Temporal Trends in Lake Erie Plankton Biomass - University of ...

J. Great Lakes Res. 31(Suppl. 2):89–110Internat. Assoc. Great Lakes Res., 2005Temporal Trends in Lake Erie Plankton Biomass:Roles of External Phosphorus Loading and Dreissenid MusselsJoseph D. Conroy 1,* , Douglas D. Kane 1 , David M. Dolan 2 , William J. Edwards 3 ,Murray N. Charlton 4 , and David A. Culver 11 Department of Evolution, Ecology, and Organismal BiologyThe Ohio State UniversityColumbus, Ohio 432102 Department of Natural and Applied SciencesUniversity of Wisconsin–Green BayGreen Bay, Wisconsin 543113 Department of BiologyNiagara UniversityLewiston, New York 141094 National Water Research InstituteEnvironment CanadaBurlington, Ontario L7R 4A6ABSTRACT. We compare the results of lakewide plankton studies conducted during 1996–2002 withdata reported in the literature from previous years to evaluate the effectiveness of continued nutrient control,the relationship between external phosphorus loading and plankton abundance, and the many predictedoutcomes of the dreissenid invasion. We found that although recent external annual phosphorusloading has not changed since reaching mandated target levels in the early- to mid-1980s, phytoplanktoncommunities have. Total phytoplankton biomass, measured through enumeration and size-frequency distributions,has increased since minima were observed in 1996 or 1997, with summer (July–September)biomasses generally greater than before the dreissenid establishment in the late 1980s. Cyanobacteriabiomass also increased during summer in all basins after the dreissenid invasion. In contrast, chlorophylla concentration has decreased in all basins during both spring and summer. However chlorophyll a concentrationwas poorly correlated with total phytoplankton biomass. Relative to the mid-1980s, crustaceanzooplankton biomass during the years 1996–2002 increased in the western basin during spring and summer,increased in the central basin during spring but remained the same during summer, and decreasedto low levels in the eastern basin. Several of these observations are consistent with predictions made byprevious researchers on the effects of reduced total external phosphorus loading and the stimulatory orinhibitory effects of dreissenid mussels. However, several were not. Results from this study, particularlythe inconsistencies with tested predictions, highlight the need for further research into the factors thatregulate plankton community dynamics in Lake Erie.INDEX WORDS:Lake Erie, plankton, chlorophyll, phosphorus, eutrophication, Dreissena.INTRODUCTION* Corresponding author. E-mail: conroy.27@osu.eduOver the past 30 years, the Lake Erie ecosystemhas dramatically changed. During the late 1960sand early 1970s, much international effort went intosampling and quantifying Lake Erie system parametersin order to understand how cultural eutrophicationhad impacted its function (Burns and Ross1972). With the passage of the Great Lakes WaterQuality Agreement (GLWQA) of 1972 and its revisionin 1978, reduced phosphorus load from municipalsources was predicted to lead to a reduction inthe total algal biomass, the incidence and extent of89

90 Conroy et al.harmful algal blooms (e.g., cyanobacterial blooms),and the frequency and duration of central basin hypoxia/anoxia(McGucken 2000, Beeton 2002). Asannual phosphorus loads to Lake Erie decreased inthe mid-1980s (Dolan 1993), decreased total phytoplanktonbiomass and a reduction in the abundanceof eutrophic indicator species (e.g., Aphanizomenonflos-aquae) suggested that Lake Erie water qualitywas indeed improving (Makarewicz 1993a). However,central basin hypolimnetic dissolved oxygenconcentrations continued to show hypoxia (concentrations< 4 mg L –1 ) during late summer (Charltonet al. 1993). More recent investigations reportedthat the frequency of cyanobacterial blooms was increasing(Vanderploeg et al. 2001, Budd et al.2001, Vincent et al. 2004, Conroy and Culver2005), suggesting that Lake Erie was returning tomore eutrophic conditions. Concomitantly, stillother researchers observed decreases in phytoplanktonbiomass (measured as chlorophyll a concentration)in the central and eastern basins (Matisoff andCiborowski 2005) with increasing total phosphorusconcentrations (Charlton and Milne 2004). Accordingly,the Lake Erie Trophic Status (LETS) studywas initiated in 2002 as a partnership between researchersfrom Canada and the United States underthe sponsorship of Environment Canada and theUnited States Environmental Protection Agency toinvestigate these seemingly contradictory phenomena(Matisoff and Ciborowski 2005).One of the main goals of GLWQA was to preventgrowth of nuisance algae (Koonce et al. 1996). Becausephosphorus is usually the growth-limiting elementin freshwater systems (Schindler 1974),external phosphorus loading to Lake Erie needed tobe reduced in order to accomplish this goal. Over$8 billion (USD, adjusted to 1990) has been spenton building and updating sewage treatment plantsalone (USEPA 2004). Millions (or billions) of dollarsmore have been spent on research, outreach,and implementation of new technologies to reduceexternal phosphorus loading to Lake Erie(McGucken 2000). During most years since theearly 1980s, these measures have worked to bringexternal phosphorus loading to Lake Erie below the11 kilotonne year –1 target load established byGLWQA (Dolan 1993, Dolan and McGunagle2005). Because successfully reducing externalphosphorus loading to Lake Erie was so expensive,it is important to ask whether the reductions haveled to reduced nuisance algal growth.The establishment of Ponto-Caspian zebra (Dreissenapolymorpha, Hebert et al. 1989) and quaggamussels (D. bugensis, May and Marsden 1992) in thelate 1980s, hereafter collectively referred to as dreissenids,signified another possible explanation for decreasingphytoplankton standing stock. As voraciousfilter feeders, these mussels were initially hypothesizedto be able to filter enough water to potentiallydeplete phytoplankton standing stocks (MacIsaac etal. 1992). Nearshore Secchi transparency increasesin the early 1990s (Holland 1993) provided indirectevidence for a reduction of phytoplankton communities.Removal of large amounts of phytoplanktoncould potentially reduce zooplankton standingstocks, possibly harming the productive lake fisherythrough reduction in food resources for young-ofthe-yearfish (MacIsaac 1996).Conversely, dreissenids may stimulate phytoplanktonstanding stock and productivity throughnutrient remineralization, i.e., conversion of ingestedparticles into soluble nutrients (Heath et al.1995, Arnott and Vanni 1996, Conroy et al. 2005a),and/or selective filtration of some algal taxa (Vanderploeget al. 2001, 2002). The remineralization ofammonia-nitrogen and phosphate-phosphorus(Heath et al. 1995, Arnott and Vanni 1996, Conroyet al. 2005a) may be especially important. Conroyet al. (2005a) compared estimated dreissenid communityexcretion with that of the zooplankton communityat a nearshore station in the western basin ofLake Erie, and found that dreissenids added approximately50 mg m –2 d –1 of ammonia-nitrogen (twicethat of the crustacean zooplankton community) and3 mg m –2 d –1 of phosphate-phosphorus (one-quarterof the crustacean zooplankton community). Becausethe nitrogen:phosphorus ratio of excreted nutrientswas below Smith’s (1983) threshold (29:1 bymass) said to favor cyanobacterial growth (Arnottand Vanni 1996, Conroy et al. 2005a), dreissenidsmay facilitate growth of these phytoplankton taxathroughout the western basin and in nearshore areaswhere physical mixing rates are high (Conroy et al.2005a). Vanderploeg et al. (2001) performed dreissenidfiltration experiments with various combinationsof natural seston and culture media and foundthat dreissenids selected against ingestion of Microcystisspp. from Lake Erie but selected for a Microcystisstrain from a laboratory culture (their Fig. 4).In this same study, they found that dreissenids selectedfor phytoplankton mixtures containing cryptophytes.The balance between stimulatory andinhibitory effects of dreissenids on various phytoplanktontaxa has not been fully elucidated, butboth effects likely dominate at different times andin different locations.

Temporal Trends in Lake Erie Plankton Biomass 91TABLE 1. Literature-derived proposed effects of dreissenids on Laurentian Great Lake total phytoplanktonbiomass, cyanobacterial biomass, and/or chlorophyll a concentration. A downward pointing arrowindicates a negative relationship was proposed; an upward pointing arrow, a positive relationship; a zero,no relationship was found; and, a dash, a relationship was not proposed.Dreissenid effect onTotal Phytoplankton Chlorophyll a CyanobacteriaStudy Spring Summer Spring Summer Spring SummerVanderploeg et al. 2001, 2002 ↓ ↑ — — — ↑Barbiero and Tuchman 2004b WB — — ↓ ↓ — —CB — — 0 ↓ — —EB — — 0 ↓ — —Makarewicz et al. 1999* WB ↓ ↓ ↓ 0 ↑ ↓CB ↑ 0 ↑ 0 ↑ 0EB 0 0 0 0 ↓ 0Conroy et al. 2005a ↑ ↑ 0 0 ↑ ↑Hecky et al. 2004 @ ↑ ↑ 0 0 0 0↓indicates a proposed negative effect, ↑ a proprosed positive effect, 0 no effect, — relationship not given, * proposedeffect for the offshore only, @ nearshore onlyVanderploeg et al. (2002), supported by severalyears’ worth of data from Saginaw Bay (their Fig.6b), proposed that during the spring, dreissenidsfreely grazed phytoplankton, reducing total phytoplanktonbiomass. However, during summer, dreissenidswere unable to control cyanobacterialblooms due to selective filtration against cyanobacteriaand, consequently, total phytoplankton biomassincreased. In direct contrast to their study,Barbiero and Tuchman’s (2004b) multi-year(1983–2004) study of water clarity throughout LakeErie before and after the dreissenid invasion foundthat transparency decreased in the western and centralbasins and increased in the eastern basin duringspring after dreissenids arrived and increased in thecentral basin but remained the same in the westernand eastern basins during summer in years withdreissenids present. However, Barbiero and Tuchman(2004b) found chlorophyll a concentrationssignificantly decreased in the western basin duringspring, supporting Vanderploeg et al.’s (2002) findings,yet concentrations decreased in all threebasins in summer, conflicting with Vanderploeg etal.’s findings. Makarewicz et al. (1999) comparedphytoplankton biomass from before (1983–88/9)and after (1989/90–93) dreissenid establishment inLake Erie and found both increases and decreasesin total phytoplankton biomass, cyanobacterial biomass,and chlorophyll a concentration, dependingon the basin and season (spring or summer) beinginvestigated. Hecky et al. (2004) have observednearshore benthic algal increases in the late 1990sthat they attributed to dreissenid re-engineering ofenergy and nutrient flow in the nearshore benthos, aphenomenon that they termed the “nearshoreshunt.” We have summarized the effects of dreissenidson total phytoplankton biomass, cyanobacteriabiomass, and chlorophyll a concentrationsproposed in the literature reviewed above (Table 1).The resultant effect of purported dreissenid-mediatedchanges to the phytoplankton community onthe crustacean zooplankton community could be eitherstimulatory or inhibitory, depending onwhether dreissenid mussels decreased or increasedphytoplankton biomass and whether their activityincreased the abundance of cyanobacteria. Furthermore,if dreissenid mussels directly compete withzooplankton for phytoplankton, we would expectdecreased crustacean zooplankton abundance(MacIsaac 1996). However, low turbulent mixingrestricts adult dreissenids’ ability to affect planktoncommunities to shallow, well-mixed areas (Yu andCulver 1999, Ackerman et al. 2001, Noonburg etal. 2003, Edwards et al. 2005), so it is unreasonable

92 Conroy et al.to expect persistent declines in offshore phytoplanktonand zooplankton to be associated withdreissenid grazing in large lakes.We combined recent lake-wide plankton surveydata with historical data to investigate whether thechronological pattern of phytoplankton and zooplanktonchanges in Lake Erie can be better explainedby observed changes in phosphorus loadingor by the establishment of dreissenid mussels in thethree basins of Lake Erie. In particular, we askedwhether or not plankton populations have continuedto decrease in concert with phosphorus loading controls,to determine whether estimated annual totalexternal phosphorus load to Lake Erie is a goodpredictor of plankton biomass, and to test publishedpredictions of the role of invasive dreissenid filterfeeders on phytoplankton community abundanceand composition. We tested whether (1) phytoplanktonbiomass (characterized by wet mass andchlorophyll a) in the western, central, and easternbasins were indeed at their historical minima in2002; (2) Lake Erie plankton biomass is directlycorrelated to annual estimated phosphorus loading;and, (3) phytoplankton and zooplankton abundancepatterns during spring and summer are consistentwith stimulatory or inhibitory effects of dreissenidmussels as proposed by previous studies (Table 1).The overall goal of this study is to better understandLake Erie plankton abundance as predicted by nutrientloading and how it may be affected by awidespread, invasive filter feeder.METHODSWe combined our recent measures of phytoplanktonbiomass (1996–2002; Conroy et al. 2005b) withthose of Munawar and Munawar (1976), DeVaultand Rockwell (1986), Makarewicz (1993a), andMakarewicz et al. (1999), our chlorophyll a concentrationdata with those of Glooschenko et al.(1974) and Makarewicz et al. (1999), and our zooplanktonbiomass data with those of Watson (1976),Watson and Carpenter (1974), Bean (1980),Makarewicz (1993b), and Weisgerber (2000), andcompared all of them with estimates of annual totalexternal phosphorus load to Lake Erie (Dolan 1993,Dolan and McGunagle 2005). Integrating manydatasets in this manner allowed us to examine atime period extending from the period of greatestcultural eutrophication in Lake Erie (1970), throughphosphorus load reductions (mid-1980s) and the establishmentof dreissenids (late 1980s and early1990s), and into recent years (late 1990s and early2000s). Unfortunately, the assembled planktondataset is neither continuous (there are large gapsbetween sampling years) nor were the same sitesvisited at the same times in each year. To controlfor these shortcomings, we have tried to draw datafrom as many different sources as possible, havesplit the available data into spring and summer periodsfor the various studies, and have used severalmeasures of central tendency (arithmetic and geometricmeans and medians) and data dispersion(standard deviations and quartiles) to better understandthe inherent variability in seasonal planktondata. Total phosphorus loading estimates are basedon Dolan (1993) and Dolan and McGunagle (2005),and include contributions from monitored and unmonitoredtributaries, atmospheric deposition, directindustrial and municipal point sources, andinput from Lake Huron. Below, we more fully describeour recent plankton dataset and the sourcesof the historical plankton data.Sampling PeriodLEPAS—The Lake Erie PlanktonAbundance StudySince 1995, an international, multi-agency, intensivesampling program (LEPAS) has been conductedto determine the abundance and biomass ofphyto- and zooplankton along with chlorophyll aconcentration, water temperature, water columndissolved oxygen concentration, and Secchi depththroughout Lake Erie (Fig. 1). Semi-monthly sampleshave generally been collected annually fromMay through September (Table 2; 1995 data are notincluded in this manuscript because sampling extendedonly through late June in that year). Allsamples were taken by personnel from the Ohio Divisionof Wildlife Fisheries Research Units (Sanduskyand Fairport Harbor, Ohio), the NationalWater Research Institute (Burlington, Ontario,Canada) or the Ontario Ministry of Natural Resources(Wheatley, Ontario, Canada). Regular annualsampling was supplemented in June, July,August, and September 2002 by cruises aboard theUSEPA’s R/V Lake Guardian to better connect withother analyses being performed for the Lake ErieTrophic Status study (this volume).Field MethodsPhytoplankton and chlorophyll a samples weretaken from an integrated water column sampleusing a tube sampler (2.5-cm ID polyvinyl chloride

Temporal Trends in Lake Erie Plankton Biomass 93FIG. 1. Lake Erie Plankton Abundance Study collection sites, 1996 through 2002. Open andclosed circles show sampling locations of the Sandusky and Fairport Fishery Research Units ofthe Ohio Department of Natural Resources, Division of Wildlife, respectively; stars show sitessampled by the National Water Research Institute; and, crosses show sampling locations fromthe Lake Erie Trophic Status Project. Note: Not all sites were sampled in all years.pipe or vinyl tube) to twice the Secchi depth. Supplementalsampling in 2002 aboard the R/V LakeGuardian used combined surface and bottom of theepilimnion (as defined by in situ SeaBird CTDtraces) water samples instead of the integrated tubesampler for phytoplankton and chlorophyll a. Watercolumn samples were dispensed into a bucket fromwhich integrated individual phytoplankton andchlorophyll a samples were taken and immediatelypreserved. For phytoplankton, a 500-mL subsamplewas preserved with Lugol’s solution; for chlorophylla samples, at least a 1,000-mL subsample wastaken and stored on ice in an amber Nalgene bottle,filtered through a Whatman GF/C (1.2-µm nominalpore size) filter, and frozen in light-proof containersfor later chlorophyll a determination.Zooplankton was sampled by vertically towing afront-weighted zooplankton net (0.5 m diameter, 64µm mesh) fitted with a General Oceanics 2030Rmodel flow meter and 500-mL jar. The net waslowered with the open end pointing downward untilthe 2-kg weight fastened to the front bridle by a 1-m line hit bottom. The net was then retrieved, allowingthe water column to be sampled both as thenet was lowered and as it was pulled up, whileavoiding collecting mud from the bottom. Sampleswere concentrated and preserved with a 4% sugarformaldehyde solution (Haney and Hall 1973). Volumesampled was calculated from the calibratedflow meter readings (m) and the cross-sectionalarea sampled by the net (0.1963 m 2 ). Four cubicmeters of water was typically sampled in the westernbasin. Proportionately larger volumes weresampled from deeper areas of the lake.

94 Conroy et al.TABLE 2. Lake Erie Plankton Abundance Study annual basin-specific phytoplankton biomass (A; mg wet mass L –1 ) and zooplanktonbiomass (B; mg dry mass L –1 ), showing begin and end sampling dates, number of samples, spring (May and June) and summer(July–September) measures of biomass central tendency (arithmetic [Mean A ] and geometric means [Mean G ] and median) and dataspread (arithmetic and geometric (lower and upper bounds) standard deviations [s A and s G , respectively] and first and third quartiles).(A) Spring Total Phytoplankton Biomass Summer Total Phytoplankton Biomass#Start End Samples Quartiles QuartilesBasin Year Date Date Sp./Su. Mean A s A Mean G s G Median (1st,3rd) Mean A s A Mean G s G Median (1st,3rd)Western 1996 22/5 25/9 123/231 0.65 0.67 0.41 (0.15,1.14) 0.44 (0.22,0.83) 0.79 1.38 0.27 (0.06,1.35) 0.32 (0.11,0.80)1997 9/5 24/9 36/57 0.63 0.70 0.41 (0.16,1.03) 0.41 (0.20,0.68) 1.03 1.26 0.53 (0.15,1.83) 0.59 (0.22,1.30)1998 26/5 28/9 47/87 1.67 1.39 1.16 (0.41,3.23) 1.15 (0.79,2.28) 5.48 9.94 2.27 (0.67,7.15) 1.83 (1.06,3.87)1999 17/5 28/9 32/53 1.25 0.84 1.03 (0.55,1.93) 0.94 (0.64,1.72) 2.52 2.25 1.86 (0.84,4.07) 1.98 (0.98,2.79)2000 2/5 18/9 23/29 1.87 1.44 1.38 (0.61,3.16) 1.39 (0.86,2.89) 2.33 2.06 1.61 (0.65,3.95) 1.91 (0.74,3.29)2001 14/5 17/9 33/28 2.20 1.23 1.86 (0.99,3.48) 2.11 (1.14,2.80) 3.80 2.86 2.97 (1.46,6.03) 2.65 (1.59,5.64)2002 7/5 30/9 21/44 3.31 6.49 1.42 (0.32,6.23) 1.68 (0.95,2.64) 3.12 4.22 0.62 (0.04,9.59) 2.04 (0.31,3.52)Central 1996 12/6 20/9 29/42 0.70 0.71 0.53 (0.26,1.06) 0.50 (0.34,0.74) 0.56 0.57 0.38 (0.15,0.97) 0.40 (0.22,0.57)1997 7/5 29/8 23/26 0.54 0.67 0.29 (0.09,1.00) 0.33 (0.13,0.62) 0.33 0.39 0.18 (0.05,0.62) 0.22 (0.10,0.37)1998 9/6 27/8 24/49 0.93 0.61 0.78 (0.42,1.43) 0.85 (0.57,1.01) 1.27 1.34 0.88 (0.38,2.01) 0.81 (0.49,1.25)1999 18/5 9/9 23/32 0.68 0.54 0.55 (0.30,1.03) 0.57 (0.37,0.75) 1.34 1.89 0.78 (0.20,3.02) 0.88 (0.63,1.33)2000 9/5 8/9 28/16 1.32 1.10 0.88 (0.34,2.33) 1.11 (0.40,2.10) 1.07 5.75 0.92 (0.51,1.67) 0.94 (0.68,1.34)2001 23/5 2/8 20/8 2.94 11.24 0.47 (0.14,1.60) 0.36 (0.29,0.56) 0.93 0.96 0.70 (0.34,1.44) 0.64 (0.44,0.88)2002 25/6 26/9 10/85 0.63 0.50 0.21 (0.02,2.76) 0.69 (0.23,0.97) 1.21 1.24 0.78 (0.29,2.12) 0.91 (0.39,1.62)Eastern 1996 24/6 18/9 4/7 0.25 0.17 0.22 (0.12,0.38) 0.18 (0.15,0.28) 0.47 0.60 0.30 (0.12,0.76) 0.28 (0.18,0.37)1997 7/5 28/8 7/12 0.09 0.13 0.05 (0.01,0.15) 0.06 (0.01,0.08) 0.38 0.73 0.16 (0.04,0.61) 0.19 (0.08,0.30)1998 8/6 25/8 10/20 0.40 0.22 0.36 (0.22,0.59) 0.33 (0.24,0.47) 3.47 11.41 0.88 (0.26,2.93) 0.68 (0.54,1.02)1999 17/5 8/9 10/15 0.95 1.04 0.58 (0.20,1.68) 0.54 (0.38,0.94) 3.87 10.38 0.73 (0.16,3.24) 0.56 (0.32,0.83)2000 1/6 29/8 11/17 0.61 0.84 0.35 (0.13,0.98) 0.27 (0.18,0.62) 0.67 0.54 0.50 (0.22,1.11) 0.54 (0.29,0.83)2001 1/5 14/9 38/42 4.08 18.98 0.93 (0.33,2.60) 0.74 (0.53,1.22) 1.10 2.39 0.56 (0.22,1.45) 0.52 (0.32,0.82)2002 1/5 17/9 8/30 1.82 2.09 0.88 (0.22,3.50) 0.78 (0.34,2.82) 1.06 1.85 0.55 (0.16,1.83) 0.50 (0.32,1.08)

Temporal Trends in Lake Erie Plankton Biomass 95(B) Spring Total Crustacean Zooplankton Biomass Summer Total Crustacean Zooplankton Biomass#Start End Samples Quartiles QuartilesBasin Year Date Date Sp./Su. Mean A s A Mean G s G Median (1st,3rd) Mean A s A Mean G s G Median (1st,3rd)Western 1996 22/5 25/9 136/332 0.149 0.156 0.084 (0.024,0.297) 0.094 (0.053,0.185) 0.090 0.131 0.035 (0.008,0.155) 0.036 (0.012,0.112)1997 9/5 24/9 61/74 0.060 0.079 0.026 (0.006,0.110) 0.025 (0.011,0.073) 0.161 0.219 0.064 (0.014,0.282) 0.056 (0.023,0.234)1998 10/6 29/9 42/102 0.110 0.092 0.070 (0.023,0.216) 0.083 (0.041,0.143) 0.098 0.095 0.058 (0.019,0.183) 0.067 (0.027,0.124)1999 17/5 28/9 25/52 0.117 0.022 0.053 (0.012,0.226) 0.060 (0.044,0.100) 0.081 0.079 0.043 (0.012,0.157) 0.052 (0.014,0.121)2000 2/5 18/9 42/46 0.100 0.103 0.040 (0.007,0.223) 0.074 (0.127,0.170) 0.171 0.189 0.092 (0.028,0.303) 0.078 (0.038,0.281)2001 14/5 17/9 30/39 0.175 0.131 0.120 (0.044,0.328) 0.162 (0.063,0.229) 0.106 0.090 0.071 (0.027,0.190) 0.085 (0.045,0.131)2002 7/5 30/9 40/55 0.069 0.082 0.025 (0.005,0.131) 0.025 (0.007,0.110) 0.174 0.157 0.109 (0.036,0.332) 0.117 (0.050,0.249)Central 1996 12/6 20/9 33/54 0.127 0.127 0.087 (0.036,0.210) 0.084 (0.047,0.153) 0.039 0.053 0.022 (0.008,0.061) 0.021 (0.011,0.042)1997 7/5 29/8 26/32 0.040 0.041 0.017 (0.003,0.087) 0.025 (0.007,0.065) 0.112 0.129 0.058 (0.017,0.194) 0.048 (0.026,0.159)1998 9/6 4/9 27/51 0.111 0.077 0.085 (0.039,0.187) 0.083 (0.055,0.180) 0.050 0.049 0.030 (0.010,0.093) 0.036 (0.013,0.066)1999 18/5 9/9 23/30 0.080 0.081 0.037 (0.008,0.182) 0.056 (0.016,0.122) 0.059 0.043 0.046 (0.021,0.098) 0.050 (0.030,0.074)2000 9/5 8/9 46/41 0.238 0.162 0.165 (0.056,0.485) 0.217 (0.112,0.334) 0.091 0.084 0.051 (0.012,0.208) 0.070 (0.026,0.131)2001 23/5 2/8 20/8 0.141 0.071 0.120 (0.064,0.227) 0.143 (0.093,0.174) 0.079 0.086 0.052 (0.020,0.134) 0.036 (0.030,0.096)2002 25/6 26/9 22/113 0.114 0.066 0.094 (0.046,0.187) 0.112 (0.052,0.159) 0.095 0.096 0.058 (0.019,0.180) 0.079 (0.029,0.123)Eastern 1996 24/6 18/9 6/8 0.055 0.012 0.054 (0.043,0.067) 0.055 (0.048,0.062) 0.020 0.009 0.018 (0.012,0.028) 0.020 (0.016,0.021)1997 2/6 28/8 8/12 0.035 0.057 0.010 (0.002,0.053) 0.006 (0.003,0.032) 0.041 0.046 0.027 (0.011,0.066) 0.025 (0.015,0.035)1998 8/6 25/8 10/11 0.026 0.028 0.011 (0.002,0.055) 0.014 (0.003,0.044) 0.042 0.028 0.036 (0.021,0.063) 0.032 (0.029,0.041)1999 17/5 8/9 7/17 0.031 0.070 0.003 (0.0003,0.030) 0.001 (0.001,0.012) 0.030 0.023 0.019 (0.006,0.063) 0.026 (0.016,0.049)2000 1/6 29/8 9/17 0.049 0.056 0.018 (0.003,0.124) 0.043 (0.007,0.073) 0.053 0.035 0.043 (0.021,0.087) 0.046 (0.030,0.070)2001 1/5 14/9 41/21 0.023 0.042 0.006 (0.001,0.039) 0.007 (0.002,0.025) 0.029 0.020 0.023 (0.012,0.047) 0.021 (0.015,0.046)2002 1/5 17/9 30/55 0.029 0.035 0.012 (0.003,0.056) 0.013 (0.004,0.047) 0.062 0.046 0.046 (0.018,0.115) 0.045 (0.034,0.084)

96 Conroy et al.Laboratory MethodsPhytoplankton whole water samples were condensedby settling in 250-mL graduated cylinders ina dark chamber for at least 3 d. Condensed sampleswere collected by drawing off the upper 220 mLand pouring the remaining 30 mL into a labeledsample vial. Enumeration of phytoplankton samplesgenerally followed the Utermöhl (1958) technique.Subsamples of approximately 3–5 mL were obtainedfrom the concentrated samples and placedinto a counting chamber. All phytoplankton generawere identified and counted using a Wild invertedmicroscope at 400×. Sequential transects of thechamber were viewed until 100 algal units (cells,filaments, or colonies) of the most common taxonwere encountered and recorded. In each sample,however, all algal units in at least two transectswere counted even if 100 algal units of the mostcommon taxa were enumerated before two transectswere completed. Dimensions for the first 20 algalunits of each enumerated taxon were measured. Forfilamentous algal taxa, all filament lengths weremeasured, summed, and recorded as the total filamentlength for each taxon. Average dimensionswere then used in geometric equations that best describedthe shape of each species according to Frostand Culver (2001; equations listed in Kane 2004)from which we computed average cell volume foreach species in a particular sample. For colonies,the mean number of cells per colony was calculatedand multiplied by the average volume per cell todetermine volume per colony. Subsequently, volumeswere converted to wet biomass (mg L –1 ) assumingthe specific gravity of phytoplankton to be1.0 (Munawar and Munawar 1976, Makarewicz1993a). Total phytoplankton biomass (mg L –1 ) wasfinally determined for all samples by summingtaxon-specific total biomass over all taxa present ina sample.Chlorophyll a concentration (µg L –1 ) was determinedusing aqueous acetone extraction accordingto USEPA Method 446.0 (USEPA 1997). Thismulti-laboratory validated, standard method correctedfor the presence of phaeophytin by measuringchlorophyll and phaeophytin absorbance beforeand after sample acidification (Lorenzen 1967). Notall total phytoplankton biomass samples had correspondingchlorophyll a concentration samples.For zooplankton enumeration, each sample wasfirst diluted to a known volume (typically500–3,000 mL) unless the sample contained few ormany zooplankters, requiring smaller or larger dilutionvolumes. All zooplankton taxa (rotifers, cladocerans,cyclopoid and calanoid copepods, and dreissenidveliger larvae) in at least two subsamples of5–10 mL were enumerated with a Wild dissectingmicroscope at 50×. Cladocerans and copepods wereidentified to species and sex while rotifers anddreissenid veligers were identified to genus. Additionalsubsamples were analyzed until at least 100individuals of the most common taxa (excludingcopepod nauplii, rotifers, and veligers) wererecorded. The lengths of the first 20 individuals ineach taxon (except rotifers and veligers) were alsomeasured to the nearest 0.05 mm with an ocular micrometer.Crustacean zooplankton biomass (i.e., excludingrotifers and dreissenid veligers) was calculated bydetermining the average individual biomass foreach taxon counted, multiplying by the number ofindividuals m –3 , and summing over all taxa. We excludedrotifers from our analysis since many ofthese zooplankton were not adequately sampledby our sampling gear due to large net mesh size(64 µm). We excluded dreissenid veligers becausewe wanted to compare only changes in the crustaceanzooplankton community. Average individualbiomass was determined using length-weight regressions(Culver et al. 1985) and the lengths measuredduring sample enumeration. Taxon-specificregression equations converted length (mm) to drybiomass (µg) for each crustacean zooplankton taxon(including eggs). Species-specific total biomasseswere summed over all taxa giving the total crustaceanzooplankton biomass (mg L –1 ) at a givensampling site, for a given date.For all recent plankton biomass measures exceptcyanobacteria biomass, we have calculated threemeasures of central tendency and data spread.These include the arithmetic and geometric meansand standard deviations, and the median and thefirst (25%) and third (75%) quartiles. We did notcalculate geometric means and standard deviationsfor cyanobacteria due to the frequent absence ofcyanobacteria in our samples. We do not presentmedians and quartiles for cyanobacteria again becauseof the high number of zeros in the data set,especially in spring samples, which often made themedian and first quartile less than 0.001 mg L –1 .We felt that both of these latter measures forcyanobacteria were uninformative, but they areavailable on request. Calculation of these threemeasures was important for two reasons. First, inorder to compare recent data to published data in anunbiased manner, we needed to calculate arithmetic

Temporal Trends in Lake Erie Plankton Biomass 97means and standard deviations because the historicaldata were summarized this way (Glooschenko etal. 1974, Watson and Carpenter 1974, Munawar andMunawar 1976, Watson 1976, Bean 1980, DeVaultand Rockwell 1986, Makarewicz 1993a,Makarewicz 1993b, Makarewicz et al. 1999, Weisgerber2000). Second, even though we had a largenumber of samples for most seasons and basins(Table 2), our data still were subject to the influenceof a few outliers with extremely high biomassvalues. Because the geometric mean, median, andquartiles are more resistant to bias caused by thepresence of outliers (Zar 1999), we used these measuresto control for their influence.Historical DatasetsEstimates of Lake Erie phytoplankton biomass bybasin were available in the literature from 1970(Munawar and Munawar 1976), 1978 (DeVault andRockwell 1986), and 1983–93 (Makarewicz 1993a,Makarewicz et al. 1999). Sampling, enumeration,and total biomass calculation methods were broadlysimilar to those used in LEPAS. The most consequentialdifference between the published and newdatasets is the sampling period (Table 3A), whichmay influence the interpretation and comparabilityof the computed central tendency measures amongsamples. Samples from 1970 were collectedmonthly from 25 stations distributed throughoutLake Erie’s three basins (Fig. 1 in Munawar andMunawar 1976) from April to December. For comparisonwith recent data, average total phytoplanktonbiomass for May through September was readfrom an optically scanned and digitized version ofMunawar and Munawar’s (1976) Figure 8. Samplesfrom 1978 were collected on nine cruises from Mayto November in the three basins of Lake Erie at 80stations (Fig. 1 in DeVault and Rockwell 1986).Total phytoplankton biomass data were read fromscanned versions of their Figures 3, 6, and 10. Phytoplanktondata were also available from samplescollected during 1979 (DeVault and Rockwell1986), but were not used in the present analysis dueto less frequent, spatially limited sampling. Samplesfrom 1983–93 were collected from stations distributedthroughout the lake (Fig. 1 in Makarewicz1993a and Makarewicz et al. 1999). Annual,lakewide averages of April and August phytoplanktondata for 1983–87 were available from Table 7of Makarewicz (1993a), whereas basin-specificgrand means were available for spring and summerfrom Tables 2, 3, and 4 from Makarewicz et al.(1999). Plankton biomasses in their 1999 paperwere broken into two periods: before the dreissenidinvasion (1983–88 for the western and centralbasins and 1983–89 for the eastern basin) and postinvasion(1989–93 in the western and central basinsand 1990–93 in the eastern basin).We obtained chlorophyll a concentration data for1970 from Glooschenko et al. (1974) from the samestations as those from which samples were analyzedfor algal taxonomic composition by Munawar andMunawar (1976). Cruise means reported in Table 1of Glooschenko et al. (1974) were compiled intospring (May and June) and summer (July–August)estimates by arithmetic averaging to enable parallelcomparisons with our 1996–2002 chlorophyll concentrationmeasurements. Spring and summerchlorophyll concentrations from 1983–93 weretaken directly from Makarewicz et al.’s (1999) Tables2, 3, and 4.Cyanobacteria biomass was available from 1970(Munawar and Munawar 1976) and 1983–93(Makarewicz et al. 1999). Cyanobacteria averagebiomass from 1970 was computed by multiplyingthe average total phytoplankton biomass determinedabove by the seasonal percent compositionvalues in Table 7 of Munawar and Munawar (1976).Biomass estimates from the 1983–93 period weretaken directly from Tables 2, 3, and 4 fromMakarewicz et al. (1999).Zooplankton total crustacean average biomassmeasurements were available in the literature from1970 (abundance data from Watson 1976, Watsonand Carpenter 1974; biomass calculations by Bean1980), 1974–75 (abundance data from Center forLake Erie Area Research; biomass calculations byWeisgerber 2000), and 1984–87 (Makarewicz1993b). Field sampling, enumeration, and biomasscalculations in all historical studies were similar toLEPAS (Table 3B). Abundance estimates (individualsm –3 ) were determined using net efficiency, towdepth, and net diameter. These estimates were moreaccurate in later studies (1984–87 and LEPAS) becauseflow meters were used on the mouths of thenets. Sampling stations and dates for 1970 (Watson1976) and 1984–87 (Makarewicz 1993b) were identicalto those given for phytoplankton (see above).Samples from 1974–75 were collected only in thewestern basin at 19 stations from April to December(Fig. 2 in Weisgerber 2000). Spring and summerbasin-specific average biomass estimates forthe 1970 samples were calculated from Bean’s(1980) Table 16 while those for 1974–75 were calculatedusing the data that contributed to Weisger-

98 Conroy et al.TABLE 3. Summary of major differences in phytoplankton (A) and zooplankton (B) sampling period, field sampling, and laboratorymethods between literature-derived and recent datasets. The sampling period pertains to the data actually used for comparisons withrecent data from LEPAS; the actual sampling period may have been longer.(A) PhytoplanktonSampling Period Station Sampling DepthPeriod Spring Summer Unstratified Stratified Magnification Enumeration Data Source1970 May–Jun., ~1 Jul.–Sept., ~1 1, 5 m 1, 5 m 300×, orgs. > 64 µm 300 units in settling chamber; Munawar & Munawarcruise mo. –1 cruise mo. –1 600×, orgs. < 64 µm diatoms on cleared slides (1976) Fig. 81978 May–Jun., ~1 Jul.–Sept., ~1 1 m, mid-depth, 1 m, 1 m ↑ metalimn., 250×, orgs. > 10 µm 2 perp. 13.6 mm long strips DeVault & Rockwellcruise mo. –1 cruise mo. –1 1 m above bottom thermocline, 1 m ↓ 500×, orgs. < 10 µm (1986) Figs. 3, 6, 10thermocl., 1 m ↑ bottom1983– Apr. (1 May Aug. 1 m, mid-depth, 1, 5, 10, 20 m 500×; diatoms @ Settling chamber; diatoms on Makarewicz et al.1993 1983–84 cruise) 1 m above bottom 1250× separate cleared slides (1999), Tables 2, 3, 41996– May–Jun. Jul.–Sep. 2× Secchi disk 2× Secchi disk 400× At least 100 units in a LEPAS2002 transparency transparency settling chamber(B) ZooplanktonSampling PeriodPeriod Spring Summer Sampling Depth Net Characteristics Enumeration Data Source1970 May–Jun., ~1 Jul.–Sep., ~ 1 Surf. to 50 m or to 40 cm dia., 64 µm, unmetered At least 200 individuals from 1 mL Watson (1976),cruise mo. –1 cruise mo. –1 1 m ↑ bottom subsamples of the undiluted sample Bean (1980)1974 May–Jun., ~1 Jul.–Sep., ~ 1 Surf. to 1 m ↑ 50 cm dia., 64 µm, metered (readings At least 200 individuals of Center for Lake Eriecruise mo. –1 cruise mo. –1 bottom were unavailable; assumed 70% eff.) one taxon from subsamples Area Research,of the diluted sample Weisgerber (2000)1983–87 Apr. (1 May Aug. Surf. to 20 m or to 50 cm dia., 62 µm, metered Followed Gannon (1971) Makarewicz1983–84 cruise) 1 m ↑ bottom (1993b) Table 21996– May–Jun Jul.–Sep. Surf. to 1 m ↑ 50 cm dia., 64 µm, metered At least 100 adults of one taxon from LEPAS2002 bottom subsamples of the diluted sample

Temporal Trends in Lake Erie Plankton Biomass 99ber’s (2000) Table 1. For 1984–87, only annual,lakewide averages could be calculated fromMakarewicz’s (1993b) Table 2 (by subtracting the“Rotifera” biomass column from the “Mean Abundance”biomass column).Phytoplankton Biomass Relationships withPhosphorus LoadTo test whether phytoplankton biomass was correlatedwith external phosphorus loading, we performedlinear regressions (Minitab 2000) with ourrecent phytoplankton data (1996–2002) and externalphosphorus loading. We were unable to expandthese relationships to previous periods due to theunavailability of data from some periods (just grandmeans were reported for 1989/90–93) or due to thelarge plankton biomass values in other years (e.g.,1970), which would have added undue influence tothe tested relationship. We performed analyses ofboth spring and summer arithmetic mean total phytoplanktonbiomass and arithmetic mean cyanobacteriabiomass versus both total external load toLake Erie and load by basin (Dolan and McGunagle2005). Significance was judged against an α-levelof 0.05 for all analyses.We also tested whether external annual phosphorusload significantly varied during the four periodsfor which we have plankton data (1970–78,1983–87, 1988–93, and 1996–2002). These four periodswere chosen because they differ in both externalphosphorus loading (high loading [typically >16 kilotonnes y –1 ] in 1970–78; low loading [typicallynear the target load of 11 kilotonnes y –1 ] in1983–87, 1988–93, and 1996–2001) and invasionstage of dreissenid mussels (no dreissenids in1970–78 and 1983–87, early dreissenid invasionstage in 1988–93, and later dreissenid invasionstage in 1996–2001). Analysis of Variance (Minitab2000) was used to determine whether these four periodsdiffered in external phosphorus loading toLake Erie. Significance was judged at an α-level of0.05 and Tukey’s HSD method for multiple comparisonswas used with a family error rate of 0.05.Testing Effects of External Loading andDreissenids on Lake Erie PlanktonTesting the predictions of external loading anddreissenid effects on Lake Erie phytoplankton requiresadequate sampling data from before and afterexternal phosphorus loading controls and the dreissenidinvasion. While post-loading and post-invasiondata were abundant (Makarewicz et al. 1999,Conroy et al. 2005b), pre-loading and pre-invasiondata were less obtainable. Furthermore, most reportsof both pre- and post-data only contain summarystatistics, not the raw data, or when the rawdata are available, they are in a form that is difficultto use (i.e., microfiche or printouts). To test thedreissenid effects predictions, therefore, we comparedour recent LEPAS phytoplankton data withpublished data through comparisons of basin- andseason-specific grand means. We subjectively comparedgrand means from four periods based uponthe level of phosphorus loading and the state of thedreissenid invasion: (1) 1970–1978, high phosphorusloading, no dreissenid mussels; (2)1983–1988/9, low phosphorus loading, no dreissenidmussels; (3) 1989/90–93, low phosphorusloading, early mussel invasion; and, (4) 1996–2002,low phosphorus loading, later in the mussel invasion.Since we did not have the original raw data,we were unable to compare data from the four timeperiods statistically. While we could have statisticallycompared annual means, this was unfeasibledue to the low power associated with few annualmeans in some periods (e.g., only two annualmeans in the 1970–78 period) or due to not havingsome annual means (i.e., only grand means were reportedfor the 1989/90–93 period in Makarewicz etal. 1999).RESULTS AND DISCUSSIONIs Lake Erie Plankton Biomass at aRecent Minimum?Determining the absolute direction and magnitudeof change of Lake Erie plankton communitiesin reference to historical data was difficult in thisstudy due to the unavailability of the original historicaldata. All trends (or lack thereof) in the datadiscussed below were determined by comparison ofrecent measures of central tendency (Table 2) withthose from previous time periods (Tables 4–7). Weargue that if the trends consistently point to differencesin the same direction (or are lacking), that thedifferences (or lack thereof) are likely biologicallyimportant. This method has been used throughoutthe Lake Erie plankton literature when more preciseinformation is unavailable (DeVault and Rockwell1986; Makarewicz 1993a, 1993b).Both spring and summer phytoplankton total wetbiomass grand means (mg L –1 ) were at their greatestlevel during the 1970–78 period. Minima wereobserved in the late 1980s or 1990s (Table 4). West-

100 Conroy et al.TABLE 4. Lake Erie total phytoplankton wet biomass (mg L –1 ) period grand means for spring (A) andsummer (B). Data from 1970–78 are from Munawar and Munawar (1976) and DeVault and Rockwell(1986); data from 1983–93 are from Makarewicz et al. (1999); and, recent data are from LEPAS.(A)Period: 1970–78 1983–88/9 1989/90–93 1996–2002SpringQuartiles GrandBasin Mean Grand Mean Grand Mean Grand Mean A,Grand s A,Grand Mean G,Grand s G,Grand Median Grand (1st, 3rd)Western 2.6 1.97 1.27 1.29 2.04 0.73 (0.24,2.27) 0.79 (0.39,1.63)Central 2.1 1.37 1.79 1.11 4.09 0.53 (0.17,1.68) 0.55 (0.30,0.94)Eastern 2.3 0.80 0.60 2.57 14.1 0.47 (0.11,1.99) 0.46 (0.20,1.01)(B)Period: 1970–78 1983–88/9 1989/90–93 1996–2002SummerQuartiles GrandBasin Mean Grand Mean Grand Mean Grand Mean A,Grand s A,Grand Mean G,Grand s G,Grand Median Grand (1st, 3rd)Western 5.9 2.51 1.79 2.20 4.78 0.68 (0.11,3.97) 0.89 (0.27,2.28)Central 3.1 0.86 0.85 1.01 1.21 0.61 (0.20,1.86) 0.70 (0.35,1.22)Eastern 1.9 0.63 0.52 1.56 5.60 0.53 (0.16,1.73) 0.50 (0.25,0.90)TABLE 5. Lake Erie chlorophyll a concentration (µg L –1 ) period grand means for spring (A) and summer(B). Data from 1970 are from Glooschenko et al. (1974); data from 1983–93 are from Makarewicz etal. (1999); and, recent data are from LEPAS.(A)Period: 1970 1983–88/9 1989/90–93 1996–2002SpringQuartiles GrandBasin Mean Grand Mean Grand Mean Grand Mean A,Grand s A,Grand Mean G,Grand s G,Grand Median Grand (1st, 3rd)Western 5.15 7.46 3.06 3.53 3.39 2.34 (0.87,6.32) 2.55 (1.30,4.62)Central 2.80 3.33 4.20 1.96 1.93 1.22 (0.40,3.68) 1.40 (0.76,2.25)Eastern 4.45 1.32 1.28 0.77 0.62 0.56 (0.24,1.32) 0.63 (0.40,0.85)(B)Period: 1970 1983–88/9 1989/90–93 1996–2002SummerQuartiles GrandBasin Mean Grand Mean Grand Mean Grand Mean A,Grand s A,Grand Mean G,Grand s G,Grand Median Grand (1st, 3rd)Western 12.80 10.20 9.20 6.55 4.62 4.85 (2.01,11.67) 5.39 (2.79,9.17)Central 4.88 3.50 2.70 2.04 1.52 1.56 (0.68,3.59) 1.53 (1.12,2.60)Eastern 3.33 2.37 2.00 1.43 0.66 1.28 (0.79,2.09) 1.47 (0.84,1.87)ern basin spring phytoplankton biomass was greatestin the 1970–78 period (Table 4), but annual valuesin 2001 and 2002 approached or exceeded thisperiod mean. Minimum western basin spring meanphytoplankton biomass values were found in 1996and 1997 (Table 2A). Central basin spring phytoplanktonbiomass was lowest in 1997 (Table 2A).The lowest period mean values were also found inthe recent (1996–2002) period (Table 4). Easternbasin spring mean phytoplankton biomass wasgreatest in the recent period (Table 4). Samplesfrom the most recent sample years (2001 and 2002)were important to this trend. Again, 1997 had thelowest biomass of any annual mean (Table 2A).Western basin summer phytoplankton biomasswas greatest in the 1970–78 period. The minimumoccurred in the 1989–93 period (Table 4). The meanbiomass in 1996 was the lowest (Table 2A) of any

Temporal Trends in Lake Erie Plankton Biomass 101TABLE 6. Lake Erie cyanobacteria wet biomass (mg L –1 ) period grand means for spring (A) and summer(B). Data from 1970 are calculated from Munawar and Munawar (1976); data from 1983–93 arefrom Makarewicz et al. (1999); and, recent data are from LEPAS.(A)Period: 1970 1983–88/9 1989/90–93 1996–2002SpringBasin Mean Grand Mean Grand Mean Grand Mean A,Grand s A,GrandWestern 0.010 0.001 0.05 0.06 0.70Central 0.068 0.010 0.03 0.01 0.03Eastern 0.177 0.005 0.02 0.01 0.04(B)Period: 1970 1983–88/9 1989/90–93 1996–2002SummerBasin Mean Grand Mean Grand Mean Grand Mean A,Grand s A,GrandWestern 1.17 0.51 0.17 0.94 4.34Central 0.22 0.07 0.05 0.30 1.02Eastern 0.29 0.03 0.05 0.86 5.40TABLE 7. Lake Erie total crustacean dry biomass (mg L –1 ) period grand means for spring (A) and summer(B). Data from 1970–75 are from Watson and Carpenter (1974), Watson (1976), Bean (1980), andWeisgerber (2000); data from 1984–87 are from Makarewicz (1993b); and, recent data are from LEPAS.(A)Period: 1970–75or 1970 1984–87 1996–2002SpringQuartiles GrandBasin Mean Grand Mean Grand Mean A,Grand s A,Grand Mean G,Grand s G,Grand Median Grand (1st, 3rd)Western 0.322 0.0808 0.108 0.127 0.050 (0.011,0.218) 0.065 (0.019,0.147)Central 0.296 0.0742 0.134 0.125 0.076 (0.020,0.286) 0.096 (0.052,0.159)Eastern 0.106 0.0614 0.030 0.043 0.009 (0.002,0.056) 0.011 (0.002,0.046)(B)Period: 1970–75or 1970 1984–87 1996–2002SummerQuartiles GrandBasin Mean Grand Mean Grand Mean A,Grand s A,Grand Mean G,Grand s G,Grand Median Grand (1st, 3rd)Western 0.332 0.0808 0.111 0.144 0.050 (0.012,0.201) 0.056 (0.019,0.149)Central 0.268 0.0742 0.076 0.086 0.043 (0.013,0.139) 0.047 (0.019,0.106)Eastern 0.274 0.0614 0.047 0.039 0.033 (0.013,0.082) 0.035 (0.020,0.065)single year. Annual means from 1998–2002 wereapproximately 50% of the 1970–78 mean biomass.However, these values were consistently higherthan the 1996–97 values (Tables 2A, 4). All meanbiomasses in the recent period except those in1996–97 were higher than those reported in the1989–93 period (Tables 2A, 4). Additionally, meanbiomasses in four of the seven recent years(1998–99, 2001–02) were equal to or greater thanthe grand mean for the 1983–89 period. Centralbasin summer phytoplankton biomass was greatestin the 1970–78 period, was lower in 1983–93, andincreased in the recent period (Table 4). For recentannual mean biomasses, only annual values for1996 and 1997 were lower than the grand means forthe period 1983–93 (Tables 2A, 4). None of the re-

102 Conroy et al.cent annual means were greater than 43% of themean biomass for the 1970–78 period (Tables 2A,4). In the eastern basin, the greatest grand meanbiomass was recorded in the 1996–2002 period, althoughthis value was affected primarily by two extremeyears (1998 and 1999; Table 2A). Exclusiveof these 2 years, 2 years’ biomasses were lower(1996 and 1997) and one was slightly above (2000).Estimates for the 2 most recent sampling years(2001 and 2002) were higher than those from1983–93 (Tables 2A, 4).These comparisons show that Lake Erie phytoplanktonbiomass is not at a recent minimum. Ofthe compiled data, the lowest mean biomasses generallyoccurred in 1996 and 1997, whereas the years1998–2002 generally had the highest mean biomassesof the three major periods since the1970–78 period. These data, measured from directalgal counts and size-frequency measurements, donot support the suggestion by other scientists thatLake Erie phytoplankton biomass was at a minimumin the late 1990s and early 2000s (Carrick etal. 2005, Ghadouani and Smith 2005), probably becausethey estimated biomass by measurement ofchlorophyll a.Data from our measurements, however, do indicatethat chlorophyll a concentration was at a minimumin the last few years (Table 5). All basin grandmeans from 1996–2002 were less than those from1970 and the mid-1980s and all except spring westernbasin chlorophyll a concentration were less thanthose from the early 1990s (Table 5). Summergrand means from 1996–2002 were greater thanthose from the spring, following the general trendreported in previous periods (Table 5).The greatest values of cyanobacteria biomass inall basins were reported in 1970. However,cyanobacteria biomass has increased in the westernand eastern basins during spring and in all basinsduring the summer since the mid-1980s (Table 6).No consistent change in spring cyanobacteria biomasshas occurred in any basin from the early1990s to more recent sampling periods (Table 6A).However, summer biomass was dramatically increasedfor the most recent period (Table 6B). Thelarge amount of interannual and spatial variabilityin the cyanobacteria data indicated by the largestandard deviation reported for the recent period(Table 6) reflects an increasing frequency in the occurrenceof samples with high cyanobacteria biomasses.Discerning recent trends in basin-specific seasonaltotal crustacean zooplankton biomass is difficultbecause data from the mid-1980s were summarizedover the whole of Lake Erie (Makarewicz1993b). Western basin crustacean biomass in the1996–2002 period was greater than that reportedfrom the mid-1980s but less than that from the1970s (Table 7). Western basin spring annual crustaceanzooplankton biomasses were generallygreater than those from the mid-1980s (5 of 7 years;Tables 2B, 7). All 1996–2002 annual average biomasseswere greater than the lowest of the annualmeans reported by Makarewicz (1993b, his Table2). The lowest recent western basin spring crustaceanzooplankton biomass was observed in 1997(Table 2B). The 1996–2002 central basin spring annualgrand mean of crustacean zooplankton biomasswas nearly twice the grand mean reported forthe mid-1980s, but was just less than one-half ofthat from the 1970s (Table 7). This grand mean wasinfluenced by the most recent three years’ data(Table 2B). The lowest annual central basin springbiomass occurred in 1997 (Table 2B); this biomasswas also less than all those reported by Makarewicz(1993b). Eastern basin spring crustacean zooplanktonbiomass was low in recent years (Tables 2B, 7)relative to that of previous periods. The 1996–2002spring grand mean (Table 7) was one-half of the1984–87 grand mean reported by Makarewicz(1993b). All eastern basin annual spring meanswere lower than the grand mean from the mid-1980s (Table 7), with the lowest eastern basinspring annual mean occurring in 2001 (Table 2B).Summer crustacean zooplankton biomass grandmeans were nearly three times higher in the 1970sthan in all other periods (Table 7). In the westernbasin, summer crustacean zooplankton biomass washigher in 1996–2002 than in the mid-1980s (Table7), with all years exceeding the 1980s grand mean(Table 2B). The 1996–2002 central basin summercrustacean zooplankton biomass grand mean wasmarginally higher than the mid-1980s (Table 7)with several years with biomasses greater than andseveral years less than the mid-1980s grand mean(Table 2B). The eastern basin 1996–2002 crustaceanzooplankton grand mean was less than themid-1980s (Table 7). All recent-period summer biomassesvalues were less than the mid-1980s annualgrand mean except for 2002 (Table 2B).Overall, total crustacean zooplankton biomasshas decreased since maxima in the 1970s. Minimalvalues were observed in 1986 for the western basinand summer 1996 for the central and eastern basins(Table 2 of Makarewicz 1993b, Table 2B). Trendssince the mid-1980s were either increasing, de-

creasing, or remained the same, depending on theseason and basin (Table 7).Does Phytoplankton Biomass Correlate withAnnual External Phosphorus Load?Phosphorus loadings to Lake Erie were significantlydifferent (one-way ANOVA, F 3,23 = 13.3, P< 0.001) among the four time periods (1970–78,1983–87, 1988–93, and 1996–2002) analyzed.Mean (±SD) external phosphorus loading was significantlygreater during 1970–78 (19.8 ± 4.9 kilotonnes)than during 1983–87 (10.7 ± 1.7kilotonnes), 1988–93 (10.1 ± 2.2 kilotonnes), and1996–2002 (10.4 ± 3.7 kilotonnes) (Tukey’s HSDtest, P < 0.05). Phosphorus loads during the threelater time periods were not significantly differentfrom one another (P > 0.05).None of the total phytoplankton biomass versusexternal phosphorus loading regressions were statisticallysignificant (P > 0.05), either when usingtotal external loads of phosphorus to Lake Erie orbasin-specific loads. Additionally, when Cyanobacteriabiomass was regressed against external phosphorusloading, no significant relationships werefound.Temporal Trends in Lake Erie Plankton Biomass 103Total Phytoplankton Biomass—Chlorophyll a RelationshipsMost studies of Lake Erie phytoplankton usechlorophyll a as a surrogate for algal abundance(e.g., MacIsaac et al. 1999, Ackerman et al. 2001,Smith et al. 2005) because chlorophyll a concentrationis easier to determine than phytoplankton biomass.Ideally, total phytoplankton biomass shouldbe accurately and precisely estimated from chlorophylla concentration. From 1996 to 2002, however,there were different trends in total phytoplanktonbiomass, chlorophyll a concentration, andcyanobacteria biomass. To further investigate therelationship between these measures of phytoplanktonabundance on a basin- and season-specificbasis, we performed linear regression analyses onthe recent (1996–2002) total phytoplankton biomassversus chlorophyll a concentration data. Weconducted two separate regressions—one using siteand date-specific data, and the other using the annualaverages. Regressions were constructed withchlorophyll a concentration as the explanatory variableand total phytoplankton biomass as the dependentvariable because chlorophyll a concentration isoften used to estimate phytoplankton biomass (Fig.FIG. 2. Phytoplankton biomass (mg L –1 ) as afunction of chlorophyll a concentration (µg L –1 )from individual stations in the western (filled circles),central (open squares), and eastern (opentriangles) basins of Lake Erie from 1996–2001 (n= 1049). Raw data are plotted in (A) (slope = 0.21,R 2 = 0.04, P < 0.001) while natural log-transformeddata are plotted in (B) (slope = 0.34, R 2 =0.07, P < 0.001). All data are from LEPAS.2A). The regression using the original data (Fig.2A; n = 1049) was highly statistically significant(Total Biomass = (0.74 ± 0.17) + [(0.21 ± 0.03) ×Chlorophyll a]; F 1,1047 = 48.11, P < 0.001) but hadlittle explanatory power (R 2 = 0.04). Natural logtransformeddata provided little improvement (Fig.2B; ln (Total Biomass) = (–0.78 ± 0.05) + [(0.34 ±0.04) × ln (Chlorophyll a)]; F 1,1047 = 77.65, P

104 Conroy et al.cant (western basin summer; Total Biomass =(–0.82 ± 1.37) + [(0.53 ± 0.19) × Chlorophyll a];F 1,5 = 7.46, P = 0.04, R 2 = 0.52. These results indicatedthat chlorophyll a concentration did not predicttotal phytoplankton biomass well during therecent (1996–2001) period.Testing Predictions of Dreissenid Effectson Lake Erie PlanktonThe abundance of research on the effect of dreissenidson Lake Erie plankton abundance over thepast 15 years has generated many predictions(Table 1). We used the results of our summary ofrecent total phytoplankton biomass, chlorophyll aconcentration, cyanobacteria biomass, and totalcrustacean biomass to test these predictions. Asseen in the results above, there were many inconsistenciesin the response of these groups both withina group (i.e., increased crustacean zooplankton biomassin the western basin but decreased biomass inthe eastern basin) and between groups (i.e., increasedsummer cyanobacteria biomass but decreasedsummer chlorophyll a concentration in allbasins). However, several predictions of dreissenideffects on Lake Erie plankton communities do havesome support from comparison of our results withthose from the mid-1980s (Makarewicz 1993a,1993b; Makarewicz et al. 1999).The increase in total summer phytoplankton biomasspredicted to occur by Vanderploeg et al.(2001, 2002) and during the spring and summer byConroy et al. (2005a) was observed: the recent annualphytoplankton biomasses (Tables 2A, 4) exceededthose of the mid-1980s (i.e., pre-dreissenidinvasion with low external phosphorus load; Table4). Similarly, the predicted increases in cyanobacteriain the summer by Vanderploeg et al. (2001,2002), in the spring in the western basin byMakarewicz et al. (1999), and in the spring andsummer by Conroy et al. (2005a) were generallyobserved (Table 6). It is noteworthy that these predictionswere based upon different mechanisms(i.e., selective filtration versus excretion). The decreasein chlorophyll a concentration observed byBarbiero and Tuchman (2004b) and Makarewicz etal. (1999) in the western basin during the 1980s andearly 1990s was observed in our more recent dataalso (Table 5). Our data were not consistent withthe remaining predictions pertaining to total phytoplanktonbiomass, chlorophyll a concentration, orcyanobacteria biomass (Table 1).Total crustacean zooplankton biomass was lowerduring the recent period than previously in the easternbasin but not the central or western basins (Tables2B,7). This observation was not entirelyconsistent with the prediction that through competition,dreissenids would negatively impact zooplanktoncommunities (but see Patterson et al. 2005).IMPLICATIONS FORFUTURE LAKE ERIE RESEARCHOne of the key observations that stimulated researchby the Lake Erie Trophic Status group in2002 was the report of historically low phytoplanktonbiomass as measured by chlorophyll a concentrationin the late 1990s (Rockwell et al. 2005).Low phytoplankton biomass was expected for tworeasons. First, through implementation of the GreatLakes Water Quality Agreement, phosphorus loadinghad decreased throughout the late 1970s and1980s (Dolan 1993, Dolan and McGunagle 2005)possibly limiting phytoplankton production(Makarewicz 1993a, Nicholls 1997). Secondly, theestablishment of high densities of dreissenid mussels(Patterson et al. 2005) was accompanied by decreasesin nearshore phytoplankton and increases inthe Secchi transparency (Holland 1993). Both predictedand observed decreases in phytoplanktonsuggested that zooplankton biomass would decreaseas well if zooplankton are food-limited. Here, wehave used the results of a multi-agency, lake-wideseasonal plankton study to test the hypothesized relationshipsamong plankton abundance and externalphosphorus loading and the presence of dreissenidmussels.Our comparison of recent plankton data to thosepreviously reported in the literature showed severalmarked trends. First, total phytoplankton biomassin 2002 was not at a minimum. While 1996 and1997 were low biomass years throughout Lake Erie,recent years’ data showed increased biomass. Easternbasin total phytoplankton biomass showed thegreatest increases since that time. However, thesedata were influenced by outliers, as evidenced by acomparison of the arithmetic and geometric means(Tables 2A, 4). Although chlorophyll a concentrationdecreased in all basins in both seasons (Table5), our data indicate that chlorophyll a concentrationdoes not predict total phytoplankton biomasswell during the recent period in Lake Erie.Cyanobacteria biomass increased in the summer inall basins, and some grand means from 1996–2002exceeded those reported from 1970 (Table 6). Totalcrustacean zooplankton biomass during the recent

Temporal Trends in Lake Erie Plankton Biomass 105period was at levels similar to, or exceeding thoseobserved during the mid-1980s in the western andcentral basins. However, zooplankton biomass decreasedin the eastern basin (Tables 2B, 7).Trends in plankton biomass could not be consistentlyexplained by either interannual changes inexternal phosphorus load or by the presence ofdreissenids. However, some changes were consistentwith patterns in these forcing functions. Hightotal phytoplankton biomass in the 1970s (Table 4)corresponds to the time of the highest externalphosphorus load (Dolan 1993). All total phytoplanktonbiomasses in the other periods (Table 4)are during times of lower phosphorus load (Dolan1993, Dolan and McGunagle 2005). Additionally,the dreissenid excretion (Conroy et al. 2005a) andselective filtration (Vanderploeg et al. 2001, 2002)hypotheses predicted recent increases in total phytoplanktonbiomass and cyanobacteria biomass duringsummer.The inconsistency between total phytoplanktonbiomass and chlorophyll a concentration trends andthe inability of chlorophyll a concentration to predicttotal phytoplankton biomass is not a new finding.Many studies have found that chlorophyll aconcentration was a poor predictor of total phytoplanktonbiomass (or cell volume) for many differentlakes (Nicholls 1976, Dolan et al. 1978,Nicholls and Dillon 1978, Tolstoy 1979, LaBaugh1995, Kalchev et al. 1996, Felip and Catalan 2000).In such relationships, a poor fit can commonly beattributed to overestimation of chlorophyll content,underestimation of total phytoplankton biomass, orboth (Tolstoy 1979). Further, converting from cellvolume to biomass is problematic due to the inclusionof vacuoles, which contribute little to functionalbiomass of cells, especially in diatoms(Smayda 1978). Similar problems occur in the conversionof cell biovolume or biomass to cell carbon,nitrogen, or other constituents (Smayda 1978).The slope of our regression relating all total phytoplanktonbiomasses to chlorophyll a concentrations(~ 0.21 µg chlorophyll mg –1 phytoplankton)was lower than those Tolstoy (1979) summarizedfrom many sources for freshwater lakes, marine andbrackish water, and freshwater and marine phytoplanktoncultures (generally 1–6 µg chlorophyllmg –1 phytoplankton) and that reported by Nicholls(1976; 3.55 µg chlorophyll mg –1 phytoplankton).The slope of our estimated relationship for westernbasin spring and summer averages (~ 1.1 µg chlorophyllmg –1 total phytoplankton), however, waswithin but, at the lower end of, the range reportedTABLE 8. Median and range values of chlorophylla percent composition of total wet phytoplanktonbiomass. Range values were either takendirectly from the literature (Ahlgren 1970 as citedby Nicholls 1976), were estimated from figures(Dolan et al. 1978, Fig. 4a), or were calculated asthe first and third quartiles of all data points (thisstudy). Where values are missing, data were notavailable to calculate the respective measure.Study Median RangeAhlgren 1970Lake Vattern 0.5%Lake Norrviken 1.5% 0.6–5.7%Nicholls 1976Holland Marsh 0.5%Dolan et al. 1978Saginaw Bay ~0.3–3.8%This studyLake Erie 0.35% 0.17–0.80%by Tolstoy (1979) and Nicholls (1976). Our estimatesof chlorophyll a percent content of wet biomassfor all of our data combined (n = 1049) werewithin the range of those reported by Ahlgren(1970, cited in Nicholls 1976) for two Swedishlakes, Nicholls (1976) for Holland Marsh, andDolan et al. (1978) for Saginaw Bay in Lake Huron(Table 8). Taken together, these data indicate thatthe slope of our regression line was low and probablyreflected the undue influence of extreme outlierswith respect to total phytoplankton biomass(e.g., high total phytoplankton biomass and lowchlorophyll a concentrations for the same sample).Since cellular chlorophyll content varies by up totwo orders of magnitude throughout the season(Nicholls and Dillon 1978) and among taxa, is affectedby nutrient concentration (Nicholls 1976)and especially light intensity (Ahlgren 1970 cited inNicholls 1976), and the regression between phytoplanktonbiomass and chlorophyll a concentrationin Lake Erie is so poor, the use of chlorophyll aconcentration as a surrogate for phytoplankton biomassshould be done with caution until the relationshipcan be better established for Lake Erie.The relationship between within-lake total phosphorusconcentration and chlorophyll a concentrationand/or total phytoplankton biomass is wellestablished for a variety of lakes (Dillon and Rigler1974, Nicholls and Dillon 1978). In Lake Erie, data

106 Conroy et al.before the dreissenid invasion showed a lower slopefor the chlorophyll a concentration versus in-laketotal phosphorus concentration compared to otherGreat Lakes (Smith et al. 2005). Smith et al.(2005), using Analysis of Covariance tests, did notfind a significant reduction in this relationship subsequentto the dreissenid invasion for the offshorewaters. The predicted reduction in chlorophyll aconcentration, total phytoplankton biomass, andcyanobacteria biomass with reduction in externaltotal phosphorus load is also well established(Marsden 1989, Jeppesen et al. 2005). Consequently,our finding of increased total phytoplanktonbiomass and cyanobacteria biomass at loweredexternal phosphorus load is noteworthy. Since therelationship between the external phosphorus loadingto the lake or to individual basins was a poorpredictor of total phytoplankton biomass in LakeErie, we suspect that internal phosphorus loading isbecoming more important. This speculation reflectsthe findings of several studies that reported phosphorusconcentrations to be increasing in Lake Erie(Makarewicz et al. 2000, Charlton and Milne2004). External phosphorus loading has apparentlynot changed significantly since the 1980s (Dolanand McGunagle 2005), and tributary phosphorusconcentrations have declined due to decreased nonpointsource loads (Richards and Baker 2002). Increasedinternal loading of phosphorus can becaused by the release of phosphorus from sedimentsduring anoxic events (Nürnberg 1991) and/or by bioticactivity (Matisoff and Wang 1998). With respectto the biota, both bioturbation by mayflies(D.D. Kane unpublished data, Bachteram et al.2005) and phosphorus remineralization from dreissenids(Conroy et al. 2005a), other benthic invertebrates(Devine and Vanni 2002), and fishes (Vanniet al. 2002, Bunnell et al. 2005) may be important.In addition to the continued monitoring of externalphosphorus loads, research into elucidating phosphorusbudgets and cycling rates for Lake Erie mustbe conducted.Increased cyanobacteria biomass since 1996 inall basins during the summer and in the western andeastern basins during spring indicates that LakeErie system health (Conroy et al. 2005b) may bedeclining. Most of the increased summer cyanobacteriabiomass is due to a resurgence throughoutLake Erie of Microcystis spp., a non-nitrogen-fixingcyanobacterium, (Vincent et al. 2004, Rinta-Kantoet al. 2005, Conroy et al. 2005a). In contrast,cyanobacterial biomass in 1970 was dominated bynitrogen-fixing taxa such as Anabaena spp. andAphanizomenon spp. (Munawar and Munawar1976). The switch to Microcystis spp. now suggeststhat either the nutrient supply is sufficient to favorthis taxon or that selective filtration by dreissenidsis great enough to affect competition betweencyanobacteria taxa. Several recent studies provideevidence that nutrient supply is important (Raikowet al. 2004, Sarnelle et al. 2005, Conroy et al.2005a) while others support selective filtration(Vanderploeg et al. 2001, 2002). Of particular importancemay be the way in which dreissenids affectnitrogen cycling in Lake Erie through theirexcretion of ammonia (Conroy et al. 2005a). Whilethe effect of dreissenids is greatest in the nearshore(Hecky et al. 2004), direct-manipulative research todetermine how dreissenids affect nutrient supply inconjunction with selective filtration is needed for usto better understand why Microcystis spp. are thedominant cyanobacterial taxa now.Variable trends were found for the crustaceanzooplankton community (Table 7). It is unclear whycrustacean zooplankton abundance would consistentlyincrease in the western basin and consistentlydecrease in the eastern basin based upon similarchanges in the total phytoplankton biomass,cyanobacteria biomass, and chlorophyll a concentration.Ingestion of cyanobacteria by eastern basincrustacean zooplankton could lead to decreased survival,reproduction, and biomass (Arnold 1971,Ghadouani et al. 2003) as the eastern basin saw thegreatest increase in cyanobacteria biomass and hasamounts approximating those in the western basin(Table 6). Zooplanktivory due to one-year-andolderand young-of-the-year rainbow smelt in theeastern basin was hypothesized to be responsiblefor decreases in zooplankton in the mid-1990s (Johannssonet al. 1999), but rainbow smelt populationsconcurrently decreased from the mid-1980sthrough at least the mid-1990s (Ryan et al. 1999).Barbiero and Tuchman (2004a), attribute decreasesin abundance of eastern basin cladocerans to the invasionof Bythotrephes longimanus. The role of invertebratezooplanktivores in affecting crustaceanzooplankton community dynamics is amplified bythe invasion of Cercopagis pengoi in both the western(Therriault et al. 2002) and eastern (D.A. Culver,unpublished data) basins. However, thecontrasting response by the crustacean zooplanktoncommunity to changes in bottom-up and top-downforces in different basins of Lake Erie remains to beexplained mechanistically.In this article we have combined the results of arecent (1996–2002) plankton study with published

Temporal Trends in Lake Erie Plankton Biomass 107plankton abundances from previous years to testwhether recent changes in phytoplankton and zooplanktonabundances are consistent with predictionsbased upon changes in external phosphorus loadingand the effects of invasive dreissenid mussels. Ourresults suggest that phytoplankton biomass (especiallycyanobacteria biomass) is increasing, and thispattern is most consistent with an effect of nutrientrecycling by dreissenids. However, zooplanktonabundances have not increased as rapidly as wouldbe expected if they are regulated by phytoplanktonabundance, suggesting important areas for furtherresearch, given their importance to recruitment ofjuvenile fish in the lake.ACKNOWLEDGMENTSWe would like to thank the numerous techniciansfor processing thousands of phytoplankton, zooplankton,and chlorophyll samples over the past 9years, particularly Nate Gargasz and Erin Haas. Wewould also like to thank the captains and crews ofthe various research vessels from which many sampleswere collected. This research was sponsored bythe Ohio Department of Natural Resources as partof the Federal Aid in Sport Fish Restoration Program(F-69-P, Fish Management in Ohio) administeredjointly by the U.S. Fish and Wildlife Serviceand the Ohio Division of Wildlife and the UnitedStates Environmental Protection Agency (GL-97590101). J.D.C. was supported as a UniversityFellow by The Ohio State University and D.D.K.was supported by a Raymond C. Osborn MemorialGraduate Fellowship from The Ohio State Universityand the Department of Evolution, Ecology, andOrganismal Biology while working on part of thisproject. We would like to acknowledge the internationaleffort and cooperative spirit that supports ourwork and the stewardship for Lake Erie shown bythe various management agencies. Without such encouragement,this work would not be possible. Extensivecomments and suggestions by twoanonymous reviewers and Jan Ciborowski greatlyimproved the manuscript.REFERENCESAckerman, J.D., Loewen, M.R., and Hamblin, P.F. 2001.Benthic-pelagic coupling over a zebra mussel reef inwestern Lake Erie. Limnol. Oceanogr. 46:892–904.Ahlgren, G. 1970. Limnological studies of Lake Norrviken,a eutrophied Swedish lake. II. Phytoplanktonand its production. Schweiz. Z. Hydrol. 32:353–396.Arnold, D.E. 1971. Ingestion, assimilation, survival, andreproduction by Daphnia pulex fed seven species ofblue-green algae. Limnol. Oceanogr. 16:906–920.Arnott, D.L., and Vanni, M.J. 1996. Nitrogen and phosphorusrecycling by the zebra mussel (Dreissena polymorpha)in the western basin of Lake Erie. Can. J.Fish. Aquat. Sci. 53:646–659.Bachteram, A.M., Mazurek, K.A., and Ciborowski,J.J.H. 2005. Sediment suspension by burrowingmayflies (Hexagenia spp., Ephemeroptera: Ephemeridae).J. Great Lakes Res. 31 (Suppl. 2):208–222.Barbiero, R.P., and Tuchman, M.L. 2004a. Changes inthe crustacean communities of Lakes Michigan,Huron, and Erie, following the invasion of the predatorycladoceran Bythotrephes longimanus. Can. J.Fish. Aquat. Sci. 61:2111–2125.——— , and Tuchman, M.L. 2004b. Long-term dreissenidimpacts on water clarity in Lake Erie. J. Great LakesRes. 30:557–566.Bean, D.J. 1980. Crustacean zooplankton production inLake Erie, 1970. M.S. thesis, The Ohio State University,Columbus, Ohio.Beeton, A.M. 2002. Large freshwater lakes: presentstate, trends, and future. Environ. Conserv. 29:21–38.Budd, J.W., Beeton, A.M., Stumpf, R.P., Culver, D.A.,and Kerfoot, W.C. 2001. Satellite observations ofMicrocystis blooms in western Lake Erie. Verh. Internat.Verein. Limnol. 27:3787–3793.Bunnell, D.B., Johnson, T.B., and Knight, C.T. 2005.The impact of introduced round gobies (Neogobiusmelanostomus) on phosphorus cycling in central LakeErie. Can. J. Fish. Aquat. Sci. 62:15–29.Burns, N.M., and Ross, C. 1972. Project Hypo. CanadaCentre for Inland Waters, Paper No. 6. United StatesEnvironmental Protection Agency, Technical ReportTS-05-71-208-24.Carrick, H.J., Moon, J.B., and Gaylord, B.F. 2005. Phytoplanktondynamics and hypoxia in Lake Erie: ahypothesis concerning benthic-pelagic coupling in thecentral basin. J. Great Lakes Res. 31 (Suppl. 2):111–124.Charlton, M.N., and Milne, J.E. 2004. Review of thirtyyears of change in Lake Erie water quality. NationalWater Research Institute Contribution No. 04-167.——— , Milne, J.E., Booth, W.G., and Chiocchio, F.1993. Lake Erie offshore in 1990: restoration andresilience in the central basin. J. Great Lakes Res.19:291–309.Conroy, J.D., and Culver, D.A.. 2005. Do dreissenidsaffect Lake Erie ecosystem stability processes? Am.Midl. Nat. 153:20–32.———, Edwards, W.J., Pontius, R.A., Kane, D.D.,Zhang, H., Shea, J.F., Richey, J.N., and Culver, D.A.2005a. Soluble nitrogen and phosphorus excretion ofexotic freshwater mussels (Dreissena spp.): potentialimpacts for nutrient remineralisation in western LakeErie. Freshwater Biology 50:1146–1162.———, Kane, D.D., and Culver, D.A. 2005b. Declining

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