influence of two daphnia species on summer phytoplankton

Journal of Plankton Research Vol.19 no.8 pp.1025-1044, 1997

Influence of two Daphnia species on summer phytoplanktonassemblages from eutrophic lakes

Peter H.Kasprzak2 and Richard C.Lathrop1

University ofWisconsin, Madison, Center for Limnology, 680 North Park Street,Madison, W153706, USA

'Present address: Wisconsin Department of Natural Resources, 1350 FemriteDrive, Monona, WI53716, USA2To whom correspondence should be addressed at: Institute of FreshwaterEcology and Inland Fisheries, Miiggelseedamm 310, D-12587 Berlin, FRG

Abstract We conducted grazing experiments to test whether larger-bodied Daphnia puticaria have adifferent effect from smaller-bodied Daphnia galeata mendotae on the composition of summer algalassemblages in eutrophic lakes. Three separate cubitainer experiments were run for 5 days in a repli-cated factorial design utilizing two algal community types and the two Daphnia species. Inorganicphosphorus and nitrogen were added to prevent nutrient limitation of the algae. Both edible andinedible size fractions of chlorophyll a increased in cubitainers without Daphnia spp. Grazer additionusually resulted in a reduction in edible chlorophyll; reductions were greater in D.pulicana cubi-tainers. Grazing by Daphnia spp. on presumed inedible chlorophyll was variable. Algal size was notalways a good predictor of grazeability. The results of this study indicate that D.pulicaria, because ofits greater filtration potential and ability to ingest larger particles, provides a stronger control oninedible-sized algae when compared to equal numerical densities of D.g.mendotae. However, Aphan-izomenon increased as a response to heavy grazing pressure by D.pulicaria on other algal species. Thissuggests that biomanipulation efforts that promote large-bodied Daphnia may not produce desirableresults if nutrient inputs remain high.

Introduction

Inorganic nutrients are of primary importance to the production and biomass ofphytoplankton in standing fresh waters (Ohle, 1953; Rodhe, 1958; Vollenweider,1976; Schindler, 1977). Herbivorous grazing, in contrast, is considered to be oneof the major loss processes of phytoplankton (e.g. Uhlmann, 1954; Nauwerk,1963; McKauley and Kalff, 1981; Pace, 1984; McQueen etaL, 1986; Carpenter andKitchell, 1988; Cyr and Pace, 1992). However, more recent investigations haveshown that the interactions between nutrients, phytoplankton and grazers arelargely influenced by food web structure (Benndorf, 1988; Gulati et al, 1990;Carpenter and Kitchell, 1993; Schindler et al, 1993). Moreover, this relationshipis modified by levels of nutrient loading and in-lake concentrations (Olsen andWillen, 1980; Benndorf, 1990; Elser and Goldman, 1991; Vanni et al, 1992;Koschel et al, 1993). Depending on the degree of nutrient limitation and thestructure of the phytoplankton and herbivore community, grazing may haveeither an inhibiting or an enhancing effect on the algae (Bergquist and Carpen-ter, 1986). Nevertheless, zooplankton filtration rates of ^0.3-0.4 day-1 have beenshown to reduce the biomass in many phytoplankton communities (Reynolds,1984a). Daphnia spp. were often found to be the most powerful filter feederswithin the community of herbivorous zooplankton (Morgan et al, 1980; Sterner,1989; Vanni and Temte, 1990).

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P.H.Kaspnak and R.CLathrop

Food-uptake mechanisms in planktonic animals are diverse, spanning therange from highly selective to non-selective feeders (Joergensen, 1966). Daphniais considered to be non-selective (Kasprzak etai, 1986) but, even in this genus, anumber of factors modify the resource-consumer relationship (Knoechel andHoltby, 1986a; Lampert, 1987). Gliwicz (1977) has shown that if particles arebeyond the range of availability, a selection is imposed, even on obligate filterfeeders like Daphnia. Nevertheless, whether a particle can be filtered from theambient suspension and subsequently ingested is first a function of its size (Burns,1968). Particles £20 (xm are usually particularly ingestible, whereas those >50-60p,m are not. For the remaining size range of particles (20-50 |xm), ingestibilitylargely depends on the shape of the algae (greatest axial linear dimension;Reynolds, 1984a).

Several authors have shown that filamentous algae, especially blue-green fila-ments, and large colonies of algae such as Microcystis, tend to impair the filtrationpotential of Daphnia (e.g. Webster and Peters, 1978; Gliwicz and Siedlar, 1980;Thompson et ai, 1982; Pearl, 1988). Therefore, Daphnia is not able to reverse thedominance of an established population of larger Microcystis or filamentous blue-green algae (Davidowicz et al, 1988). On the other hand, investigations of Daphniagut contents have sometimes revealed surprisingly large particles, indicating thatthese animals are also able to graze on the so-called 'canopy species' (Horn, 1981;Vyhnalek, 1983; Sommer et al, 1986; Sarnelle, 1992; Epp, 19%). However, differ-ences in grazing potential between small and large Daphnia may be significant.

Most of the experimental work on phytoplankton-grazing interactions wascarried out in oligotrophic or mesotrophic systems (e.g. Lehman and Sandgren,1985; Bergquist and Carpenter, 1986; Elser and Goldman, 1991). This paper,however, concentrates on the grazing influence of Daphnia pulicaria and Daphniagaleata mendotae on summer phytoplankton assemblages of eutrophic lakes.Both Daphnia species are found in many northern eutrophic US lakes. Their rela-tive dominance during the spring clear-water phase and into the early summermonths appears to be controlled by the degree of planktivory (Luecke et al., 1992;Rudstam et al, 1993; Lathrop et al, 1996). While both species have similar cara-pace length, D.pulicaria, with a much greater body mass, only dominates whenplanktivory is low. Promoting the dominance of D.pulicaria (and the similarDaphnia pulex) is often the desired outcome of biomanipulation to reduce thesummer algal problems in lakes (Shapiro et al, 1975; Benndorf, 1988; Gulati etal, 1990; Kitchell, 1992). Our interest was in evaluating the differential grazingimpacts of D.pulicaria and D.g.mendotae on phytoplankton as they develop fromthe clear-water phase into the summer bloom. Special emphasis was placed onthose groups or genera of algae that are considered resistant to grazing. Themajority of these algae may not be avoided except on the basis of size. If they aresmall enough relative to the size of grazers, they are liable to be consumed.

Method

The experimental design followed an idea developed by Lehman and Sandgren(1985). Three separate grazing experiments (Clt Q, C3) were carried out in 20 1

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Influence of two Daphnia on phytoplankton assemblages

translucent plastic bags (cubitainers) suspended in the littoral zone of LakeMendota at a depth of approximately one-half of incident solar radiation andwater temperatures of ~25°C. Each experiment ran for 5 days in the summer of19% (Table I). Six eutrophic lakes in southeastern Wisconsin, USA, served assources for natural phytoplankton assemblages, D.pulicaria (DpuT) andD.g.mendotae (Dgm). In all three experiments, Pike Lake was selected as a sourceof filamentous algae dominated by Aphanizomenon. Lake Marie, Lake Wingraand Silver Lake were chosen because their phytoplankton was characterized bynon-filamentous forms. Daphnia spp. was taken from Pike Lake, Lake Mendotaand Lake Ripley.

This phytoplankton was exposed to Daphnia grazing at three different stagesin the summer algal development: (i) middle of the clear-water phase; (ii) tran-sition stage between the clear-water phase and summer bloom; (iii) and summerbloom, respectively. In order to remove most of the crustacean zooplankton, thetest water was filtered through a 350 jim screen. Microscopic analysis confirmedthat the composition of phytoplankton was not changed by screening.

To prevent nutrient limitation of the phytoplankton and to exclude the influ-ence of their various mechanisms of nutrient recycling due to grazing, thecubitainers were supplemented with dissolved inorganic phosphorus (DIP,KH2PO4) and nitrogen (DIN, NH4NO3). The nitrogen addition amounted to 300u,g N I"1. The phosphorus addition was 100 \ig P H in experiment Q, and 200 mg

T«We L Schematic representation of the treatments

Exp. no.

c,

Q

c3

Date

15-20.06.%

30.06-0.5.07.96

21-26.08.96

27.08-01.09.96

Phytoplanktonsource lake

Pike Lake

Lake Marie

Pike Lake

Lake Wingra

Pike Lake

Silver Lake

Daphnia source lake

D.pulicaria:Lake MendotaD.g.mendotae:Pike Lake

D.pulicaria:Lake MendotaD.g.mendotae:Pike Lake

D.pulicaria:Lake MendotaD.g.mendotae.Pike Lake

Treatments

C,/Pike/NC,/Pike/N/Dg/TjC,/Pike/N/Dpu/

Q/Marie/NC|/Marie/N/£)gmC,/Marie/N/Dpu/

Q/PikeTNC/Pike/N/Dg/n(VPike/N/Dpu/

Cj/Wingra/NQ/Wingra/N/DgmCj/Wingra/N/Dpu/

CyPike/NCyPike/N/DgmCi/Pike/NIDpul

CySilver/NCySilver/N/Og/nCj/Silver/N/Dpu/

N, nutrients added; Dgm, D.g.mendotae added; Dpul, D.pulicaria added. All experiments were run intriplicates.

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PJLKaspizak and UGLathrop

P h1 in Cj and C3. DIP and DIN analyses were performed at the State Labora-tory of Hygiene in Madison using widely accepted procedures.

In order to obtain a sufficiently high grazing rate, a Daphnia concentration of-40-50 ind. H was intended. For that reason, the density of the particular popu-lation in each of the Daphnia source lakes was estimated 1 day prior to the experi-ment using a 30 cm diameter Wisconsin plankton net of 350 jim mesh size. Thenext day, an appropriate number of animals was sampled by vertical net hauls,put into a bucket, gently stirred and then added to the cubitainers. Microscopicinspection showed that there were only a few copepods and other cladocerans inthe Daphnia inocula.

After the termination of the three experiments, all cubitainers were individu-ally processed. Daphnia were separated from the water using the same 350 u,mnet, fixed with a buffered formalin-sugar mixture, and stored for later counting.A phytoplankton sample fixed with glutaraldehyde was also taken.

To measure the chlorophyll (Chi) a concentration of the samples, an appropri-ate volume of water was filtered through glass fiber filters (Gelman Scientific) andcold-extracted in methanol for at least 2 weeks. The measurement was madeusing a Turner Model 450 fluorometer. Calibration was performed usingAnacystis nidulans Chi a extracts (Sigma Chemical Co.). Pheopigments were esti-mated following acidification of the samples. Using a screen, edible Chi a was esti-mated in the particle fraction <35 u,m, whereas total Chi a was determined in theuntreated sample. Supposedly inedible Chi a was calculated by subtracting ediblefrom total Chi a.

For the Daphnia treatments, the volume containing -100 individuals wascounted and their size measured. In the nutrient-only treatments, triplicate 25 mlsamples were counted to confirm the low crustacean densities. Daphnia bodymass was calculated according to published length-dry weight relationships(Lynch et ai, 1986).

D.g.mendotae: DW (u-g) = 5.48 L (mm)2300

D.pulicaria: DW (u,g) = 10.67 L (mm)2-093

The Daphnia filtration potential in each cubitainer was calculated using amodel developed by Peters and Downing (1984). The mean maximum size of par-ticles that can be ingested by either D.pulicaria (MPP) or D.g.mendotae (MPG)was calculated according to Burns (1968).

The abundance and size structure (greatest axial linear dimension, GALD;Lehman and Sandgren, 1985) of the phytoplankton were determined using aninverted microscope following the technique of Utermdhl (1958). To get a goodestimate of the number and size distribution of the phytoplankton communityassemblage, the GALD of individual cells, colonies, and filaments was usuallydetermined until the standard error was <10% of the mean GALD. The sizedistribution of algae was estimated in a sample taken from the source lake at thebeginning of the experiment and in the cubitainers at the end of each of theexperiments. Algal identification followed Prescott (1970).

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Influence of two Daphnia on phytoplankf on assemblages

Results

Nutrients

Excess concentrations of DIP and DIN after the termination of experiment Qindicated that nutrient limitation did not occur (Table II). Concentration differ-ences between nutrient-alone and nutrient-grazer treatments were relativelysmall, indicating that recycling due to grazing and/or uptake by different phyto-plankton biomass were negligible in comparison to the amount of nutrientsadded. In experiment Q, about two-thirds of the added DIP and again one-thirdof the DIN were taken up by the Pike Lake seston. DIP and DIN were unde-tectable in C2/Wingra nutrient-alone treatments, indicating that nutrient limit-ation may have occurred by the end of the experiment. In both Q/Pike andQ/Wingra cubitainers with Daphnia, measurable amounts of DIP and DINremained, most likely as a result of recycling due to grazing or less uptake as aconsequence of lower phytoplankton biomass. In experiment C3, the sameamount of DIP and DIN as in treatment Q was added, but no nutrient measure-ments were made at the end of the experiment.

Daphnia

The number of Daphnia found in the cubitainers of experiments Q , C2 andCyPike was similar within the triplicates as well as between the experimental sets(Figure 1, Table III). However, the abundance of Daphnia spp. in C^Silver was-25 ind. H, which was much lower than intended.

While the numerical densities of the two Daphnia species added to thecubitainers were relatively similar, D.pulicaria biomasses were always muchlarger because of that species' greater weight per unit length. Because individual

Table IL Nutrient addition and concentration in the cubitainer experiments (u.g H)

No. of experiment/nutrient

PhosphorusC,/PikeC|/MarieCVPikeCyWingraCj/PikeCifSilvei

NitrogenC,/PikeC,/MarieCj/PikeCVWingraCyPikeCj/Silver

Add

200200100100200200

300300300300300300

Nut

10413617<2

--

162160160<2

--

Nut/Dp

1041283728

--

137144227103--

Nut/Dg

127154345

--

20419122862

--

add, amount of added nutrients; Nut, concentration in the nutrient treatment; Nut/Dp, concentrationin the Dfidicaria treatment; Nut/Dg, concentration in the D.g.mendotae treatment. Phosphorus wasadded as KH2PO4, nitrogen was added as NH^JC^.

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Pike/Dp Pike/Dg Marie/Dp Marie/Dg

Fig. L Concentration, mean size, individual biomass and community filtration potential of D.pulicaria(Dp) and D.g.mendotae (Dg), respectively, in experiment Q. Sources of the algal assemblages werePike Lake and Lake Marie. Vertical bars are 95% confidence limits.

biomass is one of the major factors in the filtration rate model used, the filtrationpotential in Dgm cubitainers was lower than in Dpul treatments.

Chlorophyll a

In the nutrient-only treatments, nutrient addition was followed by a strongincrease in Chi a relative to concentrations found in each lake at the beginningof the experiments (Figure 2). This response was especially pronounced for edibleChi a, but the inedible fraction also increased to varying degrees. Other thanthese general patterns, the increase in inedible Chi a in CVWingra/N was especi-ally pronounced. In addition, the relatively low concentration of edible Chi a inthis experiment was most likely due to contamination of these cubitainers withD.g.mendotae. With the exception of Q/Wingra/N (Daphnia contamination),there was a clear increase in the edible/inedible Chi a ratio in Q and Q, whereaslittle change was found in C3 (Figure 3).

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Table IIL Characterization of Daphnia in the cubitainer experiments

Treatment

Q/Pike/DpC,/Pike/DgQ/Marie/DpCi/Marie/Dg

Q/Pike/DpQ/Pike/DgCyWingra/Dp(VWingra/Dg

C3/PikeyDpC3/Pike/DgC3/Silver/DpCySilver/Dg

Daphnia(ind. 1-')

49(6)40(13)55(4)41(23)

67(6)52(5)63(2)76 (10)

55 (13)51 (10)26(2)24(5)

Mean size(mm)

133 (0.15)1.14 (0.26)1.29 (0.15)1.08 (0.02)

1.62 (0.15)1.14 (0.04)130 (0.15)1.11 (0.06)

1.31 (0.08)1.34(0.00)1.55 (0.07)1.20 (0.00)

MPP/MPG((im)

34343329

41303829

34343931

Biomass(tig DW ind."1)

19.4 (4.6)7.5 (3.5)

183 (4.3)63 (0.2)

29.4 (5.7)73 (0.6)

25.0 (5.6)6.9 (0.8)

18.8 (2.3)10.4 (0.0)26.8 (2.7)8.1 (0.0)

BiomassGigDWF)

952(111)287(70)

1010 (308)266 (153)

1996 (558)381 (17)

1572 (365)521 (64)

1044(298)526 (104)701 (29)191 (40)

Filtr. pot.(ml H day1)

859(97)246 (36)

1351 (515)331 (206)

1298 (117)336 (29)788(294)294 (43)

564 (240)353 (83)480(190)185 (67)

MPP/MPG, mean maximum particle size ingestible by D.pulicaria and D.g.mandotae calculatedaccording to Burns (1968); filtr. pot., filtration potential calculated according to Peters and Downing(1984). Individual biomass was calculated according to Lynch et al. (1986), numbers in parenthesesare 95% CL.

Addition of both nutrients and Daphnia to the cubitainers led to three generalresults (Figure 2). By comparison with the nutrient-only treatment, both Daphniaspecies in experiment Q compensated for almost all the growth of edible algae.The inedible Chi a concentration was lower in the Dpul than in the Dgm treat-ments, which were similar to the nutrient-only concentrations. This suggests thatD.pulicaria was grazing inedible-sized algae. In Q, the pattern was different. Bothspecies of Daphnia were able to keep the edible fraction of Chi a under control.Inedible Chi a remained unchanged in the Q/Pike experiment, but D.pulicariasuppressed inedible ChJ a in GyWingra. In C3 another pattern was observed. BothDaphnia species were not able to control the growth of either chlorophyll frac-tion in C3/Pike, whereas only edible Chi a was reduced in C^Silver. In general,herbivore addition usually resulted in an increased ratio of edible/inedible Chi awith no consistent difference between Dpul and Dgm treatments (Figure 3).

The pooled data from all D.pulicaria experiments indicated a tendency towarda decreasing concentration of inedible Chi a with increasing Daphnia filtrationpotential (Figure 4). The probability of having high concentrations of inedibleChi a is rather low at a filtration potential >800 ml h1 day"1. Nevertheless, theslope was found to be not significant. Filtration potential and edible ChJ a showeda clear and significant inverse relationship (r2 = 0.668, P < 0.001). The same wastrue for the ratio edible/inedible Chi a (r2 = 0.338, P < 0.002), i.e. the share of theedible fraction decreased with higher filtration intensity.

There was no significant relationship between the filtration potential ofD.g.mendotae and inedible Chi a (Figure 4). The concentration of edible Chi a,however, was significantly reduced by grazing (P < 0.001). Less of the Chi a vari-ability was explained by grazing in the Dgm treatments (r2 = 0.484) than in theDpul treatments. If the results of the nutrient-only treatments were excluded

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PJLKasprzak and R.CLathrop

I•§

40

30

20

10-

0- 1 n

I11I rjb1 M

C1

11

30

20

10

0 i n

•11B n

C1

inPike N Dp Dg Marie N Dp Og

4 0

30

20-

10-

0 in

I

II • i t

C2 60

40

20

0 In I .ftC2

1Pike N Dp Dg Wingra N Dp Dg

30

20

10

0I n n

Pike

C3

N Dp DgTreatment

30

20

10

I n I1

C3

1• edibleD inedible

Silver N Dp DgTreatment

Fig. 2. Concentrations of edible and inedible Chi a in experiments C,, Q and C3. Sources of the algalassemblages were Pike Lake, Lake Marie, Lake Wingra and Silver Lake. N, nutrient-only treatments;Dp, Dg, nutrient addition and D.pulicaria or D.g.mendotac addition, respectively Vertical bars are95% confidence limits.

from the regression analysis of Dgm treatments, no significant relationship dueto increased filtration potential was found. Grazing by D.g.mendotae significantlychanged the ratio of edible/inedible Chi a (r2 = 0.3856, P < 0.001).

Algal groups

Some examples of the response of different groups and genera of phytoplanktonto nutrient addition and grazing are summarized in Figures 5 and 6. The sizedistributions of Microcystis colonies in the source lake sample at the beginningof the experiment and in the nutrient-only treatment of CyWingra at the end ofthe experiment were completely different from the mean maximum particle sizes

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O

20%

Pike N Dp Dg Marie N Dp Dg

100%

Pike N Dp Dg

20%

Wingra N Dp Dg

100%

Pike N Dp DgTreatment

Silver N Dp DgTreatment

• edible chla @ inedible chla

Pig. 3. Percentage of edible and inedible Chi a in experiments C, and C3. The *-axis indicates thesource lakes of the phytoplankton assemblages and the treatments. N, nutrients; Dp, nutrients plusD.pulicaria; Dg, nutrient plus D.g.mendotae.

(Burns, 1968) ingestible by D.pulicaria (MPP) or D.g.mendotae (MPG; Figure 5).On the other hand, there was a clear overlap between the size of the colonies andMPP and MPG, respectively, in the Daphnia treatments, indicating that parts ofthe algal population should have been grazeable. Compared to the lake sample,Microcystis concentrations in experiment Q increased as a response to nutrientaddition when no grazers were added. It seems that by grazing, D.pulicaria wasable to compensate for part of this growth, although the differences between thetwo treatments were not significant. However, algal densities were greater in theDgm treatments than in the nutrient-alone treatments. The difference in algaldensities between the Dgm and the Dpul treatments was even more striking.While D.pulicaria suppressed the growth of Microcystis, D.g.mendotae enhancedits growth.

In experiment CySilver, the situation differed (Figure 5). The mean size ofMicrocystis colonies in the lake sample and in the nutrient-only treatments wassmaller than in both Daphnia treatments. Moreover, there were remarkabledifferences in colony size distribution. Only Microcystis in the Dgm treatmentsand MPG were found to overlap. Although variability was high, nutrient addition

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P.H.Kasprzak and R.GLathrop

Daphnia pulicaria

500 1000 1500 2000filtration potential [ml/1 d]

60

40

20

Daphnia galeata mendotae

040

1 | 30

£ 20

§ 10

0

8

inedible chl-a

edible chl-a

edible/inedible chl-a

100 200 300 400 500filtration potential [ml/1 d]

Fig. 4. Concentration of inedible and edible Chi a and the ratio of both fractions as influenced by thefiltration potential of both D.pulicaria and D.g.mendotae.

again enhanced the growth of the alga, but this time grazing by both D.pulicariaand D.g.mendotae totally compensated for the increase.

Aphanizomenon in Cj/Pike had shorter filaments in both Daphnia treatmentsthan in the lake sample (Figure 5). MPP and MPG overlapped very little with thesize of the algae in the grazer-containing cubitainers. Nutrient addition had no sig-nificant effect on the growth of Aphanizomenon. Daphnia pulicaria was able todecrease the abundance of the Aphanizomenon by -50% of that of the nutrient-only treatments. Daphnia g.mendotae did not influence Aphanizomenon densities.

In Q/Wingra, a similar pattern in size distribution of Aphanizomenon, MPPand MPG was found. Nevertheless, the results in abundance were completelydifferent (Figure 5). Nutrient addition alone had a negative effect on Aphani-zomenon; the species virtually disappeared in the cubitainers. In combinationwith D.pulicaria, however, Aphanizomenon clearly increased in density. Theinfluence of D.g.mendotae was again insignificant.

The size distributions of Ankyra, MPP and MPG in Ci/Pike obviously over-lapped (Figure 6). Moreover, the algae in the grazer cubitainers were muchsmaller compared to those in the nutrient-only treatments. Nutrient additioncaused no effect on the abundance of Ankyra, whereas Daphnia grazing clearlystimulated the alga. Daphnia pulicaria had the strongest enhancing effect.

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The size distribution of gelatinous green algae, MPP and MPG overlappedcompletely, as shown by the example of Q/Wingra (Figure 6). Nutrient additionshowed an insignificant increase in algal concentration. Both D.pulicaria as wellas D.g.mendotae decreased algal densities

The size distributions of Melosira, MPP and MPG are completely different(Figure 6). Nutrient addition caused remarkable growth. Only D.pulicariadecreased algal densities. The same pattern was true for Fragilaria in Q/Wingra,except that the reduction by D.g.mendotae was also significant (Figure 6).

Discussion

The addition of nutrients was always followed by an increase in the concentrationof edible Chi a, which is in good agreement with many other field and laboratoryinvestigations (Figure 2; e.g. Schindler and Fee, 1974; Lund and Reynolds, 1982;Koschel and Scheffler, 1985; Bergquist and Carpenter, 1986; Harris, 1986;Schindler, 1990). However, this may not apply to all populations of all species atall times. Species not limited by nutrients will not react to an increased supply(Olsen and Willen, 1980; Vyhnalek, 1983; Lehman and Sandgren, 1985). Nutri-ents also stimulated growth of inedible Chi a, though the enhancement wasusually less pronounced. Larger phytoplankton tend to grow at a lower rate,perhaps because of a lower surface to volume ratio (Banse, 1976; McCauley andBriand, 1979; Reynolds, 1984b). This factor may explain why some investigatorsfound inedible phytoplankton not to benefit greatly from increasing nutrient con-centrations (Watson and McCauley, 1988; Watson et al, 1992). The short dura-tion of the experiments and the restriction of water movement to within thecubitainers may have enhanced this tendency by providing better growing con-ditions to small algae and by selective sedimentation in disfavor of large phyto-plankton (Bloesch and Buergi, 1989).

The increase in inedible Chi a showed remarkable differences between thethree single experiments (Figures 2 and 3). One reason may have been the sizeand the composition of the inoculum. The results indicated a tendency towardshigher concentrations of inedible Chi a when the percentage in the lake sample(source of the inoculum) was high as well.

Another aspect is the seasonal development of natural phytoplankton com-munities in eutrophic lakes. According to the 'PEG-modeP of phytoplankton suc-cession, the period immediately after the clear-water phase is commonlycharacterized by colonial green algae followed in many cases by filamentouscyanobacteria (Sommer et al, 1986). Both of these algal groups are known to berelatively non-digestible, non-ingestible, or both (Porter, 1976; Gliwicz andSiedlar, 1980). The inoculum of Q/Wingra (Figure 6), for instance, had thehighest abundance of gelatinous green algae found in all experiments. Theyresponded to nutrient addition but were also able to withstand high grazing pres-sure. Aphanizomenon was below detection level in the nutrient treatment, butgrew well in the presence of grazers (Figure 5).

For edible Chi a, nutrient addition in the presence of grazers led to the expectedresults in experiments Q and Q (Figures 2 and 3). Daphnia pulicaria and

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P.H.Kasprzak and R-CLathrop

200 150

lake N Dp Dgtreatment

lake NS Dp MPP Dg MPG

400

lake N Dp MPP Dg MPG

Dg


N Dp Dgtreatment

Figs 5 and 6. Size distribution (greatest axial linear dimension, GALD) and abundance developmentof groups and genera in the cubitainer experiments. Lake, size distribution in the source lake sampleat the beginning of the experiment; N, size distribution in the nutrient-only treatments at the end ofthe experiment; Dp, size distribution in the nutrients plus D.pulicaria treatments at the end of theexperiment; Dg, size distribution in the nutrient plus D.g.mendotae treatments at the end of theexperiment Vertical bars indicate 1.5 times the standard deviation of the mean. MPP and MPG, meanmaximum ingestible particle size by D.pulicaria and D.g.mendotae, respectively, calculated accordingto Burns (1968). Vertical bars indicate 95% confidence limits.

D.g.mendotae grazed heavily on this fraction. However, this was not true forC3/Pike or, to some extent, for C^Silver. Here again, seasonal differences in thecomposition of edible phytoplankton may explain the differences. Daphniagrazing may cause rapid shifts within the phytoplankton community, resulting inthe dominance of ingestible but non-digestible algae (Kerfoot et aL, 1988).

The influence of Daphnia grazing on inedible Chi a showed almost all combin-ations of possible results. Nevertheless, there seems to be a seasonal trend in the

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60T





1000




results (Figures 2 and 3). Experiment Q occurred during the clear-water phase.At that time, inedible algae did not grow very much. Consequently, there was notmuch available to Daphnia, although some difference was found between theDpul and Dgm treatment. Later, during experiment Q, which was run near theend of the clear-water phase, inedible algae played a much bigger role, but at leastD.pulicaria was able to offset some of the algal growth. Finally, in experiment C3,which was carried out in the middle of the summer bloom, both daphnids stimu-lated the development of inedible Chi a, possibly through the elimination of com-petition from smaller, faster growing algae. This time-dependent development isalso in agreement with the existing literature (Pace, 1984; Buergi et ai, 1985;Lehman and Sandgren, 1985; Bergquist and Carpenter, 1986; Sommer etaL, 1986;Elser and McKay, 1989; Vanni and Temte, 1990).

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PJLKaspnak and R.GLathrop

As a general result of this investigation, D.pulicaria was found to have astronger negative influence on the concentration of edible Chi a and on theedible/inedible ratio. A smaller effect was found for D.g.medotae, although theconcentration of animals and their length were similar to the D.pulicaria treat-ments. Therefore, it remains uncertain whether this difference was a property ofthe species or simply a consequence of biomass and allometry (Figures 2-4).

As shown by the length-dry weight relationships, D.g.mendotae at a given sizehas a much smaller individual biomass than D.pulicaria (Lynch et al, 1986).Because biomass is a major factor in the filtration rate model used, higher filtra-tion potential was calculated for the Dpul treatments (Peters and Downing,1984). Although filtration of planktonic animals was found to be notoriously vari-able, size-dependent rate models may provide a basis for comparison (Peters,1983; Knoechel and Holtby, 1986a). However, Lampert (1988) has shownremarkable differences between model calculations and in situ measurements ofcommunity filtration rates (see also Cyr and Pace, 1993).

Burns (1969a), using a suspension of different sized plastic beads, found a verysimilar distribution of particle sizes ingested by both species. Morgan et al. (1980)indicated a maximum ingestible particle size of 35 and 40 u.m for D.g.mendotaeand D.pulicaria, respectively. Kasprzak et al. (1986) found no size-selectivegrazing of D.pulicaria in a mixture of big and small Chlamydomonas geitleri.Burns (1969b), however, refers to higher specific filtration rates in D.g.mendotae.Because she found almost no differences in size-specific body weight between thetwo species, the same is true for the absolute clearance rate. In eutrophic LakeMendota, substantially lower phytoplankton biomass and clearer water occurredin years when D.pulicaria and not D.g.mendotae dominated the crustacean plank-ton (Lathrop and Carpenter, 1992; Lathrop et al, 1996).

Body size is generally considered to be a good predictor of the maximum par-ticle size ingested as well as the filtration rate of cladocerans (Geller, 1975; Hoppand Horn, 1984; Pace, 1984; Schoenberg and Carlson, 1984; Knoechel and Holtby,1986b; Sterner, 1989). The upper limits of ingestible particle size for eitherspecies, calculated according to Burns (1968), indicate maximum differences of 5|im in experiment Q, 10 jim in C2 and 8 jim in C3. Especially in Q, D.pulicariacould take particles larger than 35 fun, the supposed threshold of inedibility,whereas the maximum size ingestible by D.g.mendotae was always lower thanthis. Therefore, different abilities to ingest larger particles may explain at leastsome of the differences found.

Another factor is the metabolic rate, as influenced by the above-mentionedsize-dependent biomass difference in both species. Given a body size of 1 mm,D.g.mendotae has a dry weight of 5.5 u-g compared to 10.7 u.g in D.pulicaria.According to Konoplev et al (1978; quoted in Peters, 1983), this is equivalent toa difference in metabolic rate of ~ 1.71. Because metabolism is in close correlationwith food uptake (Lampert, 1977), the higher metabolic demands in D.pulicariamay be another reason for its greater influence on phytoplankton.

Nevertheless, Reynolds (1984a) indicated community filtration rates >0.3 day1

to be critical for grazeable phytoplankton. Daphnia g.mendotae clearly exceedsthis level; therefore, the missing relationship between filtration potential and Chi

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a concentration within the group of grazing treatments (-100-480 ml H day1) isstill somewhat surprising. One reason might be that some small grazeable algaecan grow much faster than 0.3 day1.

The different results of Daphnia grazing concerning the fractions of edible andinedible Chi a are not necessarily reflected at the level of genera and groups(Figures 5 and 6). Compared to copepods, Daphnia is considered to be a non-selective grazer (Joergensen, 1966; DeMott and Moxter, 1991). Therefore, one ofthe major prerequisites making an alga grazeable and ingestible to this group ofanimals is size (Sterner, 1989). Other factors are also important (reviewed byLampert, 1987).

The experiments in Q/Wingra indicate that D.pulicaria had little effect onMicrocystis growth, whereas D.g.mendotae enhanced the development. On thecontrary, the results of CySilver show a strong inhibition (Figure 5). Microcystisis considered to be difficult to ingest because the colonies are usually too big andtoxic strains sometimes inhibit filtration (Thompson etaL, 1982; Fulton and Pearl,1987; Jungmann and Benndorf, 1994). However, Ferguson et al. (1982) occasion-ally found colonies up to a size of 60 u.m in the gut of D.hyalina. As shown inFigure 5, an overlap occurred between the maximum particle size ingested byD.pulicaria (MPP) as well as D.g.mendotae (MPG); therefore, grazing may havesuppressed algal growth. The differences between the outcome of both experi-ments may be explained in terms of nutrient competition (Tilman, 1981). Micro-cystis from Lake Wingra faced a lack of nutrients, as indicated by both theintensive uptake and high Chi a concentrations. The opposite was true for Micro-cystis in Silver Lake (Table II). Consequently, grazing at different levels of nutri-ent limitation may have quite different results.

A similar pattern was found for Aphanizomenon (Figure 5). In Q/Pike, D.puli-caria was able to decrease the concentration significantly (see Epp, 1996).However, nutrient-only addition in CyWingra resulted in a decreased abundanceof Aphanizomenon, whereas in the presence of D.pulicaria an increased concen-tration was found.

For Ankyra, nutrient addition was not sufficient for net growth (Figure 6). BothDaphnia species stimulated Ankyra, although the cell size indicated the speciesto be ingestible. Reynolds et al. (1982), however, found no grazing resistance inthis genus.

Colonial green algae are considered to be ingestible, but non-digestible due totheir gelatinous capsule (Porter, 1976). However, it is unclear whether there is afunctional relationship between the thickness of the mucilage layer and thedegree of protection. The results of our experiments indicate the group to be sus-ceptible to grazing, but it is also able to sustain rather high numbers (Figure 6).

Melosira and Fragilaria were surprisingly inhibited in both Daphnia treat-ments, although there was almost no overlap between the size distribution of thealgae and MPP and MPG, respectively (Figure 6). Nevertheless, Horn (1981) andVyhnalek (1983) found both diatoms in the gut of Daphnia. Dawidowicz et al.(1988) observed Daphnia breaking filaments of blue-green algae in order toingest them, so a similar breaking of the diatoms may have occurred in our experi-ments.

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P.H.Kaspriak and R.CLalhrop

In summary, nutrient addition always had an enhancing effect on the concen-trations of Chi a, although the edible and inedible fractions reacted differently.The influence of D.pulicaria and D.g.mendotae was not uniform, but indicated aseasonal change in the interaction between phytoplankton and grazers. Daphniapulicaria had a bigger influence on both fractions of Chi a than did D.g.mendo-tae. The results concerning the interaction of both Daphnia species and differentgroups and genera of phytoplankton reflect a variable picture. They indicate thatat least under the conditions of these experiments, remarkably large algae can behandled by Daphnia. On the other hand, species which are considered to begrazeable increased in abundance at rather high filtration potentials.

With respect to biomanipulation as a tool in water quality management, ourresults indicate that large-bodied Daphnia are desirable because of their greaterinfluence on the edible fraction of phytoplankton. Moreover, because themaximum size of particles that can be handled by these larger Daphnia is a func-tion of its body size, the amount of inedible algae being grazed may also increase.Therefore, the duration of the spring clear-water period may be extended becauselarge-bodied D.pulicaria effectively graze those algae typical of the transitionstage between the clear-water phase and the beginning of the summer bloom. Ourresults further indicate that the direct influence of Daphnia grazing on the com-munity structure of summer phytoplankton is rather small. However, the indirectinfluence of large-bodied grazers such as D.pulicaria may be large. Because large-bodied grazers have much greater filtration rates than equal numerical densitiesof small-bodied grazers, small, fast-growing algae are eliminated. Then largeslow-growing algae such as Aphanizomenon can develop especially when nutri-ent supply rates are high. This association between D.pulicaria (or D.pulex) andAphanizomenon has been reported in many eutrophic lakes (Hrbacek, 1964;Lynch, 1980; Ganf, 1983; Andersson and Cronberg, 1984; Pechar and Fort, 1991).Consequently, biomanipulation may not produce substantial improvements inwater clarity in lakes unless nutrient control is also implemented (Reynolds, 1994;Benndorf, 1995; Lathrop et al, 1996).

Acknowledgements

Both authors thank Steve Carpenter and an anonymous reviewer for many helpfulcomments on the draft. This research was funded in part by a grant given to P.H.K.by the German Research Foundation (# Kal206/l-l). Field and laboratory supportwere provided by the North Temperate Lakes Long-Term Ecological Researchprogram and the Wisconsin Department of Natural Recourses. As senior author,I am grateful to the Center for Limnology of the University of Wisconsin, Madison,and its people for accommodating and hosting me for almost a year. My specialthanks to Steve Carpenter for accepting me as a visiting scientist and for a numberof new insights into the field of limnology. Very many thanks to Richard Lathrop,to whom I became friend, for his help in developing and conducting the researchprogram, and for many other little problems that had to be settled during my stayin the USA. Last, but not least, my thanks to Martha Wessels and Sara Mockertfor their help in the field and for teaching me a lively English: 'hang a Louie!'

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Received on December 4, 1996; accepted on April 9, 1997

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influence of two daphnia species on summer phytoplankton

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