Hydrobiologia 377: 57–71, 1998.© 1998Kluwer Academic Publishers. Printed in Belgium. 57

Temporal variation in plankton assemblages and physicochemistryof Devils Lake, North Dakota

Harry V. Leland1 & Wayne R. Berkas21 U.S. Geological Survey, 3215 Marine Street, Boulder, CO 80303, U.S.A.2 U.S. Geological Survey, 821 East Interstate Avenue, Bismarck, ND 58501-1199, U.S.A.

Received 10 November 1997; in revised form 18 February 1998; accepted 26 March 1998

Key words:saline lakes, climate, nitrogen limitation, phytoplankton, zooplankton, community structure

Abstract

Seasonal and annual variation in biomass and structure of algal assemblages of hyposaline Devils Lake were ex-amined in relation to turbidity, ambient concentrations of major ions, trace elements and nutrients, and the standingcrop of herbivores. Lake level declined during the early years of study, but rose markedly in subsequent years ashistorically large volumes of water flowed into this hydrologically-closed basin. Winter algal assemblages weredominated (in biomass) most years by small, non-motile chlorophytes (Choricystis minor, Kirchneriella lunarisor Dunaliella sp.), orEuglenasp. in the most saline sub-basin. Spring assemblages were dominated by diatoms(Stephanodiscuscf. minutulus, Surirella peisonis, Cyclotella meneghinianaandEntomoneis paludosawere espe-cially prominent) or chlorophytes (C. minor) until the lake level rose.C. minorabundances then declined in springassemblages and diatoms (Stephanodiscuscf. agassizensisandS. niagarae; E. paludosain the more saline sub-basins) dominated. The potential for nitrogen-deficient conditions for phytoplankton growth was evidenced mostsummers and early autumns by consistently high concentrations of reactive-P relative to inorganic-N and blooms ofthe N-fixing cyanophyteAphanizomenon flos-aquae; Microcystis aeruginosatypically was a co-dominant (>30%of biomass) in these assemblages. Pulses of diatoms (S.cf. agassizensisandC. meneghiniana) occurred in summersfollowing unusually prolonged periods of calm weather or large water inflows. Physical (irradiance, turbulence)and chemical (major nutrients) variables were the primary factors associated with phytoplankton growth. Trans-parency and major nutrient concentrations accounted for more of the annual variation in phytoplankton structurethan did salinity. Seasonal abundance patterns of the dominant zooplankton (the copepodDiaptomus sicilis; thecladoceransCeriodaphnia quadrangula, Chydorus sphaericus, Daphnia pulexandDiaphanosoma birgei; and therotifersBrachionusspp.,Filinia longiseta, Keratella cochlearisandK. quadrata) also indicated variation in algalpopulations related to grazing.

Introduction

Annual variation in algal assemblages of hyposaline(3–20 g l−1 TDS) lakes in North America is poorlycharacterized, as are the environmental factors con-tributing to changes in community structure. Thephytoplankton of Pyramid Lake, Nevada, (5,300 mgl−1 TDS) is generally dominated by diatoms (com-monly Cyclotella choctawhatcheena(= kuetzingiana)andStephanodiscusspp.) in early spring, by diatomsand chlorophytes during summer, and by bloomsof Nodularia spumigenaduring summer-autumn in

some years (Galat et al., 1981; 1990). In WalkerLake, Nevada,N. spumigenaregularly dominatedthe summer phytoplankton as salinity increased from6000 to 10 000 mg l−1 TDS, with C. choctawhatch-eena, Botryococcus brauniiandDiatoma vulgarisalsoabundant; diatoms, includingChaetoceros elmorei,dominated the winter assemblage (Koch et al., 1977).Transport of allochthonous organic matter to thesedesert lakes is low, as is the amount of terrestrialnitrogen loading (Galat & Verdin, 1988). As withmany terminal lakes in arid and semi-arid areas, nu-

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Figure 1. Location of sampling sites in Devils Lake.

trient removal is due primarily to sedimentation andpermanent burial, and N-deficient conditions exist insummer (Lebo et al., 1992).

We examine seasonal and annual variation in algalbiomass and structure of phytoplankton assemblagesof the major sub-basins of Devils Lake, North Dakota,in relation to ambient concentrations of major ions,trace elements and nutrients, and the standing crop ofherbivores. The phytoplankton composition of DevilsLake previously was described by several investigators(Young, 1924; Anderson & Armstrong, 1966; Verch &Blinn, 1971) in years when the lake was considerablysmaller and more saline. The early years (1988–1992)of this study were ones of decreasing lake levels;however, in subsequent years (1993–1994)historicallylarge volumes of water flowed into the basin.

Closed-basin lakes in regions with a negative wa-ter balance, such as Devils Lake, can be a sourceof high-resolution records of past climates. Salinityreconstructions from diatom assemblages of DevilsLake faithfully track post-1900 measured variation inlake-water salinity (Fritz, 1990). However, the reliabil-ity of diatom inference models depends on knowledgeof the modern distribution of diatoms in relation toenvironmental variables controlling community struc-ture. We show that turbidity and major nutrient con-centrations account for more of the annual variationin phytoplankton structure than does salinity during aperiod (1988–1994) encompassing both drought andwet years, and that annual variation in communitystructure is high. Phytoplankton composition duringthe period of study in this shallow, turbulent lake was

characterized by low species diversity and pronouncedshifts in abundance of dominant species. Informationon the effects of frequent water-column mixing onphytoplankton dynamics generally is lacking for lakesin North America (Agbeti et al., 1997).

Study area

Devils Lake is part of a large hydrologically-closeddrainage system within the Red River of the NorthBasin (Figure 1). It consists of a series of lake sub-basins interconnected during periods of high water(as at present), but isolated during drier periods. Thelake morphometry is simple, with an abruptly-slopinglittoral area and a broad flat-bottomed pelagic zone.The lake has a present-day (1994) maximum depth of10 m. The topography of the drainage basin is hum-mocky, with shallow depressions and poorly-definedwater divides (Hobbs & Bluemle, 1987). The basinis blanketed by glacial drift derived from CretaceousPierre Shale and Pleistocene lacustrine sediments.

The hydrologic budget of Devils Lake is tiedclosely to climate, and fluctuations in the balance be-tween precipitation and evaporation result in majorchanges in lake level (Wiche, 1986) and major-ionconcentrations. Movement of water within the lakeis generally to the east, resulting in a salinity gra-dient of increasing concentration from west to east.The East Devils Lake sub-basin is isolated from Dev-ils Lake at water elevations less than 434 m (a.s.l.).The lake does not stratify thermally during ice-freeperiods, but there is an inverse temperature gradientin winter (Sando & Lent, 1995). During ice-free pe-riods, dissolved-constituent concentrations generallyare distributed uniformly with depth due to wind-driven circulation. However, the potential exists foranoxia in deeper waters during extended calm periodsin summer and under ice-cover in winter.

Methods

Water analyses

Samples taken to determine concentrations of chemi-cal constituents in water and to quantify biomass andstructure of algal assemblages were a composite ofwater from three depths of the photic zone (>1% ofincident radiation). Water was collected using a 4 lKemmerer sampling device just below the surface,

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mid-depth in the photic zone, and at 1% of incidentradiation. The depth of the photic zone (determinedusing a LI-COR quantum sensor) varied seasonallyand with sub-basin sampled, but ranged from<0.5 mto 6 m. Water transparency was measured with a20 cm Secchi disk. Seasonal (at least quarterly) watersampling was initiated in February 1988 and contin-ued through October 1994 at five locations in DevilsLake (West, Sixmile, Creel, Main, and East Bays)and in East Devils Lake. Mission Bay and the west-ern section of East Bay also were sampled the firstthree years of the study. Analytical methods for chem-ical constituents in water are described by Fishman& Friedman (1985); field procedures are describedby Sando & Sether (1993). Water analyses were con-ducted at the National Water Quality Laboratory of theU.S. Geological Survey.

Biological analyses

Biomass of observed algal species and density andage structure of planktonic invertebrate populationswere determined seasonally at all sites from Septem-ber 1988 through October 1994, and biweekly in WestBay, Main Bay, East Bay and East Devils Lake dur-ing the ice-free months of 1991. 1991 was a droughtyear characterized by low lake levels, excess supply ofnutrients at all times, and dominance ofMicrocystisaeruginosa. Duplicate sub-samples of the compos-ite water sample were preserved in 10% acid-Lugol’ssolution (APHA, 1989), and algal species were enu-merated following the method of Utermöhl (1958).Cells greater than 30µm in diameter were countedfirst at×125 magnification; smaller taxa then wereenumerated at×1250 using the strip-count method(APHA, 1989). Diatoms were identified after clearingin 30% hydrogen peroxide. Biovolumes of the moreabundant taxa were estimated by measuring cell di-mensions of 50 to 100 individuals, and using closestgeometric formulae (Willen, 1976; Tikkanen, 1986).Biovolume estimates for the less abundant taxa weremade from fewer measurements. Conversion of algalbiovolume to algal biomass was based on a specificdensity of 1.0 g cm−3. Total algal standing stock wasestimated from chlorophylla determinations (Shoaf &Lium, 1977).

Duplicate vertical hauls (50µm mesh net) throughthe water column were used to sample the zooplank-ton. The small mesh size permitted quantitative sam-pling of rotifers. Identification and enumeration ofpreserved (5% formalin) samples were conducted us-

Figure 2. Variation in dissolved solids concentration (residue at180◦C), alkalinity and lake level (meters a.s.l.) in Devils Lake. EastDevils Lake was sampled at its inlet until 1990, and in its main baythrough the remainder of the study. Variation in dissolved solids andalkalinity in Creel Bay was nearly identical to that of Main Bay;data for Creel Bay were omitted for sake of clarity.

Figure 3. Major-ion composition of waters in Devils Lake – sum-mer 1994.

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ing a four slot (1 ml) counting chamber. All animalsin eight slots were counted; whole sample counts wereused for rare species. Identifications and enumerationswere conducted by Richard Dufford (phytoplankton)and Robin Dufford (zooplankton) of Fort Collins,Colorado.

Summarization and analysis of data

Summarization of phytoplankton composition andenumeration data for each season was conducted pri-marily by correspondence analysis (CA), an indirect-gradient ordination (Hill, 1979), and canonical corre-spondence analysis (CCA), a direct-gradient method(ter Braak & Verdonschot, 1995). Stratification byseason was used to reduce seasonal variation in al-gal abundances and chemical constituents in order tofocus on inter-annual and inter-site patterns. Interpre-tations of patterns in community structure based onCA and CCA were consistent, and measured environ-mental variables accounted for a significant portionof the explained variance in CCA. Eigenvalues foraxes 1 and 2 decreased by 0.08 to 0.11 in the sepa-rate (seasonal) ordinations if environmental variableswere included (comparing CA and CCA results), andthe percent variance of species-environment relationsincreased on all axes (by 12–16% on axis 1). Bothordination analyses were performed using CANOCO3.1 (ter Braak, 1990). Species-abundance data weretransformed (log10) to reduce effects of highly vari-able population densities on ordination scores. Rarespecies (present in<2% of samples) were excluded,so summary distributions emphasize the more com-monly occurring and abundant taxa. Forward selectionof environmental variables and Monte Carlo permuta-tions were used in CCA to identify a subset of the mea-sured variables that exert statistically significant andindependent influences on algal distributions. Environ-mental variables with high variance inflation factors(>10) in CCA (ter Braak, 1990) were excluded.

Results

Major ion and nutrient concentrations

Dissolved-solids concentrations (TDS) in lake wa-ter varied inversely with lake level during the periodof study (Figure 2). When annual evaporative lossesexceeded annual inflows through direct precipitationand surface drainage, the lake level decreased andTDS concentrations increased at all sites. Conversely,

the high inflows of 1993 and 1994 contributed todecreases in TDS concentration. The major-ion com-position of water in West Bay and Sixmile Bay wassimilar to that of the inflow water. Equivalent concen-trations of all major ions generally increased eastwardthrough Devils Lake and East Devils Lake, but Na,SO4 and Cl were enriched relative to the other majorions (Figure 3). Relative decreases in Ca and alkalinity(Figure 2) were due to precipitation of CaCO3; satu-ration indices for selected minerals from all sites indi-cated supersaturation with respect to calcite (Sando &Lent, 1995).

Significant (p< 0.05) differences (Kruskal-Wallisone-way ANOVA on ranks, Dunn’s test) amongsites existed for inorganic nitrogen (NO2-N + NO3-N + NH4-N), organic nitrogen, soluble-reactive phos-phorus (SRP) and silica (Table 1). Concentrations oforganic N generally were greater in West Bay, EastBay and East Devils Lake than in Main Bay, SixmileBay and Creel Bay in winter, and greater in WestBay and East Bay in autumn as densities of the dom-inant phytoplankton declined. However, during yearsof high water inflow (1993–1994), organic N concen-trations in West Bay decreased to levels existing inMain Bay and Sixmile Bay. SRP concentrations gener-ally also were greater in West Bay, East Bay, and EastDevils Lake than in the other bays in winter. Duringyears of high water inflow, SRP concentrations in WestBay approached concentrations in Sixmile and MainBays. The temporal variation in SiO2 concentration in-dicated a potential for severe depletion (< 0.5 mg l−1

SiO2 – e.g. Tilman et al., 1982) during periods of max-imum diatom production, and a high rate of internalcycling. Concentrations of SiO2 were less in East Bayand East Devils Lake than elsewhere, and declined atall sites during years when annual evaporative lossesexceeded annual water inflow.

Consistently high concentrations of SRP relativeto inorganic N at all sites (Table 1) and the regularappearance of N-fixing algae in late summer indicatethat Devils Lake currently is potentially N-deficient inlate summer. Median total N:P ratios for sub-basinssampled ranged from 13 to 27 for the period of study.These ratios indicate balanced growth with respectto these two nutrients (e.g., Rhee & Gotham, 1980).However, soluble N:P ratios were consistently low, aswere concentrations of inorganic N; median solubleN:P ratios ranged from 0.5 to 3.7 (only West Bay wasmore variable).

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Table 1. Median (range) in concentrations of inorganic nitrogen, organic nitrogen, soluble-reactive phosphorus and silica, and the N:P ratiosfor each season during the years 1989–1994. (Silica concentrations are for the years 1989–1992, as this constituent was not determined in1993–1994.)

Inorganic N (mg l−1) Organic N (mg l−1) PO4-P (mg l−1) SiO2 (mg l−1) Soluble N:P Total N:P

West Bay

Feb. 0.62 (0.33–1.8) 4.3 (2.6–5.1) 0.27 (0.22–0.35) 35 (22–41) 2.0 (1.9–8.1) 14 (7.9–21)

May 0.07 (0.05–0.08) 2.2 (1.9–8.6) 0.01 (<0.01–0.01) 12 (7.0–18) 6.0 (4.0–7.0) 15 (12–22)

July-Aug. 0.05 (0.05–0.07) 3.8 (1.6 -5.5 ) 0.04 (<0.01–0.14) 20 (11–31) 1.1 (0.4–4.0) 15 (9.8–22)

Oct. 0.20 (0.07–1.9) 3.9 (2.0–5.0) 0.01 (0.01–0.11) 21 (16–26) 15 (6.0–90) 19 (12–43)

Sixmile Bay

Feb. 0.22 (0.15–0.29) 2.7 (2.4–3.1) 0.14 (0.06–0.22) 25 (21–29) 1.8 (1.3–2.3) 17 (8.8–25)

May 0.08 (0.05–0.13) 2.5 (2.3–2.6) 0.03 (0.02–0.16) 17 (13–21) 2.7 (0.3–4.0) 27 (9.8–33)

July-Aug. 0.05 (0.03–0.30) 3.1 (1.3–4.3) 0.10 (0.02–0.28) 17 (15–28) 0.5 (0.3–2.5) 14 (4.5–33)

Oct. 0.08 (0.03–1.5) 2.2 (1.8–3.1) 0.10 (0.02–0.19) 23 (13–27) 1.0 (0.1–12) 15 (7.6–36)

Creel Bay

Feb. 0.24 (0.13–0.26) 2.6 (2.2–2.9) 0.04 (0.04–0.20) 25 (20–29) 3.0 (1.3–5.8) 26 (9.1–34)

May 0.14 (0.04–0.47) 2.7 (1.0–3.0) 0.09 (0.02–0.20) 20 (14–26) 1.5 (0.4–5.1) 22 (4.0–41)

July-Aug. 0.05 (0.04–0.34) 3.4 (1.7–4.3) 0.12 (0.01–0.21) 18 (0.5–26) 0.5 (0.2–3.0) 15 (9.9–25)

Oct. 0.07 (0.04–1.7) 2.3 (1.8–3.2) 0.05 (0.01–0.19) 22 (12–27) 3.6 (0.2–48) 19 (6.7–51)

Main Bay

Feb. 0.26 (0.17–0.39) 2.6 (2.3–2.9) 0.09 (0.06–0.20) 24 (20–28) 2.7 (1.3–4.2) 20 (9.4–31)

May 0.12 (0.03–0.32) 2.6 (2.3–2.8) 0.06 (0.02–0.21) 21 (14–25) 2.5 (0.2–5.2) 17 (1.5–35)

July-Aug. 0.05 (0.04–0.48) 3.2 (2.2–3.8) 0.12 (0.01–0.18) 18 (1.1–25) 0.6 (0.2–3.1) 15 (10–23)

Oct. 0.05 (0.03–0.45) 2.3 (1.0–3.4) 0.07 (0.02–0.23) 23 (13–27) 0.8 (0.2–5.4) 13 (7.4–50)

East Bay

Feb. 0.77 (0.47–1.0) 3.8 (3.6–3.8) 0.24 (0.16–0.25) 13 (7.1–19) 3.2 (2.9–3.9) 15 (14–18)

May 0.07 (0.04–0.15) 3.1 (2.6–3.6) 0.10 (0.02- 0.11) 12 (8.7–13) 0.9 (0.5–2.0) 17 (15–23)

July-Aug. 0.06 (0.03–0.10) 4.0 (2.4–6.2) 0.13 (0.05–0.16) 6.3 (4.9–19) 0.9 (0.3–0.8) 15 (12–22)

Oct. 0.35 (0.07–0.68) 3.4 (3.3–4.1) 0.11 (0.03–0.20) 13 (2.0–15) 2.8 (2.0–6.7) 18 (14–40)

East Devils Lake

Feb. 0.64 (0.44–2.5) 4.1 (4.1–4.3) 0.18 (0.15–0.66) 10 (3.1–16) 3.7 (2.4–4.2) 17 (9.1–19)

May 0.05 (0.04–0.06) 4.1 (3.4–4.7) 0.08 (0.03–0.23) 6.5 (2.6–12) 0.5 (0.1–1.7) 23 (13–30)

July-Aug. 0.10 (0.04–0.34) 4.1 (3.2–5.7) 0.18 (0.08–0.27) 11 (8.5–14) 0.6 (0.1–2.2) 17 (8.7–27)

Oct. 0.05 (0.02–0.24) 3.8 (2.1–8.4) 0.08 (0.08–0.16) 6.7 (1.0–11) 1.2 (0.1–4.0) 27 (20–50)

Soluble N:P =NH4−N+NO2−N+NO3−NPO4−P

Total N:P =organic N+NH4−N+NO2−N+NO3−Ntotal P

Seasonal variation in community structure

Peaks in abundance (in biomass) of small, non-motilechlorophytes (Choricystis minorandKirchneriella lu-naris), the diatomStephanodiscuscf. minutulus,theflagellateChroomonassp., and the cyanophyteDacty-lococcopsis fascicularisfollowed ice-out in DevilsLake in 1991 (Figure 4A). The chlorophyteDunaliellasp. and the diatomEntomoneis paludosawere co-dominant taxa (each> 30% of algal standing stock)in East Devils Lake. Subsequent declines in all thesepopulations resulted in a period of minimal algalstanding stock by early June (Figure 4B), when chloro-

phytes dominated the community. Biomass of thesmall chlorophytes and the flagellate peaked again inJuly in West Bay and East Bay; in contrast, biomassof the chlorophytes continued to decline in Main Bayand East Devils Lake, andChroomonassp. was notabundant again in Main Bay until August. Populationdensities of the dominant summer species (Microcys-tis aeruginosa) in Devils Lake increased exponentiallyin June, culminating in one or more summer blooms.Similar peak densities ofM. aeruginosaoccurred inthe four sub-basins, but at different times. The diatomsStephanodiscus niagaraeand Chaetoceros muellerialso were abundant in the summer, and dominated the

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Figure 4. Seasonal variation in (A) biomass of abundant planktonic algae and (B) algal standing stock in Devils Lake during the ice-free monthsof 1991.

algal assemblage of East Devils Lake.M. aeruginosaremained abundant throughout Devils Lake in autumn1991, but was dominant only in Main Bay. Dominantspecies in autumn (October) algal assemblages of theother sub-basins wereS. niagaraein West Bay,Aph-anizomenon flos-aquaein East Bay, andCyclotellameneghinianain East Devils Lake.

West Bay is more shallow and productive (Fig-ure 4B) than other sub-basins sampled. Due to thevariety of microhabitats and greater turbulence ofits sedimentary environment, the algal assemblagein West Bay is also more diverse (p<0.01, one-way ANOVA, Student-Newman-Keuls test) than else-where. Mean (± standard deviation) sample taxa rich-ness for the period of study was as follows: WestBay, 19.5±9.5; Sixmile Bay, 11.6± 6.8; Creel Bay,11.7±5.7; Main Bay, 11.0± 5.4; East Bay, 7.8± 4.7;and East Devils Lake, 10.3± 4.6. The West Bay as-semblage includes abundant meroplanktonic species,notably the chlorophytesTetrastrum staurogeniae-formeandScenedesmus ecornisand the diatomsAula-coseira granulataandNitzschia frustulum.

Grazing by zooplankton contributed to the vari-ation in algal abundances (Figure 5). Peak springdensities ofDaphnia pulexandDiaptomus siciliscoin-cided with the June period of low algal standing stock.An increased abundance ofD. pulex in East Bay inAugust and East Devils Lake in September indicates

a potential for a second generation throughout DevilsLake. However, declines in abundance of this speciesin other sub-basins triggered dramatic increases inpopulation density of other herbivorous cladoceransthat are both smaller and less efficient grazers of al-gae. These smaller species includeChydorus sphaer-icus, Ceriodaphnia quadrangulaandDiaphanosomabirgei. None were abundant in East Bay or East DevilsLake. The abundant rotifers (Brachionusspp., Fil-inia longiseta, Keratella cochlearisandK. quadrata)are effective consumers of cyanophyte-associated bac-teria (Paerl, 1988) and appeared to co-bloom withM. aeruginosa. D. sicilis, the dominant copepod inDevils Lake and a behaviorally-flexible omnivore thatexhibits decreased selectivity at high prey densities(Vanderploeg et al., 1988), was most abundant fromMay to July and in the autumn.

The zooplankton is more dense in West Bay (Fig-ure 5) than elsewhere, probably due to the greateralgal stock. Several invertebrate species, includingBrachionus urceolaris, B. pterodinoidesand Moinaaffinis, were present only in West Bay. The communityis less diverse (p< 0.01, one-way ANOVA, Student-Newman-Keuls test) in East Bay and East Devils Lakethan elsewhere, probably due to the greater salin-ity. Mean (± standard deviation) sample taxa rich-ness for the period of study was as follows: WestBay, 10.7± 3.8; Sixmile Bay, 9.3±4.5; Creel Bay,

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Figure 5. Seasonal variation in density of abundant planktonic invertebrates in Devils Lake during the ice-free months of 1991. Copepoddensities include adults and copepodites.

9.6± 3.3; Main Bay, 9.2±3.4; East Bay, 6.6± 2.6;and East Devils Lake, 5.8± 2.3. Daphnia similisandHesperodiaptomus nevadensis, common inhabitantsof saline lakes, were present only in East Bay and EastDevils Lake.

Annual variation in community structure

The phytoplankton record (1989–1994)of Devils Lake(Table 2) indicates a high degree of annual variabilityin community composition. Cyanophytes (Microcys-tis aeruginosa, Aphanothece sp.andChroococcus sp.)were more abundant than other taxa in winter 1989algal assemblages of Devils Lake, whereasEuglenasp. dominated the East Devils Lake assemblage. Bywinter 1990, chlorophytes (Kirchneriella lunarisandDunaliella sp.) had replaced cyanophytes as domi-nants in Devils Lake, whileEuglenasp. remaineddominant in East Devils Lake. Cyclotella stellig-era was abundant but not co-dominant in Main Bay.Choricystis minorreplacedK. lunaris as the dom-inant chlorophyte in Devils Lake by winter 1992,andDunaliella sp. replacedEuglenasp. as the mostabundant species in East Devils Lake. Chlorophytesremained more abundant than other major algal groupsin winter assemblages throughout the lake as waterlevels rose, but algal standing stock declined and noone species was dominant in winter 1994.

Spring 1989 assemblages in Devils Lake weredominated (in biomass) by diatoms (Surirella peiso-nisorStephanodiscuscf.minutulusin most sub-basins,

andEntomoneis paludosain West Bay).Chroococcussp. was co-dominant in West Bay, andChoricystisminor in East Devils Lake. Diatoms generally weredominant again in 1990, but each sub-basin had adifferent assemblage structure.Surirella peisonisandStephanodiscuscf. minutulus were co-dominant inWest Bay,Diatoma tenuein Sixmile Bay,Dunaliellasp. andChroomonassp. in Main Bay, andE. palu-dosa and S. peisonisin East Bay and East DevilsLake. Pulses of the small diatoms contributed to an ex-ceptionally large algal standing stock in spring 1990,and to severe depletion of SRP and SiO2 in lakewa-ter. The chlorophyteChoricystis minorwas abundantthroughout Devils Lake in spring 1991, but diatomsremained dominant in West Bay, East Bay and EastDevils Lake. C. minor was abundant again in thespring of 1992, but diatoms dominated algal assem-blages in West Bay, Sixmile Bay and East Devils Lake.The marked increase in flow to Devils Lake in spring1993 was associated with a decline in abundance ofC.minor throughout the lake, but it remained dominantin West Bay, Sixmile Bay and East Bay.Cyclotellameneghinianawas dominant in Main Bay in spring1993 andE. paludosain East Devils Lake. By spring1994,C. minor was dominant only in East Bay. Di-atoms had replaced chlorophytes as dominants in othersub-basins (Stephanodiscuscf. agassizensisandS. ni-agarae,except in East Devils Lake whereE. paludosawas dominant). Although at least one cyanophyte wasabundant in spring assemblages each year, dominancewas not exhibited by this group.

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Table 2. Algal assemblages of Devils Lake during the years 1989–1994. Taxa included in an assemblage (+) occurred in all or most sub-basinsof Devils Lake. Taxa present only in East Devils Lake or East Bay are identified by + e. The more abundant taxa (>2% of biomass in two ormore sub-basins) are identified by X (or Xe). Dominant or co-dominant (>30% of biomass) taxa are identified by XX (or XXe).

February May

1989 1990 1992 1994 1989 1990 1991 1992 1993 1994

Chlorophyta Chlorophyta

Chlamydomonassp. + + X Chlamydomonassp. X +

Chlorella vulgarisBeyerinck X X Chlorella vulgaris + + X + X +

Choricystis minor(Skuja) Fott XX X Choricystis minor X XX XX X X

Chlorogoniumsp. + Crucigenia quadrataMorren +

Dunaliella sp. X XXe Dunaliella sp. X Xe

Kirchneriella lunarisMoebius XX X Kirchneriella lunaris X + X + +

Oocystisspp. X Oocystisspp. +

Chrysophyta (Bacillariophyceae) Chrysophyta (Bacillariophyceae)

Cyclotella meneghinianaKütz. Xe Cyclotella meneghiniana X X XX +

Cyclotella stelligera(Cleve & Grun.) + +e Cyclotella stelligera X + + +

Van Heurck Diatoma tenueAgardh. X XXe X X

Stephanodiscuscf. hantzschiiGrun. +e Entomoneis paludosa(W. Sm.) Reimer X XXe Xe X X XXe

Cryptophyta Naviculaspp. + + X X

Chroomonassp. X X X Nitzschia fonticolaGrun. +

Euglenophyta Nitzschiaspp. + +

Euglenasp. XXe XXe Stephanodiscuscf. agassizensis XX

Cyanophyta Hakansson & Kling

Aphanocapsasp. X Stephanodiscuscf. minutulus XX X X

Aphanothecesp. X +e (Kütz.) Round

Chroococcussp. X Stephanodiscus niagaraeEhrenb. X

Dactylococcopsis fascicularisLemm. + Surirella peisonisPant. XX X + X

Microcystis aeruginosaKütz. XX Cryptophyta

Oscillatoria spp. + Chroomonassp. X X X X X

Rhabdoderma sigmoidea + Cyanophyta

Moore & Carter Aphanocapsasp. + + + + +

Aphanothecesp. X + +

Chroococcussp. X

Dactylococcopis fascicularis + + +

Merismopediasp. +

Microcystis aeruginosa + X

The potential for nitrogen-deficient phytoplanktongrowth in Devils Lake was evidenced most summersby blooms of the N-fixing algaAphanizomenon flos-aquae(Table 2). The blooms occurred regularly inmost sub-basins, but peak biomass of the species var-ied, and in some years blooms did not occur (asin 1991). Microcystis aeruginosaalso was usually adominant or abundant species in summer assemblages.A. flos-aquaedominated algal assemblages of SixmileBay and East Bay in summer 1989, butM. aeruginosawas more abundant elsewhere;Planktolyngbya sub-tilus was abundant but not co-dominant. The diatomStephanodiscuscf. agassizensisreplaced cyanophytes

as dominants in summer 1990, except in Main Bayand East Bay where it was co-dominant withA. flos-aquae. M. aeruginosawas dominant throughout thelake in summer 1991, except in East Devils Lake.A.flos-aquaeand M. aeruginosawere co-dominant insummer 1992, except in East Devils Lake where onlyM. aeruginosawas abundant.A. flos-aquaewas thesole dominant in summer 1993, except in East DevilsLake. Both cyanophytes were abundant in all sub-basins in summer 1994, withCyclotella meneghinianaco-dominant in Main Bay and Creel Bay.

As cyanophyte densities declined from summerand early-autumn bloom proportions, the degree of

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Table 2. Continued.

July–August October

1989 1990 1991 1992 1993 1994 1989 1990 1991 1992 1993 1994

Chlorophyta Chlorophyta

Chlamydomonassp. + + Chlorella vulgaris X X + +

Choricystis minor + + + X Choricystis minor X + X X X

Dunaliella sp. X + Dunaliella sp. + X + +

Kirchneriella lunaris + Kirchneriella lunaris X X + +

Schroederia setigeraLemm. + + + Scenedesmus ecornis +

Chrysophyta (Bacillariophyceae) (Ehrenb.) Chod.

Chaetoceros muelleriLemm. X X Schroederia setigera + +

Cyclotella meneghiniana + XX Chrysophyta (Bacillariophyceae)

Naviculaspp. + Chaetoceros muelleri X +e

Nitzschia fonticola +e +e Cyclotella meneghiniana + X X +

Nitzschiaspp. + Cyclotella stelligera X X XXe X

Stephanodiscuscf. agassizensis XX Xe + Entomoneis paludosa XXe

Stephanodiscus niagarae XX Naviculaspp. +

Cryptophyta Nitzschiaspp. +

Chroomonassp. + + X X + X Stephanodiscuscf. agassizensis X Xe X

Cyanophyta Stephanodiscus niagarae Xe X Xe XX X

Anabaena flos-aquae + + Cryptophyta

(Lyngb.) De Breb Chroomonassp. X + + Xe X X

Aphanizomenon flos-aquae XX X XX XX X Cyanophyta

(L.) Ralfs Aphanizomenon flos-aquae X XX Xe XX XX XX

Aphanocapsasp. + X + Aphanocapsasp. + X +

Aphanothecesp. + + X Aphanothecesp. + X + X

Chroococcussp. + Dactylococcopis fascicularis +

Microcystis aeruginosa XX X XX XX X XX Microcystis aeruginosa X XX XXe X

Nodularia spumigenaMertens +e +e

Planktolyngbya subtilus(W. X

West) Anagnostidis & Komarek

Pseudanabaena mucicola + + X + +

Naumann & Huber-Pestalozzi

dominance in algal assemblages decreased. However,A. flos-aquaeandM. aeruginosaremained abundantmost years in most sub-basins.A. flos-aquaewas dom-inant or co-dominant in autumn assemblages of EastBay every year and in Sixmile Bay during droughtyears. Diatoms (Cyclotella stelligeraandChaetocerosmuelleri; E. paludosain East Devils Lake) weremore abundant than cyanophytes in most sub-basins in1989.A. flos-aquaedominated assemblages through-out the lake in autumn 1990, except in East DevilsLake whereS. niagaraeand C. meneghinianawereabundant.M. aeruginosareplacedA. flos-aquaeasthe dominant species in Main Bay and Sixmile Bayin autumn 1991.A. flos-aquaewas dominant or co-dominant in autumn assemblages from 1992 through

1994, except in East Devils Lake.Stephanodiscus nia-garaewas co-dominant in most sub-basins in autumn1993, and in West Bay and East Devils Lake in autumn1994.

Population densities of secondary producers andplanktonic consumers in each sub-basin also variedsubstantially from year to year (Figure 6). Devils Lakesupports a large standing crop of herbivorous (or om-nivorous) zooplankton dominated (in density) by thecopepodDiaptomus sicilis; the cladoceransCerio-daphnia quadrangula, Chydorus sphaericus, DaphniapulexandDiaphanosoma birgei; and the rotifersBra-chionusspp., Filinia longiseta, Keratella cochlearisandK. quadrata. D. pulexabundance was unusuallylow in spring 1989, a year characterized by dense

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Figure 6. Annual variation in density of abundant planktonic invertebrates in Devils Lake during the years 1989–1994. Data are for the seasonof maximum density. Copepod densities include adults and copepodites.

populations of diatoms (Stephanodiscuscf. minutulusand Surirella peisonis). However, population densi-ties of D. pulexwere larger throughout Devils Lakein 1990 and 1992 than in other drought years despiteprey biomass levels (non-cyanophyte phytoplankton)similar to or greater than that of other years. Springabundances ofD. sicilis, the dominant copepod, alsowere less in Main Bay, East Bay and East Devils Lakein 1989 than in other years of declining lake levels.Large daphnids were not as abundant in East DevilsLake as in other sub-basins sampled.

Rising lake levels were accompanied by substan-tial changes in the zooplankton assemblages. Springabundances ofD. pulex in West, Sixmile and MainBays in 1993, the first year of unusually large inflows,were similar to those of the previous year, but declinedmarkedly in 1994 (Figure 6). In contrast, spring abun-dances in East Bay and East Devils Lake increasedin 1994. Spring densities ofD. sicilis also declinedin West, Sixmile and Main Bays in 1994, while in-creasing in East Bay and East Devils Lake. Collapsesor marked declines in populations of the primary,small cladocerans (C. quadrangula, C. sphaericus,andD. birgei) accompanied rising lake levels in West,Sixmile and Main Bays in 1994, whereas populationsdensities of these species increased in East Bay andwere observed for the first time in East Devils Lake.The large copepodAglaodiaptomus clavipesinvadedWest, Sixmile and Main Bays in autumn 1993, andattained densities of 0.1–1.0 indiv. l−1 in summer-autumn 1994. The presence of this active predator

may account for the marked decline in small clado-cerans. The 1994 catch rates (fish/net/hour) of young-of-year sport fishes in Devils Lake did not exceedcatch rates in other years of the study (Hiltner, 1996).A. clavipeswas never abundant in East Bay or EastDevils Lake. Summer densities ofF. longisetaalsoincreased with rising lake levels in East Bay and EastDevils Lake, whereas densities of this bacterivorousrotifer remained constant or declined elsewhere.

Relations among species distributions andenvironmental variables

Canonical correspondence analyses of abundance datafor planktonic algae in Devils Lake (seasons analyzedseparately) during the years 1989 through 1994 indi-cate a high annual variation in community structure(Figure 7). The distribution of site scores on CCA axes1 and 2 for winter (February) assemblages primarilyreflects this annual variation; inter-site differences incommunity structure are minor in comparison. In con-trast, both annual and inter-site variation are expressedon primary CCA axes for other seasons.

The weighted-correlation matrices reveal signifi-cant variation of environmental factors on each of thefour CCA axes (Table 3). Transparency is expressedstrongly on axis 1, together with one or more majornutrients (SRP, alkalinity, SiO2), and this axis ac-counts for 24–29% of the explained variance. Axis2 expresses variation in major nutrient concentrations(SRP, alkalinity), available Fe in summer assemblages,

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Figure 7. Site ordinations (CCA) of abundance (biomass) data for planktonic algae in Devils Lake. The axis scale is the average standarddeviation of species turnover (ter Braak, 1986), and the eigenvalues (λ1 andλ2) indicate the maximized dispersion of species scores along theaxes. The arrows indicate significant (p<0.05) and independent physical and chemical variables. Each datum is identified by site location andyear (A-West Bay, B-Sixmile Bay, C-Creel Bay, D-Main Bay, E-Mission Bay, G-East Bay, H-East Devils Lake).

and water temperature in autumn assemblages. Thisaxis accounts for 18–22% of the explained variance.Axis 3 expresses variation in particulate nutrient con-centrations (total P, organic N), and SiO2 and pH insummer assemblages. Salinity (TDS concentration) isexpressed mainly on axis 4, and this axis accountsfor 11–16% of the explained variance. Thus avail-able light and nutrient resources accounted for moreof the annual variation in phytoplankton structure thandid salinity during the period of study. Inorganic N

correlated strongly with the primary axis expressingspecies-nutrient relations (axis 3) in winter assem-blages, but not in other seasons.

The explained variance in species-environment re-lations ranged from 64% (summer) to 77% (winter)for the study period, indicating that variation in algalassemblages of Devils Lake also is regulated by physi-cal factors (climatic) and loss factors (grazing, naturaldeath) not considered in the CCA analyses.

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Table 3. Weighted correlation-matrices showing the relationship between algal species axes and environmental variables for the years1989–1994. Environmental variables listed exerted significant (p<0.05) and independent influences on the distribution of the species(CCA).

CCA axis Temper- Transpar- Dissolved pH Alkal- Silica Inorganic Organic Reactive Total Iron Eigen- Percent

ature ency solids inity nitrogen nitrogen phosphorus phosphorus value variance of

species–

environment

relation

February

1 – 0.50 −0.17 −0.36 0.01 – 0.10 – 0.37 – – 0.44 29

2 – 0.27 −0.33 −0.02−0.27 – −0.09 – −0.41 – – 0.33 22

3 – −0.62 0.67 −0.68 0.86 – 0.85 – 0.65 – – 0.28 18

4 – −0.06 0.35 −0.43 0.19 – 0.12 – −0.12 – – 0.23 14

May

1 – 0.64 0.43 – 0.33 – 0.35 0.37 – −0.01 – 0.20 27

2 – −0.29 −0.32 – −0.64 – 0.30 0.17 – 0.06 – 0.15 20

3 – −0.04 0.10 – −0.16 – −0.28 0.47 – 0.71 – 0.15 20

4 – 0.07 0.47 – 0.08 – −0.21 −0.13 – −0.04 – 0.12 16

July–August

1 – −0.69 −0.52 −0.16−0.36 0.06 – −0.03 −0.52 – 0.13 0.23 24

2 – −0.09 −0.22 −0.17−0.35 0.10 – 0.18 0.09 – 0.58 0.19 20

3 – −0.36 0.12 −0.57−0.04 0.50 – 0.59 −0.21 – −0.01 0.16 17

4 – 0.03 0.36 −0.22 0.15−0.25 – 0.08 −0.16 – 0.21 0.10 11

October

1 0.20 0.63 0.19 – 0.40−0.43 0.19 – 0.64 −0.18 – 0.28 28

2 −0.62 −0.25 −0.00 – 0.37−0.33 −0.00 – −0.20 −0.06 – 0.18 18

3 0.54 −0.21 −0.09 – 0.32 0.14 −0.24 – 0.05 0.59 – 0.16 16

4 0.14 −0.23 −0.24 – −0.13−0.06 −0.09 – 0.02 0.27 – 0.13 13

Discussion

Historical changes in community composition

Seasonal variation in composition of the phytoplank-ton of Devils Lake was described by several in-vestigators (Young, 1924; Anderson & Armstrong,1966; Verch & Blinn, 1971; Conway, 1983) duringyears when the lake was smaller and more saline.Dominant species reported in 1970–1971 (5500 mgl−1 TDS in Main Bay) wereCyclotella bodanica,Chaetoceroscf. muelleri, Euglena elongata, Chlamy-docapsa(=Gloeocystis) major, Microcystis aerugi-nosaandAphanizomenon flos-aquae(Verch & Blinn,1971). Maximum summer densities (106 cells l−1)of M. aeruginosa(0.41) andA. flos-aquae(0.29) in1970–1971 were similar to peak densities (0.46 and0.53, respectively) of these species in Main Bay ob-served during the years 1989–1994, except in 1990and 1993 when greater densities ofA. flos-aquaeoc-curred during bloom periods. Summer assemblages in

1976–1978 (<4000 mg l−1 TDS in Main Bay) weredominated byM. aeruginosaandA. flos-aquae, andC.cf. muelleriwas abundant (Conway, 1983).

The diatom stratigraphy of surficial sediments pro-vides an historical record of changes in lake leveland salinity of Devils Lake (Fritz, 1990; Fritz et al.,1991). Lake levels have risen and salinity declinedsince the drought years of the 1930’s and 1940’s.Cy-clotella quillensisand resting spores ofC. muelleridominated phytoplankton assemblages during salineperiods, withCyclotella caspiaand benthic diatomsalso abundant. Recent years (1980’s) are characterizedin the sediment record byStephanodiscus minutu-lus andS. niagarae, species predominantly found infreshwater (< 3000 mg l−1 TDS) lakes.

Many species identified as euryhaline in salinelakes of the North American Great Plains (Ham-mer et al., 1983) are common inhabitants of Dev-ils Lake, including the diatomsAulacoseira granu-lata and Cyclotella meneghiniana; the cyanophytes

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Lyngbya birgei, M. aeruginosa, Nodularia spumi-gena, Oscillatoria tenuisandO. utermoehli; and thechlorophytesDunaliella salinaandRhizoclonium hi-eroglyphicum. Surirella peisonisis abundant only inhyposaline lakes of moderate depth (Fritz, 1990).Diatoms and cyanophytes generally dominate algalassemblages of hyposaline lakes in this region, withchlorophytes a minor component of the biomass. Dev-ils Lake, in contrast, has chlorophytes as a majorcomponent of the biomass. Small, non-motile chloro-phytes (Choricystis minorandKirchneriella lunaris)dominated winter and early-spring assemblages mostyears and were abundant throughout the year. Al-though dominant every year in summer assemblagesof East Bay,Aphanizomenon flos-aquaewas not abun-dant in East Devils Lake until 1993 and was neverdominant there. Dominance byA. flos-aquaeis notobserved typically at salinities exceeding 5000 mg l−1

TDS (Paerl et al., 1984).

Physical and chemical factors contributing tovariation in community structure

Correspondence analyses of abundance data for plank-tonic algae in Devils Lake during the period of study(1989–1994) revealed that available light and nu-trient resources accounted for more of the annualvariation in phytoplankton structure than did salin-ity. Transparency was expressed on the primary CCAaxis in all seasons. Reynolds et al. (1994) postu-lated that successful algal species in turbulent, shallowlakes are selected primarily on their ability to survivehigh-frequency irradiance fluctuations. The verticalposition of planktonic algae is constantly readjustedwith the effect that light exposure is erratic, and thereceived light dose-rate aggregately depressed. Themost successful species, within the capacity of nu-trients available, are either those that grow rapidlyor those at an advantage due to high initial inoc-ula of germinating propagules. Furthering this hy-pothesis, Gosselain et al. (1994) concluded that in-creases in light dose-rate and water temperature pro-mote development of chlorophytes in large, eutrophicrivers (Europe) and the progressive dominance (incell density) of this group over diatoms. As in Dev-ils Lake, algal assemblages of rivers sampled weredominated generally by rapidly growing unicellular,centric diatoms (Stephanodiscusspp. andCyclotellaspp.) and chlorophytes (mostly Chlorococcales). Res-ident cyanophytes grew more slowly and requiredprolonged periods of low flow to develop sizable pop-

ulations. The relatively slow-growing cyanophytesA.flos-aquaeand M. aeruginosadominate principallythrough prior recruitment of over-wintering propag-ules (Reynolds, 1993; 1994).

Although dominant in the thermally non-stratifiedwaters of Devils Lake during summer-early autumn,A. flos-aquaeand M. aeruginosaprefer a stable en-vironment where vertical position in the water col-umn can be adjusted by buoyancy alteration. Un-der such conditions, these species effectively in-crease their light-dose rate and trap more CO2, whilealso shading subsurface populations of non-buoyantspecies (Van Liere & Walsby, 1982). Furthermore,they have better kinetics for CO2 uptake than mostnon-cyanophytes, thus ensuring their dominance onceabundant (Shapiro, 1997). Small (0.5–1.0◦C) temper-ature differences between near-surface and subsurface(0.3–1 m) waters during cyanophyte blooms in DevilsLake suggest environmental alteration associated withgrowth of these species.

There appear to be two contrasting periods ofphytoplankton growth in Devils Lake: winter-earlyspring, when growth is not N-limited and summer-fall,when growth potentially is N-deficient most years. N-deficient conditions were not evidenced every year (forexample, 1991 whenA. flos-aquaewas not abundantexcept in East Bay). Soluble N:P ratios in summerranged from 0.1 to 4.0 (median of 0.8) in 1988–1994. The only systematic study of nutrient limitationin Devils Lake (Shubert, 1976) yielded inconclu-sive results. Nutrient-enrichment bioassays conductedthrough an entire year showed that inorganic N andSRP had no stimulatory effect when added singly totest waters from Creel Bay or Main Bay. However,when added in combination, these nutrients stimu-lated Chlorella sp. production, except during wintermixing or cyanophyte blooms. EDTA also stimulatedChlorella sp. production, but it was not clear that theeffect was due either to binding of Fe or trace metals.A trace-metal mixture including Fe had no stimulatoryeffect singly or in combination with inorganic N orSRP.

Cyanophyte blooms generally occur in lakes whenfluvial total-N loadings are small and concentrationsof SRP are large relative to inorganic N (Lebo et al.,1994). External sources of N and P are insignificantcompared with internal cycling of these constituents inDevils Lake (Lent et al., 1994). Sando & Lent (1995)attributed increases in mass of N and P from winter tosummer to re-suspension of nutrient-rich sediments,decomposition of organic matter, and N-fixation by

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phytoplankton. Relatively short response times (inter-nal recycling of mass) were observed for N (4.2 yr)and P (0.95 yr), indicating that nutrients are recycledrapidly. Seasonal changes in major-ion and nutri-ent benthic-flux rates are small; however, differencesbetween years in calculated fluxes of HCO3, NH4and SRP are substantial (Lent, 1994). More frequentperiods of oxygen under-saturation in near-sedimentwaters in 1990 than in 1991 contributed to increasedbenthic-flux rates of each constituent and much greaterdensities of the dominant summer phytoplankton (A.flos-aquaeandStephanodiscuscf. agassizensis).

Loss factors of biological origin contributing tovariation in community structure

The relative importance of loss factors (grazing, nat-ural death and consequent sedimentation) of biologicalorigin on the structure and diversity of phytoplanktonassemblages in Devils Lake cannot be determined withavailable data. Measured physical (transparency, wa-ter temperature) and chemical (major ions, nutrients,trace elements) variables accounted for 64–77% of theexplained variance in CCA analyses. However, selec-tion of species and the assembly of communities maybe regulated in large part by biological interactions,especially when large self-regulating algal populationsdevelop (for example, during periods of cyanophytedominance) or when significant populations of graz-ing zooplankton develop (for example, rapid growthof rotifers, as these organisms have appropriately shortgeneration times). Such events in shallow, turbulentenvironments typically are associated with relativelystable physical conditions (Reynolds et al., 1994;Gosselain et al., 1994). Expression of biological in-teractions in the selection of species and the assem-bly of communities at other times rarely is releasedfrom constraints imposed by variability in the physicalenvironment (irradiance, turbulence).

Acknowledgements

Financial support for this study was provided in partby the North Dakota State Water Commission andthe North Dakota Game and Fish Department. Wethank Robert Lent, Steven Sando, Bradley Sether,Gregg Wiche and other staff of the U.S. GeologicalSurvey who participated in sample collection, andJames Saunders of the University of Colorado whoverified zooplankton identifications. Constructive re-views of the manuscript were provided by Richard

Dufford, John Kingston, James LaBaugh, Robert Lentand Stephen Porter.

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