INDEX WORDS: Zooplankton, phytoplankton, Lake Erie, bivalves, grazing.

Transcription

1 J. Great Lakes Res. 17(4): Internat. Assoc. Great Lakes Res., 1991 Zooplankton Grazing and Phytoplankton Abundance: An Assessment Before and After Invasion of Dreissena Polymorpha Lin Wu and David A. Culver Department of Zoology 1735 Neil Avenue The Ohio State University Columbus, Ohio Abstract. The introduction of the zebra mussel Dreissena polymorpha into Lake Erie raises the question of whether it competes with the existing zooplankton community for phytoplankton. In this study, we approached this question by examining the role of zooplankton grazing in influencing Lake Erie abiotic conditions and biotic interactions during 2 years of varying zebra mussel abundances. In situ grazing experiments ( 32 P-labeled yeast cells) revealed that cladoceran species contributed >85% of zooplankton community grazing rate, whereas copepods accounted for <15%. The western basin of the lake had the highest grazing pressure on phytoplankton populations because its zooplankton community was dominated by cladocerans. Therefore, we developed filtering rate: body length models for the two most important cladoceran species, Daphnia galeata mendotae and D. retrocurva, in western Lake Erie to estimate grazing rates from body size distribution and abundance. The peak Daphnia grazing rates (>200 ml L -1 d -1 ) calculated from the models between June and early July coincided with the high Secchi transparencies found during these periods (clearwater phase) in both the year with few zebra mussels (1988) and the year with abundant mussels (1989). The impact of Daphnia grazing on the phytoplankton community is negative, directly reducing edible algal volume to <5 ml m -3. The release of Daphnia grazing pressure in August was followed by an increase in edible phytoplankton in both nearshore and offshore areas of both years. High edible algal volumes and low Secchi transparencies in August were in contrast to what we would expect if adult zebra mussels that were present throughout 1989 or veligers that were abundant in late July and August were able to overgraze phytoplankton. We concluded that the pulsed Daphnia grazing still controlled edible algal density and water transparency in 1989, even though Dreissena polymorpha was abundant in the lake in INDEX WORDS: Zooplankton, phytoplankton, Lake Erie, bivalves, grazing. Introduction In lake ecosystems, herbivorous zooplankton such as cladocerans, some copepods, and rotifers selectively consume phytoplankton and hence directly contribute to a phytoplankton seasonal succession. Studies from European lakes (Lampert 1978, Lam-pert et al. 1986, Sommer et al. 1986) suggest that, in meso- and eutrophic lakes, zooplankton undergo a spring population bloom and then a midsummer decline. A spring maximum of zooplankton grazing causes a clear-water phase and initiates phytoplankton succession toward large algal species during summer. However, in Lake Erie, the most productive lake in the Great Lakes of North America, few studies have examined the role of zooplankton grazing. This is mainly due to difficulties in determining filtering rates of zooplankton species in the field and to inadequate sampling of the rapid turnover of zooplankton and phytoplankton populations in large lakes. For example, there is no documentation in the literature on effects of zooplankton grazing on Lake Erie's water transparency and phytoplankton communities. A newly introduced bivalve, Dreissena polymorpha, became abundant in 1989 in western Lake Erie after they were first found in 1988 (D. Garton, The Ohio State University, personal

2 communication). Adults of this European zebra mussel spawn once per year in late August in western Lake Erie (W. Haag and D. Garton, The Ohio State University, personal communication), and there is a planktonic veliger larval stage before settling. Larvae prefer to settle on hard substrates (Lewandowski 1982). Both adult mussels and veliger larvae feed on suspended food particles by filtering lake water (Stanczykowska 1977). An adult mussel's ability to filter large volumes of water (9 L ind -1 d -1 ) (Reeders et al. 1989) has led to some speculation that the mussel might overgraze phytoplankton and thus could be used to increase water clarity of the lake. However, this hypothesis can not be tested by following phytoplankton abundances in the lake without understanding the impact of resident zooplankton on the lake's phytoplankton communities, particularly when the grazing ability of these mussels in western Lake Erie is unknown. In this study, we took advantage of zooplankton and phytoplankton abundance data before and after zebra mussels became abundant. We first quantified zooplankton grazing activities as a function of body size and abundance in Lake Erie. We then evaluated relationships between zooplankton grazing and water transparency and phytoplankton dynamics in the western basin. Finally, we estimated the potential impact of zebra mussels on water transparency and the phytoplankton community in western Lake Erie by comparing zooplankton grazing and phytoplankton data before (1988) and after (1989) zebra mussels became abundant. Materials and Methods Grazing Experiments We measured in situ zooplankton community grazing rates and individual filtering rates from 11 to 13 August 1987, using Haney's technique (Haney 1973) at single locations in the eastern basin (N 42 29' 52", W 79 53' 58"), central basin (N 41 55' 35", W 81 39' 43"), and western basin (N 42 35' 45", W 81 54' 30") of Lake Erie. Experiments were conducted between 1300 and 1500 h in the eastern and central basins and h in the western basin. 2-mL 32 P-labeled yeast (Rhodotorula) cells (7-µm mean diameter) were added to a tiny container suspended in the grazing chamber. Our chamber was 10 L and was closed at depth (average 7.5 m in the eastern basin, 5 m in the central and western basins) with a messenger that simultaneously released the radioactively labeled foods. After allowing zooplankton 10-min feeding, we retrieved the chamber and filtered the contents through a 64-µm net. To determine the whole zooplankton community grazing rate, we preserved all zooplankton collected by the net with a sucrose formalin solution and determined 32 P activities. A 1-mL filtrate was also collected to determine food activity in the grazing chamber. Experiments were repeated seven, six, and five times for the eastern, central, and western basins, respectively. Individual species filtering rates were obtained by immediately (within 2 h) sorting various zooplankton species under a dissecting microscope and transferring them into scintillation vials with fluor for radioisotopic analysis. Because zooplankton body size has been the most important characteristic associated with the individual filtering rates (Peters and Downing 1984, Knoechel and Holtby 1986), we measured Daphnia galeata mendotae and D. retrocurva before placing them individually into vials. Daphnia specimens were measured from the anterior end of the head to the base of the spine (to nearest 0.02 mm). For other species, we placed known numbers of individuals into each vial to calculate mean individual filtering rates (ml ind -1 d -1 ). Radioactivity was measured on 16 August 1987, in the laboratory of the National Water Research Institute, Burlington, Ontario, Canada. Grazing Rate Calculations Zooplankton grazing activities in this study were expressed as filtering rate, grazing rate, and clearance rate. Filtering rate is defined as the volume of water containing food particles filtered by an individual organism per day (ml ind -1 d -1 ), grazing rate is the filtering activity of groups of organisms per day (ml L -1 d -1 )> and clearance rate is the per cent of water cleared (or filtered) per day (Haney 1973).

3 Daily community grazing rate (GR) was calculated based on the whole zooplankton community filtering activity (disintegrations per minute, DPM) and exposure time to the food in the chamber: The individual filtering rate (FR) was calculated for individual animals as: Western Basin Field Sampling, During June through August, zooplankton were collected weekly by duplicate sampling with a metered 0.5-m diameter net of 112 µm mesh size towed vertically through the whole water column from two sites (about 740 m apart) both in a near-shore area (N 41 33' 53", W 82 47' 56") and in an offshore area (N 41 38' 67", W 82 46' 44") of the western basin of Lake Erie. Nearshore (6 m deep) and offshore (10 m deep) stations were 9.38 km apart. While these samples were not collected for the purpose of studying zebra mussels, the 2 years had greatly different abundances of adult mussels and veliger larvae and thus allowed us to examine their potential impact. We made no estimates of adult zebra mussel abundance, but recorded veliger density from our zooplankton samples. Samples were preserved immediately with a sucrose-formalin solution (40 g sucrose L -1 ) and analyzed in the laboratory. Subsamples were taken until at least 20 individuals of each abundant taxon per sample were measured using an ocular micrometer (to the nearest 0.02 mm). Cladoceran species were measured from the anterior end of the head to the base of the spine; copepods were measured from the top of the head to base of the caudal rami. All zooplankton found in each subsample were counted to determine population abundances (# L -1 ). Biomass (µg L -1 ) of each taxon was estimated as a product of its mean dry weight and abundance for each sample. Dry weights (µg) were calculated based on length and weight regressions (Culver et al. 1985). To determine algal dynamics, two integrated water samples were also collected weekly in both nearshore and offshore areas during June through August in 1988 and 1989, using a 5- cm diameter PVC pipe (3-m length). The water samples were taken by lowering the PVC pipe vertically into the water, corking the pipe, withdrawing it, and emptying the water into a 10 L bucket. One 150 ml water subsample from the bucket was then taken and preserved with a Lugol's solution and concentrated by settling for a week in 250-mL graduate cylinders. Phytoplankton in at least two replicate transects across a Utermohl chamber were identified and counted under an inverted microscope for each settled algal sample (average 372 cells/sample counted). Phytoplankton were grouped into edible and inedible algae based on anticipated ease of consumption by Daphnia. Algae classified as "edible" included flagellates, small diatoms, and nonfilamentous green algae; "inedible" were filamentous diatoms and greens, spiny greens, and bluegreen algae. Volumes of edible and inedible phytoplankton were calculated from equations based on geometric dimensions (length, width, and depth) measured for each individual species. Algal volume (ml m -3 ) was estimated based on the volume calculations. Daphnia Filtering Rate Estimation We developed filtering rate:body length regression models so that we could calculate singlespecies filtering rates using size measurements obtained from the field samples. Because the relationship between individual filtering rate and body length is a power function (Knoechel and Holtby 1986), log-transformed filtering rate and body length were used when analyzing the relation between these two parameters by linear regression analysis. D. g. mendotae and D. retrocurva are the dominant herbivorous cladoceran species during summer in the western basin of Lake Erie (Wu and Culver, unpublished data); thus filtering rate: body length models were developed only for these two species.

4 We then used the coefficients obtained for the two Daphnia species in the western basin in 1987 and body size distribution measurements obtained from 1988 and 1989 zooplankton samples to estimate western basin Daphnia individual filtering rates for each individual measured for length in 1988 and 1989 samples. These individual filtering rates (ml ind -1 d -1 ) were then averaged and multiplied by abundances of these two taxa (# L -1 ) estimated from 1988 and 1989 zooplankton samples to give estimates of grazing rates (ml L -1 d -1 ) by each Daphnia species. The grazing rates of the two Daphnia species were then added together to obtain Daphnia community grazing rates in the western basin for each sampling date in 1988 and We compared these Daphnia grazing rates with seasonal patterns of water clarity and algal volume for 1988 when zebra mussels were rare and when they were abundant. Results Zooplankton Grazing in Three Basins, 1987 In situ zooplankton community grazing rates estimated from the grazing chamber were higher in the western basin than those in the central and eastern basins (t-test, P < 0.01) (Fig. 1). The central basin and eastern basin community grazing rates, however, did not differ (t-test, P > 0.05). 68% of zooplankton community was composed of cladoceran species in the western basin. In contrast. >80% of zooplankton in the central and eastern basins were copepod species (Table 1). Moreover, >85% of community grazing was due to cladoceran grazing in all three basins while copepod species contributed < 15% of the community grazing (Table 1). D. g. mendotae in the western basin had a higher filtering rate than similar sized individuals of the same species in the central and eastern basins (ANCOVA, P < ) (Fig. 2A), but the filtering rate in the central basin did not differ from that in the eastern basin for this species (ANCOVA, P > 0.87) (Fig. 2B & C). We found a significant positive relationship between the filtering rate (ml ind -1 d -1 ) and body length (mm) for D. g. mendotae in the western basin (F = 9.99, P < ) and central basin (F = 13.03, P < 0.001) (Fig. 2A & B), but the relationship was not significant for D. g. mendotae in the eastern basin (F = 0.56, P > 0.46) (Fig. 2C). No comparison was made for the grazing rate by D. retrocurva among basins because we did not measure individual sizes in central and eastern basins.

5 Daphnia Grazing, Water Transparency, and Phytoplankton, D. g. mendotae reached its maximum biomass between 20 June and 11 July both years (Fig. ЗА & В), except that there was a decline on 6 July D. retrocurva, on the other hand, was only abundant in early June in the western basin of Lake Erie (Fig. 3C & D). The calculated Daphnia 1988 and 1989 community grazing rates (D. g. mendotae and D. retrocurva) using the coefficients a and b obtained from 1987 experiments for the western basin (Table 2) peaked between June and July and decreased to a minimum in August in both nearshore and offshore areas (Fig. 4A & B). Maximum rates were equivalent to filtering the full volume of the lake every 1.2 to 7 days (1/855 to 1/140 ml L -1 d -1 )-High Secchi transparency indicative of low algal abundance often corresponded to periods of maximum grazing rates. A decreased Secchi transparency (Fig. 4C & D) in August coincided with the decreased Daphnia grazing rates in both nearshore and offshore areas of both years, though the decline nearshore was not as obvious as that offshore. For both 1988 and 1989, edible phytoplankton volume was reduced below 5 ml m -3 during the high Daphnia grazing period in the nearshore and the offshore (Fig. 5A & B) of the western basin, and increased in August when the grazing pressure was minimum. But the increase of edible algal volume was lower in 1989 than that of 1988 in August in both sampling areas. The volume of inedible phytoplankton in 1988 started to increase in July and remained until early August (Fig. 5C & D, dash-dotted lines). Similar peaks of inedible algal volume occurred in 1989 (Fig. 5C & D, solid lines) but were much lower than those in To further quantify how phytoplankton and Secchi transparency were related to Daphnia grazing rates, we regressed the edible algal volumes and transparencies on grazing rates during June through August, 1988 and 1989 (Fig. 6, nearshore and offshore pooled). During both years edible algae decreased as the grazing rate increased (Fig. 6A & B; linear regression); conversely, water transparencies increased as the grazing rate increased (Fig. 6C & D). Veliger Larval Abundance As discussed earlier, we have no estimates of adult mussel abundances. However, veliger larvae from zooplankton hauls in 1989 were significantly more abundant than in 1988 (Fig. 7). Peak abundance occurred during late July and August in our western basin sampling areas, in contrast to Daphnia that reached its population peak before mid-july.

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7 Zooplankton Grazing Discussion Herbivorous cladocerans, particularly of the genus Daphnia, determine the grazing pressure in Lake Erie whereas copepod species contribute little to the grazing activity. Via the in situ grazing experiments, we demonstrated that the grazing rate was the highest in the western basin, in which cladoceran species dominated the zooplankton community. Previous work also suggests that the lakes with cladoceran domination have higher grazing rates than those dominated by copepods (reviewed by Lampert 1988) and rotifers (Haney 1973). Not only is the cladoceran abundance important, the size of cladoceran species also plays a crucial role in determining zooplankton community grazing pressure. Large-bodied Daphnia species often contribute most of the grazing activity (Haney 1973, Lampert and Taylor 1984, Shapiro and Wright 1984, Jarvis 1986), whereas grazing pressure by small cladocerans (e.g., Bosmina) and copepods is relatively low (Bogdan and Gilbert 1982, Gulati 1975, Zankai and Ponyi 1986). Our results from the grazing experiments also confirm that large cladocerans contributed >85% of the grazing rates measured in all three basins of Lake Erie. Thus our estimation of 1988 and 1989 grazing pressure solely from Daphnia grazing values should be representative of the zooplankton grazing activity in the western basin, given that Daphnia species were the dominant large cladocerans in the western basin.

8 We further demonstrated that individuals of the same species could have different filtering abilities in different habitats. D. g. mendotae in the western basin had significantly higher individual filtering rates than those of the same species in the central and eastern basins. The western basin is the most eutrophic part of Lake Erie (Hayward and Margraf 1987). Although community grazing rates reported from various systems show no association between the grazing levels and lake trophy (reviewed by Sterner 1989), Lampert (1988) suggested that the zooplankton individual ingestion rate for particles < 33 µm increases as lake trophic status increases. We believe the difference in Daphnia individual filtering rates in this study is most likely caused by the difference in algal abundances between western and central/ eastern basins. To compare our results with those from the filtering rate: body length regression equation (F = L 2.48 ) developed by Knoechel and Holtby (1986), we used their coefficients and our Daphnia size measurements to calculate individual filtering rates. Their model yields a 20-50% higher individual Daphnia filtering rate for the western basin of Lake Erie than the models developed in the present study. Low individual filtering rates measured may be caused by 32 P losses between preservation and picking specimens for 32 P analysis (Holtby and Knoechel 1981), but we picked animals for individual filtering measurements within 2 h of preservation. Though we did not have algal data from the period of grazing experiments (11-13 August) in 1987, our 1988 and 1989 phytoplankton data from the western basin showed that inedible algae (mostly Anabaena) volume was below 5 ml m -3 in August, indicating that interference of blue-green algae, e.g., Anabaena, during the experiments (Chow-Fraser and Sprules 1986) might not be a factor. We believe the relatively high grazing rates estimated from Knoechel and Holtby's (1986) regression model are because their regression includes a broad range of cladoceran taxa. Had they reported regressions for an individual taxon, their results might have been more like ours. Effect of Daphnia and Dreissena polymorpha on Phytoplankton Abundance When Daphnia becomes sufficiently abundant, it overgrazes phytoplankton, causing a clearwater phase as well as a shift in algal community to dominance by inedible species (Lampert et al. 1986, Sommer et al. 1986). In western Lake Erie, the high Daphnia abundance between June and early July corresponded with an increased Secchi transparency during that period in both years, especially in the offshore. The smaller change in Secchi transparency (i.e., a decreased number of particles in the water column) in the nearshore is likely due to turbidity caused by wave disturbance of sediments in this shallow area, to silt contained in the Maumee River inflow, and to boat traffic in that area during summer. Edible phytoplankton was depressed (< 5 ml L -1 ) when Daphnia grazing activity was high, and became more abundant when Daphnia grazing was the lowest. Grazing by herbivorous zooplankton (e.g., Daphnia), however, did not lead to a dominance of inedible algae in the phytoplankton community in the western basin, although inedible algal volume did increase. Sterner (1989) also suggested that inedible species dominance is not always associated with high grazing rates, unless inedible species are superior competitors in the presence of grazing. The pulsed Daphnia grazing was significantly correlated with declining edible algal volumes and increasing water transparencies in both 1988 and 1989, suggesting that Daphnia grazing alone during both years was sufficient to overgraze edible phytoplankton and to result in a clear-water phase in western Lake Erie. If adult zebra mussels were responsible for the

9 edible algal dynamics and Secchi change in western Lake Erie, we would expect a longer clear-water period in 1989 because adult mussels continued to be abundant in the bottom of the lake through the year, while Daphnia had declined. On the contrary, the Secchi transparency decreased in August of both years corresponding temporally to a period of low Daphnia grazing. Moreover, the dynamic patterns of edible algal volumes were similar between 1988 and 1989: relatively low during high Daphnia grazing periods, and high after the release of grazing pressure. In August 1989, not only were adult zebra mussels present, but veliger larvae also reached maximum abundances in western Lake Erie. However, the grazing pressure by veliger larvae was much lower than Daphnia grazing activity. When we used the minimum (0.09 mm) and maximum (0.31 mm) sizes of veliger larva found from our 1989 samples, the filtering rate: body size regression model developed by Knoechel and Holtby (1986), and our maximum veliger abundance (100 L -1 ), we obtained grazing rates by veliger larvae ranging from 2.9 to 64 ml L -1 d -1, whereas Daphnia grazed >200 ml L -1 d -1 in early summer. These are very liberal estimates of grazing rates because veliger larvae probably have grazing rates more like rotifers than like cladocerans. Even so, the veliger larval grazing rates calculated were too low to effectively reduce algal abundances and consequently to influence water clarity.

10 The results of the present study demonstrated strong correlations between Daphnia grazing and edible algal dynamics and Secchi transparency in years before and after zebra mussels became abundant in western Lake Erie. The presence of adult mussels throughout summer of 1989 did not lead to a prolonged high Secchi transparency in the lake. However, density of adult mussels may be patchy in Lake Erie because zebra mussels prefer hard or vegetated substrates for settlement (Stanczykowska 1977); but much of the western basin has muddy bottom and the shoreline is not covered by vegetation. Accordingly, the impact of zebra mussels on pelagic communities may be patchy as well. Therefore, in addition to the studies on filtering ability of zebra mussels (both particle size and type), more information is needed on estimation of population numbers and their dynamics in the western Lake Erie. Finally, grazing by Daphnia, especially before August, cannot be ignored when assessing the impact of Dreissena polymorpha on the phytoplankton community and upon lake clarity.

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12 Acknowledgments We thank D.R.S. Lean, National Water Research Institute, Burlington, Ontario, Canada, for preparing radioactively labeled foods and for the help with the radioisotopic analysis. We thank the National Water Research Institute for the opportunity to perform our grazing experiments on the R/ VLIMNOS. This work is also a result of research sponsored (in part) by the Ohio Sea Grant Program, project #R/ER-8 under grant #NA84AA-D-00079, the National Sea Grant College, National Oceanic and Atmospheric Administration, U.S. Department of Commerce, and from the State of Ohio, and the Instruction and Research Computer Center of the Ohio State University.