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Contrasting rates of spread of two congeners, Dreissena polymorpha and Dreissena rostriformis bugensis, at different spatial scales.

ABSTRACT Examining congeners can help identify critical differences between species that affect invasion and spread. We examined Dreissena polymorpha (zebra mussel) and Dreissena rostriformis hugensis (quagga mussel), which are important invaders in freshwater and share general ecological characteristics, to determine whether they had similar rates of invasion at different spatial scales (global, regional, local, and individual water bodies) from the time of first introduction to the present. We also contrasted differences in ecological and population characteristics that could influence speed of spread. Although D. polymorpha and D. r. bugensis are relatives and share a common native habitat, morphology, lifestyle, life history, and dispersal potential, D. polymorpha was found to be a better invader than D. r. bugensis at most spatial scales throughout their invasion history. Spread at the regional scale in North America was the same for both species, but the initial rate of invasion by zebra mussels far outpaced the spread of quagga mussels both in the United States and in Europe. The estimated lag time between initial introduction and maximal population size is 5 times shorter for D. polymorpha than for D. r. bugensis, which may be an important factor affecting the speed with which this species can spread. Differences in population dynamics may facilitate the increased rates of spread of D. polymorpha relative to D. r. bugensis, especially at smaller spatial scales.

KEY WORDS: aquatic invaders, spread at different spatial scales, Dreissena polvmorpha. Dreissena rostriformis bugensis, population dynamics, rate of spread


During the past 50 years, since Elton (1958) first drew attention to the issue, we have seen an exponential increase in the number of introduced species, many of which are affecting biodiversity and natural ecosystems function, and are responsible for millions of dollars of impact on global economies (e.g., Pimentel et al. 2005, Keller et al. 2007). We know that the process of invasion operates at different spatial scales, from initial introductions facilitated by human activity to entirely new regions (e.g., new continents or seas), to secondary spread from those initial sites of introduction across regions, to local spread among all suitable habitats. Mechanisms that facilitate (or inhibit) invasion are likely to operate differently at different spatial scales, and the traits of organisms that make them effective invaders may be different at different spatial scales (Karatayev et al. 2007).

At present, we do not know whether there are generalizations among taxa regarding the features that enhance (or retard) invasion rates and secondary spread at different spatial scales, or whether such features are correlated. Contrasting congeners, when one species is an invader and another is not, has been used as a tool to identify characteristics within taxa that may facilitate invasion (e.g., Kolar & Lodge 2001, Devin & Beise1 2007). However, many invaders are related to a variety of species with different characteristics, making it difficult to select an appropriate "control," and a selected -control" species may become an invader in the future if environmental conditions and/or new vectors and mechanisms of spread become available. In addition, there can be differences among species in the vectors responsible for their spread that can confound comparisons. Contrasting 2 known invaders in the same systems that have similar life histories and vectors responsible for their spread, but with different patterns of invasion, especially at different spatial scales, may provide a more powerful comparison.

Dreissena polymorpha (Pallas, 1771), the zebra mussel, and Dreissena rostriformis bugensis (Andrusov, 1897), the quagga mussel, are both important invaders in freshwater systems, cooccur in their native habitat, and have very different histories of invasion. Although both species of Dreissena were introduced to North America at about the same time, during the mid-1980s (Mills et al. 1996, Carlton 2008), D. polymorpha is widely recognized as one of the most widespread invaders in freshwater throughout the northern hemisphere. D. r. bugensis has gained attention because of its recent rapid spread to western North America and to new regions of Europe. It has also been recently reported that in water bodies where they co-occur, D. r. bugensis displaces D. polymorpha (reviewed in Mills et al. 1996, Orlova et al. 2004, Orlova et al. 2005, Nalepa et al. 200%, Nalepa et al. 2009b, Zhulidov et al. 2010). Because of their importance as invaders, there are very good records of the spread of both of these species since their first introduction across Europe and in North America. In particular, in North America we have excellent data of first records of introduction and secondary spread at all spatial scales, including individual water bodies (Benson & Raikow 2009, Benson et al. 2009).

The main objective of this study was to use long-term data from North America and Europe to test whether the rates of spread of D. polymorpha and D. r. bugensis were different at different spatial scales.


We used published data on the year of first report of invasion of D. polymorpha and D. i". bugensis at different spatial scales to determine rates of spread. Because reporting of new introductions is often by political rather than geographical units (Karatayev et al. 2007), we used a combination of political units and geographical features to determine different spatial scales. For North America, we used the year of the first report of invasion within states or provinces for the largest spatial scale in other words, invasion across regions within a continent (Benson & Raikow 2009, Benson et al. 2009). For the regional spatial scale in Europe, we used the reports of first occurrence from a variety of sources (Appendix 1 ). Because of the nature of reporting, within Europe the first records were from individual countries or from major geographical regions within countries, especially in large countries (such as Russia or France). In all cases, only first occurrences were considered for invasion, not multiple sightings within one region. We analyzed these data for North America and Europe together (global spread), as well as for the United States alone.

Excellent data are available for the year of invasion of counties within states as well as for individual lakes, reservoirs, and rivers within the United States (Benson 8,: Raikow 2009, Benson et al. 2009), but, unfortunately, no comparable data exist for Europe. Therefore, at smaller spatial scales we were only able to examine data for spread in the United States.

We used the first report of D. polymorpha and D. r. bugensis" through time to assess the speed of invasion at each spatial scale. The invasion speed was calculated as the slope, of the cumulative number of invasions through time. We plotted cumulative invasion curves for each spatial scale for each dreissenid species, which were fitted with linear regressions to compare the speed of invasion by testing the difference among slopes. Although some parts of several cumulative curves were not linear (e.g., were curvilinear or exponential, indicating an acceleration in spread through time), they were sufficiently approximated with linear regressions (P < 0.05, F test) for comparison of slopes. When this was not the case, the data were log-transformed to achieve linearity. To test for differences in the speed of spread among time periods, we compared the first half and second half of the time period, or we looked for natural breaks in the slope, to divide the data into groups. Multiple comparisons of the slopes were performed according to Zar (1996) with a method that is analogous to ANOVA, and a post hoc Tukey test for multiple comparisons on pairwise combinations of slopes. Such post hoc tests take into account multiple testing, thus P values do not need to be adjusted for multiple testing. Student's t-test was used in cases when regression elevations (differences in line intercepts) were compared (Zar 1996). Unless otherwise stated, statistical hypotheses were rejected at P < 0.05.

To test whether species/population-level traits that differ between zebra and quagga mussels could affect their relative abilities as invaders, we examined the lag time between when zebra and quagga mussels were first introduced to a water body and when their populations were abundant. We used published information on the number of years from first detection until maximum density in introduced water bodies. We also compared the relative abundance of these two species in different types of water bodies where they co-occur. We compared populations of these species in lakes and reservoirs with and without large profundal zones with those found in rivers and canals.


Global Spread

We found a significant overall difference in the speed of spread within Europe and North America for both species through time (F (4, 267) = 369.3, P << 0.001: Table 1). During the 19th century, D. polymorpha spread across regions of Europe at an exponential rate (97.8% of variance explained by an exponential model) for ~70 y (1800 to 1867; Fig. 1). Spread essentially stopped at the time of the Industrial Revolution and increased pollution of the freshwaters of Europe (1868 to 1987 (Kinzelbach 1992): Fig. l). During the second half of the 20th century (1988 to 2008), a second period of exponential spread occurred (79.7% of variance explained) both within Europe and North America. The linear portion of this second period of spread (slope, 1.16) was significantly faster than that during the 19th century (slope, 0.35), and also significantly faster than during the first half of the 20th century (slope, 0.05: P < 0.001 for both pairs, Tukey tests: Table 1).

In contrast, D. r. bugensis remained restricted to its native range until the first half of the 20th century. Since the 1940s, D. r. bugensis spread throughout the Dnieper River and colonized newly constructed reservoirs (Zhuravel 1965, Orlova et al. 2005, Zhulidov et al. 2010). Initial spread from the 1940s to the 1980s was slow across Europe, and then increased exponentially in Europe and in North America, where it was introduced in the mid-1980s (Fig. 1: see also Mills et al 1996). The global spread of quagga mussels after the mid-1980s (slope, 0.84) was significantly faster than its prior rate of spread (slope, 0.02: P << 0.001. Tukey test). The recent rate of global spread of quagga mussels in North America and Europe combined from the mid-1990s to 2008 (slope, 0.84) was faster than that of zebra mussels during the 19th century in Europe (slope, 0.35: P < 0.001, Tukey test), and not significantly different than the recent rate of spread of zebra mussels in North America and Europe combined (slope, 1.07: P > 0.20, Tukey test: Table 1).


Spread at Different Spatial Scales in the United States

We compared the rates of spread of D. polymorpha and D. r. bugensis at regional (states), local (counties), and water body scales for just the United States (Fig. 2).

Regional Scale

Although both dreissenid species were introduced into North America at about the same time (Mills et al. 1996, Carlton 2008), by 2008 D. polymorpha had colonized more than twice as many states (25) as D. r. bugensis (12), almost 8 times more counties (443 vs. 59), and more than 15 times more water bodies than D. r. bugensis (673 vs. 44).

To determine whether the overall rate of spread of zebra mussels differed from that of quagga mussels, we log-transformed the data. We found no significant difference in the overall rate of spread for these two species (D. polymorpha 1988 to 2008, slope, 0.578; D. r. bugensis 1991 to 2008, slope, 0.576; P > 0.50, Tukey test). We did find a significant difference between the elevations (intercepts) of the regression lines, indicating that there was an initial rapid spread of zebra mussels to many states (elevation: D. polymorpha, 0.69; D. r. bugensis, 0.26; P < 0.001, t-test), but that subsequent spread of these two species was similar.

Overall, we found significant differences in the rates of regional spread for different time periods for each of these two species (F (3, 31) : 11.45, P < 0.001). D. polymorpha spread exponentially in the United States (95.8% of variance explained) after its initial introduction into North America (1988 to 1998), invading 20 states in 10 y. The following 10 y (1999 to 2008), the rate of regional spread of this species slowed, and only 5 additional states were colonized (slope, 0.41 vs. 1.96; P < 0.001, Tukey test). In contrast, during the first years after initial detection (1991 to 1997), D. r. bugensis spread to only 5 states (slope, 0.64), an invasion rate much slower than that of D. polymorpha (slope, 1.96; P < 0.025, Tukey test). The following 10 y (1999 to 2008), quagga mussels spread to an additional 7 states (Wisconsin, Indiana, Illinois, Arizona, California, Nevada, and Colorado; slope, 0.66), a rate of spread not significantly different than the previous period (P > 0.50, Tukey test; Fig. 2).


We examined whether the rate of spread of zebra mussels differed before and after 1993 (an apparent natural break in the data), and whether there were differences in the rate of spread of quagga mussels during that same time period. Overall, we found a significant difference among the rates of spread for these 2 species for each time period (F (3, 31) = 30.0, P << 0.001). The initial rate of spread of zebra mussels from 1988 to 1993 was far more rapid (slope, 3.31) than for 1994 to 2008 (slope, 0.35; P < 0.001, Tukey test). Because of the low number of observations from 1991 to 1993, the rate of spread for this early time period for quagga mussels could not be compared. Spread of quagga mussels from 1994 to 2008 (slope, 0.51) was not different from that of zebra mussels over the same time period (P> 0.10, Tukey test), but was much slower than the initial spread of zebra mussels (P << 0.001, Tukey test; Table 1).

Local Scale

At the local scale, the spread to new counties within states for D. polymort)ha was at a faster rate (log-transformed slope, 1.43) than for D. r. bugensis (log-transformed slope, 0.71; P < 0.001, Tukey test) from 1988 to 2008. There was also a statistically significant difference between elevations (D. polymorpha 3.12 vs. D. 7". bugensis 2.58; P < 0.001, t-test).

We found an overall significant difference in the rates of local spread for each species across different time periods (F (3, 31) = 111.4, P << 0.001). The initial rate of spread of D. polymorpha from 1988 to 1997 (slope, 36.31) was significantly faster than from 1998 to 2008 (slope, 13.79: P < 0.001, Tukey test). For D. r. bugensis, the rate of spread was not different from when it was first detected (1991) through 1997 (slope, 2.39) and more recently, from 1998 to 2008 (slope, 3.72; P > 0.100, Tukey test). For both time periods, the local spread of zebra mussels was much faster than that for quagga mussels (P < 0.001 in all cases, Tukey tests: Table 1).

Water Body Scale

At the smallest spatial scale (individual water bodies), zebra mussels spread at a faster rate from 1988 to 2008 than quagga mussels (log-transformed slopes, D. polymorpha 1.91 vs. D. 7". bugensis 1.35; P < 0.001, Tukey test). In this case, there was no significant difference between elevations (D. polymorpha 1.41 vs. D. r. bugensis 2.25: P 0.199, t-test).

The rate of invasion of water bodies for these two species also differed (F (3, 31) = 163.2, P << 0.001). The early spread of zebra mussels, from 1988 to 1997 (slope, 24.40), was slower than subsequent spread from 1998 to 2008 (slope, 38.78; P < 0.001, Tukey test). A similar escalation in the rate of spread has not been seen in quagga mussels; the rate of spread from 1991 to 1997 (slope, 1.25) was not different than the spread from 1998 to 2008 (slope, 2.28; P> 0.50, Tukey test). For all time periods, the rate of spread of zebra mussels was substantially faster than that of quagga mussels (P << 0.001 in all cases, Tukey tests; Table 1).

For states that have been invaded by zebra (27 states) or quagga (15 states) mussels, we tested whether the total area of a state was correlated with the number of counties or the number of lakes invaded. Similarly, we tested whether the number of counties invaded within a state was correlated with the number of water bodies invaded for both species.

For zebra mussels, there was no correlation between state area and the number of counties invaded (Spearman r = 0.277, P > 0.05), or the number of water bodies invaded (Spearman r = 0.268, P > 0.05). Within states, there was a significant correlation between the number of counties invaded and the number of water bodies invaded by zebra mussels (Spearman r = 0.889, P < 0.05).

For quagga mussels, larger states had more counties invaded than smaller states (Spearman r = 0.681, P < 0.05). This pattern is largely driven by western states, which are large and have recently been invaded by quagga mussels. However, there was no correlation between the area of a state and the number of water bodies invaded (Spearman r = 0.214, P > 0.05) or the number of counties within a state that were colonized and the number of water bodies colonized (Spearman r = 0.506, P > 0.05).

Population Lag Time

We found that the time lag between when each species was first detected in a water body (Table 1) and when it reached its maximum population density was much shorter for D. polymorpha than for D. r. bugensis (P < 0.001, Mann-Whitney test; Table 2). The variance among water bodies was surprisingly low. For zebra mussels, this lag time was 1-4 y, with an average of 2.5 [+ or -] 0.2 y (SE; n = 13). For quagga mussels, the lag time was longer, and ranged from 6-19 y, with an average of 12.2 [+ or -] 1.5 y (n=9).


Within their native range in the Dnieper River Delta and Dnieper-Bug Liman, Ukraine, which has no profundal zone, the 2 species have been dominant in different areas of water bodies or in different years in the same water body (Table 3). There are relatively few data for lakes where both species of dreissenid have invaded. We found that for three invaded lakes with no or a small profundal zone, zebra mussels dominate or both species remain abundant, even after 20 y of coexistence (Table 3). However, for 6 lakes and reservoirs with large profundal zones, D. r. bugensis was dominant after 9 y or more of coexistence. In 3 rivers and canals, D. polymorpha generally dominates, especially in shallow areas (Table 3).


Although D. polymorpha and D. r. bugensis are closely related and share a native habitat, a common morphology, lifestyle, and life history; use similar vectors for transport; have similar dispersal potential; and have both become important invaders of freshwater throughout the northern hemisphere, D. polymorpha has spread at a faster rate than D. r. bugensis at most spatial scales throughout their invasion history (Table 1). The only exception is the overall rate of spread at the regional scale since their introduction to North America, which was not significantly different for these two species. However, even at this spatial scale, D. polymorpha had an initial spread that was very rapid, followed by a period of slower spread (probably because there were fewer sites available for invasion). Meanwhile, D. r. bugesis appears to have had a slow and steady rate of spread at the regional scale. Even at this large scale, the rate of invasion by zebra mussels initially far outpaced the spread of quagga mussels both in the United States and in Europe.

Within the United States, D. polymorpha initially spread across regions at an exponential rate, and then slowed with the saturation of nearby regions after 1993 (Fig. 2). After zebra mussels had spread throughout North America's Great Lakes and its large-scale spread to new states slowed (as nearby states were all invaded), quagga mussels began to increase in abundance in the shallow portions of lakes Ontario and Erie, and more recently in Lake Michigan. By 1995, 37% of the dreissenids in the shallow portions of Lake Ontario were quagga mussels; this proportion increased to 59% by 1998, 93% by 1999, and 99% by 2003 (Watkins et al. 2007). In 2008, there was an abundance of D. r. bugensis in 200 benthic samples from Lake Ontario, but no D. polymorpha were found (Dr. Christopher Pennuto, pers. comm.). Similar changes in dominance were seen in Lake Erie (Dermott & Dow 2008), especially in the central and eastern basins, which are deep (Patterson et al. 2005, A. Karatayev et al., unpublished data). Quagga mussels represented 44% of all dreissenids in Lake Erie by 1993 (Dermott & Dow 2008), and 97% of the dreissenids across the whole lake by 2002 (Patterson et al. 2005). Only in the shallow western basin of Lake Erie have zebra mussels remained abundant. In June 2009, although the western basin was dominated by D. r. bugensis, 12% of all dreissenids sampled were D. polymorpha (A. Karatayev et al., unpublished data). In Lake Michigan, zebra mussels were more abundant than quagga mussels until 2002: however, since 2004, quagga mussels have greatly increased in density and biomass, and are now dominant (Nalepa et al. 2010).

Although zebra mussels can spread downstream via connected waterways through larval dispersal (Schneider et al. 2003), recreational boats are the primary vector for the spread of dreissenids among regions and water bodies in the United States (Padilla et al. 1996, Buchan & Padilla 1999, Johnson et al. 2001, Bossenbroek et al. 2007). In the United States, patterns of spread of zebra mussels across the landscape are best described by the movement of recreational boaters, rather than by the reaction-diffusion spread that is seen in some other types of invaders (Padilla et al. 1996, Buchan & Padilla 1999). With the increase in the abundance of quagga mussels in shallow areas, boaters are currently more likely to be transporting D. r. bugensis than zebra mussels from source populations, primarily the Great Lakes. The long-distance "trailering" of boats is likely responsible for the recent rapid spread of D. r. bugensis and its new introductions into the western United States (Brown & Stepien 2010). There was no correlation between the area of a state and the number of counties or water bodies invaded by zebra mussels. For quagga mussels, larger states had more counties invaded than smaller states, but this pattern is largely driven by recently invaded western states, which are large. The lack of a correlation between the number of counties within a state that were colonized and the number of water bodies colonized for quagga mussels, but a significant correlation for zebra mussels, likely indicates that the zebra mussel has had greater local spread than quagga mussels, and is more likely to have saturated its spread in some areas. It will be interesting to see whether this pattern changes for the quagga mussel as its invasion progresses.

Many invaders show long lag times between initial introduction and large population size (Williamson 1996, Crooks & Soule 1999, Kiritani & Yamamura 2003). This lag time may range from less than 1 y to decades, depending on the population dynamics of the species and habitats they invade (Kiritani & Yamamura 2003, Simberloff & Gibbons 2004, Daehler 2009). The population lag time for quagga mussels was almost 5 times longer than that of zebra mussels. The longer lag time between initial introduction and large population sizes for D. r. bugensis may indicate that quagga mussels are more vulnerable to Allee effects (Schreiber & Lloyd-Smith 2009). Thus, once introduced, they may be less likely to establish, especially in water bodies where zebra mussels have already invaded and in lakes without a large profundal zone.

The shorter lag time for zebra mussels may be the key to their invasion success. The ability of zebra mussels to capitalize rapidly on secondary spread is likely responsible for the escalating rates of spread at the local and water body scales. It is unclear whether the rate of D. r. bugensis spread at these smaller spatial scales will change. However, as more lakes are invaded by quagga mussels it is likely that secondary spread will become more important, allowing quagga mussels to have an increased rate of spread at all spatial scales.

Differences in the rates of spread at different spatial scales and population dynamics of zebra and quagga mussels may reflect their evolutionary histories and performance under different environmental conditions. Both species co-occur and are codominant in their native range in the Dnieper River Delta and Dnieper-Bug Liman (Markovskiy 1954. Moroz & Aleksenko 1983, Zhulidov et al. 2010). This pattern of codominance may reflect different advantages of each species under different environmental conditions. More than 130 species of dreissenids were found in the ancient Pannon basin in Central Europe during the Miocene and Pliocene epochs. Historically, dreissenids occupied all types of water bodies and all types of bottom substrates. They were common from shallow littoral zones to silty profundal zones in lakes (Geary et al. 2000). The vast majority of this diversity disappeared with the Pleistocene glaciation, leaving few remnants, including zebra and quagga mussels. Currently, there are several water bodies where zebra and quagga mussels coexist in their native range, as well as in water bodies they have invaded (Table 3). These 2 species appear to have different sensitivities to temperature, salinity, and low oxygen conditions. Zebra mussels tolerate warmer water and higher salinities than quagga mussels (reviewed in Karatayev et al. 1998). The zebra mussel also has a greater rate of byssal thread production and higher attachment strength (Peyer et al. 2009), which makes it well adapted to areas with higher water velocity and waves, and may facilitate its attachment to macrophytes and boats. Quagga mussels have a much higher tolerance to low oxygen concentrations than zebra mussels, and are able to live on finer sediments than zebra mussels, especially those found in the profundal zones of large lakes (Mills et al. 1996, Karatayev et al. 1998).

Although there was extensive ship traffic between the native region of both species of Dreissena and the rest of Europe, unlike zebra mussels, which rapidly spread across Europe, D. r. bugensis remained restricted to its native range for more than 150 y (Fig. 1). Similarly, in North America, although both species colonized the Great Lakes at the same time, there was a substantial delay in the spread of quagga mussels compared with zebra mussels at all spatial scales (Fig. 2). Why were the mechanisms and vectors of spread so successful for D. polymorpha, but less so for D. r. bugensis? During the 19th and early 20th centuries, the major mechanism for the spread of dreissenids across Europe was vessel hulls and rafts transported through the canals and rivers with adult mussels attached (Kinzelbach 1992). In North America, the most effective mechanism of overland spread of dreissenids has been recreational boats with attached mussels (Padilla et al. 1996, Buchan & Padilla 1999, Johnson et al. 2001). Differences in the strength of attachment (Peyer et al. 2009) as well as differences in the spatial distribution of these two species when they first invade (e.g., animals in the profundal zone are less likely to attach to boats) may have played an important role in the differences seen between the spread of these two species. In addition, initially shallow areas of rivers and canals were the habitats in Europe that were colonized by zebra mussels. These habitats may not be favorable for D. r. bugensis, which prefer quiet areas of deep lakes and reservoirs (Orlova et al. 2005). During the second half of the 20th century, the construction of large, deep reservoirs likely became stepping-stones for D. r. bugensis invasion (Orlova et al. 2005, Karatayev et al. 2007). in addition, the advent of new vectors of spread during the 20th century that were not available during the initial spread of zebra mussel spread in Europe during the 19th century, such as ballast water, combined with the increased rates of commercial and recreational boat traffic, including overland movement of pleasure boats, changed the potential for the spread of both species (Karatayev et al. 2007). Although zebra mussels win the race for invading new waters, quagga mussels, despite their slower rate of spread at decadal timescales, will likely become more important and conspicuous, especially in water bodies with a large profundal zone, in North America and elsewhere.

First reports of zebra mussels (Dreissena polymorpha) and quagga
mussels (Dreissena rostriformis bugensis) in water bodies in
various regions of Europe.

Year     Region                             References

                                D. polymorpha

1800s    Ukraine, Dnieper River             Starobogatov &
                                             Andreeva (1994)
1800s    Belarus                            Karatayev et al. (2003)
1803     Lithuania                          Schlesch (1937)
1824     Great Britain, London              Kerney & Morton (1970)
1825     Poland, Gdansk                     Kinzelbach 1992
1826     The Netherlands, Rotterdam         Kerney & Morton (1970)
1827     Germany, near Berlin               Kinzelbach (1992)
1830     Germany, Hamburg                   Kerney & Morton (1970)
1832     Czech Republic, Elbe River         Kinzelbach (1992)
1834     Great Britain, Scotland            Kinzelbach (1992)
1835     France, near Reims                 Kinzelbach (1992)
1835     Austria                            Kinzelbach (1992)
1840     Denmark, Copenhagen                Kerney & Morton (1970)
1848     Estonia                            Kinzelbach (1992)
1847     Russia, upper Volga River basin    Kinzelbach (1992)
1854     Sweden, near Malmo                 Kinzelbach (1992)
1855     Germany Wesser River               Kinzelbach (1992)
1855     France, Seine River, near Paris    Kinzelbach (1992)
1855     Latvia                             Kinzelbach (1992)
1858     Switzerland                        Kinzelbach (1992)
1861     Germany, ME, near Czech Republic   Kinzelbach (1992)
1863     France, Loire River                Kinzelbach (1992)
1864     Russia, near Sankt Petersburg      Kinzelbach (1992)
1865     France, near Nice                  Kinzelbach (1992)
1865     Germany, near Bremen               Kinzelbach (1992)
1866     France, Garonne River              Kinzelbach (1992)
1868     Poland, Order River, near          Kinzelbach (1992)
1930     Sweden, near Stockholm             Kinzelbach (1992)
1932     Hungary, Lake Balaton              Sebestyen (1937)
1962     Alpine region                      Kinzelbach (1992)
1965     Alpine region                      Kinzelbach (1992)
1971     Italy, Lake Garda                  Starobogatov & Andreeva
1993     Ireland                            Pollux et al. (2003)
2001     Spain                              Bij de Vaate et al.
                              D. r. bugensis

1941     Ukraine, Dnieper Reservoir         Zhuravel (1952)
1980     Russia, Don River                  Zhulidov et al. (2005)
1988     Ukraine, Dniester River            Shevtsova (2000)
1992     Russia, Volga River and Caspian    Antonov (1993)
2001     Russia, Moscow River               Lvova (2004)
2004     Romania, Danube River              Micu & Telembici (2004)
2005     Moldova, Dniester River            Son (2007)
2006     The Netherlands, Rhine River       Molloy et al. (2007)
2007     Germany, ME River                  Van der Velde &
                                             Platvoet (2007)


This study was supported in part by the U.S. EPA grant The Nearshore and Offshore Lake Erie Nutrient Study to C. Pennuto, A. Karatayev, A. Perez-Fuentetaja, L. Burlakova, G. Matisoff, J. Kramer, D. Bade, J. Conroy, and E. Marschall. We appreciate the assistance of the Captain and crew of the U.S. Environmental Protection Agency's R/V Lake Guardian and Marissa Hajduk (Buffalo State College) in collecting samples from Lake Erie. We thank Karen O'Quin, Associate Dean, and the Women in Science and Mathematics Series at Buffalo State College, which provided support for D. K. P. D. K. P. also acknowledges the Helen C. Whitely Center, at Friday Harbor Laboratories.


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(1) Great Lakes Center, Buffalo State College, 1300 Elmwood A venue, Buffalo, NY 14222," (2) The Research Foundation of The State University of New York, Buffalo State College, Office o['Sponsored Programs, 1300 Eh,wood A venue, Bishop Hall B17, Buffalo, NY 14222-1095,'- Department of Ecology and Evolutton, Stony Brook University, Stony Brook, N Y 11794-5245, (4) Cornell Biological Field Station, 900 Shackelton Point Road, Bridgeport, N Y 13030

* Corresponding author. E-mail:

DOI: 10.2983/035.030.0334
Summary of the relative rates of invasion of Dreissena
polymorpha and Dreissena rostriformis bugensis.

                 Overall Rate    Rate of Spread Among
Scale            of Spread       Time Periods

Europe and North America
  Global                         ([DP.sub.1988-2008] = [DB.sub.1980-
                                  2008] > [DP.sub.1800-1867 >
                                 [DP.sub.1868-1987] > [DB.sub.1941-

United States
  Regional       DP = DB         [DP.sub.E] > ([DB.sub.E] =
                                 [DB.sub.L]) > [DP.sub.L]

  Local          DP [much less   [DP.sub.E] [much less than] DPI
                 than] DB        [much less than] ([DB.sub.E] =

  Water body     DP [much less   [DP.sub.L] [much less than]
                 than] DB        [DP.sub.E] [much less than]
                                 ([DB.sub.E] = [DB.sub.L])

DB, Dreissena rostriformis bugensis: DP, Dreissena polymorpha; E, early
period of spread, 1988 to 1997 for DP and 1991 to 1997 for DB; L, late
period of spread, 1998 to 2008.

The number of years from first detection to maximum population
density of Dreissena polymorpha and Dreissena r. bugensis in
different water bodies.

                                                 Year with
                                       First      Maximum
Water Body                            Detected    Density

D. polymorpha
  Lake Balaton, Hungary                 1932       1934
  Kuybyshevskoe Reservoir, Russia       1956       1958
  Kamskoe Reservoir, Russia             1960       1962
  Lake Lukomskoe, Belarus               1972       1975
  Lake Naroch, Belarus                  1989       1993
  Long Point Bay, Lake Erie, US         1989       1992
  Lake Erie (lakewide), US              1989       1992
  Saginaw Bay, Lake Huron, US           1990       1992
  Hudson River, US                      1991       1992
  Seneca River, US                      1991       1993
  Oneida Lake, US                       1991       1992
  St. Lawrence River, Canada            1992     1994-1995
  Southern Lake Michigan, 16-30 m       1989       1993
  Average ([+ or -] SE) for D.
Dreissena r. bugensis
  Lake Ontario, US                      1990       2003
  Lake Eric, US                         1989       2002
  Southern Lake Michigan, 16-31 m       1997       2008
  Soulanges Canal, Canada               1990       2002
  Volga Delta, Russia                   1992       2000
  River Don, Russia (sites              1980       1999
   1, 6-8, 11)
  Manych River, Russia                  1980       1999
   (sites 12-15)
  Kuybyshev Reservoir, Russia           1992       2001
  Saratov Reservoir, Russia             1992       1998
  Average ([+ or -] SE) for D. r.

                                          Year with
Water Body                                 Density        Source

D. polymorpha
  Lake Balaton, Hungary                       2             1
  Kuybyshevskoe Reservoir, Russia             2             1
  Kamskoe Reservoir, Russia                   2             1
  Lake Lukomskoe, Belarus                     3             1
  Lake Naroch, Belarus                        4             1
  Long Point Bay, Lake Erie, US               3             1
  Lake Erie (lakewide), US                    3             2
  Saginaw Bay, Lake Huron, US                 2             1
  Hudson River, US                            2             I
  Seneca River, US                            2             1
  Oneida Lake, US                             l             1
  St. Lawrence River, Canada                 2-3            1
  Southern Lake Michigan, 16-30 m             4             3
  Average ([+ or -] SE) for D.         2.5 [+ or -] 0.2
Dreissena r. bugensis
  Lake Ontario, US                           13             4
  Lake Eric, US                              13             2
  Southern Lake Michigan, 16-31 m            11             3
  Soulanges Canal, Canada                    12             5
  Volga Delta, Russia                         8             6
  River Don, Russia (sites                   19             7
   1, 6-8, 11)
  Manych River, Russia                       19             7
   (sites 12-15)
  Kuybyshev Reservoir, Russia                 9             6
  Saratov Reservoir, Russia                   6             6
  Average ([+ or -] SE) for D. r.     12.2 [+ or -] 1.5

1, Reviewed in Burlakova et al. (2006); 2, Patterson et al.
(2005); 3, Nalepa et al. (2010); 4, Watkins et al. (2007); 5,
Ricciardi & Whoriskey (2004); 6,  Orlova et al. (2004); 7,
Zhulidov et al. (2006).

The relative abundance of Dreissena r. bugensis (quagga mussels)
within a water body and the number of years of coexistence with
Dreissena polymorpha (zebra mussels) for different types of water
bodies in Europe and North America.

                                            Years of      of Quagga
Water Body, Country, Year                  Coexistence     Mussels

Native range
  Dnieper-Bug Liman, Ukraine, 2006,                          22%
  Bug Liman, Radsad settlement,                              54%
   Ukraine, 2006
  Dnieper River, Kherson City,
   Ukraine, 2006:
    3 m in depth                                             95%
    1 m in depth                                             12%
  Verevchina River, Kherson City,                            68%
   Ukraine, average for 2001, 2006,
Lakes and reservoirs without large
profundal zone
  Kanevskoe Reservoir, Ukraine, 2001:
   <1.5 m                                      21        Not dominant
   >2 m                                        21          Dominant
  Dniester Liman, Ukraine, 1988                20        Not dominant
  Lake Erie, US, western basin, 2009           18            88%
Lakes and reservoirs with large
profundal zones
  Dneprovskoe Reservoir, Ukraine, 1965         24          Dominant
  Lake Ontario, US, 2008                       19            >99%
  Lake Erie, US, central basin, 2009           19            >99%
  Lake Erie, US, eastern basin, 2009           19            >99%
  Southern Lake Michigan, 16-30 m               9            >99%
  Kuybyshevskoe Reservoir, Russia, 2001         9          Dominant
Rivers and canals
  River Don, Russia (sites 1, 6-8, and         24            12%
   11), 2004
  Manych River, Russia (sites 12-15),          24            39%
  Soulanges Canal, Canada:
    2002, canalwide                            12            79%
    2003, surface of the canal wall            13            30%
    2003, bottom of the canal                  13            100%

Water Body, Country, Year                  Source

Native range
  Dnieper-Bug Liman. Ukraine, 2006,          1
  Bug Liman, Radsad settlement,              1
   Ukraine, 2006
  Dnieper River, Kherson City,
   Ukraine, 2006:
    3 m in depth                             1
    1 m in depth                             1
  Verevchina River, Kherson City,            I
   Ukraine, average for 2001, 2006,
Lakes and reservoirs without large
profundal zone
  Kanevskoe Reservoir, Ukraine, 2001:
   <1.5 m                                    2
   >2 m                                      2
  Dniester Liman, Ukraine, 1988              3
  Lake Erie, US, western basin, 2009         4
Lakes and reservoirs with large
profundal zones
  Dneprovskoe Reservoir, Ukraine, 1965       5
  Lake Ontario, US, 2008                     6
  Lake Erie, US, central basin, 2009         4
  Lake Erie, US, eastern basin, 2009         4
  Southern Lake Michigan, 16-30 m            7
  Kuybyshevskoe Reservoir, Russia, 2001      8
Rivers and canals
  River Don, Russia (sites 1, 6-8, and       9
   11), 2004
  Manych River, Russia (sites 12-15),        9
  Soulanges Canal, Canada:
    2002, canalwide                          10
    2003, surface of the canal wall          10
    2003, bottom of the canal                10

Except for the native range where the species coexisted for
thousands of years, zebra mussels were detected earlier than
quagga mussels. 1, Zhulidov et al. (2010); 2, Silaeva & Protasov
(2005); 3, Dr. Alexander Goncharov (pers. comm., 2008); 4, A.
Karatayev et al., unpublished data; 5, Zhuravel (1965); 6, Dr.
Christopher Pennuto (pers. comm., 2008); 7, Nalepa et al. (2010);
8, Orlova et al. (2004); 9, Zhulidov et al. (2006); 10, Ricciardi
& Whoriskey (2004).
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Author:Karatayev, Alexander Y.; Burlakova, Lyubov E.; Mastitsky, Sergey E.; Padilla, Dianna K.; Mills, Edwa
Publication:Journal of Shellfish Research
Article Type:Report
Geographic Code:100NA
Date:Dec 1, 2011
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