J. N. Am. Benthol. Soc., 2002, 21(2):238–252 q 2002 by The North American Benthological Society
Changes in the benthic algal community and nutrient limitation in Saginaw Bay, Lake Huron, during the invasion of the zebra mussel (Dreissena polymorpha) ROBERT W. PILLSBURY1,5, REX L. LOWE2, YANG DONG PAN3, JENNIFER L. GREENWOOD4
AND
University of Michigan Biological Station, 9008 Biological Road, Pellston, Michigan 49769 USA 2 Biology Department, Bowling Green State University, Bowling Green, Ohio 43403 USA 3 Environmental Sciences and Resources, Portland State University, Portland, Oregon 97207 USA 4 Institute of Ecology, The University of Georgia, Athens, Georgia 30602 USA
1
Abstract. We conducted a series of nutrient manipulation experiments over the first 5 y of Dreissena colonization in Saginaw Bay, Lake Huron, to evaluate benthic algal nutrient limitation and community composition. We placed nutrient-diffusing substrata in the littoral zone of the Bay during 1991 (early Dreissena colonization) and from 1992 to 1995 (post-Dreissena colonization). The treatments consisted of P, N, and P1N additions, and a control. Chlorophyll a decreased through time from 1992 to 1995. Phosphorus limited biovolume only in 1994. Treatments with P additions had significantly more chlorophyll a than the controls each year after 1992. This result was consistent with an observed decrease in dissolved P throughout the study. Nitrogen additions had no significant effect throughout the 5-y period. Major shifts in species composition did not result from nutrient additions but rather seemed to be consistent with changes in light penetration and Dreissena herbivory. Our data demonstrated that the pre-Dreissena benthic algal community was dominated by tychoplanktonic diatoms (i.e., Aulacoseira granulata and Tabellaria fenestrata), which would be susceptible to filter-feeding Dreissena. Early postinvasion conditions were marked by an increase in light penetration, and benthic algae were dominated by filamentous green algae (mostly Spirogyra sp.). Late post-invasion conditions were marked by a reduction of light caused by planktonic blooms of Microcystis sp., which were resistant to zebra mussel herbivory. The benthic algal dominance shifted to periphytic diatoms (i.e., Gomphonema clevei), which were also resistant to zebra mussel filter-feeding. A new equilibrium may be developing where Dreissena herbivory limits tychoplanktonic diatoms, which promotes Microcystis bloom, which in turn limits Dreissena filtering rates. Key words:
zebra mussel, Saginaw Bay, benthic algae, periphyton, nutrients, light.
The introduction of an exotic species can produce drastic effects on the composition and community structure of the invaded ecosystem (Elton 1958, Mooney and Drake 1986). Invading species may also provide the best evidence that a single species can control the functions of an entire ecosystem (Vitousek 1986). The invasion of the zebra mussel, Dreissena polymorpha (Pallas), into productive regions of the Laurentian Great Lakes ecosystem may be one of the most dramatic examples. In 1988, zebra mussels were first reported in North America in Lake St. Clair near Detroit, Michigan (Hebert et al. 1989). They had been accidentally introduced into the lake by a rePresent address: Department of Biology and Microbiology, University of Wisconsin Oshkosh, 800 Algoma Boulevard, Oshkosh, Wisconsin 54901-8640 USA. E-mail:
[email protected] 5
lease of ship ballast (Mackie et al. 1989, Cairns and Bidwell 1996), and soon spread to other regions of the Great Lakes and to many navigable rivers east of the Rocky Mountains (Nalepa and Schloesser 1993). Zebra mussels are highly prolific (Nalepa et al. 1995), producing planktonic larvae that settle and colonize hard substrata preferentially (Stanczykowska and Lewandowski 1993), reaching densities typically as high as 30,000 adult zebra mussels/m2 (Nalepa et al. 1995). Zebra mussels are prolific filter-feeders (Kryger and Riisga¨rd 1988, Reeders et al. 1993, Fanslow et al. 1995) and can effectively filter a wide size range of particles, from 750 mm (Ten Winkel and Davids 1982) to 1 mm (Jørgensen et al. 1984, Silverman et al. 1996). High densities of zebra mussels can significantly decrease plankton densities and increase water clarity (Stanczykowska et al. 1976, MacIsaac et al. 1992, Hol-
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land 1993, Leach 1993, Reeders et al. 1993, Fahnenstiel et al. 1995b, MacIsaac 1996). Densities of bacteria (Cotner et al. 1995), protozoa (Lavrentyev et al. 1995), and zooplankton (Shevtsova et al. 1986, MacIsaac et al. 1991) can also be reduced by filtering activities. Ingested seston is processed and fecal pellets are deposited on the bottom of the lake (Griffiths 1993). Plankton that is collected but not ingested is aggregated in mucus and is also deposited as pseudofeces (Ten Winkel and Davids 1982). We hypothesized that, as zebra mussels colonized Saginaw Bay, Lake Huron, they would indirectly increase benthic algal production by increasing light, enhancing nutrient availability to benthic algae from feces and pseudofeces deposited on the lake floor, and by decreasing resource (e.g., nutrient) competition from phytoplankton (Lowe and Pillsbury 1995, MacIsaac et al. 1992, MacIsaac 1996). Benthic algal species that spend at least part of their life cycle in the water column would also likely be negatively impacted. The objective of our study was to examine changes in nutrient-resource limitations and species composition in the benthic algal community of Saginaw Bay during the first 5 y of the zebra mussel invasion. Methods Study site Saginaw Bay is a large, shallow embayment of Lake Huron (Fig. 1), with historically high nutrient and phytoplankton concentrations (Vollenweider et al. 1974, Smith et al. 1977, Bierman and Dolan 1981, Stoermer et al. 1983, Kreis et al. 1985, Stoermer and Theriot 1985). The bottom substratum consists primarily of limestone and dolomite bedrock and large cobble, ideal for zebra mussel colonization. Our study site was located near the center of the Bay, ;2 km north of Big Charity Island (lat 44.03.10 N, long 83.26.31 W). This offshore location minimized the effects of direct human disturbances and storm runoff. The substrata at this site consisted of cobble and patches of sand at a depth of 5.0 to 6.0 m (Lowe and Pillsbury 1995). This site was close to Station 19 of a broader survey of the Bay (Fahnenstiel et al. 1995b, Lowe and Pillsbury 1995).
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Nutrient-diffusing substrata Field activities. Each year, from 1991 to 1995, modified clay flowerpots were deployed in the Bay as nutrient-diffusing substrata (NDS) (Fairchild et al. 1985). The pots were filled with either 2% agar (control treatment, C), 0.75 M NaNO3 in 2% agar (N treatment), 0.05 M Na2HPO4 in 2% agar (P treatment) and both 0.75 M NaNO3 and 0.05 M Na2HPO4 in 2% agar (P1N treatment). Each year, a minimum of 4 NDS were deployed for each treatment (Table 1). The NDS were attached with silicone adhesive to cement patio blocks to provide stability on the lake bottom. All patio blocks were preconditioned in a mesotrophic lake in northern Michigan (Douglas Lake, at the University of Michigan Biological Station) for $1 mo prior to attachment of NDS and deployment in Saginaw Bay. SCUBA divers deployed the NDS at the research site randomly but no closer than 20 cm to its nearest neighbor. NDS were deployed each year near the end of July and exposed for 23 to 36 d (Table 1). SCUBA divers carefully retrieved the NDS after exposure by placing a close-fitting, plastic beaker over each one, while slowly prying it free from the cement blocks, and immediately placing both beaker and pot into a plastic bag. The bags were then transported to the surface. This procedure permitted the reliable collection of loosely attached algae from the NDS while minimizing the collection of nearby phytoplankton. At the surface, each NDS was immediately placed on ice and in an insulated cooler to be transported to the laboratory. Laboratory procedures. In the laboratory, the periphyton was scraped off the sides of the NDS and washed into a basin. The periphyton suspension was homogenized in a blender for 15 s to break up large aggregates. Total volume of the suspension was recorded and a subsample volume was filtered onto a glass fiber filter (pore size ,0.45 mm) and frozen for subsequent chlorophyll analysis. Chlorophyll a concentrations were measured and corrected for phaeophytin (acetone extraction, APHA 1985) using a Perkin Elmer Lamba-6 UV-Vis spectrophotometer. At least 300 algal cells or colonies from each replicate sample were identified to species and enumerated using a Palmer–Maloney counting chamber at a magnification of 4303.
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Location of research site (Station 19) in Saginaw Bay, Lake Huron.
In addition, permanent diatom slides were prepared from the periphyton suspension by cleaning aliquots with 30% H2O2 and K2Cr2O7 and mounting in Naphraxt (van der Werff 1955). At least 300 diatom valves were counted and identified to species at 10003 magnification. Diatom slides were used to confirm species identity of living diatoms in the corresponding Palmer–Maloney counts. At least 10 cells/taxon were measured to determine average cell dimensions. The dimensions were applied to standard geometric shapes, which approximated the shape of each taxon, and species biovolumes were calculated.
Zebra mussel collection To estimate zebra mussel densities, 7 to 10 rocks were randomly collected by SCUBA divers along 2 transects (one at 2.5 m and another at 5.5 m depth) near the NDS site (Lowe and Pillsbury 1995) at the beginning and end of each experiment. Each transect started at the anchor and continued in a random direction until the appropriate number of cobblesized rocks had been found. In the laboratory, zebra mussels longer than 1.0 mm were enumerated on each rock and NDS. The exposed surface area of the rocks was calculated by
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TABLE 1. Experimental design of 5 nutrient-manipulation studies conducted in Saginaw Bay, Lake Huron. N 5 N additions, P 5 P additions.
Year
No. of pots deTreatment ployed
No. of pots recovered
Starting date
Duration (d)
1991
Control N P N1P
4 4 4 4
2 2 2 2
July 25
29
1992
Control N P N1P
12 12 12 12
12 12 12 12
July 22
36
1993
Control N P N1P
4 4 4 4
4 3 3 4
July 17
23
1994
Control N P N1P
4 4 4 4
3 4 4 4
July 23
33
1995
Control N P N1P
5 5 5 5
5 5 5 5
July 18
29
wrapping it in a single layer of aluminum foil, weighing the foil, and comparing its mass to that of a 10 cm2 piece of foil. Physical and chemical measurements Light (photosynthetically active radiation, PAR) was measured at 5 m depth each year during our monthly collections in June, July, and August with a LiCor Li-192SA underwater quantum sensor (2p) that was cosine corrected. Reference measurements were taken at the surface. These measurements were taken during productivity incubations, which were all conducted between 1000 h and 1400 h (Lowe and Pillsbury 1995). Measurements were taken at least hourly during the 3.5 h productivity incubations. Secchi depth measurements were also taken during each monthly sampling event. Total suspended solids (TSS), planktonic chlorophyll a, particulate organic C (POC), total P (TP), soluble reactive P (SRP), NO3, NH4, and SiO2 data were taken from Nalepa et al. (1996)
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and T. L. Nalepa (NOAA Great Lakes Environmental Research Lab, Ann Arbor, Michigan, personal communication). Data analysis The effect of nutrient treatment on the density of common algal species densities was tested with a 1-way ANOVA (Zar 1993). A taxon was considered to be common if its relative abundance was .5% (of the total treatment abundance) in at least 1 treatment. Prior to analysis, all data were log-transformed (ln(x11)) to conform with normality assumptions (Zar 1993). Although desirable, a 2-way ANOVA using treatment and year as independent variables was not done because taxa common in one year were absent in other years, thus violating an assumption of the test (normal distribution). The non-parametric Kruskal–Wallis test was used if assumptions for the parametric test were severely violated (species were absent more than once per treatment). Multiple pairwise comparisons examining significant differences between the control and nutrient manipulations (Bonferroni test) were conducted if the ANOVA was significant (p , 0.05). Only relative abundance data were available for 1991. These data were arcsine-transformed prior to analysis. The interactive effects of nutrient additions and time (i.e., year) on algal biomass (chlorophyll a and total biovolume) were tested with a 2-way ANOVA on data from 1992 to 1995. Data from 1991 were not included because biomass could not be estimated for that year. Water-column variables for selected years were compared by forming year-groups based on gross benthic algal characteristics and applying a t-test to determine if conditions were significantly different between these periods. Correspondence analysis (CA) was performed to summarize species variance and detect underlying patterns of species distribution. CA is an ordination technique, which places samples along a few ordination axes based on the similarity of species among samples (Hill 1973). In CA, ordination axes (latent variables) are selected to best explain species variance (Hill 1973). Therefore, CA can summarize species variance by low-dimensional representations (a few CA axes) and reveal underlying species distribution patterns. Taxa with relative biovolumes .1% (of the total sample biovolume) in $5 samples were
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FIG. 2. Mean (1SE) densities of zebra mussels at Station 19 in Saginaw Bay from 1991 to 1995. Zebra mussels did not appear until July 1991 and were not found in significant numbers (.10/m2) until August 1991.
included in the analysis. CA was performed using CANOCO version 3.1 (ter Braak 1987, ter Braak 1990). Results Zebra mussel densities Zebra mussels first appeared at our site in July of 1991 and their densities peaked in 1992 at .70,000/m2 (Fig. 2). Zebra mussels did not colonize the NDS.
phyll a concentrations (Bonferroni pairwise comparisons, p , 0.05) in the controls from 1992 to 1995 (1992 . 1993 . 1994 . 1995) (Fig. 4). In 1992, no significant difference was detected among nutrient treatments. P and P1N treatments had significantly more (p , 0.005) chlorophyll a in all other years (Fig. 4). Benthic algal chlorophyll a concentrations also varied significantly with treatment (p , 0.0001), year (p , 0.0001), and had a significant treatment 3 year (p , 0.0001) interaction.
Benthic biovolume and chlorophyll a
Changes in species composition
P and N1P additions only produced a significant increase from the control in benthic algal biovolume in 1994 (Fig. 3, Bonferroni multiple comparison test, p , 0.001). Total benthic algal biovolume varied significantly with treatment (p , 0.0001) and year (p , 0.0001) with a significant interaction (p , 0.0001) between these variables from 1992 to 1995. Benthic algal biovolume on control treatments progressively decreased from 1992 to 1995. Bonferroni pairwise comparisons yielded: 1992 . 1993 5 1994 . 1995 (p , 0.001). There was a significant decrease of chloro-
Seventy-three taxa had a relative abundance .1.0% in $1 sample over 5 y. Table 2 lists the % biovolume for the most abundant taxa. In 1991, tychoplanktonic diatoms (such as Aulacoseira granulata and Tabellaria fenestrata) dominated the benthic algal community (Fig. 5, Table 2). No significant differences in species composition among nutrient treatments were found, although low replicate numbers (n 5 2) may have obscured potential nutrient effects. Filamentous green algae (Spirogyra sp. and Cladophora glomerata) dominated all communities in 1992 (Fig. 5, Table 2). A comparison of bio-
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FIG. 3. Mean (1SE) algal biovolume from 4 experiments (1992–1995) using nutrient-diffusing substrata at Station 19 in Saginaw Bay, Lake Huron. Algal biovolume for year 1991 could not be calculated because of the loss of sample volume information. N 5 N addition, P 5 P addition.
FIG. 4. Mean (1SE) periphyton chlorophyll a concentration from 4 experiments (1992–1995) using nutrientdiffusing substrata at Station 19 in Saginaw Bay, Lake Huron.
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TABLE 2. Mean % of total algal biovolume of common taxa that accumulated on nutrient-diffusing substrata from 1991 to 1995. N 5 N addition, P 5 P addition.
Year
GomAulacoCocco- pho- GomNaviseira Clado- neis nema pho- Mou- cula granu- phora pedi- angus- nema geotia salinaTreatment lata sp. culus tatum clevei sp. rum
NitzTabelschia RhoicoStigeo- laria dissi- sphenia Spiro- clonium fenespata curvata gya sp. sp. trata
1991
Control N P N1P
35.9 41.7 22.0 18.6
0.0 0.0 0.0 0.0
0.2 0.5 0.1 0.0
0.3 0.4 0.7 0.2
0.0 0.0 0.0 0.0
5.0 2.3 0.0 0.0
1.6 0.6 10.5 5.3
0.2 0.3 10.2 6.0
0.0 0.0 0.0 0.0
0.0 0.0 0.0 0.0
0.0 0.0 0.0 0.0
20.4 24.6 8.6 14.6
1992
Control N P N1P
0.0 0.1 0.0 0.0
10.9 11.8 15.2 15.6
0.1 0.1 0.8 0.9
0.0 0.0 0.0 0.0
0.0 0.0 0.0 0.0
7.0 8.1 3.3 5.2
0.0 0.0 0.0 0.1
0.0 0.0 0.0 0.0
0.0 0.0 0.5 0.4
32.5 31.0 27.6 24.2
1.4 1.8 10.4 8.2
0.3 0.2 0.2 0.1
1993
Control N P N1P
0.0 0.0 0.0 0.0
0.0 0.0 0.0 0.0
0.0 0.5 1.5 3.9
0.1 0.0 0.0 0.0
0.2 0.0 0.0 0.0
0.3 2.6 2.9 1.1
0.4 0.9 14.8 6.1
0.0 0.0 0.6 0.2
0.1 0.0 0.2 0.2
91.0 86.3 60.4 75.2
0.0 0.0 0.6 1.5
0.0 0.0 0.0 0.0
1994
Control N P N1P
0.0 0.0 0.0 0.0
0.0 0.0 0.0 0.0
0.2 0.0 0.0 0.9
0.8 0.5 0.4 0.1
0.0 0.0 0.0 0.0
1.1 0.1 0.0 0.0
0.4 0.3 6.3 0.5
0.0 0.0 0.1 0.1
0.0 0.0 0.0 0.0
71.5 78.7 87.9 82.7
0.0 0.0 0.0 0.0
0.0 0.0 0.0 0.0
1995
Control N P N1P
0.0 0.0 0.0 0.0
0.0 0.0 0.0 0.0
4.6 4.2 16.8 14.8
1.2 24.8 1.8 25.8
58.6 20.3 11.6 0.0
0.0 0.0 0.0 0.1
1.8 0.0 0.7 0.6
0.0 0.0 0.0 0.0
0.3 0.0 14.5 7.3
0.0 0.0 0.0 0.0
0.0 0.0 0.0 0.0
0.0 0.0 0.0 0.0
volumes showed that the filamentous green algae Stigeoclonium sp. and Mougeotia sp., and the diatoms Gomphonema angustatum, Cocconeis pediculus, and Rhoicosphenia curvata were significantly (p , 0.05) more abundant in the P treatment than in the control. Navicula salinarum, Stigeoclonium sp., Mougeotia sp., C. pediculus, and R. curvata were significantly (p , 0.05) more abundant in the N1P treatment than in the control. Spirogyra sp. was significantly (p , 0.05) less abundant in the N1P treatment relative to the control. Algal population biovolume did not differ significantly between N and control treatments except for R. curvata, which was significantly (p , 0.05) lower in the N treatment. In 1993, the periphyton community was dominated in all treatments by Spirogyra sp. (Fig. 5, Table 2). The N1P treatment had a significantly greater abundance of N. salinarum and C. pediculus compared to the control (p , 0.05). No significant differences were found when the N treatment was compared to the control. Spirogyra sp. also dominated all treatments in 1994 (Fig. 5, Table 2). When compared to the
control, the nutrient-addition treatments showed there were no significant differences in biovolume between the control and the treatments, except for an increase of Spirogyra sp. in the P and N1P treatments (p , 0.05 in both cases). The 1995 periphyton community reverted back to diatom dominance (Fig. 5), with Gomphonema clevei being the dominant species in the control (Table 2). The abundance of this species in the N and N1P treatments was significantly (p , 0.05) lower than in the control. The relative abundances of C. pediculus and R. curvata were significantly (p , 0.05) higher in the P treatment than in the control. Gomphonema angustatum, G. subclavatum, R. curvata, and C. pediculus were significantly (p , 0.05) higher in the N1P treatment than in the control. Correspondence analysis The first 2 CA axes explained 53.2% of the algal species variance and produced 3 distinc-
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FIG. 5. Relative biovolumes of tychoplanktonic diatoms (i.e., Aulacoseira granulata and Tabellaria fenestrata), filamentous green algae (i.e., Spirogyra sp., Stigeoclonium sp., Cladophora sp., and Mougeotia sp.), and periphytic diatoms (i.e., Gomphonema angustatum, G. clevei, Cocconeis pediculus, Navicula salinarum, Nitzchia dissipata, and Rhoicosphenia curvata) plotted for each nutrient addition treatment from 1991 to 1995. N 5 N addition, P 5 P addition.
tive clusters, which could be identified by years: 1) all 1991 samples, 2) all 1992, 1993, and 1994 samples, and 3) all 1995 samples (Fig. 6). Such clustering suggested that the difference in spe-
cies composition was much greater among years than among nutrient treatments. The first CA axis may represent a shift from settled planktonic diatoms to benthic filamen-
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FIG. 6. Correspondence analysis (CA) of the relative biovolumes of algal taxa appearing on nutrient-diffusing substrata at Station 19 in Saginaw Bay. CA groups—1 5 1991: pre-Dreissena colonization; 2 5 1992–1994: early post-Dreissena colonization; and 3 5 1995: late post-Dreissena colonization. Many of the symbols within clusters overlapped. N 5 N addition, P 5 P addition.
tous green algae. This axis was negatively loaded by Spirogyra sp. and positively loaded by planktonic diatoms such as A. granulata and T. fenestrata. This shift was coincident with the zebra mussel invasion of Lake Huron. Community structure was similar among samples in 1992, 1993, and 1994, when zebra mussels were abundant. However, species composition shifted again to periphytic diatoms such as G. clevei from 1994 to 1995 as summer blooms of Microcystis sp. decreased the light reaching the lake bottom to pre-Dreissena conditions. Water-column measurements TSS, planktonic chlorophyll a, and POC for the filamentous green algal period (1992–1994) were lower than periods when diatoms were dominant (Table 3). The mean TSS was significantly (t-test, p 5 0.012) reduced from 2.77 to 1.58 mg/L. The mean planktonic chlorophyll a concentration was significantly (p 5 0.006) reduced from 3.49 to 1.83 mg/L, and mean POC
was reduced (although not significantly) from 0.69 to 0.49 mg/L. The mean light conditions (PAR) were significantly (p 5 0.038) greater (215.3 mmol m22 s21) during filamentous green algal dominance compared to diatom-dominated periods (98.5 mmol m22 s21). The mean summer (June, July, and August) Secchi disc depth was greatest during filamentous green algal dominance and significantly (p 5 0.003) different from periods of diatom dominance (4.7 m compared to 2.5 m). The summer means of nutrients in the water column above the research site measured by Nalepa et al. (1996) and T. L. Nalepa (personal communication) did not show any significant trends, except for SRP, which decreased significantly (1991 . 1994 5 1995, p 5 0.05) over this period (Table 3). Discussion We documented 2 major shifts in benthic algal species composition and biovolume as zebra
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TABLE 3. Summer means (SE, June to August) of physical and chemical variables from Saginaw Bay, Lake Huron, measured above the research site from 1991 to 1995. TSS 5 total suspended solids, Chl. a 5 chlorophyll a, POC 5 particulate organic C, PAR 5 photosynthetically active radiation, TP 5 total P, SRP 5 soluble reactive P. Secchi depth and PAR were measured by the authors. All other data are from Nalepa et al. (1996) or T. J. Nalepa (NOAA Great Lakes Environmental Research Lab, Ann Arbor, Michigan, personal communication). Variable
1991
1992
1993
1994
1995
Secchi disc depth (m) TSS (mg/L) Chl. a (mg/L) POC (mg/L) Light (PAR, mmol m22 s21) TP (mg/L) SRP (mg/L) NO3 (mg/L) NH4 (mg/L) SiO2 (mg/L)
2.0 (0.0) 2.87 (0.27) 3.87 (0.68) 0.70 (0.05) 95 (55) 6.8 (1.1) 1.4 (0.3) 0.22 (0.05) 16.9 (2.1) 0.80 (0.23)
4.8 (0.9) 1.57 (0.37) 1.66 (0.08) 0.53 (0.09) 145 (27) 6.3 (6.3) 1.1 (0.0) 0.41 (0.01) 16.4 (4.3) 0.68 (0.27)
4.6 (0.9) 1.73 (0.47) 2.00 (0.83) 0.43 (0.17) 338 (83) 7.5 (2.0) 0.7 (0.1) 0.32 (0.05) 18.8 (3.3) 0.70 (0.16)
4.7 (0.8) 1.43 (0.52) 1.83 (0.66) 0.49 (0.17) 163 (71) 7.0 (1.7) 0.5 (0.1) 0.29 (0.01) 12.9 (4.8) 0.74 (0.08)
3.0 (0.6) 2.67 (0.77) 3.11 (1.21) 0.69 (0.24) 102 (38) 5.5 (1.1) 0.2 (0.1) 0.26 (0.05) 14.3 (3.1) 1.17 (0.19)
mussels became a dominant part of the ecosystem over the 5 y of our study. Our study site also was subjected to unpredicted events such as a decrease in available P (SRP) and changes in light penetration. Determining, with certainty, the major causal factors responsible for all of these changes is difficult; we could not experimentally manipulate many of these factors, so the strength of our inferences is limited. However, zebra mussels are still spreading to new systems at a rapid rate and, although the corresponding responses of other phytoplankton communities are often similar to the changes seen in Saginaw Bay (Holland 1993, Leach 1993, Nicholls and Hopkins 1993, Fahnenstiel et al. 1995b), changes in the benthic algal communities are largely unreported. Although changes in the benthic algal community cannot yet be conclusively explained, we believe our longterm examination of this community can provide insights for further studies. Algal communities before and during Dreissena colonization Dreissena invaded Saginaw Bay late in the summer of 1991 (Lowe and Pillsbury 1995, Nalepa et al. 1995). We found no Dreissena at our study site in late June 1991, 9 Dreissena/m2 in July, and 15,190 Dreissena/m2 in late August (Lowe and Pillsbury 1995). Therefore, significant numbers of zebra mussels appeared only near the end of summer 1991, after the periphyton community in our colonization experiment had become established. A study of the natural
rock substrata at our research site during 1991 found no major shifts in algal community composition from May to late August (Lowe and Pillsbury 1995), which suggests that the benthic algal community was not impacted at this early colonization stage. Since then, zebra mussel densities have remained .10,000/m2 (Fig. 2). Although there are no benthic algal community records for Saginaw Bay prior to 1991, there are reliable records for phytoplankton and nutrient levels (Smith et al. 1977, Bierman and Dolan 1981, Stoermer and Theriot 1985, Fahnenstiel et al. 1995b), which show high concentrations of chlorophyll and nutrients in Saginaw Bay similar to those found in 1991. Also, Fahnenstiel et al. (1995b), Bierman et al. (1984), and Nalepa et al. (1999) have documented relatively stable patterns of summer Secchi depth prior to 1992 (for 1974–1980 and 1991, x¯ 6 SE 5 1.14 m 6 0.09), which would have resulted in relatively stable light conditions for benthic algal communities (Fig. 7). In summers when filamentous green algae dominated (1992–1994), the Secchi depth was significantly (t-test, p 5 0.002) higher (x¯ 5 1.87 6 0.16 m) than other summers, which suggests that our benthic algal data from summer 1991 represents a typical pre-zebra-mussel-invasion summer. The pre-invasion plankton community of Saginaw Bay was dominated by diatoms (Fig. 6, CA cluster 1). Dense summer blooms of planktonic diatoms captured much of the light before it reached the lake bottom (Table 3). Most living diatoms found on the bottom (i.e., A. granulata
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FIG. 7. Mean secchi depth values taken from monthly (April–October) sampling programs all over Saginaw Bay, Lake Huron (from Nalepa et al. 1999).
and T. fenestrata) were unattached to the substratum and were normally planktonic. Therefore, these taxa could be readily captured and consumed by the filter-feeding zebra mussels. Algal communities after Dreissena colonization (1992–1994) After a peak in 1992, Dreissena densities decreased at our site (Fig. 2) and throughout Saginaw Bay (Nalepa et al. 1999). The mean ashfree dry mass of mussels also decreased 65% baywide from 1991 to 1993 as phytoplankton densities dropped (Nalepa et al. 1995). It seems likely that zebra mussel densities fell because of a depletion of their food source. Zebra mussel densities continued to fall at our site after 1993 (Fig. 2), but a baywide survey by Nalepa et al. (1999) indicated overall Dreissena density had stabilized, although there was a high amount of variation over time and location. Secchi depth readings from 1992 to 1994 were .23 those found in 1991 at our site (Table 3). Similar changes were observed (Nalepa et al. 1999) across the whole bay (Fig. 7). Fanslow et
al. (1995) demonstrated that the high densities and high filtering rates of Dreissena in Saginaw Bay could alone account for the decrease in phytoplankton. Bridgeman et al. (1995) found that zooplankton grazing rates from 1991 to 1992 drastically declined in Saginaw Bay and could not explain the drop in phytoplankton levels. From 1990 to 1993, no relationship could be found across Saginaw Bay between planktonic chlorophyll a and nutrients (Nalepa et al. 1999). Decreases in phytoplankton abundance associated with Dreissena have also been observed in other systems (Holland 1993, Leach 1993, Nicholls and Hopkins 1993, Fahnenstiel et al. 1995b). We observed a 4-fold increase in benthic algal biomass from late August 1991 to August 1992 on natural rock substrata adjacent to our experimental plots (Lowe and Pillsbury 1995). This increase in biomass was caused by filamentous green algae; the same shift in species composition was observed on our NDS. Filamentous green algae on natural substrata at this site increased under higher light conditions (compared to deeper sites) along a depth gradient in both 1991 and 1992 (Lowe and Pillsbury 1995).
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Filamentous green algae like Spirogyra sp. and Cladophora sp., which dominated our site from 1992 to 1994 (Fig. 6, CA cluster 2) have also dominated other systems (Graham et al. 1982, Shortreed and Stockner 1983, Turner et al. 1987, Hill 1996, Graham et al. 1996) once light levels increased. Diatoms (corresponding to CA cluster 1, Fig. 6) appear to have lower light requirements than filamentous green algae (Hill 1996). This observation agrees with Fahenstiel et al. (1995a) who found Saginaw Bay was light-limited before the zebra mussel invasion, and by Nalepa et al. (1999) who calculated that the baywide drop in phytoplankton productivity was roughly compensated for by the increase in benthic algal productivity. Macrophytes and macroalgae biomass also increased in nearshore littoral zones of Saginaw Bay during this time (Skubinna et al. 1995), presumably because of the increase in light penetration. Algal communities after Dreissena colonization (1995) Midsummer blooms of the blue-green alga Microcystis sp. dominated the phytoplankton in 1995 (Fig. 6, CA cluster 3) (Heath et al. 1995, RWP, unpublished observations). Large blooms of Microcystis are normally associated with eutrophic conditions but no shift in the trophic status of Saginaw Bay was observed (Fahnenstiel et al. 1995b). Heath et al. (1995), Lavrentyev et al. (1995), and H. A. Vanderploeg (NOAA Great Lakes Environmental Research Lab, Ann Arbor, Michigan, personal communication) found that zebra mussels avoided filtering colonies of Microcystis. Although the reason for this selective filtering is not known, there are 2 possible explanations: 1) unpalatable taste—Microcystis blooms often produce taste and odor problems (APHA 1985) with the production of the toxin microcystin (Moore 1977); and 2) Dreissena have trouble handling the large, amorphous colonies of Microcystis with thick mucilaginous sheaths around the cells (Lee 1980). Microcystis may have been successful because of a lack of competition from normally present phytoplankton. In 1995, filamentous green algae were virtually absent and diatoms dominated the benthic community again. The diatom-dominated communities from 1991 and 1995 were very different, and formed 2 distinct groups in our CA analysis (Fig. 6). In 1995, this community was dominated
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by truly periphytic (attached) forms of diatoms. These diatoms adhere to substrata using mucilaginous secretions and therefore would be resistant to zebra mussel filter-feeding because they are not characteristically part of the plankton. Benthic algal biomass decreased from 1992 to 1994 and became increasingly limited by P (Fig 3, Fig 4) as SRP levels at the site decreased (Table 3). Although P loadings to Saginaw Bay were constant from 1991 to 1995, baywide SRP levels dropped in a similar manner (Nalepa et al. 1999). Heath et al. (1995) observed an initial increase in SRP in mesocosms, constructed in Saginaw Bay, that contained zebra mussels. SRP levels declined towards the end of the experiment (day 6). This trend may be a result of P uptake by zebra mussels (either stored in the tissue or deposited as feces or pseudofeces) or increased benthic algal biomass (Nalepa et al. 1999). SRP may have been taken up at greater rates by the remaining, faster-growing, ungrazed phytoplankton (Heath et al. 1995). Bacterial and protozoan communities in Saginaw Bay have also been affected by the Dreissena invasion (Cotner et al. 1995, Lavrentyev et al. 1995), which could also affect P dynamics. Although there was evidence of P limitation in Saginaw Bay throughout this period for the phytoplankton (Heath et al. 1995, Johengen et al. 1995), there was no evidence of P limitation in the benthic community until 1993. The periphytic diatoms seen in 1995 may become a more persistent part of the benthic algal community of Sagninaw Bay for a number of reasons. First, the filter-feeding zebra mussels are likely to have a negative impact on the tychoplanktonic diatom community as seen in 1991. Second, there is strong evidence to suggest that the zebra mussel densities have stabilized in Saginaw Bay after 1993 at a level that can still substantially affect the phytoplankton community (Nalepa et al. 1999). Third, reduced competition from the tychoplanktonic diatoms may allow blooms of Microcystis, which are resistant to zebra mussel grazing, to persist, which could decrease light penetration. Fourth, these conditions may favor periphytic diatoms because they are also resistant to zebra mussel grazing. In summary, the zebra mussel invasion coincided with large changes in the benthic algal community. Benthic algal dominance changed from tychoplanktonic diatoms (1991) to filamen-
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tous green algae (1992–1994) to periphytic diatoms (1995). Yearly nutrient-addition experiments did not produce major shifts in species composition. As dissolved P levels decreased, P became increasingly limiting for total benthic algal biovolume until 1995 when reductions in light may have limited growth. Nitrogen never limited benthic algal growth. The shifts in benthic algal community composition were consistent with changes in available light and zebra mussel filtering. The appearance of planktonic Microcystis blooms may regulate zebra mussel densities and help mediate the persistence of benthic algal communities dominated by periphytic diatoms. Acknowledgements This research was supported with grants from the Cooperative Institute for Limnology and Ecosystems Research, National Sea Grant, and Ohio Sea Grant. Ship time was provided in part by the US Environmental Protection Agency. Laboratory facilities were provided by the University of Michigan Biological Station, Great Lakes Environmental Research Lab, and Bowling Green State University. Steve Francoeur, Randy Litteral, Jerry Yotkois, Joanne Roehrs, Mike Roehrs, Vern Bingman, and Larry McDevitt assisted with SCUBA. Dave Szymanski and Donna Nicholson assisted with algal samples. Tom Nalepa and Tom Johengen provided the chemical data for the research site. Dennis Geniac provided a boat and expert guidance on the bay. Tom Nalepa provided valuable comments on an early draft of the manuscript. Literature Cited APHA (American Public Health Association). 1985. Standard methods for the examination of water and wastewater. 16th edition. American Public Health Association, American Water Works Association, and Water Pollution Control Federation, Washington, DC. BIERMAN, V. J., AND D. M. DOLAN. 1981. Modeling of phytoplankton-nutrient dynamics in Saginaw Bay, Lake Huron. Journal of Great Lakes Research 7:409–439. BIERMEN, V. J., D. M. DOLAN, AND R. KASPRZYK. 1984. Retrospective analysis of the response of Saginaw Bay, Lake Huron, to reductions in phosphorus loadings. Environmental Science and Technology 18:23–31.
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BRIDGEMAN, T. B., G. L. FAHNENSTIEL, G. A. LANG, AND T. F. NALEPA. 1995. Zooplankton grazing during the zebra mussel (Dreissena polymorpha) colonization of Saginaw Bay, Lake Huron. Journal of Great Lakes Research 21:567–573. CAIRNS, J., AND J. R. BIDWELL. 1996. Discontinuities in technological and natural systems caused by exotic species. Biodiversity and Conservation 5: 1085–1094. COTNER, J. B., W. S. GARDNER, J. R. JOHNSON, R. H. SADA, J. F. CAVALETTO, AND R. T. HEATH. 1995. Effects of zebra mussels (Dreissena polymorpha) on bacterioplankton: evidence for both size-selective consumption and growth stimulation. Journal of Great Lakes Research 21:517–518. ELTON, C. 1958. The ecology of invasions by animals and plants. Chapman and Hall, London, UK. FAHNENSTIEL, G. L., T. B. BRIDGEMAN, G. A. LANG, M. J. MCCORMICK, AND T. F. NALEPA. 1995a. Phytoplankton productivity in Saginaw Bay, Lake Huron: effects of zebra mussel (Dreissena polymorpha) colonization. Journal of Great Lakes Research 21: 465–475. FAHNENSTIEL, G. L., G. A. LANG, T. F. NALEPA, AND T. H. JOHENGEN. 1995b. Effects of zebra mussel (Dreissena polymorpha) colonization on water quality parameters in Saginaw Bay, Lake Huron. Journal of Great Lakes Research 21:435–448. FAIRCHILD, G. W., R. L. LOWE, AND W. B. RICHARDSON. 1985. Algal periphyton growth on nutrient-diffusing substrates: an in situ bioassay. Ecology 66: 465–472. FANSLOW, D. L., T. F. NALEPA, AND G. A. LANG. 1995. Filtration rates of zebra mussels (Dreissena polymorpha) on natural seston from Saginaw Bay, Lake Huron. Journal of Great Lakes Research 21:489– 500. GRAHAM, J. M., P. ARANCIBIA-AVILA, AND L. E. GRAHAM. 1996. Physiological ecology of a species of the filamentous green alga Mougeotia under acidic conditions: light and temperature effects on photosynthesis and respiration. Limnology and Oceanography 41:253–262. GRAHAM, J. M., M. T. AUER, R. P. CANALE, AND J. P. HOFFMANN. 1982. Ecological studies and mathematical modeling of Cladophora in Lake Huron. 4. Photosynthesis and respiration as functions of light and temperature. Journal of Great Lakes Research 8:100–125. GRIFFITHS, R. W. 1993. Effects of zebra mussels (Dreissena polymorpha) on the benthic fauna of Lake St. Clair. Pages 417–437 in T. F. Nalepa and D. W. Schloesser (editors). Zebra mussels: biology, impacts, and control. Lewis Publishers, Ann Arbor, Michigan. HEATH, R. T., G. L. FAHNENSTIEL, W. S. GARDNER, J. F. CAVALETTO, AND S. HWANG. 1995. Ecosystem-level effects of zebra mussels (Dreissena polymorpha):
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