Variation in Lake Michigan Plankton: Temporal, Spatial, and Historical Trends

J. Great Lakes Res. 27(4):467–485 Internat. Assoc. Great Lakes Res., 2001

Variation in Lake Michigan Plankton: Temporal, Spatial, and Historical Trends† Hunter Carrick*,1, Richard P. Barbiero2, and Marc Tuchman3 1Department

of Biological Sciences University at Buffalo Buffalo, New York 14060 2DynCorp

I & ET Inc. 6101 Stevenson Avenue Alexandria, Virginia 22304 3Great

Lakes National Program Office U.S. Environmental Protection Agency Chicago, Illinois 60604

ABSTRACT. Lake Michigan has been impacted by excessive material loading and invasion by exotic species; however, few studies have evaluated the recent basin-wide response of the lake to these changes, particularly given the reduction of phosphorus loads since the 1970s. From 1994–95, quarterly measurements were made of physical-chemical conditions, plankton biomass, and plankton species composition at 18 stations throughout the lake (n = 111). Sampling sites were clustered according to their physicalchemical similarity; these zones corresponded with depositional regions in the lake (Deep water, Shallow water, and Impacted regions). While plankton biomass did not vary among lake-zones, species composition was zone-specific suggesting that several factors (food web structure, nutrient cycling, and physical mixing) may determine the distribution of species throughout the lake. Plankton biomass and gross composition (phyla) were variable in time (seasons), and exhibited predictable succession patterns. Phytoplankton peaked in June corresponding with the upward mixing of nutrients, while zooplankton peaked during mid-stratification (August) when water temperatures were most warm. Finally, the basin-wide estimates for both total phosphorus and phytoplankton biomass were lower compared with historical estimates (measured in 1970s) and significant differences were not observed between near- and offshore regions. Despite this, the data also show that phytoplankton species composition varies widely throughout the lake, and that some nearshore sites do support impacted assemblages. INDEX WORDS: Lake Michigan, plankton, lake-zones, trends, total phosphorus.

INTRODUCTION The Saint Lawrence Great Lakes constitute 20% of the world’s supply of fresh water (Wetzel 1983), and have undergone much change over the past 100 years that can be related to human-induced physical, chemical, and biological perturbations (Colborn et al. 1990). The ability to measure such change is,

in part, limited by sampling intensity, given the size and the fact that perturbations are not expressed homogeneously throughout the Great Lakes basin (Harris 1984). For instance, nutrient loading has had a regional effect in Lake Michigan that required specific modeling of the response and loading restrictions (Schelske 1980). While phosphorus loading to Michigan has been reduced over the past 20 years, the in-lake response at a single offshore site is not clear (Johengen et al. 1994). Moreover, nonindigenous mussels (Driessensia polymorpha, and D. bugensis) have had measurable effects on water quality in nearshore regions in both Lakes Huron (Fahnenstiel et al. 1995) and Erie (Holland 1993),

*Corresponding author: E-mail: [email protected] Current address: School of Forest Resources, Fisheries Division, Pennsylvania State University, University Park, PA 16802 †In celebration of his retirement from academic service, this paper is dedicated to Claire L. Schelske for his contribution to our knowledge of the Great Lakes.

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although their influence on these lakes as a whole is not well understood (Nalepa and Fahnenstiel et al. 1999). Lake Michigan is the second largest of the five St. Lawrence Great Lakes (average depth 100 m), and is one of the largest lakes (surface area 57,750 km2, volume 4,920 km3) world-wide (Herdendorf 1982). The lake supports productive and important fisheries (Beeton 1969, Schelske and Carpenter 1992), and is a central resource for the large human population that surrounds it. Despite this, few studies have evaluated recent basin-wide conditions relative to the many changes that impinge on the lake, particularly the reduction of phosphorus loads since the 1970s. During the 1970s Rousar (1973) measured strong nearshore-offshore differences in total phosphorus (TP) and phytoplankton along a transect from Chicago to the center of the southern basin. Bartone and Schelske (1982) measured environmental conditions at 200 sites throughout the lake during the mid-1970s. Their results indicate that nearshore stations (on average) had higher chlorophyll, total-P, and chlorides, while water transparency was lower nearshore. During the 1980 to 1990s, other studies have measured conditions at select reference sites in the lake (Fahnenstiel and Scavia 1987). In this paper, basin-wide variation in water physical-chemical conditions and plankton abundance in Lake Michigan was assessed, and these conditions were evaluated relative to those determined from previous studies carried out in the 1970 to 1980s. Eighteen in-lake stations were sampled (northsouth, near-offshore) during key temporal periods along the seasonal progression (mixing, early-stratification, mid-stratification, and late-stratification; Fahnenstiel and Scavia 1987). The dataset was assembled by the U.S. Environmental Protection Agency and consisted of physical-chemical measures and phyto- and zooplankton species composition during the 1994–95 period (n = 111). The study addresses three specific hypotheses: 1) do physicalchemical conditions vary among sampling sites in Lake Michigan, such that sites can be grouped together (lake zones)? 2) do plankton biomass and taxonomic composition (phylum, division, order) vary in time (season) and space (sampling stations)? 3) do levels of total phosphorus and plankton biomass differ between nearshore and offshore sites, and are these levels different from those previously reported in the literature?

FIG. 1. Map of Lake Michigan indicating 18 sampling sites (and a single reference site in Lake Huron).

MATERIALS AND METHODS Lake Sampling Scheme Routine sampling was conducted in Lake Michigan from 1994–95 at 14 to 18 fixed, in-lake stations and one station in Lake Huron (n = 116, Fig. 1 and Table 1). The sampling sites were selected to provide information on a great range of conditions throughout the lake. The Lake Huron site served as a reference to contrast conditions in Lake Michigan with those outside the mixing zone between Lakes Superior and Michigan (Schelske 1985). Seven synoptic cruises were scheduled in order to sample during the four thermal periods that characterize the bulk of seasonal variation in Lake Michigan (Scavia and Fahnenstiel 1987): spring isothermy (April), initialstratification (June), mid-stratification (August), and

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TABLE 1. A summary of Lake Michigan sampling stations (1994-95) and one station in Lake Huron (#54). Stations were categorized into lake zones according to similarilies in physical-chemical conditions. Sampling Periods (n) Apr, Aug, Oct (5)

Station Location Latitude (N) Longitude (W) 45° 30′ 59″ 83° 24′ 58″

Impacted (3 stations) 05 32.6 24 40.6 72 27.3

Apr, Jun, Aug, Oct (7) Apr, Aug, Oct (5) Apr, Aug, Oct (5)

42° 00′ 02″ 45° 29′ 35″ 45° 48′ 18″

87° 25′ 04″ 87° 02′ 04″ 84° 55′ 01″

Shallow (7 stations) 110 12.5 140 37.8 180 67.7 240 42.2 280 82.5 310 12.6 340 40.9

Apr, Jun, Aug, Oct (6) Apr, Jun, Aug, Oct (7) Apr, Jun, Aug, Oct (6) Apr, Jun, Aug, Oct (7) Apr, Jun, Aug, Oct (7) Apr, Jun, Aug, Oct (7) Apr, Jun, Aug, Oct (7)

44° 40′ 47″ 44° 41′ 04″ 44° 40′ 56″ 43° 20′ 59″ 43° 21′ 17″ 42° 42′ 05″ 42° 40′ 58″

87° 20′ 29″ 87° 16′ 23″ 86° 13′ 37″ 87° 10′ 07″ 87° 14′ 47″ 86° 13′ 49″ 86° 19′ 10″

Deep (8 stations) 18 157.3 19 100.1 23 90.2 27 102.2 380 78.1 40 184.0 41 257.8 47 186.6

Apr, Jun, Aug, Oct (7) Apr, Aug, Oct (5) Apr, Jun, Aug, Oct (7) Apr, Jun, Aug, Oct (6) Apr, Jun, Aug, Oct (7) Apr, Aug, Oct (5) Apr, Jun, Aug (3) Apr, Jun, Aug, Oct (7)

42° 43′ 58″ 43° 00′ 58″ 43° 08′ 01″ 43° 36′ 08″ 42° 41′ 07″ 44° 45′ 43″ 44° 44′ 14″ 45° 10′ 35″

87° 00′ 01″ 86° 38′ 46″ 87° 00′ 01″ 86° 54′ 53″ 86° 27′ 28″ 86° 57′ 59″ 86° 43′ 20″ 86° 22′ 16″

Zone Station 54

Depth (m) 123.4

late-stratification just prior to fall isothermy (October). No June samples were collected in 1995. At each station, water column profiles for temperature, light transmission, and conductivity were measured by lowering a Seabird STE-19 CTD from surface to near bottom at 0.1 m intervals. Eleven physicochemical parameters were determined from whole water samples collected with a Niskin rosette sampler at depths of 1, 5, 10, and 20 m (Table 2). Phytoplankton samples were collected from equal aliquots of water gathered from these four depths; this composite sample was preserved with Acid Lugol’s solution prior to enumeration. Zooplankton were collected from vertical net hauls (0 to 20 m) using a 0.5 m Wisconsin-type net (mesh size 153 μm); these samples were narcotized and preserved with sugar formalin prior to enumeration. A pairwise comparison of several physical-chemical attributes (Table 2) revealed that estimates measured from integrated (0 to 20 m) and the average of discrete water column samples were not different (paired t-test, p > 0.05). Thus, this was used as a

basis for matching average water column data with integrated plankton information (biomass and taxonomic composition). Analytical Procedures Physicochemical Measurements Several physical-chemical attributes were determined from discrete water samples. Turbidity was measured using a nephelometror. Hydrogen ion concentration was measured using a standard pH meter, while alkalinity was determined by titrating subsamples with 0.1N HCL to a pH of 4.5. Concentrations of soluble and total nutrients (Si, N, and P) were measured on a Technicon II Autoanalyzer using standard colorimetric reactions. Total Kjeldahl nitrogen (TKN) was measured by an ultramicro semiautomated method (Jirka et al. 1976) and nitrate (NO3-N) was reduced to nitrite in a copper cadmium column (Armstrong et al. 1967). Total P (unfiltered) and soluble P (filtered through 0.45 μm

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Carrick et al. TABLE 2. Physical-chemical parameters measured among three lake zones in Lake Michigan (1994-95). Lake Zone Shallow n = 47 106.9 5.3

Parameter Alkalinity (μS/cm)

Statistic X SD

Impacted n = 17 96.6 8.3

Chloride (mg/L)

X SD

10.0 0.8

10.5 0.9

10.3 0.3

Conductivity (μS/cm)

X SD

251.3 24.3

283.1 15.1

267.6 25.4

Max. Depth (m)

X SD

33.4 5.8

42.5 24.5

137.3 54.3

Mixing Depth (m)

X SD

21.3 10.1

19.3 19.1

66.7 74.8

NO-2-NO3 (μg/L)

X SD

200.0 60.0

240.0 70.0

240.0 60.0

pH (units)

X SD

SiO2 (μg/L)

X SD

400.0 160.0

380.0 220.0

380.0 250.0

Temperature (°C)

X SD

13.1 6.7

11.8 6.7

11.4 7.4

Total P (μg/L)

X SD

4.9 1.4

4.8 1.6

4.7 1.2

Turbidity (NTU)

X SD

0.45 0.09

0.50 0.26

0.50 0.28

7.77 0.37

Millipore) were determined by digestion with persulfate, and analysis using the molybdenum blue method (APHA 1989). Soluble silica (SiO 2) was measured on filtered water (0.45 μm Millipore), following the industrial method no. 186-72W (Technicon Instrument Corp. 1973). Mixing depth was determined from each CTD profile, as the water column depth where changes in water temperature were > 1°C per meter (Wetzel 1983). Biological Measurements Phytoplankton biovolume and species composition were determined using the Utermohl technique (Utermohl 1958). Aliquots (25 mL to 50 mL) were

8.23 0.28

Deep n = 47 102.4 7.3

8.06 0.38

settled onto coverslips, and the entire area of the coverslip was systematically scanned with an inverted microscope (magnification 500X). All individuals encountered were identified to the lowest subgeneric level possible. In addition, diatom relative abundance was determined from permanent slides (magnification 1,250x). The data were collated with the Utermohl counts to estimate final cell densities for all diatom species. Zooplankton biomass and species composition were determined using a plankton counting wheel (McCaulay 1984). Again, all individuals encountered were identified to the lowest taxonomic level possible. Immature organisms were delineated by

Variation in Lake Michigan Plankton size and placed into categories (copepodite stages, nauplii). The cell and body volumes of all plankton species were estimated by determining the average dimensions from ten randomly chosen individuals of each taxon in each sample (magnification 200 to 400X). The average dimensions were then applied to the geometric configuration which best approximated the shape of each taxon (spheres, prolate spheres, and cylinders). Volumes were subsequently converted to biomass assuming a specific weight of 1.0 g/mL.

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sessed among common species using cluster analysis as described above. The similarity among common algal species (>10% of total biomass in one collection) was evaluated by comparing the sum of their biomass among all sites. Ecological niches were inferred from the collective autecology of the species placed into specific clusters by the analysis. Hierarchical clustering was used because it is sensitive to presence-absence of the observations, which is relevant to species composition data (Pielou 1984). RESULTS

Statistical Procedures Cluster analysis was used to classify the 19 inlake sampling sites according to their physicalchemical similarity (lake zones, Table 1). Similarity matrices were constructed (Euclidean distances), from which dendrograms were derived using complete linkage cluster analysis (Manly 1986). Cluster analysis was also run on values that had been converted to z-scores, to confirm the robustness of cluster results. The correspondence among lake sites was assessed by comparing their similarity among 11 physical-chemical variables (Table 2). All data used in this and the analyses described below were log transformed, and met assumptions of normality and homogeneity of variances (Zar 1983). Statistical analyses were performed using Statview (v.4.5) and Data Desk Pro (v. 5.0) for the Macintosh. The hypothesis that plankton biomass and taxonomic composition (Divisions of algae, Orders of crustaeans, and Phylum Rotifera) varied among sampling dates and lake zones (excluding station 54 in Lake Huron) was tested. The intent was to identify general temporal and spatial trends in these data using a tiered set of analyses. First, gross variation in plankton biomass was assessed using oneway analysis of variance (ANOVA), where lake zone, date, and year were considered single, fixed factors. Second, time and space dependent variation in plankton biomass and taxonomic composition were evaluated using one-way ANOVA, where date and lake zone were treated as blocked factors. This approach was necessary because single samples were enumerated from each sampling site-date combination, making it difficult to truly factor out separate effects of time and space. The blocked analyses statistically separated time versus space variation, given the inherent design of this study (Zar 1983). Third, distribution patterns were as-

Ambient Environmental Conditions and Lake Zonation Sampling stations were classified using hierarchical cluster analysis. All 18 Lake Michigan stations were classified into one of three lake zones based on their similarity in values for eleven physicalchemical variables (Fig. 2; Table 2). Eight sites formed the first cluster that occurred in deep waters near or beyond the 100 m depth contour (sites 47, 19, 27, 23, 380, 18, 40, and 41). The second cluster was composed of three impacted sites that were situated in or near major tributaries, such as the Straits of Mackinaw, Milwaukee Harbor, and Green Bay

FIG. 2. Similarity among sampling sites (as Euclidean distance) in terms of their physical and chemical attributes as determined by hierarchical cluster analysis. Site codes are listed in Table 1.

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Carrick et al.

(sites 72, 5, and 24, respectively). The remaining seven sites formed a third cluster that corresponded to a shallow water region inside the lake’s 100-m contour (sites 140, 110, 280, 180, 240, 340, and 310). Physical-chemical conditions in Lake Michigan varied spatially along nearshore-offshore gradient (Table 2). In terms of nutrients, dissolved silica were higher at nearshore (the sum of impacted and shallow sites) compared with offshore sites (unpaired t-test, t = 2.52, df = 31, p = 0.02). Alkalinity, chloride, conductivity, and pH showed little variation among sites (coefficient of variation, all < 10%). While nitrate, total-P, and turbidity demonstrated greater spatial variance, no significant differences existed between near and offshore sites (p > 0.05). As expected, water depth and mixing depth were higher at offshore sites. The water depth at sampling sites ranged from < 20 m along the southern shore to a depth of > 200 m at station 41 in northern offshore region (t = 7.22, df = 29, p < 0.0001). Similarly, mixing depth ranged from 5 to > 40 m, along this same near- to offshore gradient (t = 3.19, df = 29, p < 0.07). Variation in Plankton Biomass Both phyto- and zooplankton biomass varied significantly among sampling periods, while no gross differences were noted among lake zones (Fig. 3; Table 3). Phytoplankton biomass varied more than two-orders of magnitude among the samples analyzed over the 24-month study (n = 111, range 44 to 1,830 mg/m 3). Phytoplankton was highest at impacted sites compared with shallow and deep sites; however these differences were not significant (Fig. 3; Table 3). Seasonally, phytoplankton biomass was greatest during initial thermal stratification (June), followed by levels measured during mixing (April), while levels were lowest during the mid and late stratification (October and August). Moreover, biomass was greater in 1994 compared with 1995; this was true whether June samples were include or excluded from the analysis. Zooplankton biomass also varied more than twoorders of magnitude among the samples analyzed (n = 111, range 1 to 200 μg/L). Zooplankton did not vary along this near to offshore gradient (Fig. 3; Table 3). Zooplankton biomass was greatest during mid-stratification (August) compared with the other sampling periods, and no differences were observed between years. When analyzed separately using a blocked

ANOVA design, differences in the seasonal variation in plankton biomass were noted among lake zones (Fig. 3; Table 4). No significant differences in phytoplankton biomass among dates were observed for impacted sites, while biomass at shallow sites was greatest during June and April sampling periods. At deep sites, phytoplankton biomass was only higher in June. Zooplankton biomass in all three zones was highest in August, although these differences were most significant at deep sites. Very few differences in plankton biomass were observed among lake zones when evaluated during specific sampling dates. Distribution of Plankton Groups The phytoplankton assemblage was composed primarily (averaged over all dates and sites) of diatoms (44.5%), chrysophytes, (21.7%), and cryptophytes (17.7%). Several algal groups (chlorophytes, cyanobacteria, euglenoids, dinoflagellates) were minor contributors (< 10% each, collectively 16.1%) to total phytoplankton biomass (Fig. 4). The zooplankton assemblage was composed of cladocerans (24.4%), copepods, (23.9%), and rotifers (15.5%). Immature forms and nauplii were also abundant (18.1% and 17.9%, respectively), while several other animals (Mysis, Leptodora) were minor contributors (< 0.1%) to total biomass (Fig. 4). The timing and trajectory of phytoplankton seasonal succession differed among lake zones (Fig. 4; Table 5). At impacted sites, diatom biomass was greatest in April, while biomass of the other algal divisions (chrysophytes, cryptophytes and chlorophyte-cyanobacteria) showed no difference among sampling dates. In the shallow zone, diatom biomass differed among all dates, with the highest levels being realized in June and corresponding with a peak in chrysophyte biomass. Shallow cryptophyte biomass was similar in June, April, and October, and these levels were all higher than its biomass in August. No apparent temporal differences were observed for the chlorophytes-cyanobacteria group. Temporal succession in the deep zone was similar to that just described for the shallow zone. During specific thermal periods, phytoplankton groups were heterogeneously distributed throughout Lake Michigan (Fig. 4; Table 5). During isothermal mixing (April), only chrysophytes varied spatially, achieving their highest standing stocks occurring at impacted sites, followed by shallow sites, and being least abundant at deep sites. In June, diatoms were

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473

FIG. 3. Phyto- and zooplankton biomass measured among lake zones and sampling intervals in Lake Michigan (average + one standard error).

most abundant in the shallow zone, while cryptophytes and chlorophytes-cyanobacteria were more abundant in shallow and deep waters compared with the impacted sites. During the August sampling, the biomass of all four divisions were not different among zones, while in October, diatoms achieved higher biomass at the impacted and shallow sites. Zooplankton seasonal succession differed among lake zones; however, the temporal pattern was not consistent for all zooplankton groups (Fig. 4; Table 6). At impacted sites, the biomass of rotifers was greatest in August and October, relative to June and April sampling periods, while cladoceran biomass was highest in August. Copepod biomass was also high in August, occurred at intermediate levels in June and April, and was lowest in October. Nauplii biomass was low in April, peaked in August, and

occurred at intermediate levels in June and October. In the shallow zone, the biomass of rotifers and cladocerans steadily increased throughout the year, such that their biomass was low in April, reached intermediate levels in June, and peaked in August and October. Copepod biomass at shallow sites was similar in August, April, and June, but decreased significantly in October. Nauplii biomass was similar in June, August, and October, relative to lower standing stocks in April. Zooplankton temporal succession in the deep zone was similar to that just described for the shallow zone. Distribution of Plankton Taxa A total of 384 taxa were encountered during the course of the study. Of these, cluster analysis classified the 26 most common phytoplankton taxa into

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TABLE 3. Variation in plankton biovolume assessed with 1-way ANOVA (where **P < 0.01, and ***P < 0.001). Underlining indicates those elements that do not significantly differ (P < 0.05). Plankton Assemblage Phyto

Zoop

Main Factor Region Period Year

df 2 2 1

F-value 1.1 14.9*** 12.9**

Deep Aug 95

Region Period Year

2 2 1

1.2 10.5*** 1.7

Deep Apr 95

Pairwise Comparison (mean ranking low to high) Shallow Impact Oct Apr 94 Shallow Oct 94

Impact Jun

Jun

Aug

TABLE 4. Variation in plankton biovolume assessed with 1-way ANOVA (where +P < 0.1, **P < 0.01, and ***P < 0.001). Underlining indicates those elements that do not significantly differ (P < 0.05). Plankton Assemblage Phyto

Zoop

Blocked Factor Impacted Shallow Deep

df 13 43 43

April June August October

28 11 30 30

2.6+ 2.3 2.1 1.0

Impacted Shallow Deep

13 42 43

13.8*** 2.5+ 4.0**

April June August October

28 10 30 30

F-value 0.9 15.7*** 4.3**

0.1 0.4 0.6 0.6

three major groups based upon their temporal and spatial occurrence (Fig. 5, Table 7). The first cluster contained five taxa (Sphaerocystis schroeteri, Dictyosphaerium pulchellum, Aulocesira granulata, Mallomonas pseudocoronata, and Dinobryon cylindricum) that were distributed along a series of sites progressing from impacted, shallow, and finally to the deep water region of the lake. The second cluster was composed of two subclusters, each defining species groupings based upon their seasonal occurrence. The first subcluster consisted of six taxa that were widely distributed (ubiquitous) in time or space (Rhodomonas minuta, Rhizosolenia gracilis,

Pairwise Comparison (mean ranking low to high) Oct Aug Jun Oct Aug Apr Aug Oct Apr Deep Shallow Deep Shallow

Shallow Deep Shallow Deep

Impact Impact Impact Impact

Apr Apr Apr

Oct Oct Oct

Jun Jun Jun

Impact Deep Shallow Deep

Deep Shallow Deep Shallow

Shallow Impact Impact Impact

Apr Jun Jun

Aug Aug Aug

Cryptomonas erosa, Fragilaria crotonensis, Tabellaria flocculosa, and Aulocesira islandica). The second subcluster contained seven taxa that were most abundant during isothermal mixing to initialstratification (Gymnodinium helveticum, Asterionella formosa, Aulocesira italica v. subarctica, Chrysochromulina parva, Dinobryon sociale, Cyclotella comta, and Synedra ulna). The third cluster (eight taxa) was a mixed assemblage of diatoms, cyanobacteria, a cryptophyte, and a chrysophyte that were most abundant in impacted and shallow sites (Anabaena cyanaea, Cryptomonas spp., Stephanodiscus hantschii, Cyclotella comensis, Os-

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FIG. 4. Percent composition of phyto- and zooplankton taxonomic groups (as the sum of plankton biomass) measured among lake zones and sampling intervals in Lake Michigan.

cillatoria limnetica, Stephanodiscus niagarae, Anabaena flos-aquae, and Chrysospherella longispina). Common zooplankton taxa were also classified into three major groups based upon their temporal and spatial occurrence (Fig. 5, Table 7). The first cluster contained four zooplankton taxa (Daphnia retrocurva, Ceriodaphnia spp., Mesocyclops edax, and Notholoa spp.) that were most abundant at both impacted and shallow sites in the lake (nearshore assemblage). The second cluster grouped taxa into two subclusters based upon their temporal occurrence. Several taxa that were abundant during earlystratification were classified into the first subcluster (Leptodiaptomus spp., Cyclopoid copepodites, Leptodiaptomus ashlandi, Diayclops spp., and Daphnia galeata), while the second subcluster contained six

taxa that were abundant during mid-stratification (Polyartthra vulgaris, Mesocyclops spp., Leptodiaptomus minutus, Polyartthra major, Bosmina longirostris, and Asplanchna spp.). The last cluster contained eight zooplankton taxa that were most abundant in the deep region of the lake and were referred as an offshore assemblage (Limnocalanus macruus, Calaniod copepodites, Synchaeta spp., Keratella cochlearis, Epischura lacustris, Leptodiaptomus sicilus, Skistodiaptomus oregonensis, and Keratella crassa). DISCUSSION Environmental Variation in Lake Michigan Limited environmental differences were observed between nearshore (a composite of both impacted

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TABLE 5. Temporal and spatial variation in phytoplankton taxonomic composition assessed using 1-way ANOVA blocked by lake zone or date (where +P < 0.1, *P < 0.05, **P < 0.01, and ***P < 0.001). Underlining indicates those elements that do not significantly differ (P < 0.05). Taxonomic Group Bacillariophyta

Blocked Factor Impacted Shallow Deep April June August October

F-value 2.7+ 26.7*** 13.0*** 1.9 8.3** 0.7 3.4*

Oct Oct Oct Deep Impact Deep Deep

Chrysophyta

Impacted Shallow Deep April June August October

1.9 4.0** 4.8** 12.9*** 0.2 0.7 1.5

Aug Oct Apr Deep Deep Shallow Impact

Oct Aug Aug Shallow Shallow Deep Shallow

Apr Apr Oct Impact Impact Impact Deep

Jun Jun Jun

Cryptophyta

Impacted Shallow Deep April June August October

0.8 5.2** 3.3* 0.1 3.3+ 0.9 1.2

Jun Aug Aug Deep Impact Impact Impact

Aug Oct Oct Impact Deep Shallow Deep

Oct Apr Apr Shallow Shallow Deep Shallow

Apr Jun Jun

Chlorophyta/ Cyanobacteria

Impacted Shallow Deep April June August October

1.5 1.9 4.8** 0.3 3.8+ 0.3 1.2

Jun Apr Apr Deep Impact Shallow Shallow

Apr Oct Oct Shallow Shallow Deep Deep

Oct Aug Aug Impact Deep Impact Impact

Aug Jun Jun

and shallow sites) versus offshore sites during 1994–95; these findings contrast with studies during the 1970s that identified considerable spatial differences (Rousar 1973, Bartone and Schleske 1982). While strong site differences in plankton biomass and water chemistry were not evident in this study, dissolved silica concentrations were lower in nearshore waters (unpaired t-test, p < 0.05). In contrast, Bartone and Schelske (1982) measured significant nearshore (< 50 m depth) versus deep (> 50 m depth) differences in 4 of 6 water chemistry parameters. In their study, chlorophyll, total-P, and chloride were all higher at nearshore

Pairwise Comparison (mean ranking low to high) Jun Aug Aug Apr Aug Apr Shallow Impact Deep Shallow Shallow Impact Shallow Impact

Apr Jun Jun

sites, while dissolved silica was lower (unpaired ttest, p < 0.05). Their comparison was also based upon sampling from May to October in 1976 at 200 sites distributed throughout the lake. Rousar (1973) collected samples from May to October 1971 at 5 stations along a transect from Sturgeon Bay, WI to Ludington, MI. Although no statistical comparisons were made on these data, both chlorophyll-a and total-P concentrations were more than 2-fold higher at the nearshore compared with the offshore station. Despite the fact that near-offshore differences in plankton biomass were not observed, spatial variation in plankton species composition was measured

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TABLE 6. Temporal and spatial variation in zooplankton taxonomic composition assessed using 1-way ANOVA blocked by lake zone or date (where *P < 0.05, **P < 0.01, and ***P < 0.001). Underlining indicates those elements that do not significantly differ (P < 0.05). Taxonomic Group Rotifera

Blocked Factor Impacted Shallow Deep April June August October

F-value 6.0** 15.4*** 41.8*** 1.1 1.0 1.4 0.6

Apr Apr Apr Deep Deep Shallow Deep

Copepoda

Impacted Shallow Deep April June August October

16.9*** 2.9* 5.7** 0.2 0.1 0.9 0.9

Oct Oct Oct Impact Deep Deep Deep

Apr Jun Jun Deep Shallow Shallow Shallow

Jun Aug Aug Shallow Impact Impact Impact

Aug Apr Apr

Cladocera

Impacted Shallow Deep April June August October

6.3** 10.0*** 8.0*** 1.2 0.2 0.2 0.2

Jun Apr Apr Deep Impact Deep Deep

Apr Jun Jun Shallow Deep Shallow Shallow

Oct Oct Oct Impact Shallow Impact Impact

Aug Aug Aug

Immature/ Nauplii

Impacted Shallow Deep April June August October

12.5*** 3.0* 1.7 1.1 0.6 1.1 0.3

Apr Apr Apr Impact Deep Shallow Shallow

Oct Oct Oct Shallow Shallow Deep Deep

Jun Aug Jun Deep Impact Impact Impact

Aug Jun Aug

(see below). This finding is similar to previous studies in Lake Michigan, where distinct near versus offshore plankton assemblages were identified. These regional plankton assemblages were thought to be maintained by differences in the planktivorous predators between near and offshore sites that had little effect on zooplankton biomass, but did indeed coincide with shifts in species composition (Evans and Jude 1986, Lehman 1988). Regardless, the data seem to indicate that environmental conditions in near versus offshore waters in Lake Michigan have become more similar since the 1970s. The three lake zones identified here corre-

Pairwise Comparison (mean ranking low to high) Jun Oct Jun Oct Jun Oct Shallow Impact Shallow Impact Deep Impact Shallow Impact

Aug Aug Aug

sponded with the bathemetry of Lake Michigan (Cahill 1981, Conley et al. 1986). For instance, the deep water sites occurred over Cahill’s northern depositional basin, which is a long, deep depression (> 80 m depth) that runs up the axis of the north half of the lake or over the smaller Grand Haven depositional basin (Cahill 1981). The sites classified in the shallow zone group (< 80 m depth) were situated over the large non-depositional area either along the coastal shelf that extends around the perimeter of the lake, or along the shallow ridge that separates the southern and northern basins (Cahill 1981). The three sites categorized as im-

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Carrick et al.

FIG. 5. Similarity among species (as Euclidean distance) based on their temporal and spatial distribution in Lake Michigan, as determined by hierarchical cluster analysis. Species codes are listed in Table 4.

Variation in Lake Michigan Plankton pacted consisted of shallow (< 40 m depth) sites situated near major tributaries. For instance, the high nutrients and conductivity at site 24 near the mouth of Green Bay were most likely the product of high material loads there, which historically constitutes a large fraction of the total load to the lake (Schelske 1975). A similar situation occurs at the other two sites (5 and 72), which receive high material loads from urban centers in Milwaukee-Chicago and Grand Traverse Bay. High material loading in areas like the impacted sites have caused measurable declines in local dissolved silica concentrations and light transparency relative to the rest of the lake (Schelske and Callender 1970). The multivariate classification of these sites using cluster analysis was useful in resolving environmental zones in the Lake Michigan, and as expected, the analysis excluded the single Lake Huron site from the main classification given the lower conductivity of the water there (Schelske 1985). Seasonality in Plankton Biomass and Composition: Temporal Trends The seasonal changes measured here are characteristic of oligo- to mesotrophic lakes (Hutchinson 1967, Wetzel 1983), and typical for plankton assemblages in the upper Great Lakes (Munawar and Munawar 1981). Phytoplankton seasonal succession is generally influenced by a combination of nutrient availability and differential loss rates primarily attributable to sedimentation and grazing mortality (Scavia and Fahnenstiel 1987). Zooplankton seasonality is largely driven water temperature and food availability which influences growth and development (Hutchinson 1967, Balcer et al. 1984). However, changes in planktivore populations (fish and invertebrates) have led to shifts in zooplankton species composition and phytoplankton biomass (Scavia et al. 1986). The algal bloom observed throughout the lake during the spring mixing to initial stratification period (Fig. 3) was similar in magnitude to that described by Fahnenstiel and Scavia (1987) in offshore waters of Lake Michigan. The annual spring bloom is a common temporal feature in Lake Michigan (Bartone and Schelske 1982), as well as other temperate lakes (Hutchinson 1967, Wetzel 1983), that occurs when nutrient concentrations are high and zooplankton biomass is comparatively low. This bloom did not contain nuisance species, but rather diatoms (Asterionella formosa, Aulocesira italica v. subarctica, Cyclotella comta) and

479

chrysophytes (Chrysochromulina parva, Dinbryon sociale) that grow well under high light and turbulence (Fahnenstiel and Scavia 1987, Wetzel 1983). Available phosphorus and silicon that is mixed throughout the water column after ice-out (Conley et al. 1988) subsequently fuels phytoplankton growth that is limited by both nutrients in Lake Michigan (Schelske et al. 1986). The spring zooplankton assemblage was dominated by adult copepods (Cyclops spp., Leptodiaptomus ashlandii), immature copepidites and nauplii, and a cladoceran (Daphnia galeata; Fig. 5), all of which are also typical for the lake (Evans et al. 1980). The ability of adult calaniod copepods to graze on abundant spring nauplii (Warren 1983) and large diatoms (Vanderploeg 1994) may account for their prevalence during this thermal period (Fahnenstiel and Scavia 1987). Interestingly, the annual differences in phytoplankton biomass observed here are likely attributable to the timing of this spring bloom relative to the sampling, which is reflected by the relationship between spring phytoplankton biomass and temperature (r = 0.66, n = 45, p < 0.0001). The mixed phytoplankton assemblage observed at most sites following thermal stratification consisted of nanoflagellates (chrysophytes, cryptophytes, and chlorophytes) typical of the summer assemblage previously described for offshore waters in Lakes Michigan (Fahnenstiel and Scavia 1987), Huron (Carrick and Fahnenstiel 1989), Ontario (Gray 1987), and Superior (Munawar et al. 1978). High nanoflagellate growth rates (Carrick et al. 1992), coupled with their negligible sedimentation rates (Scavia and Fahnenstiel 1987), more than compensates for the grazing pressure exerted by the mixed zooplankton assemblage present during the summer (Carrick et al. 1991), and thus may explain their abundance throughout the lake. The smaller bloom of cryptophytes observed in the fall (October–November period) coincides with the release of nutrients during, or just prior to, isothermal mixing (Bartone and Schekske 1982, Carrick and Fahnenstiel 1989). Moreover, high concentrations of adult zooplankton following thermal stratification is likely attributable to the maturation of cladocerans (Bosmina longirostris) and rotifers (Asplanchna spp., Polyarthra major, and P. vulgaris). This seasonal progression is expected given more favorable temperatures required for growth and development by rotifers (Stemberger 1979, Stemberger and Evans 1984) and cladocera (Hawkins and Evans 1979) in Lake Michigan.

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Carrick et al. TABLE 7. Groupings of plankton taxa according to their distribution patterns in Lake Michigan as determined by cluster analysis. The order of taxa corresponds to the dendrograms that appear in Figure 5. Cluster Interpretation Taxon

Abundance (Greatest to least) Taxon Code Date Zone Phytoplankton Assemblage

Nearshore-Offshore Assemblage Sphaerocystis schroeteri Chod. Dictyosphaerium pulchellum Wd. Aulocesira granulata (Ehr.) Ralfs Mallomonas pseudocoronata Pre. Dinobryon cylindricum Ehr.

SPHsch DICpul AULgra MALcau DINcyl

Aug, Oct Oct Jun, Aug, Oct Aug Jun

24, 40, 110, 340 24, 340, 41 310, 24, 380, 5 23, 19, 340, 5 23, 72, 27,280,240

Ubiquitous Assemblage Rhodomonas minuta Skuja Rhizosolenia gracilis H.L. Smith Cryptomonas erosa Ehr. Fragilaria crotonensis Kitton Tabellaria flocculosa (Roth) Kutz. Aulocesira islandica

RHOmin RHIgra CRYero FRAcro TABflo AULisl

all dates Jun, Apr, Aug all dates Aug, Jun Oct Jun, Apr, Aug Jun, Apr

all sites all sites all sites all sites all sites all sites

Spring Assemblage Gymnodinium helveticum Penard Asterionella formosa Hass. Aulocesira italica Mull Chrysochromulina parva Lackey Dinobryon sociale Imhof Cyclotella comta (Ehr.) Kutz Synedra ulna (Nitz.) Ehr.

GYMspp ASTfor AULita CHRpar DINsoc CYCcom SYNuln

Apr, Jun Jun Jun, Apr Jun, Apr Jun Aug Jun

5, 110, 72, 310 all sites all sites 280, 23, 5, 19,140 280, 27, 23, 380 24, 5, 140, 40 340, 380, 110, 140

Impacted-Nearshore Assemblage Anabaena cyanaea Dr. & Daily Cryptomonas spp. Stephanodiscus hantschii Grun. Cyclotella comensis Grun. Oscillatoria limnetica Lemm. Stephanodiscus niagarae Ehr. Anabaena flos-aquae (Lyngb) Breb Chrysospherella longispina Lautb.

ANAcya CRYspp STEhan CYCcom OSClim STEnia ANAflo CHRlon

Aug, Oct all dates Apr Aug, Oct Jun all dates Aug, Oct Oct

24, 40, 180 310, 24,40,280, 27 310, 18, 380 72, 110, 5, 40,180 110, 340 72, 24, 280 280, 40, 340 19, 18, 240, 23, 5

Cluster Interpretation Taxon Zooplankton Assemblage Nearshore Assemblage Daphnia retrocurva Forbes Ceriodaphnia spp. Mesocyclops edax Forbes Notholca spp.

Taxon Code

DAPret CERspp MESeda NOTspp

Date

Aug Aug Aug Apr, Aug

Greatest Abundance Zone

24, 180, 110 24, 110, 140,180 24, 110 24, 110 (Continued)

Variation in Lake Michigan Plankton TABLE 7.

481

(Continued) Taxon Code

Greatest Abundance Date Zone

Cluster Interpretation Taxon Early-Stratification Assemblage Leptodiaptomus Nauplii Copepodite Nauplii Leptodiaptomus ashlandii Mar. Cyclops spp. Daphnia galeata Sars

LEPnau COPnau LEPash CYCspp DAPgal

Aug, Jun, Oct Aug, Jun, Apr Aug, Apr, Jun Aug, Jun, Apr Aug

all sites all sites all sites all sites 47, 240, 280

Late-Stratification Assemblage Polyartthra vulgaris Carlin Cyclops Nauplii Leptodiaptomus minutus Lillj. Polyartthra major Burckhardt Bosmina longirostris O.F. Muller Asplanchna spp.

POLvul CYCnau LEPmin POLmaj BOSlon ASPspp

Aug, Oct Aug, Jun, Oct Aug, Apr Aug, Oct Aug, Oct Aug, Oct

all sites all sites all sites all sites 110,24,72,140 24, 72, 18, 47

Offshore Assemblage Limnocalanus macruus Sars Limnocalanus Nauplii Synchaeta spp. Keratella cochlearis Gosse Epischura lacustris Forbes Leptodiaptomus sicilus Forbes Skistodiaptomus oregonensis Lil. Keratella crassa Ahlstrom

LIMmac LIMnau SYNspp KERcoc EPIlac LEPsic SKIore KERcra

Jun, Apr Apr Oct Aug Oct, Aug Apr Aug Aug

27, 23, 280, 380 all sites 18, 280, 240, 27 all sites all sites 240, 380, 23 24, 47, 180, 41 all sites

Zonation of Plankton Species Composition: Spatial Trends Environmental zones supported unique plankton assemblages, despite the fact that plankton biomass did not vary widely throughout Lake Michigan (Tables 3 to 6). Much of the spatial variation in species composition observed in this study occurred along a nearshore-offshore gradient. Some of these differences are likely the result of differences in food web structure, nutrient supply, and physical mixing regimes between lake regions. Distinct near versus offshore zooplankton assemblages have been noted in earlier studies (Hawkins and Evans 1979, Bartone and Schelske 1982, Gannon et al. 1982). The nearshore assemblage of zooplankton identified was composed of cladocera (Ceriodaphnia, Daphnia retrocurva) and the copepod Mesocyclops edax, all of which are adapted to warmer average temperatures (Balcer et al. 1984). At the same time, offshore sites supported a zooplankton assemblage dominated by adult calanoid copepods (Limnocalanus macrurus, Leptodiaptomus sicilus, L. oregonensis, Epischura lacustris) and im-

mature copepods, all of which are likely remnants of the winter assemblage that can persist throughout the year (Evans et al. 1980). This spatial variation in zooplankton species composition has also been attributed to differences in food web structure between these regions. For example, Evans (1990) identified a similar offshore zooplankton assemblage consisting of these larger body-sized species, which she related to a relaxation in planktivorous fish predation in offshore waters. It is not surprising that the impacted-shallow region supports a unique phytoplankton assemblage that may be shaped in part by their proximity to both external and internal nutrient loads. High nearshore loads can result from wind resuspension of nutrient-laden sediments, and upwelling of nutrient-rich hypolimnetic water, thereby promoting shifts in plankton species compositions over large coastal regions in the Great Lakes (Schelske et al. 1980, Dunstall et al. 1990). The impacted phytoplankton assemblage observed here was composed of species capable of tolerating considerable environmental degradation. In particular, Anabaena cyanea and A. flos-aquae are indicators of moderate

482

Carrick et al. TABLE 8. Comparison between historic and current estimates for total phosphorus and phytoplankton biomass in Lake Michigan. Parameter Nearshore Year Value Total Phosphorus (μg/liter) 1970 15.2 1977 8.3 1994–95 5.0 Phytoplankton Chlorophyll-a (μg/liter) 1970 4.7 1977 2.8 1994-95 0.7

Offshore Value

Ratio

Literature Source

8.1 7.2 4.5

1.87 1.15 1.11

Rousar 1973 Bartone and Schelske 1982 This study

2.1 1.8 0.5

2.23 1.56 1.23

Rousar 1973 Bartone and Schelske 1982 This study

Phytoplankton Biomass (mg/m3) 1970 840 160 5.25 Munawar and Munawar 1975 1994-95 444 382 1.16 This study Values for Rousar (1973) were taken from his Table 1. Values for Bartone and Schelske (1982) were taken from their Table 3. Values for this study represent average estimates for the nearshore (both impacted and shallow sites) and offshore regions (deep sites).

cultural eutrophication in Green Bay (Stoermer and Stevenson 1979), Saginaw Bay, Lake Huron (Stoermer and Theriot 1985), and western Lake Erie (Munawar and Munawar 1981); similar cyanobacterial species have also been associated with silica depletion (Schelske et al. 1971). Stephanodiscus niagarae and S. hantschii also tend to thrive in areas receiving high nutrient loads in the Great Lakes (Stoermer and Stevenson 1979). Cyclotella comensis became dominant in the Great Lakes after 1970 in areas of high nutrient loading (Stoermer and Tuchman 1979), possibly because it is thought to be a superior competitor for silicon. Cryptomonas spp., Oscillatoria limnetica, and Chrysosphrella longispina all thrive in enriched nearshore areas in the Great Lakes (Stoermer and Stevenson 1979). An assemblage was also identified that reflects near-offshore coupling, whereby a set of species occurred along a series of sites extending from the nearshore out into open water. In northern Lake Michigan, the distribution of both Sphaerocystis schroeteri and Dictosphaeria pulchllum extended from nearshore Green Bay out to sites 40 and 41 in the offshore waters, while in the southeastern portion of the lake Aulocesira granulata extends nearshore from site 310 offshore to site 380. Such near to offshore couplings can be induced by strong winds that transport distinct assemblages from nearshore bays and coastal sites into adjacent offshore waters (Schelske et al. 1974). Similar to our work, Schelske et al. (1983) recorded a distribution pattern for sev-

eral species that extended from locally enriched regions of Green Bay out into the open water region. It is presumed that these populations are seeded from local nutrient sources and eventually are carried to deep water according to predominant water circulation patterns that can link near and offshore regions in both southern and northern depositional basins in Lake Michigan (Schwab 1983). Several species were widely distributed throughout the lake and were not limited in their occurrence. Of these, Cryptomonas erosa and Rhodomonas minuta are two of the most abundant, widespread species in the Great Lakes (Munawar and Munawar 1981, Carrick and Fahnenstiel 1995), perhaps due to their swift growth rates (Carrick et al. 1992). Similarly, the diatoms Rhizosolenia gracilis, Fragilaria crotonensis, and Tabellaria flocculosa are widely distributed in Lake Michigan and the Great Lakes as a whole (Munawar and Munawar 1975, Stoermer 1978). The extensive distribution of these diatoms is not surprising, given that they tolerate a broad range of temperature (Stoermer and Ladewski 1976) and nutrient conditions (Lowe 1974). Status of the Lake Michigan Ecosystem: Historical Trends Historically, near to offshore differences in plankton biomass and water quality have been observed throughout the St. Lawrence Great Lakes, and are viewed as an indication of cultural eutroph-

Variation in Lake Michigan Plankton ication from nearshore sources (Schelske 1980). For instance, Glooschenko et al. (1973) identified distinct distribution patterns for both chlorophyll and primary production in Lake Huron, where values measured in Saginaw Bay were significantly higher compared with those determined at open water sites. Kwiatkowski (1978, 1984) also observed differences in nearshore and offshore sites in Lakes Ontario and Huron, and he attributed these differences to nearshore point-source discharges of nutrients. By the same token, phosphorus reduction practices appear to be responsible for improvements in water quality in Lake Erie (Makarewicz and Bertrum 1991) and Lake Ontario (Gray 1987, Schelske 1991, Johengen et al. 1994). Such improvements are particularly evident close to nutrient inputs, which may serve as an index of system-wide recovery (Schelske 1980). While Lake Michigan has experienced significant phosphorus load reductions over the past 20 years, the response of the lake appears to be complex. TP values have increased and chlorophyll has remained unchanged at an offshore site that has been monitored from 1980 to 1990 (Johengen et al. 1994). Using the data from this study, the basin-wide average for total phosphorus concentration appears to have decreased since the early 1970s, and little difference now exists between nearshore versus offshore waters (Table 8). TP estimates derived from transect data taken during the early 1970s, indicate that nearshore concentrations (15.2 μg/L) were approximately 2-fold higher than offshore (8.1 μg/L) values (Rousar 1973), and both values were larger than the TP estimates reported here. Despite the limited temporal resolution of the sampling in this study, it does provide a more basin-wide comparison (18 sites distributed throughout the lake), although there are limitations in drawing such comparisons. Concomitant with lower TP values, the 1994–95 phytoplankton biomass estimates reported here are lower compared with those measured during the early 1970s (Rousar 1973, Bartone and Schelske 1982), and nearshore estimates are now similar to those measured offshore (Table 8). Having said this, there are still observed differences in species composition between near and offshore regions in the lake. The shallow and deep-water phytoplankton assemblages were similar to those described by Bartone and Schelske (1982) in 1976, and Fahnenstiel and Scavia (1987) for the 1983 to 1986 period. The impacted assemblage observed here was defined in part by several nuisance cyanobacteria species, although they occurred at lower levels rela-

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tive to their prevalence during the early 1970s when material loading to the lake was comparatively high (Danforth and Ginsburg 1980, Schelske and Stoermer 1971). The similarity identified here between near versus offshore TP and phytoplankton biomass is consistent with the idea that Lake Michigan may be achieving some equilibrium with external nutrient loading. If the estimates are an adequate sample of basin-wide TP concentrations, then such a reduction would appear to be commensurate with reductions in P-loading to the lake (Johengen et al. 1994). Despite this, the data also show that phytoplankton species composition varies widely throughout Lake Michigan, and that some nearshore areas do support impacted assemblages. ACKNOWLEDGMENTS We thank the crew of the R/V Simmons for their assistance in collecting the field samples. J. Goldsmith helped to compile some of the data. The manuscript benefited from the comments of two anonymous reviewers. This research was supported by U.S. EPA grant # 985551010 to H. Carrick. REFERENCES APHA. 1989. Standard methods for the examination of water and wastewater. American Public Health Association, Washington, D.C. Armstrong, F.A.J., Stearns, C.R., and Strickland, J.D.H. 1967. The measurement of upwelling and subsequent biological processes by means of the Technicon AutoAnalyzer and associated equipment. Deep Sea Res. 14:381–389. Balcer, M.D., Korda, N.L., and Dodson, S.I. 1984. Zooplankton of the Great Lakes: A guide to indentification, and ecology of the common Crustacean species. Madison: Univ. of Wisconsin Press. Bartone, C.R., and Schelske, C.L. 1982. Lake-wide seasonal changes in limnological conditions in Lake Michigan in 1976. J. Great Lakes Res. 8:413–427. Beeton, A.D. 1969. Changes in the environment and biota of the Great Lakes. In Eutrophication: causes, consequences, correctives, ed. G.A. Rohlich, pp. 150–187. Nat. Acad. Sci., Washington. Cahill, R.A. 1981. Geochemistry of recent Lake Michigan sediments. Illinois State Geological Survey, Champaign, IL, Circular 517. Carrick, H.J., and Fahnenstiel, G.L. 1989. Biomass, size structure, and composition of phototrophic and heterotrophic nanoflagellate communities in Lakes Huron and Michigan. Can. J. Fish. Aquat. Sci. 46:1922–1928. ——— , and Fahnenstiel, G.L. 1995. Common planktonic

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