Limnoperna fortunei versus dreissena polymorpha: population densities and benthic community impacts of two invasive freshwater bivalves.
Invasive species (Research)
Invasive species (Environmental aspects)
Bivalvia (Environmental aspects)
Zebra mussels (Research)
Zebra mussels (Environmental aspects)
Karatayev, Alexander Y.
Burlakova, Lyubov E.
Karatayev, Vadim A.
|Publication:||Name: Journal of Shellfish Research Publisher: National Shellfisheries Association, Inc. Audience: Academic Format: Magazine/Journal Subject: Biological sciences; Zoology and wildlife conservation Copyright: COPYRIGHT 2010 National Shellfisheries Association, Inc. ISSN: 0730-8000|
|Issue:||Date: Dec, 2010 Source Volume: 29 Source Issue: 4|
|Topic:||Event Code: 310 Science & research|
|Geographic:||Geographic Scope: Argentina Geographic Code: 3ARGE Argentina|
ABSTRACT In this study, for the first time, using similar methods,
we compared the population density and distribution across different
substrate types of Limnoperna fortunei and Dreissena polymorpha, as well
as their impacts on the composition of benthic communities. Data on L.
fortunei were obtained in Rio Tercero Reservoir, Argentina, whereas
studies on D. polymorpha were conducted in North America and Europe. We
found that, similar to the zebra mussel, L. fortunei creates high
densities on hard substrates in the littoral zone, and avoids soft
substrates in the profundal zone; however, the overall population
density of L. fortunei in a water body seems to be higher than that of
zebra mussels. Additional studies on Limnoperna are needed to confirm
this hypothesis. The effect of L. fortunei on macrobenthos is very
similar to the effect of D. polymorpha and is associated with an
increase in the overall diversity, density, and biomass of native
macroinvertebrates in druses compared with bare sediments. The presence
of L. fortunei druses in the littoral zones of Rio Tercero has increased
the average species richness of native benthic invertebrates per sample
by almost 70% and their density and biomass by threefold, positively
affecting epifaunal organisms and negatively burrowing invertebrates and
unionids. In the near future, the freshwaters of North America may be
colonized by L. fortunei, resulting in strong impacts on entire invaded
ecosystems and devastating impacts on native unionids, especially in the
southern regions of the United States, which are not colonized with
KEY WORDS: invasive species, Limnoperna fortunei, zebra mussel, Dreissena polymorpha, distribution, density, impacts on zoobenthos
The strong ecological and economic impacts of the zebra mussel (Dreissena polymorpha (Pallas, 1771)), well documented both in Europe and in North America, make this mollusc the most aggressive freshwater invader in the northern hemisphere (reviewed in Karatayev et al. 1997, O'Neill 1997, Karatayev et al. 2002, Karatayev et al. 2007b). Much less information is available on the other invasive byssate bivalve, the golden mussel (Limnoperna fortunei Dunker, 1857). L. fortunei is a freshwater mytilid native to mainland China that was introduced into Hong Kong, Taiwan, and Japan between 1965 and 1990 (Morton 1975, Nakai 1995). In 1989 to 1990, L. fortunei invaded South America (Pastorino et al. 1993), where it has already spread across Argentina, Uruguay, Paraguay, Bolivia, and Brazil, having significant economic and ecological impacts (Boltovskoy et al. 2006, Boltovskoy et al. 2009). The overall impacts of both species on the areas invaded are scale dependent and are determined by the number of water bodies colonized (regional scale) and the population density in each of them (water body scale). Different factors govern the spread and distribution of L. fortunei and D. polymorpha at different spatial scales, affecting their population densities and environmental impacts (Karatayev et al. 2007b). Both species have similar length (typically approximately 20-30 mm; maximum, about 42-46 mm), and usually live about 3-4 y (reviewed in Karatayev et al. 2007a). They are sessile suspension feeders with a planktonic larval stage and high reproductive capacity, which allows them to colonize large areas quickly, producing significant local and systemwide effects (reviewed in Karatayev et al. 2007a, Karatayev et al. 2007b). Although the local effects are chiefly associated with their ability to form aggregations (druses) and physically change substrates, providing shelter and food for other benthic organisms, the systemwide effects are associated with their filtering activities. Being powerful suspension feeders, they greatly enhance benthic-pelagic coupling in the ecosystems they invade (reviewed in Karatayev et al. 1997, Darrigran 2002, Karatayev et al. 2002, Vanderploeg et al. 2002, Boltovskoy et al. 2006, Karatayev et al. 2007a, Boltovskoy et al. 2009). Because both local and systemwide effects depend primarily on the presence and activity of individual organisms, the magnitude of the overall impact strongly correlates with their population densities. Therefore, information on their distribution and abundance is critically important for understanding and predicting their ecological impacts. Although for Dreissena such surveys are numerous (e.g., reviewed in Karatayev et al. 1998, Patterson et al. 2005, Burlakova et al. 2006), for Limnoperna, information on population densities over large areas is restricted to a single comprehensive survey (Boltovskoy et al. 2009), all other abundance data being isolated records of peak densities (Darrigran 2002, Boltovskoy et al. 2006). Although this constraint imposes limitations on comparisons between the 2 bivalves, the fact that we have had extensive experience with both species and used similar methods allows us to address several key issues involving parallels and contrasts between these mussels. In this study we compare the population density and distribution across different substrate types of L. fortunei and D. polymorpha, as well as their impacts on the composition of benthic communities.
Limnoperna fortunei Distribution
Samples were collected in Embalse Rio Tercero, a mediumsize reservoir located in Cordoba Province, central Argentina (32[degrees]11'S, 64[degrees]13'W). The surface area of the reservoir is 47 [km.sup.2], its average depth is 10.1 m, and its volume is 0.48 [km.sup.3] (Boltovskoy et al. 2009). The reservoir was built in 1936 for hydroelectric power supply, and became a cooling reservoir for a 600-MW nuclear power plant in 1983. Large water-level fluctuations (up to 10 m) were typical for this water body before 1983. After the nuclear power plant was built, these fluctuations were substantially reduced, although during dry periods more than 17% of the reservoir bottom is occasionally exposed to air (Mariazzi et al. 1992). The littoral zone is dominated by rocks and sand, whereas deeper areas are mostly covered with mud. At the time of sampling, macrophytes were scarce, most likely because of the high water-level fluctuations.
All samples used to determine the distribution and abundance of L. fortunei were collected in December 2006 along 18 transects as a part of a larger survey (Boltovskoy et al. 2009). All transects were initiated on the shore and ran perpendicularly to the shore toward the center of the reservoir. Transects were distributed based on bathymetry and types of bottom sediments to represent all major habitat types adequately (Boltovskoy et al. 2009). For each transect, samples were collected from 3-10 sites at depths ranging from 2-19 m. Shallower areas were not sampled because all mussels in depths of less than 3 m were dead as a result of a recent drawdown. Each sample was collected by a scuba diver who retrieved all the specimens encompassed by a 50 x 50-cm metal frame (0.25 [m.sup.2] area quadrat) randomly placed from the boat. On hard bottoms, all rocks with mussels encompassed by the quadrat were removed or, when they were immobile or too large to remove, all adhering mussels were detached manually. On soft bottoms, the surface sediments within each quadrate down to 5 cm were examined and all mussels removed. Within 48 h of sampling, mussels were counted and weighed to the nearest 0.01 g, after removing water from their mantle cavity (wet weight, soft tissue plus shell).
Dreissena polymorpha Distribution
To compare the population densities and distribution of L. fortunei with D. polymorpha statistically, we needed primary data from other water bodies colonized by D. polymorpha obtained with similar methods of collection. Therefore, we used data obtained during our previous study in Belarus with a very similar experimental design and collection methods (Karatayev 1983, Burlakova et al. 2006). For these studies, Dreissena samples were collected from the glacial lakes Lukomskoye (data collected in 1978), Naroch (1993 to 1995, 1997, 2002), Myastro (1993, 1995, 2002), Batorino (1993, 1995, 2002), and Reservoir Drozdy (1995; Table 1). Lake Lukomskoe was sampled in July 1978 along 14 transects. For each transect, samples were collected at 0.5, 1, 2, 3, 4, 5, 6 m using scuba gear, and on silt substrates at 8 m using an Eckman grab (Karatayev 1983). The Eckman grab was very effective for sampling silt sediments, where only occasionally small Dreissena druses were found. Lakes Naroch, Myastro, and Batorino were sampled each year in July or August. We sampled 8 transects in Lake Naroch and 5 transects in lakes Myastro and Batorino. For each transect in these 3 lakes, up to 10 replicate samples were collected at 0.5-, 1-, 1.5-, 2-, and 3-m depths, and then at an interval of 1 or 2 m down to the maximum depth where D. polymorpha was found. At less than 8 m, samples were collected by divers based on a 0.25-[m.sup.2] quadrat, whereas at deeper sites on silt substrates an Eckman grab was used. A detailed description of our Dreissena sampling protocol was published previously (Karatayev 1983, Burlakova et al. 2006). Similarly to the L. fortunei study, all D. polymorpha samples were washed through a 550-[micro]m mesh, and within 48 h of sampling all zebra mussels larger than 1 mm in shell length were counted, opened with a scalpel to remove water from the mantle cavity, and the entire sample was weighed to the nearest 0.01 g after blotting dry on absorbent paper (wet weight, soft tissue plus shell) (Burlakova et al. 2006).
The impact of L. fortunei on the benthic community was studied in Rio Tercero Reservoir in Cordoba, Argentina, in December 2006. Twenty samples were collected at 3.5 m depth on silty sand within the same 5 x 10-m area: 10 samples of L. fortunei aggregations (druses) and 10 samples of bare sediments (without L. fortunei druses). L. fortunei druses were collected with their substrates by a diver, placed in zip-locked bags, and brought to the surface. Benthic samples were collected with a tube dredge sampler 7.2 cm in diameter (surface area, 0.004 [m.sup.2]). All samples were washed through a 500-[micro]m sieve and fixed with 10% buffered formaldehyde. All organisms from all samples were identified to the lowest possible taxonomic level, counted, and weighed after blotting dry on absorbent paper (total wet weight). Druse surface area was estimated as the projection on the surface; the mean area of the druses analyzed was 0.0058 [+ or -] 0.002 [m.sup.2].
To compare the effect of L. fortunei on benthic invertebrates with those of D. polymorpha, we used our data obtained in June 2007 in Lower Nashotah Lake, Wisconsin. In this lake we collected 12 samples at 2.5 m depth on silty sand within a single 5 x 10-m area, including 6 samples of Dreissena druses and 6 samples of bare sediments. Samples were analyzed using the same protocol as for L. fortunei.
The average mass of the mussels in a sample was calculated as the ratio between the total mass of the animals and their number in the sample. To compare the average mass, density, and biomass of D. polymorpha and L. fortunei, we used Kruskal-Wallis tests (because many samples contained no mussels; density = 0), separately for each substrate (Zar 1996), and multiple comparisons of mean ranks for all groups. All statistical tests were performed with the aid of Statistica software (STATISTICA version 6, StatSoft, Inc.). Effects were considered statistically significant at P < 0.05. When multiple tests were conducted on the same data, we used a sequential Bonferroni correction to adjust the critical alpha considered for statistical significance (Rice 1989). When appropriate, we present the critical alpha with the results of each statistical test.
Macroinvertebrate community structures were assessed using macroinvertebrate abundance (density, measured in individuals per square meter; and biomass, measured in grams per square meter) and diversity indices. PRIMER 6 version 6.1.6, Primer E-Ltd.) was used to analyze differences in benthic communities. To assess and visualize differences between macroinvertebrate community composition, we used nonmetric multidimensional scaling, which calculates a set of metric coordinates for samples, most closely approximating their nonmetric distances (Legendre & Legendre 1998). The sample-to-sample similarity of macroinvertebrate community composition (density and biomass) was assessed with the aid of the Bray-Curtis index (Bray & Curtis 1957, Clarke 1993) based on square root transformed abundance data. Differences between assemblages were assessed by analysis of similarities (ANOSIM). ANOSIM is a resampling technique that uses permutation/randomization methods on Bray-Curtis similarity matrices to identify differences among groups of samples with subsequent pairwise comparisons (Clarke 1999). The SIMPROF test routine was used to test for structure in the data. To characterize diversity in druse and sediment communities, we used the univariate Margalefs index of species richness; to describe the variability in the multivariate structure of these communities, we used relative multivariate dispersion. The comparative index of multivariate dispersion (Warwick & Clarke 1993) was calculated as a measure of increased variability between druse and sediment communities; this index varies between 0 (no difference) and 1 (maximum difference).
Distribution Within a Water Body
L. fortunei was found in 36 of the 68 samples obtained. Densities and biomass of L. fortunei varied significantly with substrate type (P < 0.001, Kruskal-Wallis test), being lowest on silt, medium on sandy substrates, and very high on rocks and gravel (Tables 1 and 2). The rocky and sandy substrates were most common at 4-8.5 m, resulting in the highest densities and biomass of L. fortunei at these depths. Because of the recent drawdown, all L. fortunei found above 3 m were dead. Silty bottoms were generally barren of L. fortunei, except for isolated druses formed around solid objects lying on the sediment, such as wood debris, bottles, and so forth, that occasionally were very large. In fact, one of the largest druses recorded was found on silt below 10 m, on a plastic bottle. On sandy substrates we found numerous L. fortunei druses that used sand grains or small pebbles glued together with byssal threads as a substrate for their attachment (Fig. 1). At the time of our sampling, the population consisted of subadult and adult individuals. The smallest L.fortunei found was 2 mm; the largest was 50.5 mm long (Fig. 1).
Comparison of the distributional data for L. fortunei in Rio Tercero Reservoir with that of D. polymorpha in 5 European lakes indicates that in both cases, the largest densities and wet biomass were usually found on rocks and gravel, whereas the lowest densities were always found on silt (Table 1). We found that on gravel and sand, L. fortunei densities and biomass were significantly higher than those of zebra mussels (Table 1). We also found that the average mass of L. fortunei was higher than that of D. polymorpha on rocks, gravel, and silty sand (Table 2).
Impacts on the Benthic Community
We found a total of 20 taxa (species and higher taxa) of macroinvertebrates in druses of L. fortunei (excluding Limnoperna), and 16 taxa in the bare sediments near the druses (Table 3). Nine taxa were found both in druses and in the sediments. The average diversity of native benthic invertebrates per sample was significantly higher (P < 0.0003, t-test) in L. fortunei druses than in the sediments. Communities in bare sediments were also characterized by a much larger variability between samples; the very high index of multivariate dispersion values (0.9-1.0, Table 3) allows rejecting the null hypothesis of no differences in the variability between these communities.
[FIGURE 1 OMITTED]
The average number of species, total density, and biomass of benthic communities were significantly higher in L. fortunei druses (P < 0.001, 2-sided t-test, Table 3). Nearly all taxa were much more abundant in druses than in bare sediments (Table 4). Differences were especially large for gastropods, leeches, caddisflies, mayflies, and chironomids. Only oligochaetes were more abundant in the sediments than in Limnoperna druses.
Similarly, a significant increase in the diversity, density, and biomass of bottom invertebrates (diversity and density, P < 0.001; biomass, P = 0.0023; 2-sided t-test) was found in Dreissena druses compared with bare sediments (Tables 3 and 4). Burrowing mayflies (Hexagenia sp.) were found in bare sediments but not in Dreissena druses.
Assemblages of native benthic invertebrates associated with the druses differed significantly from those found in the nearby bare substrate (global R = 0.46, P = 0.001, ANOSIM; P = 0.01, SIMPROF test; Fig. 2). These conclusions held when we aggregated data from species to higher taxonomic levels (genus, family, order, and class, all P = 0.001, ANOSIM).
Population Density and Potential Systemwide Effect
The ecological impact of both L. fortunei and D. polymorpha is associated with their role as biofilters and is therefore determined by their filtration rate and the overall population density in a given water body. Being powerful suspension feeders, both species filter large volumes of water, transferring energy and material from the water column to the bottom, greatly enhancing benthic-pelagic coupling, and inducing major changes in the colonized ecosystems (reviewed in Karatayev et al. 2007a). Although for L. fortunei our comparisons are based on distribution and population density data from a single water body, abundant previous information indicates that, similar to D. polymorpha, the golden mussel dearly favors the hard substrates of the littoral zone and avoids the soft bottom of deeper areas (see review in Boltovskoy et al. 2006) (Table 1). Thus, the general pattern of distribution within a water body is generally similar for the 2 bivalves. However, because the numerical density of L. fortunei across all substrates combined appears to be higher than that of the zebra mussels, the overall population density of L. fortunei in a water body may be also higher. Furthermore, because filtration rate is tightly coupled with biomass, and because L. fortunei is larger than D. polymorpha, at similar densities it may attain higher biomass levels and is therefore a more powerful "biofilterer" than the zebra mussel. As a result, the time required for L. fortunei to filter a volume of water equivalent to that of the water body is often substantially shorter than that of D. polymorpha (Fig. 3). Thus, although further studies are needed, we anticipate that L. fortunei may have a stronger systemwide effect than D. polymorpha.
Impacts on the Benthic Community
Both European and North American studies have shown that aggregations of zebra mussels create new 3-dimensional habitats for different invertebrates, whereas their pseudofeces and feces provide an abundant food supply for detritivores (reviewed in Karatayev et al. 1997, Karatayev et al. 2002). Shelters created by D. polymorpha have been shown to be the primary mechanism for increased abundance of macroinvertebrates, especially snails and amphipods (Botts et al. 1996, Stewart et al. 1998). Similar to the zebra mussel, L. fortunei transforms a 2-dimensional surface of hard substrate into a 3-dimensional structure, altering the habitat and providing shelter and food for other benthic invertebrates (Sylvester et al. 2007, Sardina et al. 2008). Therefore, the mechanism by which L. fortunei affects benthic assemblages is very similar to the one described for D. polymorpha (reviewed in Karatayev et al. 2002, Burlakova et al. 2005; Karatayev et al. 2007a, Karatayev et al. 2007b, Ward & Ricciardi 2007).
Dreissena druses have positive effects on the majority of native bottom invertebrates, including turbellarians, leeches, gastropods, some oligochaetes, and chironomids (Karatayev et al. 1983, Botts et al. 1996, Karatayev et al. 1997, Stewart et al. 1998). On the other hand, negative effects have been reported for several species of oligochaetes (Afanasiev 1987), and devastating effects on native unionid bivalves (reviewed in Burlakova et al. 2000). Our results show that the effects of L. fortunei on native benthic organisms are very similar to those of the zebra mussel (Table 3). The density of turbellarians, molluscs, leeches, mayflies, and chironomids was from 3-20 times higher in druses than in nearby sediments (Table 3). Crustaceans and caddisflies were found exclusively in L. fortunei druses. On the other hand, oligochaete densities were 25 times higher in the sediments than in L. fortunei druses (Table 3). Although we did not find any amphipods in Rio Tercero, they were extremely abundant in L. fortunei druses collected in Rio de la Plata (authors' unpublished data). Similarly to D. polymorpha, L. fortuneis overgrowth may cause the mortality of native unionids (Darrigran & Drago 2000, Darrigran 2002). The only 3 unionid specimens (1 alive, 2 dead) found in our Rio Tercero survey were heavily overgrown by L. fortunei (Fig. 1).
Although we used a different sampling protocol, our data largely agree with recent South American studies on the effects of L. fortunei on the associated fauna (Darrigran et al. 1998, Darrigran & Drago 2000, Sylvester et al. 2007, Sardina et al. 2008). However, an interesting difference is that, in contrast with these reports, our data indicate that the effect of the mussel on oligochaetes is negative (rather than positive). This difference suggests a species-specific effect, whereby different species are affected differently. Freshwater oligochaetes comprise both infaunal (burrowing), and epifaunal species; it is conceivable that the oxygen depletion associated with the large amounts of organic matter derived from the mussels' feces and pseudofeces (Sardina et al. 2008) inhibits the development of burrowing species, while still providing an advantageous medium for the epifaunal forms. Incidentally, in Rio Tercero Reservoir, the burrowing oligochaete Branchiura sowerbyi was found in the nearby sediments, but not in L. fortunei druses (Table 4). Similarly, in Lake Lower Nashotah, the burrowing mayfly Hexagenia was found in bare sediments, but not in Dreissena druses. Facilitation by habitat modifiers in general, and by filter-feeding bivalves in particular, is a well-known phenomenon, but effects on the benthic fauna are often modulated and even reversed by specific makeups (particularly in oligochaetes associated with mussels (Afanasiev 1987, Spooner & Vaughn 2006)), suspended sediment concentration (Norkko et al. 2006), geographical location (Buschbaum et al. 2009), season (Spooner & Vaughn 2006), sediment characteristics (Radziejewska et al. 2009), and sometimes by more intricate relationships (multispecies interactions, nonlinear biotic/abiotic interactions, threshold effects) that elude straightforward generalizations (Cummins et al. 2001). In this case, both L. fortunei and D. polymorpha, being powerful ecosystem engineers, physically alter benthic substrates and change dramatically associated macroinvertebrate communities.
[FIGURE 2 OMITTED]
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Potential Effect on North America
Although on the continental scale, as a result of temperature limits, L. fortuneis northward spread in northern America may be limited when compared with that of D. polymorpha, in central and southern regions of North America, Limnoperna may colonize many more water bodies than zebra mussels (Ricciardi 1998, Karatayev et al. 2007a, Karatayev et al. 2007b, Oliveira et al. 2010). It was shown that L. fortunei has a much wider tolerance to several key abiotic factors than D. polymorpha, including upper temperature limit (35[degrees]C for L. fortunei vs. 33[degrees]C for D. polymorpha), salinity (15[per thousand] for L. fortunei vs. 6[per thousand] for D. polymorpha), low pH values (5.5 for L. fortunei vs. 7.3 for D. polymorpha), calcium (around 3 mg/L for L. fortunei vs. 25 mg/L for D. polymorpha), and dissolved oxygen (0.5 mg/L for L. fortunei vs. 1.8 mg/L for D. polymorpha) (reviewed in Karatayev et al. 2007a, Karatayev et al. 2007b). Thus, on a regional scale, L. fortunei has a clear advantage in spreading among water bodies that are too warm and/or too acidic for D. polymorpha. Hence, in the near future, the freshwaters of North America may be colonized by another invader that, in certain regions, may be even more aggressive than the zebra mussel. The ecological consequences of this invasion may be similar to or even stronger than those of zebra mussels, including strong positive effects on epifaunal benthos (e.g., exotic amphipods and gastropods), negative effects on burrowing organisms, and devastating impacts on native unionids. The negative effect on unionids may be especially strong in southern regions of the United States, particularly if L. fortunei invades soft-water habitats that serve as refuges for threatened unionids against zebra mussels infestation (Ricciardi 1998).
This work was supported by the following grants: Faculty Research grant no. 114123 from Stephen F. Austin State University (to A. K., L. B., D. P., D. B., and D. P. Molloy, 2006-2007); EX-096 (University of Buenos Aires), Fundacion Williams and PICT 2004 25275 (ANPCyT) (to D. B.), and by Research Foundation of SUNY.
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ALEXANDER Y. KARATAYEV, (1) * LYUBOV E. BURLAKOVA, (1,2) VADIM A. KARATAYEV (3) AND DEMETRIO BOLTOVSKOY (4)
(1) Great Lakes Center, Buffalo State College, 1300 Elmwood Avenue, Buffalo, NY 14222; (2) The Research Foundation of The State University of New York, Buffalo State College, Office of Sponsored Programs, 1300 Elmwood Avenue, Bishop Hall B17, Buffalo, NY 14222-1095; (3) City Honors School, 186 East North Street, Buffalo, NY 14204; (4) Department of Ecology, Genetics and Evolution, University of Buenos Aires, C1428EHA Buenos Aires; Consejo Nacional de Investigaciones Cientificas y Tecnicas, and Museo Argentino de Ciencias Naturales "Bernardino Rivadavia," Argentina
* Corresponding author. E-mail: email@example.com
TABLE 1. Limnoperna fortunei and Dreissena polymorpha densities (per square meter), and total wet biomass (grams per square meter) across different substrates in water bodies in Argentina and in Belarus. Substrate Water Body Rocks Limnoperna fortunei (Argentina) Rio Tercero Reservoir Density 3,909 [+ or -] 917 (14) Biomass 2,302 [+ or -] 508 (100) Dreissena polymorpha (Belarus) Lake Lukomskoye Density NR Biomass Lake Naroch Density 2,206 [+ or -] 378 (22) Biomass 804 [+ or -] 163 (100) Lake Myastro Density 1,644 [+ or -] 806 (4) Biomass 1,024 [+ or -] 567 (100) Lake Batorino Density NR Biomass Drozdy Reservoir Density 4,048 [+ or -] 1,552 (2) Biomass 845 [+ or -] 303 (100) All water bodies Density 2,257 [+ or -] 339 (28) Biomass 839 [+ or -] 147 (100) P Kruskal-Wallis test Density 0.31 Biomass 0.055 Substrate Water Body Gravel Limnoperna fortunei (Argentina) Rio Tercero Reservoir Density 3,938 [+ or -] 1,121 (6) Biomass 2,859 [+ or -] 945 (100) Dreissena polymorpha (Belarus) Lake Lukomskoye Density NR Biomass Lake Naroch Density 1,456 [+ or -] 296 (6) Biomass 378 [+ or -] 148 (100) Lake Myastro Density 248 [+ or -] 25 (3) Biomass 72 [+ or -] 11 (100) Lake Batorino Density NR Biomass Drozdy Reservoir Density 2,281 [+ or -] 954 (6) Biomass 1,065 [+ or -] 466 (100) All water bodies Density 1,545 [+ or -] 427 (15) Biomass 591 [+ or -] 214 (100) P Kruskal-Wallis test Density 0.073 Biomass 0.024 * Substrate Water Body Sand Limnoperna fortunei (Argentina) Rio Tercero Reservoir Density 1,302 [+ or -] 1,046 (7) Biomass 576 [+ or -] 456 (71) Dreissena polymorpha (Belarus) Lake Lukomskoye Density 267 [+ or -] 90 (32) Biomass 55 [+ or -] 16 (69) Lake Naroch Density 119 [+ or -] 39 (215) Biomass 31 [+ or -] 9 (25) Lake Myastro Density 699 [+ or -] 340 (12) Biomass 402 [+ or -] 231 (58) Lake Batorino Density 965 [+ or -] 517 (6) Biomass 215 [+ or -] 97 (50) Drozdy Reservoir Density 5,829 [+ or -] 2,808 (6) Biomass 2,310 [+ or -] 891 (69) All water bodies Density 307 [+ or -] 85 (271) Biomass 105 [+ or -] 30 (34) P Kruskal-Wallis test Density 0.030 Biomass 0.017 * Substrate Water Body Silty Sand Limnoperna fortunei (Argentina) Rio Tercero Reservoir Density 1,007 [+ or -] 596 (10) Biomass 554 [+ or -] 298 (90) Dreissena polymorpha (Belarus) Lake Lukomskoye Density 3,620 [+ or -] 1,091 (16) Biomass 1,055 [+ or -] 255 (100) Lake Naroch Density NR Biomass Lake Myastro Density NR Biomass Lake Batorino Density NR Biomass Drozdy Reservoir Density 808 [+ or -] 664 (4) Biomass 470 [+ or -] 403 (100) All water bodies Density 3,058 [+ or -] 913 (20) Biomass 938 [+ or -] 221 (100) P Kruskal-Wallis test Density 0.035 Biomass 0.159 Substrate Water Body Silt Limnoperna fortunei (Argentina) Rio Tercero Reservoir Density 29 [+ or -] 27 (31) Biomass 24 [+ or -] 23 (7) Dreissena polymorpha (Belarus) Lake Lukomskoye Density 140 [+ or -] 57 (37) Biomass 69 [+ or -] 27 (41) Lake Naroch Density 116 [+ or -] 60 (42) Biomass 26 [+ or -] 14 (10) Lake Myastro Density 91 [+ or -] 91 (22) Biomass 56 [+ or -] 56 (5) Lake Batorino Density 43 [+ or -] 41 (29) Biomass 13 [+ or -] 13 (7) Drozdy Reservoir Density 0(7) Biomass All water bodies Density 97 [+ or -] 29 (137) Biomass 38 [+ or -] 13 (16) P Kruskal-Wallis test Density 0.177 Biomass 0.190 * Significant at P < 0.025 (Kruskal-Wallis test with Bonferroni correction). Cell values are means [+ or -] SE of sample size (top number) and percent of quadrats with zebra mussels (bottom number in parentheses). Tests of significance (Kruskal-Wallis test) compared the density and biomass of D. polymorpha and L. fortunei. NR, not recorded. TABLE 2. Limnoperna fortunei and Dreissena polymorpha average individual mass (total wet mass of body and shell, measured in grams, mean [+ or -] SE) across different substrates. Substrate Water Body Rocks Gravel with Sand Limnoperna fortunei Rio Tercero Reservoir 0.640 [+ or -] 0.076 0.638 [+ or -] 0.067 Dreissena polymorpha Lake Lukomskoye NR NR Lake Naroch 0.452 [+ or -] 0.139 0.242 [+ or -] 0.043 Lake Myastro 0.633 [+ or -] 0.071 0.291 [+ or -] 0.033 Lake Batorino NR NR Drozdy Reservoir 0.211 [+ or -] 0.006 0.466 [+ or -] 0.029 P, Kruskal-Wallis test 0.001 * 0.005 * Substrate Water Body Sand Silty Sand Limnoperna fortunei Rio Tercero Reservoir 0.504 [+ or -] 0.030 0.594 [+ or -] 0.088 Dreissena polymorpha Lake Lukomskoye 0.290 [+ or -] 0.056 0.357 [+ or -] 0.041 Lake Naroch 0.373 [+ or -] 0.033 NR Lake Myastro 0.549 [+ or -] 0.143 NR Lake Batorino 0.256 [+ or -] 0.051 NR Drozdy Reservoir 0.431 [+ or -] 0.057 0.469 [+ or -] 0.096 P, Kruskal-Wallis test 0.064 0.0162 * Substrate Water Body Silt Limnoperna fortunei Rio Tercero Reservoir 0.770 [+ or -] 0.066 Dreissena polymorpha Lake Lukomskoye 0.402 [+ or -] 0.075 Lake Naroch 0.207 [+ or -] 0.025 Lake Myastro 0.618 Lake Batorino 0.253 [+ or -] 0.053 Drozdy Reservoir NR P, Kruskal-Wallis test 0.060 * Significant at P < 0.0167 (Kruskal-Wallis test with Bonferroni correction)/ Tests of significance (Kruskal-Wallis test) compared the average individual mass of D. pohmorpha and L. fortunei. TABLE 3. Total and average species richness (number of taxa found), density (per square meter), wet biomass (grams per square meter), and the coefficient of variation of density (CV) of native macroinvertebrates (excluding L. fortunei and D. polymorpha) in Rio Tercero Reservoir, Argentina, and Lake Lower Nashotah, Wisconsin. Rio Tercero Reservoir Parameters Sediments Limnopevna Druses Total species recorded 16 20 Species per sample 5.6 [+ or -] 0.9 10.3 [+ or -] 0.6 Density/[m.sup.2] 4,650 [+ or -] 123 15,313 [+ or -] 284 CV of density (%) 11 8 Biomass (g/[m.sup.2]) 8.91 [+ or -] 0.25 30.75 [+ or -] 0.50 CV of biomass (%) 11 7 Relative multivariate 1.449 0.551 dispersion IMD substrate vs. druse 0.908 communities Margalef's species 1.776 1.972 richness Lake Lower Nashotah Parameters Sediments Dreissena Druses Total species recorded 9 32 Species per sample 2.7 [+ or -] 0.8 16.5 [+ or -] 1.2 Density/[m.sup.2] 833 [+ or -] 21 18,165 [+ or -] 156 CV of density (%) 7 4 Biomass (g/[m.sup.2]) 2.71 [+ or -] 0.13 33.03 [+ or -] 0.30 CV of biomass (%) 14 5 Relative multivariate 1.484 0.516 dispersion IMD substrate vs. druse 1.0 communities Margalef's species 1.19 3.161 richness Cell values are means [+ or -] SE. Diversity indices (calculated on densities), including relative multivariate dispersion, index of multivariate dispersion (IMD), and Margalefs species richness are given for each community. TABLE 4. Density per square meter (average [+ or -] SD) and occurrence (percent of samples with the taxon, in parentheses) of macroinvertebrates (excluding L. fortunei and D. polymorpha) in Rio Tercero Reservoir, Argentina, and Lake Lower Nashotah, Wisconsin. Rio Tercero Reservoir Taxon Sediments Turbellaria Dugesia tigrina NR Planaria sp. NR Turbellaria total NR Gastropoda Amnicola limosus NR Biomphalaria sp. 25 [+ or -] 79 (10) Gundlachia moricandi NR Gyraulus circumstriatus NR Physella sp. NR Stenophysa marmorata NR Gastropoda total 25 Bivalvia Pisidium sp. NR Sphaerium sp. NR Bivalvia total NR Oligochaeta Branchiura sowerbyi 50 [+ or -] 105 (20) Stylaria lacustris NR Oligochaeta sp. 2,050 [+ or -] 1,707 (100) Oligochaeta total 2,100 Hirudinea Glossiphonia sp. 75 [+ or -] 121 (30) Helobdella brasiliensis 225 [+ or -] 558 (20) Helobdella fusca NR Helobdella stagnalis 325 [+ or -] 528 (60) Hirudinea total 625 Decapoda Aegla scamosa NR Amphipoda Hyalella azteca NR Ceratopogonidae Culicoides sp. 50 [+ or -] 105 (20) Chironomidae Chironomus sp. NR Cricotopus sp. NR Cryptochironomus sp. 100 [+ or -] 129 (40) Dicrotendipes tritomus NR Dicrotendipes sp. 50 [+ or -] 158 (10) Harnischia sp. 150 [+ or -] 394 (20) Larsia sp. 300 [+ or -] 350 (60) Microtendipes gr. chloris NR Microtendipes pedellus NR Nilothauma sp. NR Polypedilum halterale NR Polypedilum illinoense NR Polypedilum sp 275 [+ or -] 702 (30) Procladius sp. 75 [+ or -] 121 (30) Pseudochironomus sp. NR Tanytarsus sp. 750 [+ or -] 957 (80) Tribelos jucundus NR Chironomidae total 1,700 Coleoptera Stenelmis sp. NR Ephemeroptera Caenis sp. 25 [+ or -] 79 (10) Ephemeroptera sp. NR Hexagenia sp. NR Maccaffertium mexicanum integrum NR Ephemeroptera total 25 Megaloptera Sialis sp. NR Odonata Argia sp. NR Chromagrion sp. NR Epitheca princeps princeps NR Odonata total NR Trichoptera Agraylea sp. NR Cyrnellus fraternos NR Cyrnellus sp. NR Mystacides sp. NR Oecetis sp. 125 [+ or -] 317 (20) Orthotrichia sp. NR Limnephiloidea sp. NR Trichoptera total 125 Rio Tercero Reservoir Taxon Limnoperna Druses Turbellaria Dugesia tigrina NR Planaria sp. 21 + 67 (10) Turbellaria total 21 Gastropoda Amnicola limosus NR Biomphalaria sp. NR Gundlachia moricandi 172 [+ or -] 109 (80) Gyraulus circumstriatus NR Physella sp. NR Stenophysa marmorata 289 [+ or -] 322 (70) Gastropoda total 461 Bivalvia Pisidium sp. NR Sphaerium sp. 12 [+ or -] 36 (10) Bivalvia total 12 Oligochaeta Branchiura sowerbyi NR Stylaria lacustris NR Oligochaeta sp. 82 [+ or -] 147 (30) Oligochaeta total 82 Hirudinea Glossiphonia sp. 43 [+ or -] 135 (10) Helobdella brasiliensis 547 [+ or -] 448 (100) Helobdella fusca NR Helobdella stagnalis 4,181 [+ or -] 2,132 (100) Hirudinea total 4,771 Decapoda Aegla scamosa 136 [+ or -] 295 (40) Amphipoda Hyalella azteca NR Ceratopogonidae Culicoides sp. NR Chironomidae Chironomus sp. NR Cricotopus sp. 14 [+ or -] 43 (10) Cryptochironomus sp. NR Dicrotendipes tritomus NR Dicrotendipes sp. 3,744 [+ or -] 1928 (100) Harnischia sp. NR Larsia sp. 1,932 [+ or -] 846 (100) Microtendipes gr. chloris 205 [+ or -] 319 (40) Microtendipes pedellus NR Nilothauma sp. NR Polypedilum halterale NR Polypedilum illinoense NR Polypedilum sp 43 [+ or -] 135 (10) Procladius sp. NR Pseudochironomus sp. NR Tanytarsus sp. 661 [+ or -] 586 (80) Tribelos jucundus NR Chironomidae total 6,599 Coleoptera Stenelmis sp. NR Ephemeroptera Caenis sp. 2,382 [+ or -] 1,576 (100) Ephemeroptera sp. 13 [+ or -] 42 (10) Hexagenia sp. NR Maccaffertium mexicanum integrum NR Ephemeroptera total 2,395 Megaloptera Sialis sp. NR Odonata Argia sp. NR Chromagrion sp. NR Epitheca princeps princeps NR Odonata total NR Trichoptera Agraylea sp. 21 + 66 (10) Cyrnellus fraternos 781 [+ or -] 907 (100) Cyrnellus sp. NR Mystacides sp. NR Oecetis sp. NR Orthotrichia sp. NR Limnephiloidea sp. 35 [+ or -] 75 (20) Trichoptera total 837 Lake Lower Nashotah Taxon Sediments Turbellaria Dugesia tigrina NR Planaria sp. NR Turbellaria total NR Gastropoda Amnicola limosus NR Biomphalaria sp. NR Gundlachia moricandi NR Gyraulus circumstriatus NR Physella sp. NR Stenophysa marmorata NR Gastropoda total NR Bivalvia Pisidium sp. 42 [+ or -] 102 (17) Sphaerium sp. NR Bivalvia total 42 Oligochaeta Branchiura sowerbyi NR Stylaria lacustris NR Oligochaeta sp. NR Oligochaeta total NR Hirudinea Glossiphonia sp. NR Helobdella brasiliensis NR Helobdella fusca NR Helobdella stagnalis NR Hirudinea total NR Decapoda Aegla scamosa NR Amphipoda Hyalella azteca NR Ceratopogonidae Culicoides sp. NR Chironomidae Chironomus sp. 167 [+ or -] 204 (50) Cricotopus sp. NR Cryptochironomus sp. NR Dicrotendipes tritomus NR Dicrotendipes sp. NR Harnischia sp. NR Larsia sp. NR Microtendipes gr. chloris NR Microtendipes pedellus NR Nilothauma sp. NR Polypedilum halterale 125 [+ or -] 209 (33) Polypedilum illinoense NR Polypedilum sp NR Procladius sp. NR Pseudochironomus sp. NR Tanytarsus sp. 83 [+ or -] 129 (33) Tribelos jucundus 208 + 292 (50) Chironomidae total 625 Coleoptera Stenelmis sp. NR Ephemeroptera Caenis sp. 42 1- 102 (17) Ephemeroptera sp. NR Hexagenia sp. 83 [+ or -] 129 (33) Maccaffertium mexicanum integrum NR Ephemeroptera total 125 Megaloptera Sialis sp. 42 [+ or -] 102 (17) Odonata Argia sp. NR Chromagrion sp. NR Epitheca princeps princeps NR Odonata total NR Trichoptera Agraylea sp. NR Cyrnellus fraternos NR Cyrnellus sp. NR Mystacides sp. NR Oecetis sp. NR Orthotrichia sp. NR Limnephiloidea sp. NR Trichoptera total NR Lake Lower Nashotah Taxon Dreissena Druses Turbellaria Dugesia tigrina 840 [+ or -] 467 (100) Planaria sp. 29 [+ or -] 72 (17) Turbellaria total 869 Gastropoda Amnicola limosus 27 [+ or -] 66 (17) Biomphalaria sp. NR Gundlachia moricandi NR Gyraulus circumstriatus 184 [+ or -] 157 (67) Physella sp. 966 [+ or -] 1,034 (100) Stenophysa marmorata NR Gastropoda total 1177 Bivalvia Pisidium sp. 66 [+ or -] 105 (33) Sphaerium sp. NR Bivalvia total 66 Oligochaeta Branchiura sowerbyi NR Stylaria lacustris 27 [+ or -] 66 (17) Oligochaeta sp. 570 [+ or -] 388 (100) Oligochaeta total 597 Hirudinea Glossiphonia sp. NR Helobdella brasiliensis NR Helobdella fusca 39 +95 (17) Helobdella stagnalis NR Hirudinea total 39 Decapoda Aegla scamosa NR Amphipoda Hyalella azteca 2,668 [+ or -] 1422 (100) Ceratopogonidae Culicoides sp. 31 [+ or -] 75 (17) Chironomidae Chironomus sp. 27 [+ or -] 66 (17) Cricotopus sp. NR Cryptochironomus sp. NR Dicrotendipes tritomus 1,569 [+ or -] 661 (100) Dicrotendipes sp. N R Harnischia sp. NR Larsia sp. 158 [+ or -] 140 (67) Microtendipes gr. chloris NR Microtendipes pedellus 2,148 [+ or -] 953 (100) Nilothauma sp. 27 [+ or -] 66 (17) Polypedilum halterale 690 [+ or -] 353 (100) Polypedilum illinoense 86 [+ or -] 210 (17) Polypedilum sp NR Procladius sp. 29 [+ or -] 72 (17) Pseudochironomus sp. 347 [+ or -] 620 (50) Tanytarsus sp. 2,417 [+ or -] 1,383 (100) Tribelos jucundus 3,197 [+ or -] 2,613 (100) Chironomidae total 10,697 Coleoptera Stenelmis sp. 26 [+ or -] 65 (17) Ephemeroptera Caenis sp. 1,257 [+ or -] 1,083 (100) Ephemeroptera sp. NR Hexagenia sp. NR Maccaffertium mexicanum integrum 163 [+ or -] 399 (17) Ephemeroptera total 1,419 Megaloptera Sialis sp. 152 [+ or -] 203 (50) Odonata Argia sp. 167 [+ or -] 144 (67) Chromagrion sp. 60 [+ or -] 93 (33) Epitheca princeps princeps 56 [+ or -] 88 (33) Odonata total 283 Trichoptera Agraylea sp. NR Cyrnellus fraternos NR Cyrnellus sp. 27 [+ or -] 66 (17) Mystacides sp. 26 [+ or -] 65 (17) Oecetis sp. NR Orthotrichia sp. 87 [+ or -] 151 (33) Limnephiloidea sp. NR Trichoptera total 141 NR, not recorded.
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