is important for completion of the life cycle of Dreissena. Several other organisms, however, are capable of excluding dreissenids from substrates, including sponges, mud-tubes building amphipods, filamentous algae, coelenterates, and other byssate bivalves (see Molloy et al., 1997).
Although a lot of species were found to be natural enemies of Dreissena, the reports of their more or less significant suppressing effects on the mussels’ populations are rare and concern just local areas. Taking this into account, Molloy et al. (1997) conclude that the idea that natural enemies could eliminate dreissenids is “far more hopeful than realistic”.
Means of Movement and DispersalTop of page
Natural dispersal of dreissenids is realised via planktonic larvae, the veligers. New sites within an invaded waterbody become colonised by veligers that are carried by local, mainly wind-driven, water currents. The waterbodies located along the rivers and streams are invaded due to downstream drift of the larvae from donor upstream populations (Carlton, 1993; Orlova et al., 2005; Son, 2007). Dreissena larvae remain as plankton for more than a week during summer temperatures (Hillbricht-Ilkowska and Stanczykowska, 1969). In the autumn, when water temperature declines, this period may last for more than a month (see Lvova et al., 1994).
Vector Transmission (Biotic)
Dreissenids can attach to various submerged objects, including macrophytes (Horvath and Lamberti, 1997) and invertebrates with sufficiently hard outer surfaces, e.g. amphipods (Dedju, 1967) or crayfish (Brazner and Jensen, 2000). Subsequent drift of uprooted macrophytes and active migrations of invertebrates may result in introductions of the mussels into new areas. Waterfowl have also been suggested as a possible vector for transporting adult and/or larval dreissenids between isolated waterbodies (within the gut or on feathers). Nevertheless, experimental evidence (Johnson and Carlton, 1996) and field observations (Karatayev et al., 2003) suggest that such bird-mediated transfers are highly unlikely.
Shipping has been identified as the primary invasion pathway for dreissenids, including D. rostriformis bugensis (Orlova et al., 2005). The mussels can travel with a vessel either as adults attached to the hull or as planktonic larvae within ballast water. For example, ballast water is the most likely vector of D. rostriformis bugensis introduction into North America (Mills et al., 1994) and into western Europe (de Vaate, 2010). Accidental overland transitions of dreissenids at local and national levels are very often implemented via transportation of recreational boats and fishing gear (e.g., Johnson and Carlton, 1996; Padilla et al., 1996; Johnson et al., 2001; Karatayev et al., 2003; Minchin et al., 2005). Experimental studies indicate that, given temperate summer conditions, adult D. rostriformis bugensis may survive overland transportation for 3 days (Ricciardi et al., 1995a). In Lake Mead, Nevada-Arizona, D. rostriformis bugensis veligers survived approximately five days in warmer summer time, whereas under cooler autumn conditions they survived 27 days (Choi et al., 2013). It was also found that veliger survival times increased with an increased level of larval development.
Intentional introductions of dreissenids, though possible, have not been reported in the literature.
Pathway CausesTop of page
|Fisheries||Fishing gear transported overland is one of the primary vectors for D. r. bugensis introductions||Yes||Yes||Orlova et al., 2005; Ricciardi et al., 1995|
|Interbasin transfers||Shipping though interbasin canals and overland transportations of recreational boats/fishing gear||Yes||Yes||Orlova et al., 2004; Ricciardi et al., 1995; Wong and Gerstenberger, 2011|
|Interconnected waterways||Facilitating the natural spread via downstream drift of planktonic larvae||Yes||Yes||Orlova et al., 2005; Son, 2007|
Pathway VectorsTop of page
|Bait||Larvae can be transported with water in bait buckets||Yes||Yes||Johnson et al., 2001|
|Floating vegetation and debris||Can be carried by water currents whilst attached to uprooted macrophytes||Yes||Horvath and Lamberti, 1997|
|Machinery and equipment||Transported on macrophytes entangled on boat trailers or on anchors||Yes||Yes||Johnson et al., 2001|
|Ship ballast water and sediment||Yes||de Vaate AB, 2010; Orlova et al., 2005|
|Ship hull fouling||Yes||Yes||Orlova et al., 2005|
|Water||Larvae dispersed by wind-driven and downstream water currents||Yes||Yes||Orlova et al., 2005|
Impact SummaryTop of page
|Environment (generally)||Positive and negative|
Economic ImpactTop of page
The invasion of D. rostriformis bugensis into numerous European and North American waterbodies has resulted in a number of adverse impacts, both environmental and economic. Due to their ability to colonise hard surfaces, these mussels become a major fouling problem for raw water-dependent infrastructures, causing damage and increased operating expenses. The mussels invade and clog water-intake pipes and water filtration systems of the municipalities and electric generating plants, fire prevention systems, navigation dams, docks, buoys, hulls of the commercial and recreational vessels, etc. (Molloy, 1998). In the USA alone, the estimated costs associated with Dreissena total about 1 billion dollars per year (Pimentel et al., 2005).
Environmental ImpactTop of page
Impacts on Biodiversity
Dreissenid mussels, including D. rostriformis bugensis, are typical “ecological engineers”, i.e. species that “directly or indirectly control the availability of resources to other organisms by causing physical state changes in biotic or abiotic material” (Jones et al., 1994; 1997). Much more information on ecological impacts is available for D. polymorpha than for D. rostriformis bugensis. However, similar life histories and ecological niches of these two species imply their impacts to be also very similar.
As suspension feeders that attach to hard substrates and form large populations, dreissenids are functionally different from most benthic freshwater invertebrates. Due to filtration of large volumes of water, they transfer energy and matter from the water column to the benthos, providing a strong direct link between planktonic and benthic components of the ecosystem (benthic-pelagic coupling, or “benthification”), and thus induce significant alterations in the processes of invaded ecosystems (see Karatayev et al., 1997; 2002, 2007; Idrisi et al., 2001; Vanderploeg et al., 2002; Mills et al., 2003; Burlakova et al., 2005).
The filtering activity of Dreissena leads to increased water transparency and light penetration, decreased concentrations of seston and organic matter, decreased biochemical oxygen demand, and increased concentrations of ammonia, nitrates, and phosphates (see Karatayev et al., 1997, 2002; Vanderploeg et al., 2002; Burlakova et al., 2005). As D. rostriformis bugensis has higher filtration rate than D. polymorpha (Diggins, 2001), the former are likely to have greater environmental impacts associated with filtration than the latter. At the same time, D. rostriformis bugensis excretes less ammonia and phosphates than its congener (Conroy et al., 2005).
Large aggregations of Dreissena alter the physical three-dimensional structure of benthic habitats and provide shelter and food for other invertebrates. Shells of the dead mussels often form reef-like structures that also become inhabited by various invertebrate species (see Karatayev et al., 1997; 2002; 2005; and also section “Biology and Ecology: Associations”).
Invasion of Dreissena results in decreased phytoplankton density and chlorophyll concentrations (see Karatayev et al., 1997; 2002, 2007; Idrisi et al., 2001; Vanderploeg et al., 2002; Mills et al., 2003; Burlakova et al., 2005). However, the increased nutrients flux from the mussels in combination with selective grazing can facilitate certain algal species, for example, cyanobacteria that cause water blooms (Vanderploeg et al., 2001; Pillsbury et al., 2002, Raikow et al., 2004).
Zooplankton abundance usually declines after invasion of Dreissena. This decrease may result from competition for food (phytoplankton, planktonic bacteria, and other suspended particles), direct filtering of small-sized zooplankton, or from more complex interactions, such as increased predation of zooplankton by fish (see Karatayev et al., 1997; 2002; 2007; Kryuchkova and Derengovskaya, 2000; Wong et al., 2003; Kissman et al., 2010).
Macrophytes and periphyton
Increased water transparency and light penetration caused by filtering activity of Dreissena allows submerged macrophytes and periphyton algae to grow deeper and, thus, cover larger portions of the bottom of a waterbody. This effect has a positive feedback as macrophyte beds can further be used by the mussels as a substrate for attachment (see Karatayev et al., 1997; 2002; 2005; Vanderploeg et al., 2002).
The impact of Dreissena on fish communities may be both positive and negative, as well as direct and indirect, depending on the feeding mode of the fish. The mussels can quickly become a major diet component of molluscivorous fish in recently invaded waterbodies. At least 38 fish species, including some well-known invaders, like round goby (Neogobius melanostomus), were field-documented to consume attached dreissenids. Many species also consume veligers of Dreissena, which can comprise over 70% of the zooplankton density in summer period (Molloy et al., 1997). Indirect positive impact of Dreissena on benthic feeding fish can result from an increased abundance of native benthic macroinvertebrates associated with the mussels’ aggregations (see Karatayev et al., 1997; 2002; and also section “Biology and Ecology: Associations”). Indirect negative impacts on planktivorous fish may result from decreased density and biomass of zooplankton organisms in Dreissena-invaded waterbodies.
Parasites and commensals
D. rostriformis bugensis serve as a host to about 20 taxa of parasites and commensals, including ciliates, trematodes, nematodes, oligochaetes, chironomids and mites (see section “Biology and Ecology: Associations”). Among these are helminths whose adult stages parasitize in fish (the trematode Bucephalus polymorphus) and waterfowl (the trematodes of the family Echinostomatidae) (Chernogorenko and Boshko, 1992; Yurishinets, 1999). Therefore, invasion by D. rostriformis bugensis may, at least theoretically, lead to worsening of the parasitological situation in a waterbody.
Negative impacts on native biodiversity
Although most studies conducted in Europe and North America demonstrated positive effects of dreissenid mussels on native benthic species (e.g. amphipods, isopods, leeches, turbellarians, hydrozoans, oligochaetes and chironomids), some natives are negatively affected. The unionid mussels are of special concern in this respect (Schloesser and Nalepa, 1994; Karatayev et al., 1997; Schloesser et al., 1998; Ricciardi et al., 1998; Burlakova et al., 2000). When attached to the shells of unionids, dreissenid mussels impede their burrowing and moving through the sediments. Extra weight of the unionids can also result in their burial in soft sediments. More importantly, attached Dreissena prevent unionids from opening their valves for respiration, feeding and reproduction, and also prevent closing of the valves. The most severe mass mortalities of native unionids occur during the initial stages of colonisation of a waterbody, when dreissenid populations are rapidly growing. With time, however, this negative impact becomes weaker, making possible the co-existence of Dreissena and unionids (Karatayev et al., 1997; Burlakova et al., 2000).
Introduction and subsequent proliferation of D. rostriformis bugensis and D. polymorpha in the Laurentian Great Lakes have coincided with dramatic declines in density and biomass of the burrowing amphipods Diporeia hoyi, which had supplied about 20% of the fisheries energy budget in the region (Dermott and Munawar, 1993; Dermott, 2001; Lozano et al., 2001; Dermott et al., 2005; Nalepa et al., 2006). Reasons for the negative response of Diporeia to these mussels are not clear. One possible explanation is that dreissenids are outcompeting Diporeia for available algal food (Dermott and Munawar, 1993; Dermott, 2001; Lozano et al., 2001). Evidence suggests, however, that the reason is more complex because the amphipods have completely disappeared even from those localities where dreissenids are rare or absent and food is abundant (Nalepa et al., 2006). A recent study by Dermott et al. (2005) has demonstrated that feeding of Diporeia on pseudofaeces of D. rostriformis bugensis results in a significant mortality in the amphipods. The exact mechanism of low survival of Diporeia in this experiment is unknown but might be related to the nutritional quality of pseudofaeces or associated waste metabolites.
Threatened SpeciesTop of page
|Threatened Species||Conservation Status||Where Threatened||Mechanism||References||Notes|
|Actinonaias ligamentina (mucket)||No details No details||Canada; USA||Fouling||Schloesser et al., 1998|
|Amblema plicata (threeridge)||No details No details||Canada; USA||Fouling||Schloesser et al., 1998|
|Anodontoides ferussacianus (cylindrical papershell)||No details No details||Canada; USA||Fouling||Schloesser et al., 1998|
|Cyclonaias tuberculata (purple wartyback)||NT (IUCN red list: Near threatened) NT (IUCN red list: Near threatened)||Canada; USA||Schloesser et al., 1998|
|Diporeia||No details No details||Canada; USA||Competition - monopolizing resources; Poisoning||Dermott et al., 2005; Nalepa et al., 2006|
|Elliptio dilatata (spike)||No details No details||Canada; USA||Schloesser et al., 1998|
|Epioblasma torulosa rangiana (Northern riffleshell)||National list(s) National list(s); USA ESA listing as endangered species USA ESA listing as endangered species||Canada; USA||Fouling||Schloesser et al., 1998|
|Epioblasma triquetra (snuffbox)||USA ESA listing as endangered species USA ESA listing as endangered species||Canada; USA||Fouling||Schloesser et al., 1998|
|Fusconaia flava (Wabash pigtoe)||No details No details||Canada; USA||Fouling||Schloesser et al., 1998|
|Lampsilis ovata (pocketbook)||NT (IUCN red list: Near threatened) NT (IUCN red list: Near threatened)||Canada; USA||Fouling||Schloesser et al., 1998|
|Lampsilis siliquoidea (fatmucket)||No details No details||Canada; USA||Fouling||Schloesser et al., 1998|
|Lasmigona complanata (white heelsplitter)||No details No details||Canada; USA||Fouling||Schloesser et al., 1998|
|Lasmigona costata (fluted-shell)||No details No details||Canada; USA||Fouling||Schloesser et al., 1998|
|Leptodea fragilis (fragile papershell)||No details No details||Canada; USA||Fouling||Schloesser et al., 1998|
|Ligumia nasuta (Eastern pondmussel)||NT (IUCN red list: Near threatened) NT (IUCN red list: Near threatened)||Canada; USA||Fouling||Schloesser et al., 1998|
|Ligumia recta (black sandshell)||NT (IUCN red list: Near threatened) NT (IUCN red list: Near threatened)||Canada; USA||Fouling||Schloesser et al., 1998|
|Obliquaria reflexa (three-horn wartyback)||No details No details||Canada; USA||Fouling||Schloesser et al., 1998|
|Obovaria olivaria (hickorynut)||LC (IUCN red list: Least concern) LC (IUCN red list: Least concern)||Canada; USA||Fouling||Schloesser et al., 1998|
|Obovaria subrotunda (round hickorynut)||NT (IUCN red list: Near threatened) NT (IUCN red list: Near threatened)||Canada; USA||Fouling||Schloesser et al., 1998|
|Pleurobema cordatum (Ohio pigtoe)||NT (IUCN red list: Near threatened) NT (IUCN red list: Near threatened)||Canada; USA||Fouling||Schloesser et al., 1998|
|Potamilus alatus (pink heelsplitter)||LC (IUCN red list: Least concern) LC (IUCN red list: Least concern)||Canada; USA||Fouling||Schloesser et al., 1998|
|Ptychobranchus fasciolaris (kidneyshell)||LC (IUCN red list: Least concern) LC (IUCN red list: Least concern)||Canada; USA||Fouling||Schloesser et al., 1998|
|Pyganodon grandis (giant floater)||No details No details||Canada; USA||Fouling||Schloesser et al., 1998|
|Quadrula quadrula (mapleleaf)||LC (IUCN red list: Least concern) LC (IUCN red list: Least concern)||Canada; USA||Fouling||Schloesser et al., 1998|
|Strophitus undulatus (creeper)||No details No details||Canada; USA||Fouling||Schloesser et al., 1998|
|Truncilla donaciformis (fawnsfoot)||No details No details||Canada; USA||Fouling||Schloesser et al., 1998|
|Truncilla truncata (deertoe)||No details No details||Canada; USA||Fouling||Schloesser et al., 1998|
|Villosa fabalis (rayed bean)||EN (IUCN red list: Endangered) EN (IUCN red list: Endangered); National list(s) National list(s); USA ESA listing as endangered species USA ESA listing as endangered species||Canada; USA||Fouling||Schloesser et al., 1998|
|Villosa iris (rainbow)||No details No details||Canada; USA||Fouling||Schloesser et al., 1998|
Social ImpactTop of page
D. rostriformis bugensis can negatively affect recreational activities of humans in different ways. In recreational boats, for instance, they can attach to the water intake slots of coolant pipes, leading to damage of the engine from overheating. Hulls’ fouling can increase fuel consumption because of greater drag (Minchin et al., 2002).
Risk and Impact FactorsTop of page Invasiveness
- Proved invasive outside its native range
- Highly adaptable to different environments
- Tolerates, or benefits from, cultivation, browsing pressure, mutilation, fire etc
- Capable of securing and ingesting a wide range of food
- Fast growing
- Has high reproductive potential
- Has high genetic variability
- Altered trophic level
- Damaged ecosystem services
- Ecosystem change/ habitat alteration
- Increases vulnerability to invasions
- Infrastructure damage
- Modification of hydrology
- Modification of natural benthic communities
- Modification of nutrient regime
- Negatively impacts human health
- Negatively impacts tourism
- Reduced amenity values
- Threat to/ loss of endangered species
- Threat to/ loss of native species
- Transportation disruption
- Competition - monopolizing resources
- Pest and disease transmission
- Interaction with other invasive species
- Rapid growth
- Highly likely to be transported internationally accidentally
- Difficult to identify/detect as a commodity contaminant
- Difficult/costly to control
UsesTop of page
D. rostriformis bugensis do not possess any economic value and social benefits; however, its use as a biomonitor of metal contamination has been investigated by Johns (2011).
Uses ListTop of page
- Pollution indicator
DiagnosisTop of page
Several genetic markers based on the COI gene and mitochondrial 16S and 28S ribosomal DNA restriction fragments have been developed to identify D. rostriformis bugensis at either of its life cycle stages (Baldwin et al., 1996; Claxton et al., 1997; Stepien et al., 1999; Therriault et al., 2004). These markers can be successfully used to reveal attached D. rostriformis bugensis in mixed populations of morphologically similar molluscs, as well as in plankton samples during the early period of colonisation, when attached individuals are not yet present on hard substrates in a waterbody.
Detection and InspectionTop of page
Individuals of D. rostriformis bugensis can relatively easily be identified in the field using the descriptions provided by May and Marsden (1992), Pathy and Mackie (1993) and Domm et al. (1993). Larvae of D. rostriformis bugensis can be collected using plankton nets. The larvae are much more difficult to identify because of their microscopic size and similarity to those of other species, e.g., D. polymorpha, Corbicula fluminea and Mytilopsis leucophaeata. However, Nichols and Black (1994) provide a valuable key for identification of the larval forms of D. rostriformis bugensis.
Similarities to Other Species/ConditionsTop of page
Among several extant dreissenid species, only two, i.e. Dreissena polymorpha and D. rostriformis bugensis have expanded their ranges far outside their native Ponto-Caspian region. Being rather similar in morphology, these two species can easily be confused when surveying invaded waterbodies. In a discovery in the Laurentian Great Lakes in 1989 (Mills et al., 1996), D. rostriformis bugensis was considered to be D. polymorpha until a genetic study by May and Marsden (1992) showed that North American waters were invaded by one more dreissenid species. Rosenberg and Ludyanskiy (1994) reviewed the systematic literature on Dreissena and examined the type material from Russia, and found that D. rostriformis bugensis from the Great Lakes correspond to D. bugensis sensu stricto. Another dreissenid species with which D. rostriformis bugensis are likely to be confused with is the dark false mussel, Mytilopsis leucophaeata, a mollusc that is native to brackish and fresh waters of North America (Pathy and Mackie, 1993).
Prevention and ControlTop of page
A special issue of the journal Aquatic Invasions has been devoted to 'Quagga mussels in the western United States' which includes papers on the management of quagga mussel, see guest editorial by Wong and Gerstenberger (2011).
Early warning systems
Open-access internet databases and thematic websites prove to be the most effective early warning systems concerning invasive species (Panov et al., 2004). This is especially true for the databases that include maps of the regional distributions of alien species. Such maps allow scientists and managers to monitor the ongoing spread of a species and predict what regions are at the greatest risk of invasion in the near future. The following sites provide particularly detailed information on distribution of D. rostriformis bugensis within its current range:
- US Geological Survey Nonindigenous Aquatic Invasive Species Database (http://nas.er.usgs.gov)
- DAISIE Database on Alien Species in Europe (http://europe-aliens.org/)
Following the first discovery of quagga mussel in the UK in 2014, the GB Non-Native Species Secretariat issued an alert (NNSS, 2014) and the Environment Agency contacted water users in the locality. Biosecurity measures to check, clean and dry equipment and vessels in the area are being used to prevent spread and the extent of occurrence is being monitored. A website has been set up to report sightings (NNSS, 2014).
Invasion of D. rostriformis bugensis into North American waterbodies has resulted in significant ecological impacts (Vanderploeg et al., 2002) and huge expense (Pimentel et al., 2005). Many natural resources agencies are thus conducting public education programmes that give practical guidance on how to help prevent the further spread of the mussels. These programmes include publication of leaflets and booklets, talks given to target audience such as recreational boaters and sport fishers, presentations to the mass media, etc. Similar informational campaigns in Europe are not so well established, probably due to the lessened impact by Dreissena in European waterbodies.
There are no ecologically-sound, wide-scale measures for eradication of D. rostriformis bugensis within waterbodies.
As D. rostriformis bugensis has a planktonic larval stage, which theoretically can be carried with water currents to any part of a waterbody, the containment or zoning of this species is virtually impossible.
Hickey (2010) provides an overview of the quagga mussel crisis that took place in Lake Mead National Recreation Area in Nevada, USA, in 2007, and the steps that were taken to control the species.
Dreissena often form thick encrustations on man-made structures or within raw water systems, negatively affecting their operation and efficiency. There are various methods of physical/mechanical control of these mussels, including scrapping, scrubbing, pigging, high-pressure water jetting, heated water treatment, etc. (ZMIS, 2002). Hot water sprays are also suggested by Comeau et al. (2011) - a spray temperature of 60ºC for 5 sec is recommended for mitigating fouling. Low-voltage AC currents have also been investigated as a potential means for preventing settlement and attachment by D. bugensis using steel rods and plates with the current running through them. Complete prevention of settlement near the intake of a pulp and paper plant was achieved using this method (Fears and Mackie, 1995).
In recent trials with the bacteria Pseudomonas fluorescens strain CL0145A, Molloy et al. (2004) achieved >90% adult Dreissena kill. The mussels (both D. rostriformis bugensis and D. polymorpha) were found to die from intoxication due to a natural product present within bacterial cells. In a separate study of the P. fluorescens CL0145A toxicity, neither native North American unionid mussels (Molloy, 1998) nor several other not-target species demonstrated any mortality (Daniel P Molloy, New York State Museum, personal communication, 2008). The method applying this bacterial strain for Dreissena control has been patented and currently is being developed for commercialization. It was also reported that high-density (0.42 fish/m3 or 1.90 fish/m2) redear sunfish (Lepomis microlophus) in an infested lake enclosure removed adult D. rostriformis bugensis efficiently and appeared to suppress their growth and recruitment. Redear sunfish is a species native to the southeastern USA that has become a popular, stocked sportfish in the southwest (Wong et al., 2013).
The main control technologies for Dreissena macrofouling focus on molluscicides such as chlorine, bromine, ozone, aromatic hydrocarbon compounds, and quaternary ammonium compounds. Although many chemical treatments have been tested (Waller et al., 1993; Claudi and Mackie, 1994; EPRI 1993; McMahon et al., 1994; Wright and Magee, 1997), chlorination is most widely used. The main advantage of using chemical treatments is that they can be engineered to protect almost the entire facility (Claudi and Mackie, 1994). However, toxic materials have to be discharged back to the environment, where they cause serious negative impacts on numerous non-target species. Therefore, new methods for targeted removal and control of D. rostriformis bugensisare under continuous investigation.
No integrated pest management programmes for D. rostriformis bugensis have been developed so far.
Monitoring and Surveillance
Monitoring is extremely important not only for initial detection of Dreissena but also for gathering additional information such as the life cycle stage that invading mussels are in, their abundance, and the effectiveness of implemented control. Therefore, an effectively run monitoring programme may be of great value for developing economically-effective control strategies (ZMIS, 2002).
There are two categories of Dreissena monitoring strategies (ZMIS, 2002):
Initial inspection: intended to determine if infestation is currently exist, where the mussels are located, and if the population densities require control measures. The focus of this strategy is to examine large volumes of water for planktonic mussel larvae and/or to inspect large surface areas for attached mussels.
Long-term monitoring programmes: including long-term records of spawning, settlement times and rates, and growth rates. Such record keeping can provide reliable information for the future on: 1) time of initial detection of the mussels in any of their life cycle stages; 2) seasonal/annual patterns of settling/colonisation, and 3) planning and evaluating control activities.
Detailed descriptions of the methods used in both strategies of monitoring can be found in the Zebra Mussel Information System (ZMIS, 2002).
Dewatering of infested structures to expose Dreissena to lethal levels of desiccation is one of the most readily applied, efficacious and environmentally neutral mitigation strategies. This approach is especially effective in the case of raw water systems such as navigation locks and water intake structures that are designed to be periodically dewatered for maintenance (Claudi and Mackie, 1994; Ussery and McMahon, 1995).
Gaps in Knowledge/Research NeedsTop of page
D. rostriformis bugensis began to spread outside its native range only in the first half of the twentieth century, and thus has attracted disproportionately less attention from researchers than its congener species, D. polymorpha. This explains the existence of several significant gaps and uncertainties in our current knowledge of biology and ecology of the D. rostriformis bugensis, including:
- reasons for slower geographical spread when compared with D. polymorpha;
- environmental requirements, especially in relation to temperature, oxygen, pH, turbidity, mineralization, and depth;
- physiology, especially rates of filtration, respiration, and excretion of nutrients under different environmental conditions;
- natural enemies;
- reasons for displacement of D. polymorpha in co-invaded waterbodies;
- reasons for decline of populations of the burrowing amphipods Diporeia spp. in North American waterbodies where D. rostriformis bugensis is present.
ReferencesTop of page
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ContributorsTop of page
09/06/14 Updated by:
David Wong, SUNY Oneonta, USA
27/03/08 Original text by:
Sergey Mastitsky, Belarusian State University, Biology Faculty, General Ecology Dept., Nezalezhnasti 4 ave., 220030 Minsk, Belarus.
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