Habitat Heterogeneity and The Functional Signifiance of Fish in River Food Webs Author(s): Mary E.

Power Reviewed work(s): Source: Ecology, Vol. 73, No. 5 (Oct., 1992), pp. 1675-1688 Published by: Ecological Society of America Stable URL: http://www.jstor.org/stable/1940019 . Accessed: 16/04/2012 13:23
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IFcologt'

73(5), 1992, pp. 1675-1688 1992 by the Ecological Society of Amenica

HABITAT HETEROGENEITY AND THE FUNCTIONAL SIGNIFICANCE OF FISH IN RIVER FOOD WEBS'
Departmentof Integratvfe Biology, ULniversity Califbrnia,Berkelea,Berkeley, of California 94720 USA
MARY

E.

POWER

.lbstract. Predation by fish(roach, II(esJerolelucas s)';n;netricus, and steelhead Oncoon biota associated with boulderuiYnchus ;nhvkiss) produced strongcascading effects

in bedrocksubstrates pools of a northern Californiariver,but not on gravel-dwelling biota. in Enclosure-exclosure experiments theSouth Fork Eel River ofnorthern California(39044' N, 123039' W) showed that fish,by suppressingdensitiesof damselflynymphsand other small predators,released algivorous chironomids (Iseudochir'onomalus richardsoni)from predation.Chironomids in turndramaticallyreducedalgal standingcrops. In contrast, fish had littleeffect algae or invertebrates on associated withgravel.Gravel-dwelling heptageniid mayflies were behaviorallyinhibitedfromusingtops of stones in fishenclosures,and stone surfaceshad more chironomid tubes in fishenclosures than in fishexclosures. However, no effects epilithicalgae or densitiesof invertebrates on comparable to those of biota on in boulder-bedrocksubstrates weredetected.These spatiallyvarying predator effects a river parallel resultsfrommarine benthic systems,where strongeffects large predatorsdocof umented forrocky intertidalhabitats and unvegetatedsoftbottoms are not conspicuous in seagrass beds.
ver coitnnunities; stronginteractions; Kev words: benthos;fish;food webs; omnivore: refuges;ri stdbstrate heterogeneity: trophiccascades.

habitats thatlackrefuges (Huffaker 1958, Hastings1977, INTRODUCTION The effects predators on their prey depend not Caswell 1978, Crowley 1981, Holt 1984). of Substratesin riversand streams vary considerably only on biological attributesof both, but also on the in theirpatchinessand quality as habitatsand refuges settingof their interaction.Predators that are functionally importantin one environmentalsettingmay (Hart 1978, Minshall 1984, Hurynand Wallace 1987). play only a minor role in another. For example, the In riverreaches where sediment supply fromthe watershedis high relative to the capacity of the riverto starfish f'isaster is a keystone species structuring ingravel sediments will tertidal communitiesalong theWashington Statecoast, transportbedload, fine-grained cover much of the bed (Dietrich et al. 1989). Boulders but may be "just another starfish"in Alaska (Paine will emergeas habitatislands 1980:670). Predatorimpacts may vary over space for and bedrockformations fromperiodicallymobile gravel beds. Conversely,in a numberof reasons. Fretwell(1 977, 1987) and Oksanen et al. (1 98 1) predictthatthe functional significance rivers that are "sediment-starved" relative to their capacities, coarse bedrock and boulder subof predatorsshould shiftalong gradientsof environ- transport In mental productivity. habitats too unproductiveto strateswill predominateon the bed surface(Dietrich sediments support permanent predator populations, transient et al. 1989), and theisolated depositsof finer may function habitatislands forgravel-dwelling as bipredatorindividuals mightoccur, but would be incaota. pable of limiting populationsoftheirprey(but see Holt For a riverreach of the first type,I compare previ[1984. 1985] and T. Oksanen [1990] fordiscussions of of on ouslyreported (Power 1990a) effects fish thebiota Predatorimpactsalso varyover space spillovereffects). of boulder-bedrockhabitatislands withnew resultson in relationto structural variation of the environment on with (Huffaker 1958, Smith 1972). The efficiency which fisheffects biota of the gravel bed. I used direct predators deplete their prey declines with increasing behavioral observationsand diet data to ascertainthat Losses to predationcan be fishfed in both microhabitats,and an enclosure-exavailabilityof preyrefuges. by which varies with the de- closure experimentto assess theirdirectand indirect offset preyimmigration, greeof habitatisolation(Holt 1984, Cooper et al. 1990). impacts on lower trophiclevels. All else being equal, the net impacts, or functional of significance, predatorsshould be weakestin continuous habitats with refuges,and strongestin isolated
I Manuscript received8 July199 1; revised22 October 199 1 accepted 28 October 199 1.
STUDY SITE AND BIOTA

The studysite is a 1-kmreach of the South Fork of

the Fel River (39044'

County,California,USA. The studyreach is surrounded byan old-growth conifer forest dominatedby Douglas fir(Isciiudotsuiga mnczn-iesil') and coastal redwood

N, 123039' W) in Mendocino

1676

MARY E. POWER

Ecology, Vol. 73, No. 5

(Seqiuo)ia selmperlwires). Nearly all precipitation falls

between October and April (Anderson et al. 1987). Followingwinter floods.baseflowdischargedropsfrom 10-25 m3/s to <1 m3/sduringthe summer,and the river slows to forma series of large lentic pools connected by shortriffles. mid-June1989, an estimated In of 30)/4) the wetted area in the 1-km study reach was lentic(flow <5 cm/s): by late Julythis lenticarea was 59%/o. late August, 60%. and by early September, by 86'/%. The bed of riverpools was largely composed ofgravel particles2-64 mm in median diametersurrounding boulders >256 mm in median diameterand emergent bedrock formations.In the 1-km study reach, the estimatedpercentage area projectedto the watersur(by face) of boulders and bedrock in the wetted channel increased from39% to 44% to 50% from 14 February to 20.Julyto 10 September,because lateralgravelbars dried as water levels dropped. During winterfloods, gravel is transported around the more stationary boulders and bedrock. Biota on boulder and bedrock "islands" are less subjectto abrasion thanbiota on smaller stonesduringepisodes of bed movement(Hynes 1970, Sousa 1979, McAuliffe1984, Powerand Stewart1987). Because the active channel maintained by winter floods is wide (z30 m), duringsummer much of the riverbed is sunlit. Turfsof filamentous green macroalgae (primarilyCladophora gloincrala L.) develop on boulders or bedrock outcrops,probablyby vegetative regrowthfrom basal pads that survive winterscour. of During most years. turfs Cladophora attain lengths of several metresby June.and, in places, Cladophora canopy covers most of the riversurface(Power 1990a, b. c). Gravel substratesare thinly coated withdiatoms and detritusformost of the year. Short,attached filamentsofgreenalgae first appear on pebble and cobble substrateonly in late summer or fall of most years, suggesting infrequent recruitment from zoospores (Power 1990c). While some invertebrates occur on both gravel and turf-covered boulders, many taxa are specialized for one microhabitator the other(Minshall 1984, Dudley et al. 1986). Heptageniidmayfly common prinymphs, mary consumers in gravels, are morphologicallyspecialized, with flattened bodies that enable the insects to wedge themselvesinto crevices and spaces between stones (Hynes 1970:123). Gravel sediments are also inhabited by tube-dwellingchironomids, stoneflies,

alopteran larvae (Sialils sp.), and a varietyof mayflies (baetids. siphlonurids, ephemerellids) occur in both microhabitats. The most common fishin the study reach in early summerare Californiaroach,Ilesperolcucas stmmn l ciicus) and juvenile steelhead (Oncorhynchus ;uvkiss in[=LSaIho gairdneri]).In contrastto habitat-specific vertebrates described above, these fishesswim freely betweengraveland turf-covered boulders.By midsummer,roach and thefewoverwintering stickleback (Gastcrosteis acIIlealu.S)

produce large numbers of fry.

METHODS

Enclosures/exclosures

Food webs were allowed to develop in the presence or absence of large fishin 12 large (6 m2) pens. Pens were 3 m long x 2 m wide x 1.3 m high,with walls of plastic screen lined with black plastic shade cloth. Most stream invertebratesand fish fry could pass throughthe 3-mm mesh shade cloth walls. The shade cloth extended 60 cm below the bottom edge of the wall, and this skirtwas anchored with gravel to preclude passage of large fish. Otherwise, the enclosed riverbed was unmodified.Periodic hand cleaningand driftdeflectors 20 cm wide aluminum flashing of set at the water surface ;1 m upstream frompens kept drifting detritus fromclogging pen walls. Each pen was built around boulders or bedrock that supportedCladophora turfs. These boulders or bedrock islands were surroundedby gravel inside each pen, which was contiguous with gravel outside enclosures. During July when flow inside and outside pens in pools was too low to measure, rates of fine sediment outfall were similar inside pens (X + 1 SE = 0.78 ? 0.06 mg cm 2 d ', n = 104) and in the open river(1.05 +
0.18 mg-cm '-d ', i = 23) (l = 1.35, P > .1 from Welch's approximate t test forsamples with unequal

variance [Zar 1984:131]). Maximum water depths in pens rangedfrom62 to 83 cm, overhead forest canopy measured on a sphericaldensiometer(Lemmon 1957) ranged from3 1.8 to 69.5% open, and boulder or bedrock covered 27-58% of the enclosed area (projected to the watersurface).(The remaining area was gravel.) in The 12 pens were distributed groups of fourover a 1-km reach. Within each group, two pens were selected randomlyto be stockedwithfish ("enclosures"): the other two were left unstocked enclosureses"). naucorids (lhrtisuas inormH)on), and dragonfly (aeshStocked enclosuresreceived 20 juvenile steelhead(28nid. gomphid,and libellulid)nymphs.(Cladophora turfs 50 mm SL [standard length,Lagler et al. 1977:403]) on boulders and bedrock harbor perchingdamselfly and 40 roach (30-70 mm SL). Physical attributesof (lestid and coenagrionid) nymphs,hydrophilidbeetle pens in bothtreatments (means ? l SE) wereon average larvae (Inochrus sp.), and a guild of algal-weaving chi- similar. Maximum depths,canopies (% open), and / -onomids dominated by thespecies Pseudochironornus boulder-bedrockwere: 72 ? 1 cm, 54.4 ? 6.3'%, and richardsoni(Power 1990a, h). Oligochaete worms as- 37 ? 3% in stocked enclosures,and 78 + 4 cm, 51.5 sociated with detritusin chironomid retreats are also ? 3.8%, and 38 ? 5% in enclosures, respectively. Fish common in algal turfs(Power 1990h). Caddis larvae were size matched among enclosures. Stocked groups sp., (Lupidostonma Gumiagasp., Ilic/ops vchcsp.), meg- reflectedproportionsand size distributionsof fishes

October 1992

SPATIALLY VARYING TROPHIC CONTROL BY FISH

1677

(427 roach, 186 juvenile steelhead,and 1 stickleback) the study captured by trappingand electroshocking began. Densities reachin earlyJune,whenexperiments of fishin enclosures (10 individuals/) were within rangesobserved (5-48 individuals/) near largeturfcovered boulders in the open river,but were higher estithan overall fish densities (1-2 individuals) mated from electroshockingsurveys of larger river reaches encompassing both gravel and boulder-bedrocksubstrates (Brownand Moyle 1989; M. Power and data). J. Nielsen, unpublished

nificationin the laboratory.The presence or absence in algae, and detritus theirguts ofdiatoms,filamentous was noted. Macroinvertebrateswere identifiedand measured under dissecting microscopes (10-70 x). of Publishedregressions head capsule widthto drymass (Smock 1980) were used to estimate dry biomass of ingestedinvertebrates. Cladophora biomass sampled fromcores was measured as damp mass (after50 spins in a salad spinner which was convertedto dry mass according [dryer]), dry to theregression: mass = 0.09 (damp mass) + 0.02, r2= 0.98 (Power 1990b). Epilithicalgae were sampled Sampling fromcobble surfacesby aspiratingareas within 1-cm2 Algal standingcrops and condition were monitored templates. Cells were counted in a Palmer chamber, in nondestructively each pen at 23-48 sites along five and cell counts were convertedto dry mass estimates boul- by assuming0.420-0.904 mgash-free mass per 106 dry cross-streamtransects,where these intercepted ders or bedrock. At sites spaced at 10-cm intervals cells (fromestimatesof Stevensonand Stoermer[ 1982] of along each transect,I noted dominant and subdomi- fordiatoms),and thatdiatoms had ash contents 50% nant taxa of macroscopicallyconspicuous algae, mea- (Winberg 1971). sured the visually estimatedmodal heightof these alBehavioral observations gae, and theirconditionand density(% canopy cover) I observed fishto compare the feedingbehavior of (see Powerand Stewart[1987] formoredetailsofmethods). No macroscopicallyconspicuous algae were ob- caged and free-swimming individuals,and to estimate effort (numberof bites) thatcaged individserved on gravel substratesin pools, inside or outside the feeding the uals allocated to turfson boulders and bedrock, and of enclosures,throughout 6-wk experiment. In addition, at the onset of experiments June),3 to gravel substrates.Visibility was excellent, as the (5 wk (22 June),and 5-6 wk (16 and 24 July)afterwards, waterwas clear and < 1 m deep, the surfacewas calm, I collected cores of algae and of sedimentsfrompens and I was able to stand within 1-2 m of the fish I and fromnearbysites in the open riverforsamples of observed,near outerwalls of enclosuresor on the river observations,I would wait quialgae and associated biota. Organisms in gravel sub- shore.Beforeinitiating strateswere sampled with a 6.4 cm diameter metal etlyfor20 min. Withinthistime,fishdisturbedby my corerthatwas pushed 5 cm intothebed. These samples approach resumed apparentlynormal activities. To quantifyfeedingrates and microhabitatuse by were elutriatedin the fieldand preservedin 70% ethI anol. Attached algal turfsand associated organisms fish, recordedthe bitesof a focalindividual fortimed from boulderand bedrockoutcropswerecollectedwith periods of 1-9 min. During observations,I noted the 9.0 cm diameter cores, fittedat the top end with a species and estimated the lengthof the fish,and reboulders, three-layeredsleeve cut from nylon stockings. The corded the bites it allocated to turf-covered enclosurewalls, or the watersurface. sleeve (mesh size of -0.3 mm) retainedorganismsas gravelsediments, the the sample was liftedthrough watercolumn, until Most observationsstopped after5 min or when I lost into plastic bags and sightof the focal individual. To reduce bias and dethe sample could be blackflushed preserved(see Power [1990a] fordetails of methods). pendence in observations,I chose focal individuals by Block effects were insignificant, and were dropped a systematicspatial rule. I visually divided each enand fromthe analysis. Algal biomass and the densities of closureor observedopen area intosix sections:left and downstream thirds, center, sides ofupstream, the dominant invertebrateprimary consumers and right predatorsfromenclosures,enclosures,and open sites and selected sequential focal individuals in nonadjawere subjected to planned comparisons at the end of cent sections. on feeding As a second checkforenclosureeffects fish theexperiment withone-wayKruskal-Wallistests,followed by Dunn's nonparametric multiplecomparison behavior,I used theMorisita-HornIndex (Krebs 1989) For to estimate overlap in microhabitatuse by enclosed test(Zar 1984:200) when resultswere significant. fish: some ofthepredatory heteroscedasticity and free-swimming invertebrates, among samples could not be eliminatedby data trans2 PijPik I formation. applied the relatively conservativeKrusCH = 2 P., + 2>2 kal-Wallis test forall comparisons so that the assessvariables was ment of treatmenteffects different for notconfoundedbytheuse oftestswithdifferent power. wherepi is the proportionof resource i used by conAt the end of the experiment,gut contentsof en- sumerj or k. CH ranges from 0 (no overlap) to 1.0 closed and freeswimmingroach and steelhead were (complete overlap). Enclosed fishsometimes foraged examined. Individuals weredissectedunder 10 x mag- on enclosurewalls,whichwerenotavailable as foraging

1678
TABLE

MARY E. POWER

Ecology, Vol. 73, No. 5

1. Roach and juvenile steelhead feedingrates epilithic algae from 1-cm2areas circumscribedby a 12 July template.These algal samples were preservedin vials inside and outside enclosures, June-14 (bites/min) 1989. and later counted under 400 x in the in 2% formalin, laboratory. Inside Outside Fish A 1 SE 11 V 1SE ti SL (cm) 3 4 5 6 7
Roach (lesperolucias

Feeding behavior of enclosed roach and steelhead conspecificsin resembledthatof theirfree-swimming both rateand substratechoice. Size-specificper capita 17 8 .02 .01 .05 .05 " feedingrates, except for the smallest (3 cm SL) size invkiss) Steelhead (Onchorhvxnchus class of roach,weresimilarforenclosed and free-swim3 6 8 .01 .01 .01 .00 ming fishof both species (Table 1). In addition, roach 4 12 7 .01 .03 .01 .01 among gravels, and steelheadapportionedtheirfeeding 5 17 .02 5 .02 .04 .01 19 1 6 .02 .02 .01 boulder substrates,and the water surfacesimilarlyin enclosures and in the open river(Fig. 1): overlaps in were theallocation ofbitesto thesethreemicrohabitats roach and fish. Feeding observa- C, = 0.98 forenclosed and free-swimming substrates for free-swimming steelhead. tions on enclosure walls were not included in com- C, = 0.95 forenclosed and free-swimming juvenile steelhead alloputationsof overlaps betweenenclosed and free-swim- Enclosed and free-swimming cated more bites to the water surfacethan did roach miingroach and steelhead. (Manly's alpha) of enclosed fish Preferenceof roach and steelhead for boulder vs. (Fig. 1). Preferences gravel substrateswas computed as Manly's alpha for for boulder-bedrock vs. gravel substrateswere 0.68 sugundepletedresources(Chesson 1978, Krebs 1989:396): and 0.77 for roach and steelhead, respectively, gestingthat enclosed individuals of both species prea,,1 lt'b, I'J, + _n,, tlie,
1.0Ci)

.00 .04 .03 .04 .03

.00 .02 .01 .01 .01

4 11 40 64 48

sls tletricus)

RESULTS

.16 .04 .03 .06 .05

.06 .01 .02 .02 .03

7 8 8 14 8

Fish feeding behavior

Stee IRoach

index forboulder-bedrock where a,, is the preference

substrate.
r;,

0.8 -

stratesallocated to boulder-bedrock,n,,is the propor- H 0. outside tion of boulder-bedrocksubstratein enclosures(based 0 and ns, on area projected to the water surface),and rg, are the proportionsof bites allocated to gravel subof stratesand proportions substratesin enclosures,re- 0 spectively(r,,+ r,, 1; n,, + n,,= 1; Manly's alpha ranges from0 [complete avoidance] to 1.0 [exclusive 0 QL 0.0 selection]). Wall Surface Boulder-Turf Gravel On 14 July(week 6), 1 counted mayflieson tops of stones (28-64 mm estimated median diameter) in all 1.0 P FG enclosures. Afterapproaching an enclosure for these Steelhead mingroacha)ad counts,I would standquietlyfor20 min. Then I count0D4 -ED 0.8 on ed the mayflies top of everyotherstone lyingalong a longitudinaltransect from the downstream to the inside El~~ 0 H 0.6 upstreamend of an enclosure. Dark heptageniidmayMoutside stones. 0 flieswerequite visible against the light-colored Afterrepeatingthese counts on each of threedays, I 0.4collected stones fromall enclosuresforcensuses of in- 0 sectsclinging all surfaces, to and for samples ofepilithic and I bEo i en optdprtetet diatoms grown on top surfaces.To choose stones, I stretched metretape along the lengthof each encloa sure. and picked the stone undereach 20-cm interval. Wall Surface Boulder-Turf Gravel Selected stones and associated biota were netted(0.3bedFIG. 1. Proportionof bitesallocated turf-covered to mm mesh) and transferred ziplock plastic bags at rock, to and surface enclosed free-swimand gravel, thewater by werepicked ming After macroinvertebrates thewatersurface. roach andsteelhead Histogram areaverages bars (a) (b). offand chironomid tubes were counted, I aspirated and 1 SE OfSixmeanscomputed treatment. per

is the proportion of bites on benthic sub-

October 1992
-U >5 t

SPATIALLY VARYING TROPHIC CONTROL BY FISH

1679

Roach Diet by Number

40

Steelhead Diet by Number

40

a
El

b
f free-swimming 12) (n enclosed (n =15)

020 -

free-swimming=23) (n enclosed (n=25)

. -3

30

-I

2.0

1.0 -

1.0 -

ci~~
Z
a)

F'1r414~~~~1~~ZLT
CZ

II~~~~!

0.0

O) (n
CZ a-)
0TE7

E
0

)c

E
-0

175 -175-

FI.

150 -

iE
-F
(1)

cz125 100(

El free-swimming enclosed

150 and
125
100

El free-swimming El enclosed

50 -50
(" LU

I
II
25 -

25

-00

~~~~~~~~~~~~~~~~~~0

HI

and FiG. 2. Numbers of invertebrates individual free-swimming enclosed roach (a) and steelhead (b), and estimated per biomass of these invertebrates roach (c) and steelhead (d) guts. "hept" =heptageniid mayflies;"mayf' =other mayflies; in ..chiro" chironomids;"dipt" =other dipterans;"nauic" =naucorid bugs,"gerr" =gerrids;"drag" =dragonflies;"dams"= damsclflies:"cadd" =caddisf'ijes; "'elm" =etmid beetles; "hydro" =hydrophilid beetles; "plec" =stoneflies; and "siat" sialids; "unid" =unidentified. Data are averages with 1 SE.

erred boulder to gravel substratesfor feeding.Preferences of free-swimming fishcould not be assessed because the relative availability of the two substrate types withintheirhome rangeswas unknown. Fish gut contents Guts of roach and steelhead (both >30 mm SL) collected at the end of the experimentcontained both gravel-and algae-dwelling insects(Fig. 2a-d). Fourteen categories (orders or families of insects and an unidentified category)were discriminated.No significant could be detected in the frequency condifferences of sumptionof any of these categoriesby free-swimming vs. enclosedroachor steelhead(ttestson arcsine-squareroot-transformed proportions,with a critical level of .004 calculated by the Bonferroni criterion).Mayflies were major componentsof the diets of both roach (20 and 26%, respectively, the individuals counted in of freeand enclosed fish)and steelhead (51 and 38% of the individuals counted in freeand enclosed fish,respectively). Damselfly larvae were, because of their large size, importantcomponents of the biomass ingested by free-swimming roach and freeand enclosed

steelhead,althoughtheywerenot numerousin fish guts (Figs. 2c, d). Chironomid larvae were infrequentin both roach and steelhead guts,and were insignificant componentsoftheir dietsbybiomass (Fig. 2a-d). Roach also consumed filamentousalgae and diatoms in addition to arthropods, while steelheadwere strictly carnivorous (Power 1990a). Impacts of fishon boulder-bedrock biota At the onset of the experiment,algal turfscovered all siteson boulder-bedrocksubstrates sampled in both enclosuresand exclosures(Power 1990a). Subsequently,algal standingcrops declined in all pens and in the open river. Declines were greatestin enclosures with fish,and least in enclosures(Fig. 3). Five weeks after experimentsbegan, algae on boulders in stocked and unstockedpens differed conspicuously(Power 1990a) and significantly (Table 2, Dunn's multiplecomparison test indicated significant differences between enclosuresand enclosures[P < .02]). In six out ofsix stocked enclosures,Cladophora turfs werereducedto low,prostratemats only 1-2 cm high,with a webbed, knotted appearance characteristic infestation algal-weavof by

1680
TABLE

MARY E. POWER

Ecology,Vol. 73, No. 5 6), and open sites

2. Results of Kruskal-Wallistestsfordifferences among fishenclosures(n = 6), fishexclosures(n (n = 3). Kruskal-Wallis Variable Algae Chironomids Odonates Megalopterans Total mayflies Large mayflies Large mayflies Chironomids Plecopterans Megalopterans Total mayflies Large mayflies
*

Units (damp mass/cm2) (individuals/cm2) (individuals/cm2) (individuals/cm2) (individuals/cm2) (individuals/cm2) (individuals/cm2) (individuals/cm2) (individuals/cm2) (individuals/cm2) (individuals/cm2) (individuals/cm2)

Date Algal turfs 16 July 16 July 16 July 16 July 16 July 16 July 22 June Gravel 24 24 24 24 24 July July July July July

H 8.23 8.64 8.01 5.25 6.23 1.79 9.68* 4.86 5.17 2.11 2.16 1.79

P .016 .013 .018 .072 .044 .409 .008* .088 .075 .348 .339 .409

Results graphed Fig. 3 Fig. 4a Fig. 4c Fig. 4d Fig. 4e Fig. 4f Fig. 4f Fig. 4g Fig. 4h Fig. 4j Fig. 4k Fig. 41

occurredin planned comparisons of densities in samples taken at the end of the experiment. ing midges (Power 1990a). In six out of six unstocked exclosures. (ladophora remained erect and became heavily overgrown with diatoms and cyanobacteria (Nostoc sp.). In exclosures, large amounts of Nostoc sloughed off of (ladophora and floated to the water

differences 22 June.Large mayflies on were the onlysampled taxon to show significant differences 22 June;all othersignificant

From an unplanned, a posterioricomparison (Dunn's procedure)of large-mayfly densitiesat the experimentmidpoint,

Attached Algae (mostly Cladophora)

5000

j
E
0'

4000 -a30002000----

.-

- nofish 0---- open

fish

CZ)

5 Jun

22 June

16 July

FIG. 3. Changes in algal standingcrops over the course of the experimentin enclosures,enclosures,and the open river. Points are averages + 1 SE of six means per cage treatment, six means fromopen wateron 22 Juneand threemeans from open water on 5 June and 7 July(each mean is computed fromthreesubsamples per cage or open riversite).

surfaceor sank to the bed. Almost no Nostoc was produced in stocked enclosures (Power 1990a). Pseudochironornus Midge densities (predominantly richardsoni)increased markedlyin enclosures,exclosures, and in the open river from5 to 22 June. Subdensitiesof chironomidlarvae decreased in sequently, all habitats, but by 16 Julywere 10 times higherin enclosures than enclosures (Fig. 4a, Table 2; Dunn's differmultiple comparison test indicated significant ences between enclosures and enclosures [P < .02]). enclosureswereassociated Chironomiddeclines in fish withloss of algal habitat.Densities of chironomidsper unit biomass of algae remained nearlyconstantin enclosures from22 June to 16 July,but dropped in fish exclosures and the open river(Fig. 4b). and densitiesin enclosures Reductionsofchironomid the open rivercoincided with increases in densitiesof from invertebrates fish (Power 1990a) and predatory fry 22 Juneto 16 July.More odonates (Fig. 4c) (primarily larvae (Fig. nymphs)and megalopteran lestiddamselfly 4d) were collected fromcores in fishenclosures than in enclosures or the open river(Power 1990a). By 16 different July, odonate densities were significantly and megalopterandensities were among treatments, which nearlyso (Table 2). Fryofroach and stickleback, by earlyJulyhad appeared in the open river,recruited to enclosuresbut not to enclosures (Power 1990a). Densities of large (head capsule width >0.5 mm)

(indiboulder-bedrockand gravel substrates:(a) chironomids in turfs FIG. 4. Densities of insect larvae in turf-covered viduals per unit area): (b) chironomids in turfs(individuals per unit algal biomass); (c) odonates (mostly lestid damselfly in nymphs) in turf;(d) megalopterans(mostly Sialis sp.) in turf;(e) total ephemeropterans turf:(Q large (head width >0.5 in mm) ephemeropterans turf;(g) chironomidsin gravel; (h) plecopteransin gravel; (i) odonates in gravel; (j) megalopterans in in (mostlySialis sp.) in gravel; (k) total ephemeropterans gravel; (1) large(head width >0.5 mm) ephemeropterans gravel. in Bars are ? 1 SE. Note differences scale on the y axes.

October 1992

SPATIALLY VARYING TROPHIC CONTROL BY FISH

1681

Turf Biota
120000-

Gravel
10000 8000 80 6000 --

Biota

E 100000-E
S >
C:

Chironomids

Chironomids
fish no fish
-

80000600004000020000 20000
*/'/ Xu

Vo > >

4000 2000

-- -

open

0
60 2)

4
5 Jun 22 Jun 16 Jul

Chironomids
E

1000 750 -

5 Jun

22 Jun

24 Jul

Pegaoptera

5000 403500

500 2

>
0 300

~~~~~~~~~v2505 Jun 22 Jun 16 Jul 0 5 Jun 2500 22 Jun 24 Jul

C\1 C
E

200ate

Odonaes

E
0i -0

2000 1500 1000

Odonates

Ci) V001

~~~~~~~~~~~e-~
0

>100

~~~~~~~~~
22 Jun 16 Jul

>

~~5QQ

5 Jun

5 Jun

22 Jun

24 Jul

-~~~~
20 100/25

200

Meaopea1j ~~~~E
>ag

~~~~~~~~~~~750-

4
/~~~~

Megaloptera

peeotr

500
00

5-0

5 Jun

22 Jun

16 Jul

0
3000-

250002000015000

5 Jun

22 Jun

24 Jul

e Total Ephemeroptera
I

kTotalEphemeroptera

~~~~~~~20001000
--

V 10000

V--

>

c 5000
0 15000*ln0 5 Jn

22 Jun

16 Jul
2500-

5 Jun

22 Jun

u u

-~~~~ 5000 *~~~~

> 5000

I f ~~~~~~CjLarge Ephemeroptera fLarge Ephemeroptera E 2000 50 100001c

-, / / 50 ~~~~~~~~~~~~~~~~~~~~~00
1000>~~~~~~~~C 00 V~~~~~~>

1682
TABLE

MARY E. POWER 3.

Ecology, Vol. 73, No. 5

Estimated dry biomass (mg/cm2) algae and arthropodssampled in gravel and turfs boulders and bedrock. of on Fish Boulders Gravel No fish Boulders Gravel Boulders 5 June 1989 (onset of experiment) 25.77 0.211 0.118 0.063 0.392 0.000 0.002 0.000 0.002 0.200 0.061 0.010 0.271 0.100 0.125 0.0004 0.225 0.74-1.48 1.20 23.90 0.498 0.141 0.083 0.722 0.000 0.015 0.0004 0.015 29.08 46.88 0.090 0.032 0.008 0.130 0.200 0.002 0.001 0.203 1.54-3.08 0.64 26.90 0.738 0.046 0.117 0.901 0.000 0.009 0.000 0.009 29.86 100.11 0.112 0.017 0.004 0.113 0.000 0.021 0.001 0.022 1.77-3.54 6.04 Open Gravel

Primaryproducers Algae Primary(1P) consumers Mavflies Caddisflies Midges Total Secondary (20) consumers Odonates Plecopterans Megalopterans Total

Resource/consumer ratios Algae/I cons. 73.39 1?/'?cons. 196.00 Primaryproducers Algae Primary(1?) consumers Mayflies Caddisflies Midges Total Secondary (2?) consumers Odonates Plecopterans Megalopterans Total

22 June 1989 (midway through experiments) 12.02 0.460 0.046 0.340 0.432 0.0051 0.003 0.0002 0.052 0.173 0.013 0.010 0.196 0.055 0.009 0.011 0.075 1.02-2.04 2.61 11.20 0.371 0.010 0.420 0.801 0.051 0.002 0.000 0.053 14.00 15.71 0.153 0.023 0.010 0.186 0.064 0.013 0.009 0.086 1.08-2.15 2.16 14.91 1.394 0.065 0.420 1.879 0.008 0.0004 0.003 0.011 7.94 170.81 0.100 0.052 0.004 0.156 0.073 0.019 0.010 0.104 1.28-2.56 1.50

Resource/consumer ratios Algae/IOcons. 27.82 10/2'cons. 8.31 Primaryproducers Algae Primasy (I1?) consumers Mavflies Amphipods Caddisflies Midges Total Secondary (20) consumers Odonates Stoneflies Alderflies Total

16 July 1989 (end of experiment) 3.03 0.023 0.004 0.020 0.096 0.143 0.072 0.000 0.007 0.079 0.20-0.40 0.033 0.000 0.001 0.005 0.039 0.200 0.003 0.044 0.247 5.13-10.26 0.16 17.59 0.062 0.014 0.049 0.010 0.135 0.597 0.000 0.029 0.626 130.30 0.22 0.20-0.40 0.040 0.000 0.003 0.009 0.052 0.000 0.000 0.027 0.027 3.85-7.69 1.93 8.83 0.199 0.035 0.093 0.033 0.360 0.000 0.000 0.004 0.004 24.53 90.00 0.20-0.40 0.089 0.000 0.030 0.003 0.122 0.100 0.009 0.007 0.116 1.64-3.28 1.052

Resource/consumer ratios Icons. 21.18 Algae/l cons. 1.81 11?20

mayflies increasedfrom5 to 22 Junein fish enclosures (Fig. 4f) and were significantly higherthan in enclosures on that date (Table 2, Dunn's multiplecomparison test indicated significant differences between enclosures and enclosures [P < .01]). Subequently, mayflies decreased in all cages and the open river(Fig. 4e, f). Decreases of mayfliesin turf-covered boulders

of enclosurescoincided withthe buildup of predatory in invertebrates these cages. These results, and resultsfromseparateexperiments can showing that small predatoryinsectsand fishfry cause fourfoldreductions in the numbers of midges colonizing C(ladophora (Power 1990a), indicate that roach and steelhead, by suppressingsmall predators,

October 1992
1200 C\jE

SPATIALLY VARYING TROPHIC CONTROL BY FISH

1683

E
-

1000 80 l|Fish

No fish

800600

400200(n, T U , X E c 0) Ci) E co- P

oC) 00

Z>0oN~~c3-~,<

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c

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C 01)

's

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CZ

ci

areas aspirated on threecobbles FIG. 5. Taxonomic composition and abundance of algae in samples collected fromI1-cm2 fromeach cage. Bars are means with 1 SE of averages fromsix enclosuresand six exciosures. Generic names on the x axis and (Aphanochacteto ,4nkistrodesmus), diatoms (Epiare sequentiallycyanobacteria(Nostoc to Schizothrix),chiorophytes to themnia 4mphipleura); "bgs" =blue-green algae (cyanophytes); "ig" =large ( >20 ,um diameter); "g" =green algae (chlorophytes);"sml" =Usmall (<20 gm diameter).

release algivorouschironomids,whichin turnsuppress algae. During the biologicallyactive summer season, 96-98% of the plant biomass and 70-84% of the arthropod primaryconsumer biomass in pools of the on South Fork Eel were associated withturfs boulderbedrock substrates(Table 3). Because pools comprise 60-80% of the wettedriverarea duringsummer,these at the food chain dynamicsinfluence rivercommunity large. Impacts of fishfeedingon gravel hiota of cascading effects fishon In contrastto the strong, and algal turfsof boulders and bedthe invertebrate on rock, few fisheffects the biota of gravel were apparent. Algal standingcrops on gravel particles were scant,and theirtaxonomic compositions were similar in stocked and unstockedenclosuresat the end of the experiment(Fig. 5). Of all taxa examined, only differences in Nostoc between treatmentsapproached significance(P = .003 froma t test,NS at the criticallevel for criterion the of.002 computed fromthe Bonferroni 26 taxa compared). Nostoc on gravel in fishenclosures was probably sloughed fromthe copious Nostoc that on overgrewCladophora turfs boulders in the absence of fish(Power 1990a). Most of the "epilithic" diatom cells counted had a senescent or empty appearance, suggestingthat they were also detrital outfall from healthierassemblages of the same taxa foundgrowing on epiphytically Cladophora (J. Marks,personal comm1utn1icatiOni).

nificant treatment effects(Fig. 4g), although there were significantly more chironomid tubes (occupied and empty) on the top surfaces of stones collected from enclosures than from enclosures (P = .02, Mann-Whit-

ney U, Fig. 6). (These resultsare unchangedwhen tube counts are normalized forthe surfacearea of stones.) Densities of chironomidtubes on stone surfacesmay in have been higher enclosuresbecause fishsuppressed foraging heptageniidmayflies.More mayflieswere by counted on top surfacesof stones in enclosuresthan in enclosures during three daytime censuses (P = .02, Mann-WhitneyU, Fig. 7a). When entirestones were and othnetted,however,the numbersof heptageniids er large, mobile insects clingingto stone surfacesdid not differ betweenenclosuresand enclosures(Fig. 7b).

Chironomid 15 ci)
C 0

Tubes

on Stones

10. al)

X5

oXXX

Fish
FIG. 6.

No Fish

showed no siginvertebrates Mayfliesand predatory in nificant differences abundance in gravel cores sampled from enclosures and enclosures throughoutthe (Fig. 4h-1,Table 2). Similarly,densitiesof experiment chironomidlarvae in gravel cores also showed no sig-

Numbers of chironomidtubes counted on stones 32-64 mm median diameter collected fromenclosures and exciosures. Bars are means (with I SE) Of Six averages per of treatment counts fromthreestones per cage. Stones were at collectedsystematically evenlyspaced, predetermined points along longitudinaltransects.

1684

MARY E. POWER

Ecology, Vol. 73, No. 5

1.2
0

.5

0 )

0.8

0.8-

000

Fish
4.-

No Fish

._~~~~1 CZ4 D O
00 0 CZ 2

Sw

El Stocked

S S S /S -j w 0Unstocked

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7-C

FIG. 7. (a) Number of mayflies (mostly heptagenjids) sightedon stones on the beds of enclosures and exclosures. of Bars are means (with I SE) Of Six averages per treatment counts on 32-34 stones per pen. Observations were made on every other stone >28 mm median diameter that lay along a longitudinaltransectfromthe downstreamto the upstream end of each pen. (b) Numbers of individuals clingingto cobbles (64-128 mm median diameter) netted fromenclosures and exelosures. Bars show means with I SE forthe taxa capcobbles:"Hept" =heptageniidmayflies-, turedon netted "Siph" "Baet" =baetid mayflies;"Ephem" =siphlonuridmayflies-, "Plec" =plecopterans, "Lepid"= =ephemerellidmayflies-, and Lepidostoma (caddisfly)-, "Coena" =coenagrionid dam-

hiotnassin graw'cand /cewl 7Trophic

on tw.-fi b)ouddersin rit'erpoolS

Dry biomass of attached algal turfsdecreased in various treatments from ;25 mg/cm2 at the onset of exat the end of the periments on 5 June to 3-18 f epiexperiment in md -July (Table 3). The bio a lithic algae on gravels in enclosures, exelosures, and open sites in pools appeared similar and very scant throughout the 6-wk experiment, but was only sampled at the endpoint in mid-July, when standing crops (dry masses) were estimated from cell counts to range from 0.17-0.36 mg/cm2 . Algal standing crops were, in midJuly, one to two orders of magnitude greater on boulder-bedrock substrates than on pool gravel. Epibenthic primary consumers associated with algal turfs on boulders (mayflies, caddisflies, chironomids,

amphipods) had a collectivebiomass estimatedat 0.4and at 0. 10.9 mg/cm2 at the onset of the experiment, at 0.4 mg/cm2 theend. The collectivebiomass of these in algivore-detritivores gravel was estimated at 0.10.04and from 0.3 mg/Cm2at theonsetofexperiments, at 0. 1 mg/cm2 the end. Primaryconsumer biomass, was 4 times higheron averaged across all treatments, turf-covered bouldersthanin pool gravelin earlyJune, 6.5 times higherin late June, and 3 times higherby mid-July (Table 3). and Epibenthiccarnivores(odonates, megalopterans, plecopterans) had a collective biomass estimated at in on 0.002-0.015 mg/cm2 turfs boulders in earlyJune (Table 3). In gravel,this guild had a higherestimated composed oflarge biomass (0.02-0.23 mg/cm2),largely nymphs,which did not occur in turfs.In dragonfly consumer biomass, collectivebiocontrastto primary was estimated to be mass of predatoryinvertebrates 17 times higher in gravel than on boulders in early biomass was invertebrate June.By late June,predatory this onlytwiceas highin gravels.By mid-July, biomass distributionwas reversed. Averaged across all treatments, predatoryinvertebratebiomass was twice as boulders as in gravel,due to the high on turf-covered exclosures(Table withinfish increaseofthesepredators 3). Resource: consumer biomass ratios were generally higher for boulder-bedrock than for gravel-dwelling consumers might that turf-dwelling biota, suggesting be less food limited. In earlyJune,ratios of algal bioconsumerswere30-65 forturfmass to thatof primary covered boulders,and 0.6-3.2 forgravelbiota (assuming similar algal standing crops in gravels to those (Table 3). By the end of the estimated for mid-July) these ratios ranged from2 1-130 forturfexperiment, dwellingorganisms,and from 1.4-9.2 forbiota associated withgravel. Over the course of the experiment, these resource: consumer ratios were 1-2 orders of in thanin gravels.In earlyJune, magnitudehigher turfs ratios of primaryconsumers to epibenthiccarnivores ranged from46-196 forturffauna, and from 1-5 for these ratios ranged from gravel fauna. By mid-July, 0.2-1.8 for turffauna and 0.2-1.9 for gravel fauna (Table 3). of The proportion the biota in riverpools associated on withgravel vs. tufts boulders and bedrock was esstanding crops in open pool timated by multiplying sites by the proportionof pool area occupied by these substrates.These computations suggestthat in June, conprimary 98% of the algal, 84% of the invertebrate carnivore primary sumer,and 24% of the invertebrate on biomass was associated withturfs boulders.By midtheseestimateswere96, 70, and 3%, respectively. July,
DISCUSSION

on effects fishwerestrong boulder-bedof Predatory rock substratesand weak in gravel substratesin pools of the South Fork Eel. These results parallel results

October 1992

SPATIALLY VARYING TROPHIC CONTROL BY FISH

1685

frommarine benthic systems,in which the effects of epibenthicpredatorsdocumented forrockyintertidal and unvegetatedsoft-sediment habitats are not conspicuous in seagrassbeds (Peterson1979, Wilson 1991). Spatial variationin predatorimpactscan lead to spatial variationin thenumberoffunctionally significant (sensu Frctwell 1977) trophiclevels in benthicfood webs, even withoutloss of species fromtop trophic levels. In boulder-bedrockmicrohabitatsof the South Fork Eel, fishwere functionally significant fourth-level as consumers in a food chain. By suppressingpredatory invertebrates and fishfry, fishreleased algivorouschironomids. which in turn lowered standing crops of attached algae. As predictedby food chain dynamics theory(Hairston et al. 1960, Fretwell1977, 1987, Oksanen et al. 1981), standingcrops of algae on boulders and bedrock were lower in fishenclosures with four trophiclevels than in fishenclosureswiththreetrophic levels (Power 1990a). Fish also fed on gravel substratesimmediatelyadjacent to boulder-bedrockformations, theyhad no but detectableeffects thereon invertebrate algal standing or crops. Differences betweenboulder-bedrockand gravel withrespectto isolation,cover,seasonal disturbance, productivity, and local prey characteristics may conof tributeto shiftsin the functionalsignificance fish between the two microhabitats. IIa!itat isolation and (age effects Predator impacts on prey in patches, or cages, depend on rates of prey depletion relative to prey immigration rates (e.g., Holt 1984, T. Oksanen 1990, Cooper et al. 1990). In pools of the South Fork Eel, boulders and bedrock emerge as habitat islands from thegravel bed. In addition,turf-dwelling invertebrates in riversare oftenweak swimmers(Hynes 1970), and, in lentic pools, would not be passively dispersed by flow.Therefore, biota to immigration turf-dwelling by buildersin enclosuresmight less likely offset be to losses to fishpredationthan immigration gravel-dwelling by biota fromadjacent gravel outside cages. Features of cages that impede migrationof stream insects,such as small-mesh walls or solid floors,can of effects enclosed predators artificially exaggerate (Frid and James 1988, Cooper et al. 1990, Wilson 1991). Cooper et al. (1990) foundthatstudiesusingcages with 3-mm mesh were more likelyto detectsignificant fish effects invertebrates on than studies with cages with 6-mm mesh. During the summer period of roach and in sticklebackrecruitment the South Fork Eel, 6-mm mesh walls would have permittedpassage of fishthat within a few weeks would have been capable of attackinglargerinsects(head capsule width >0.5 mm). This would also preventdetectionof fisheffects among In treatments. turfs boulders,densitiesof large inon sect taxa such as damselflynymphs increased in exthattheseinsectswerenot impeded closures,indicating by 3-mm mesh walls, eitherbecause theycould cross

them,or because subgravelor aerial dispersalpathways (Williams and Hynes 1976) were available to them. Cages also preventfishfrommoving among sites to feed,and can increasetheirfeeding impacts,even when the densities and per capita feedingrates of enclosed fishare withinthe rangeobserved forfree-ranging fish in similar microhabitats (Butler 1989). Inferences can be drawn about the importanceof these effects the in South Fork Eel fromobservations of insect and algal densities in enclosures and enclosurescompared with densities in open sites. At the end of the experiment, algal standingcrops sampled in open sites were intermediate betweenstandingcrops sampled in enclosures and enclosures(Fig. 3). The densities of chironomids were similar in open sites and enclosures,and significantlyhigherin enclosures;thesedifferences were particularly apparent when chironomid densities were normalized foralgal standingcrops, which betterreflectshabitatavailable forthese small organismsthan planar area (Fig. 4a, b). In contrast,the densities of predatory odonates and megalopterans sampled in open sites were more similar to densities in fishenclosures than in enclosures(Fig. 4d, e). The second resultsuggests that invertebrate predatorscan be depressed to similar densitiesby fishpredationat ambient and enclosed (and possiblyelevated) levels. Why,then,were chironomid densities so low in open sites, given the low measured densities of invertebrate predators?A likely explanation is that additional small predators, in particularfishfry, which could not be sampled with cores, also preyedon midges in open habitats(Power 1990a). In addition,densitiesofboth midgesand predatory invertebratesin the study reach at large were probablynot accuratelyestimatedby the limitednumber of samples collected fromopen sites in the vicinity of the pens. Larger scale transectsurveysand visual reconnaissance have shown that duringyears of algal blooms, Cladophora in the main channel of the South Fork Eel becomes densely infestedwith tuft-weaving midges,and that these infestations precede the alga's decline (Power 1990a, h). If levels of fishpredation were elevated in enclosures relative to open-channel habitats, their impacts on midges and algae may be accelerated. Nevertheless,these experimentalresults support the hypothesisthat fishpredation on small, intermediatepredatorsbringsabout the eventual infestationof macroalgae by midges in the open river channel. PhBsical refuges frompredation A second explanationforthefailureto detectsimilar fisheffects gravel biota is that refuges on provided by interstitial spaces in gravelsgreatly reduce foraging efof ficiency fish (Coleman and Hynes 1970, Hynes 1970, Williams and Hynes 1974, Brusven and Rose 1981, Hemphill and Cooper 1984, Minshall 1984, Williams 1984, but see Reice 1983, Flecker and Allan 1984). Cover provided by real or simulatedmacrophytes also

1686

MARY E. POWER

Ecology, Vol. 73, No. 5

in reduced predationby fishon invertebrates soft-bothabitats(Crowder and Cootomed littoralfreshwater per 1982, Savino and Stein 1982, Gilinsky 1984, Hershey 1985) and marine habitats(Reise 1977, Peterson 1982, Virnsteinet al. 1983, Robertson 1984, Summersonand Peterson1984, Wilson 1991). In theSouth Fork Eel, however, invertebratesin macroalgae on boulders,except foralgae-weavingmidge larvae, were in moredepletedby fish thanwereinvertebrates gravel. Differential prey vzlnerahilitv frommacroalgae by tuft-weavRetreatsconstructed ing midgesdefendthem fromfishbut not invertebrate predators. In field and laboratory feedingtrials, we have found that silk-reinforced algal tuftsafford chironomidlarvae apparently against completeprotection fish,but not against predatoryinvertebrates (lestids, aeshnids, and naucorids) (Power et al. 1992). Despite theirheavy consumption of algivorous mayflies(Fig. 2), fish had negativeindirect of effects algae on boulders because their predation on small predators released tuft-weaving midges, a key herbivore guild (Power 1990a). Many temperate freshwater fishes,like roach and steelhead in the South Fork Eel, feedopportunistically at several trophiclevels (Vadas 1990). Feedingimpacts of potentially omnivorous fish are, however, constrainedby the size, morphology, behavior of their or prey(Drenneret al. 1978, Werneret al. 1983, Osenberg and Mittelbach 1989). In a southern Californiastream, troutsuppressed large,mobile invertebrate predators, whilemorecryptic, gravel-dwelling insectsshowed tendencies to increase in the presenceof trout(Hemphill and Cooper 1984, Cooper 1988). Several otherstudies in freshwater ponds have shown thatfishpredationon larger,more conspicuous, or more active taxa such as odonates (Crowder and Cooper 1982, Menzie 1978 cited in Gilinsky 1984) and predatorychironomids increasedpop(Cuker 1981, Gilinsky 1984) indirectly ulations of herbivorouschironomids. Fish effects may not have been detected in gravel in microhabitats the South Fork Eel because preythere were vulnerable to both top and intermediatepredain and tors,so thatinvertebrates fishfry enclosureshad impacts similar to those of fish in enclosures. This hypothesisis supportedby the increase of large mayfliesin enclosuresfrom5 Juneto 22 June,followedby theirsubsequentdecline in enclosuresin mid-July after odonate and megalopterandensitieshad built up (Fig. 4f). Disturbance,productivity, the energy and
I1aSC of/gravel vs. boulder wnicrohabitats

Lakes Cladophora recoveringfrom ice scour (Blum 1982). Cladophora in the South Fork Eel proliferates in the springon boulder and bedrock substrates,but not on more severelyscoured gravels (Power 1990a, c). As Cladophora proliferates, do highlynutritious so diatoms that grow epiphytically the macroalga. In on contrast, darker,stagnant, the siltygravelbeds of pools supportlow standingcrops of algae and invertebrates (Fig. 4, Table 3), suggesting that gravel beds of pools are more seasonallydisturbedand less productivethan largersubstrates. Diatoms sampled fromthe gravel bed appeared senescentor empty,and may have been derived in large part fromepiphytes(with which theyoverlapped taxboulders (J. onomically) sloughed from turf-covered Other indirecteviMarks, personal comnmnunication). on dence thatdiatoms were not activelygrowing pool gravels came from their lack of response to mayfly activity.Although behavioral depression of mayflies by fishmay have promoted the persistenceof chironomid tubeson top surfaces cobbles in fish of exclosures, on therewas no corresponding effect epilithicdiatoms, which were equally abundant in enclosuresand exclosures. Also, despite their diurnal avoidance of stone
surfaces, mayflies in enclosure gravel were as abundant

that they could as mayfliesin exclosures, suggesting feed on detritusthat infiltrated gravel interstices.If detriprimaryconsumers fed primarily infiltrating on where tus, theycould remain withingravel interstices crops theywould be less available to fish.Low standing of prey,coupled withthe lower per capita availability of prey near or in interstitial refuges,may have depressed foraging profitability gravel substratesfor of fishbelow the thresholdrequired for fishto impose significantimpacts, as predicted by Fretwell (1977, 1987) and Oksanen et al. (1981). Changes in trophiccontroloi'er sinall spatial scales This studyand others(Power 1984, 1987, Power et al. 1989, Schlosser and Ebel 1989, Peckarskyet al. 1990) demonstrateabrupt change over small spatial scales (centimetres)in the functionalimportance of and microhabpredatorsin rivers.Preycharacteristics itat isolation,cover, disturbance,and productivity remain to be investigated factorsthatseparatelyor in as of combinationaltercontrolbypredators lowertrophic levels in the Eel River. Shiftsin impacts of predators over small spatial scales provide opportunities study to the constraintsplaced on predatorsby theirhabitats. We need to know more about these constraintsif we will are to predictwhereand whentrophicinteractions be strong(Menge and Sutherland 1976, Paine 1980, Hansson 1989, Menge and Olson 1990).

(ladophora, the dominant macroalga in northern Californiarivers,is scoured fromall substrates winby ACKNOWLEDGMENTS ter floods. Spring regrowthappears to be vegetative I thankS. Kupferberg, Marks, J. Nielsen, and B. Rainey J. frombasal pads, as has been documented for Great forhelp in the fieldand the laboratory, Kotanen, W. Sousa, P.

October 1992

SPATIALLY VARYING TROPHIC CONTROL BY FISH

1687

and an anonymousreviewerforstatistical advice, and B. Dietrich,T. Dudley, P. Kotanen, L. Oksanen, W. Sousa, and T. Wootton forvaluable comments on the paper.
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