Kirk, 1991. Inorganic Particles Alter Competition in Grazing Plankton. the Role of Selective...

8/13/2019 Kirk, 1991. Inorganic Particles Alter Competition in Grazing Plankton. the Role of Selective Feeding.

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Ecology, 72(3), 1991, pp. 915-923? 1991 by the Ecological Society of Amenica

INORGANIC PARTICLES ALTER COMPETITION IN GRAZINGPLANKTON: THEROLE OF SELECTIVE FEEDING'

KEVINL. KIRK2Department fBiologicalciences, artmouth ollege, anover, ewHampshire 3755USA

Abstract. Suspended sediments clay and silt particles) ifferentially nhibit ladoceranpopulations, but not rotifer opulations, and can change the outcome of competitionbetween rotifers nd cladocerans in favor of rotifers Kirk and Gilbert 1990). This paperprovides a mechanistic xplanation for he population and community ffects f suspendedclay. Feeding experiments with radioactively abeled phytoplankton ells (Cryptomonas)showed that the presence of suspended clay ( 1.2 mm body length)mechanically nterfere ith mall, undefended otifers.Large cladocerans are competitively uperior to roti-fers, nd often ause the suppression or extinction frotifers Gilbert 1988).Any physical or biological fac-tor hatdifferentially uppresses ladocerans more thanrotifers may cause a change in competitive outcome,and thus may change zooplankton community truc-ture. n laboratory ompetition xperiments, he pres-

ence of inorganic suspended sediment clay and silt)particles reversed he usual competitive dominance ofcladocerans over rotifers. n the absence of suspendedclay, the rotifer eratella cochlearis was outcompetedby the cladocerans Daphnia ambigua and Ceriodaph-nia dubia. However, when suspended clay was present,the rotifer ominated the cultures, nd the cladoceranswere reduced to near extinction. The effect f sus-pended clay at the community evel was explainedmechanistically t the population evel:suspended claydecreased the survivorship, ecundity, nd populationgrowth ates of cladocerans, but not of rotifers Kirkand Gilbert 1990).

Field observations support the hypothesis hat sus-pended sediments affect zooplankton community

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916 KEVIN L. KIRK Ecology, Vol. 72, No. 3

structure y changing he relative bundance of rotifersand cladocerans n favor of rotifers. ladoceran abun-dance is often ow in lakes that are turbid with sus-pended sediments Adalsteinsson 1979, Hart 1986,Koenings et al. 1990). The relative abundance of ro-tifers nd cladocerans in two basins of Lake Myvatn,

a turbid ake in Iceland, appears to be determined bysuspended sediment concentration. n the less turbidbasin, cladocerans primarily . longispina) dominateand rotifers re suppressed. n the more turbid basin,cladocerans are rare and rotifers re abundant (Adal-steinsson 1979).

Differences n the feeding modes, food-size niches,and food-size selectivities f rotifers nd cladoceransmay be responsible for the differential ffect f sus-pended clay on these two groups. Herbivorous cladoc-erans range n body size from 0.3 to 3 mm. Most usea feedingmode formerly escribed s filter eeding, utmore accurately described as suspension feeding e.g.,Gerritson t al. 1988).Metachronal movements f theirthoracic feeding ppendages pump water through nenclosed bronchial chamber, and suspended particlesare collected by the setules of these appendages. Foodparticles re then transferred p a ventral food grooveto the mouth Cannon 1933). Many particles may becaptured, handled, and ingested imultaneously. Cla-docerans ngest particles anging n size from .5 to 40Am (Burns 1968, DeMott 1982, 1985, Porter et al.1983, Bogdan and Gilbert 1984, 1987, Gophen andGeller 1984). In addition, many cladocerans are non-selective feeders, nd ingest particles n proportion otheir abundance in the environment Lampert 1974,DeMott 1982, 1985, Brendelberger 985). Because oftheir elatively onselective eedingmode, and becausethe food-size niches of cladocerans overlap the rangeof suspended sediment particle izes commonly foundin nature 0.5-2 gin), cladocerans ngest uspended ed-iments Arruda et al. 1983, Gliwicz 1986). Ingestionof suspended sediment particles reduces the ngestionrates on nutritious hytoplankton ells, perhaps due tomechanical nterference ith he collection r ngestionof phytoplankton ells (Arruda et al. 1983, McCabeand O'Brien 1983, Hart 1988).This reduction n phy-

toplankton ngestion ate may cause the reductions ncladoceran abundance often observed in turbid akes.Herbivorous rotifers re much smaller than cladoc-

erans 0.08-0.3 mm) and have a very different eedingmode. Many rotifer pecies are raptorial. As they wimthrough he water propelled by bands of cilia on theiranterior end, they randomly encounter and captureindividual prey tems, ranging n size from to 18 Am(Bogdan and Gilbert 1984, 1987, Gilbert and Bogdan1984, Rothhaupt 1990). Thus, the food-size niche ofrotifers s much narrower han that of cladocerans anddoes not nclude particles n the ize range f uspendedsediments. n addition, rotifers eed selectively, ndpreferentially ngest arge algal cells, particularly lag-ellates, over smaller lgal cells or bacteria Bogdan and

Gilbert 1984, 1987, Gilbert and Bogdan 1984, Roth-haupt 1990). There are no data concerning he effectsof suspended sediments on the phytoplankton nges-tion rates of rotifers, r on their ability to collect oringest uspended sediment particles. However, I sus-pect that rotifers, ecause of their elective feeding e-

havior and food-sizeniches, re able to avoid ingestingsuspended sediment particles, nd thus avoid the det-rimental ffects f suspended sediments.

The overall goal of this paper is to understand hemechanisms responsible for the differential ffect fsuspended clay on rotifer nd cladoceran populations,and thus to determine the mechanistic basis for thechanges n competitive utcome n the presence f sus-pended clay. compare the effect f suspended clay onthe phytoplankton ngestion atesof a variety f rotiferand cladoceran species. I also examine the selectivityof rotifers nd cladocerans when fed a mixture f phy-toplankton ells and clay particles s a way to quantifytheir elative bilities o ngest hytoplankton ellswhileavoiding clay particles. test wohypotheses: irst, hatthe phytoplankton ngestion rates of cladocerans, butnot of rotifers, re decreased in the presence of sus-pended clay, and second, that rotifers elect phyto-plankton cells over clay particles to a greater xtentthat do cladocerans. The effect f cladoceran body size,both within nd between species, s also considered.

METHODS

Clonal cultures of five cladoceran species (Cerio-daphnia dubia, Daphnia ambigua, D. galeata mendo-tae, D. magna, and D. pulex) and three rotifer pecies(Keratella cochlearis f. tecta, K. crassa, and Synchaetapectinate) were maintained n the laboratory t 20'Cin glass-fiber-filtered ond water nd fed Cryptomonassp. (isolated by John Gilbert). n order to obtain cla-docerans of nearly qual size, individuals of the sameage (within 1 d) were used in all experiments; his re-sulted n a range of cladoceran body lengths ypically< I0 of the mean within ny given experiment.

Stocksuspensions of claywere prepared s described

in Kirk and Gilbert 1990). Briefly, lay collected froma soil sample was repeatedly boiled in sodium hypo-chlorite to eliminate organic matter, washed by cen-trifugation, nd size fractionated y settling. Minera-logically, heclaywascomposed of a mixed-layer llite/smectite R. Reynolds, personal communication). Thecoarse size fraction sed here had a mean particle izeof 1,im, and 95 of the particles were


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June 1991 ZOOPLANKTON FEEDING AND COMPETITION 917

ments, with 5-6 replicate beakers per treatment. n thefirst reatment, nimals were simultaneously xposedto labeled phytoplankton nd labeled clay. This treat-ment enabled the selectivity or phytoplankton verclay to be determined. n the second, or control, reat-ment, nimals were exposed to labeled phytoplankton

without he presence f suspended clay. Phytoplanktoningestion ates n the control nd suspended clay treat-ments were compared to determine o what extent hepresence of suspended clay affected he phytoplanktoningestion ate. n all experiments hytoplankton on-centration was 5000 cells/mL, nd clay concentrationwas zero or 50 mg/L. Suspended clay concentrationsof 50 mg/L re common in shallow akes and reservoirs(see Kirk and Gilbert 1990).

Dual-label feeding xperiments wereconducted withmixtures of 32P-labeled phytoplankton ells and 3H-labeled clay particles, sing techniques imilar o thoseused by Lampert 1974), DeMott (1982), and Bogdanand Gilbert 1984). The phytoplankton pecies used,Cryptomonas sp., is an ovate cell 7 x 14,gm in length(Gilbert nd Bogdan 1984), and was grown n unialgalbatch cultures n modified Marine Biological Labora-tory MBL) medium (Stemberger 1981). To radioac-tively label the Cryptomonas cells, 6 mL algal suspen-sion of 6-8 d old cultures was diluted with 6 mLphosphate-free MBL in plastic centrifuge ubes. Twoto four MBq of carrier-free 2P-orthophosphate NewEnglandNuclear) was added to each tube, nd the ubeswere incubated under continuous llumination. After18-36 h, the phytoplankton erewashed twice by cen-trifugation, nd resuspended n 0.2-gim filtered ondwater. The concentration f the resulting abeled stocksuspension was determined by counting ells in a he-mocytometer, nd the final labeled suspension wasmade by diluting the stock in 0.2-,gm filtered ondwater. The clay was labeled by adsorbing 3H-lysine(New England Nuclear) onto the surfaces of the clayparticles. Ten millilitres f a 2500 mg/L clay suspen-sion were incubated with 200 Bq 3H-lysine t roomtemperature or 2 h on a rotary haker. The clay wasthen washed twice by centrifugation nd resuspendedin filtered ond water.

Animals were acclimated for 2-5 h in nonlabeledsuspensions having the same algae and clay concen-trations hat they would experience during he feedingperiod. Acclimation nd feedingwere conducted t 200in a walk-in ncubator, nder fluorescent ights. Duringthe acclimation period, 1-6 cladoceran individuals ofa given species fewer ndividuals for arger ody sizes)were contained in 20-mL suspensions in 40-mL dis-posable plastic beakers; 50-100 rotifer ndividuals werecontained n 10-mL suspensions. The clay was kept nsuspension y gently wirling hebeakersby hand aboutevery 30 min. To initiate a feeding period, an equalvolume (10 or 20 mL) of labeled suspension was rap-idly poured into a beaker containing cclimated ani-mals. After 5-min feeding eriod, the contents f the

beaker were poured through Nitex net filter 200-gmmesh for cladocerans, 48-,4mmesh for rotifers) luedto the bottom of a plexiglass tube. Fifty-100 mL ofice-cold, carbonated water were poured through hefilter o simultaneously inse nd narcotize he nimals.Tubes containing ladocerans were plunged into ice-

cold, carbonated water, and cladocerans were trans-ferred with a pipette to glass scintillation ials within1min. Rotifers werewashed with 1 buffered ormalininto a petri dish, and transferred ith glass micropi-pettes to scintillation ials within 5 min. Individualsfrom single replicate feeding eaker were placed intoa single cintillation ial. Animals were solubilized byadding 1 mL Protosol New England Nuclear) to eachvial and agitating n a rotary haker at room temper-ature for 1 d. Ten millilitres Aquasol II scintillationcocktail New England Nuclear) and four drops glacialacetic acid were added to each vial. The acid neutral-ized the basic Protosol and reduced chemilumines-cence (DeMott 1982). After etting he vials sit for 1 dto eliminate any residual chemiluminescence, he ra-dioactivity n each vial was assayed using a BeckmanLS5800 liquid scintillation counter. Quenching andcounting fficiency ere determined or ach vial usingexternal tandardization.

Since the abeled phytoplankton nd clay were pres-ent in the same suspension during he feeding xperi-ments, t s possible that the clay adsorbed 32P-labeleddissolved organic matter released by the labeled phy-toplankton cells. In order to minimize this possiblecross-labeling f clay with 32P, he abeled phytoplank-ton and clay were combined for only 1 min beforethey were used in an experiment. A preliminary x-periment howed that no cross-labeling ccurred. Fivethousand cells per millilitre f 32P-labeled Cryptomo-nas cells were ncubated n 0.2-gm filtered ond waterfor 4 h. The phytoplankton ells were then centrifugedout, and the supernatant, which contained 32P-labeleddissolved organic matter, was used in a feeding xper-iment with unlabeled clay. D. ambigua fed this claysuspension showed no accumulation of radioactivityabove background ounts K. L. Kirk, personal obser-vations).Another potential ross-labeling roblem may

occur because Cryptomonas ells may themselves n-gest 3H-labeled clay particles. Other Cryptomonasspecies have been shown on ingest small particles(Porter t al. 1985). However, sincephytoplankton ellswere in contact with 3H-labeled clay for only a shorttime, cross-labeling hould be insignificant.

Differences n algal ingestion ates between the firstand second treatments with and without clay) wereanalyzed using t tests Sokal and Rohlf 1981).Selectivefeeding, r the ngestion f a prey tem out of propor-tion to its abundance in the environment, was indexedusing a (Chesson 1983). Possible values for XA (selec-tivity or lgae) range from (no algae eaten) to 1 onlyalgae eaten). An aA of 0.5 indicates nonselective feed-ing, nd the null hypothesis f nonselective eedingwas



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Algal Ingestion Rate(103 cells/h)

0 20 40 60Cladocerans

Ceriodaphnio dubic (0.98 mm) ***

Dophnia ambiguc (1.33 mm) 0* Control* With clay

D.goleato mendotae (1.99 mm) *

D.mogno (1.23 mm)(2.26 mm) **

D.pulex (1.16 mm)(1.73 mm)

(2.74 mm) ,:4 NS

(106 cells/h)

0 20 40 60Rotifers

Kerotello cochlearis NSK. cross NS

Synchoeto pectinato N S

FIG. 1. Effect f 50 mg/L suspended clay on the algal (Cryptomonas) ngestion rates of five species of cladocerans andthree pecies of rotifers. ladoceran body engths re given n parentheses. Means + SE. t tests f significant ifference etweenclay treatment nd control: NS = not significant P > .05); **P < .01; ***P < .001.

analyzed using t tests to compare the observed Ca to0.5 (Chesson 1983). Differences etween A valuesweretested using Tukey's multiple-comparison means test(SAS 1985).

RESULTS

The phytoplankton ngestion ates of all five peciesof cladocerans were reduced by 13-83 in the presenceof 50 mg/L coarse suspended clay (Fig. 1). These re-ductions were statistically ignificant P < .05) for llcladocerans except large (2.74 mm body length) D.

pulex. In contrast, he phytoplankton ngestion ratesof three species of rotifers were not significantly e-duced (Fig. 1).

Smaller cladocerans were more inhibited by sus-pended clay than were arger ladocerans. The percentinhibition of phytoplankton ngestion rate was nega-tively correlated with cladoceran body size (P < .05;Fig. 2A). Within cladoceran species, the smaller, u-venile individuals were more inhibited by suspendedclay than were larger adults. For example, the algalingestion rate of juvenile D. pulex (1.16 mm bodylength) ecreased by 68 in the presence of suspendedclay, whereas that of young adult D. pulex (1.73 mm)decreased by 49 . The algal ingestion ate of uvenileD. magna (1.23 mm) decreased by 74 in the presence

of suspended clay, whereas hat f young dult D. mag-na (2.26 mm) decreased by 50 .

All cladocerans and rotifers howed significant e-lectivity or phytoplankton ells over clay particles: Avalues were significantly 0.5 for ll animals (all P 10NTU. Hart 1988) found that the ngestion ates of D.gibba, D. barbata, and D. longispina decreased as sus-pended sediment concentrations ncreased above 55NTU.

In contrast o these results, Koenings et al. (1990)present data that suggest hat the algal ingestion rateof D. galeata mendotae was increased n the presenceof suspended sediments. However, they did not mea-sure ingestion rate directly, ut estimated t by mea-suring he rate of decline n chlorophyll concentrationin ars containing ladocerans. Chlorophyll concen-tration was used as an index of phytoplankton bun-dance. The rate of decline in chlorophyll over a 2-dperiod was two times greater n jars containing us-pended glacial flour particles 1-30 jim) than in jarswithout suspended sediments. They attributed heseresults o higher lgal feeding ates by the cladoceransin the presence f uspended ediments. However, theirexperiments had no controls, without cladocerans.Therefore, n alternative xplanation s that the directeffects of suspended sediments on phytoplanktonabundance, rather han the effects n cladoceran feed-ing, caused the greater ate of decline of chlorophyllin ars containing uspended sediments. For example,suspended sediments may have reduced light evels,causing eductions n phytoplankton hotosynthesis ate

(Grobbelaar 1985), or reductions n the concentrationof chlorophyll per cell.The differential ffect f suspended clay on rotifers

and cladocerans s also observed at clay concentrations>50 mg/L. The algal ingestion rate of the cladoceranD. ambigua was reduced by 87 by 200 mg/L sus-pended clay; the ngestion ateof the rotifer . pectinatewas unaffected K. L. Kirk, personal observations).

Selective eeding

The results from the treatment n which animalswere imultaneously resented with lgae and clay sup-port he econd hypothesis: otifers ere more selective

00-

c)

C Cd0

8A

Ca) - A D

A

C 60- D

) L) A A

40- A Ca C

C 20-0 AU D;DD 4-o 0.5 1.0 1.5 2.0 2.5 3.0a)La:

0.9 B

A A

0.8 AA A A

0.7 - A

0.6 0.5 1.0 i.5 2.0 2.5 3.0

Cladocercn Body Length (mm)FIG. 2. (A) Relationship etweenmean ladoceran ody

length nd percent ecreasenalgal ngestion ate nthe res-ence of 50 mg/L lay s compared ocontrols ithout lay.Spearman'sank orrelationoefficientSokal ndRohlf 98 ),r = -0.72; P < .05. (B) Relationship between mean cladoc-eran ody ength ndmean electivity or lgae ver lay A).r, = 0.85; P < .01. Species abbreviations: Cd Ceriodaphniadubia; Da Daphnia ambigua; Dgm D. galeata mendotae; DmD. magna; Dp D. pulex.

for lgae over clay than were cladocerans Fig. 3). Thispattern s reflected n previous studies of the relativesize-selectivities f rotifers nd cladocerans when fedmixtures f small and large particles. Cladocerans, par-ticularly aphnids, ngest mall < 2 gm) as well as largeparticles DeMott 1982, 1985, Porter t al. 1983, Bog-

dan and Gilbert 1984, 1987, Gophen and Geller 1984),while most rotifers o not ngest articles 4 Am Bog-dan and Gilbert 1984, 1987, Gilbert nd Bogdan 1984,Rothhaupt 1990).

Nonselective feeding was correlated with reductionsin algal ingestion rate in the presence of clay. Thoseanimals that were ess selective for lgae over clay aremore inhibited by the presence of suspended clay (P< .01; Fig. 4). In particular, ladocerans are less se-lective than rotifers, nd the algal ingestion rates ofcladocerans, but not of rotifers, re reduced n the pres-ence of suspended clay.

Suspended clay reduces cladoceran feeding ates byinterfering ith the collection and ingestion of algalcells. Cladocerans ingest arge amounts of suspended



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atA

0.6 0.7 0.8 0.9 1.0Cladocerans

Ceriodophniodubic (0.98 mm) A

Dophniu ombiguc 1.33 mm) A,B

D.galeoto mendotoe 1.99 mm) B

D.mogna (1.23 mm) A(2.26 mm) A,

D.pulex .16 mm) A,B(1.73 mm) A,B

(2.74 mm) B

Rotifers

Kerotella cochlecrisW

K.cross CSynchoeta pectinoto C

FIG. 3. Selectivity or lgae (aA) of five pecies of cladocerans and three pecies of rotifers when simultaneously fferedalgal cells (Crvptomonas) and suspended clay particles. An asA of 0.5 indicates nonselective feeding; n asA of 1.0 indicatesingestion f only algal cells. Means + SE. Bars labeled with the same letter re not significantly ifferent Tukey's multiplecomparison means test, xperimentwise rror rate = 0.05).

clay, s shown by their elatively ow selectivity alues.The presence of large amounts of suspended clay inthe gut causes a reduction n the rate of thoracic ap-pendage beating, decreasing the amount of water

pumped through he bronchial hamber, nd thus de-creasing lgal ingestion ate. n addition, collected clayparticles clog the food groove in the region near themouth and cause the rejection of boluses containingboth algae and clay, also decreasing he algal ingestionrate (Kirk 1988). Thus, collected and ingested sus-pended clay particles educe cladoceran phytoplanktonfeeding ates by mechanically nterfering ith both thecollection and ingestion f phytoplankton ells.

Although rotifers were more selective than cladoc-erans, both groups elected lgae over clay:all A valueswere significantly 0.5 (Fig. 3). It is likely that this

selective feeding on algal cells is passive, not active.Passive prey selection results from differences n theability of a predator to encounter, apture, or ingestdifferent rey tems. n active prey election, predatorencounters prey tem, nd is able to eat it, but avoidsor rejects t (Gilbert 1980). Most rotifer pecies, be-cause of their raptorial feeding mode and the mor-phology f their eeding pparatus, simply annot cap-ture mall tems such as clay particles r bacterial cells(Gilbert and Bogdan 1984). Thus, the observed selec-tion of algal cells by rotifers may be passive. Activeselection by rotifers annot be ruled out, however. Re-jection of clay particles fter ollection, perhaps on thebasis of taste DeMott 1986), is one possible mecha-nism for ctive selection. Cladocerans collect argepar-

tides (>2 gim) uch as algal cells on their horacic p-pendages with greater fficiency han smaller particles,such as clay. Thus, algal cells are captured t a greaterrate. Cladocerans have no mechanism for orting ap-

tured particles, r for electively ejecting lay particlesprior o ingestion, o they re unlikely o exhibit ctiveprey election.

The success of a suspension-feeding ooplankter nthe pelagic environment depends upon its ability toingestnutritious articles while voiding nonnutritiousor toxic particles. n nature, phytoplankton nd bac-

0

o 100

. 80A

U) A

c: 60_ AAv 40 A

20o A

' 0.6 0.7 0.8 0.9 .0

FIG. 4. Relationship etween mean selectivity aA) and

percent ecrease n algal ngestion ate n the presence f 50mg/L oarse lay, for ladocerans A) and rotifers -). r, =-0.78; P < .01.



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June 1991 ZOOPLANKTON FEEDING ANDCOMPETITION 921

terial cells of various nutritional ualities are presentalong with noxious or toxic cyanobacterial cells andrelatively onnutritious articles uch as detritus, al-cite crystals, nd suspended silt nd clay particles e.g.,Arruda et al. 1983, Melack 1985, Vanderploeg et al.1987). The ability of cladocerans to utilize small food

particles


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922 KEVIN L. KIRK Ecology,Vol. 72, No. 3

itive outcome in the presence of suspended clay. Cla-docerans are less selective than rotifers, nd thereforeingest uspended clay particles o a greater xtent. Thisreduces algal ingestion ates of cladocerans, but not ofrotifers. he reductions n algal ingestion ates of cla-docerans reduces their population growth rates, and

changes the outcome of competition between rotifersand cladocerans in favor of rotifers. n nature, thesemechanisms may change the relative bundance of ro-tifers nd cladocerans in zooplankton communities.

ACKNOWLEDGMENTS

I thank Rae Barnhisel, Carol Folt, John Gilbert, NelsonHairston, Jr., nd two anonymous referees or heir ommentson the manuscript. am especially ndebted to John Gilbertfor roviding stimulatingaboratory nvironment. axineBeanprovided xcellentechnicalssistance. eff inor, oryNislow, nd Robert eynolds elped nalyze he lay. ClydeGoulden provided the Ceriodaphnia dubia culture. his studywas supported by the Dartmouth College Cramer Fund, En-vironmental Protection Agency grant R-814210 to J. J. Gil-bert and W. C. Kerfoot, nd National Science Foundationgrant BSR-8415024 to J. J. Gilbert.

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