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Transactions of the American Fisheries Society, 1982, vol. 111, iss. 3, pp. 255-266. http://afs.allenpress.com http://afs.allenpress.com/archive/1548-8659/111/3/pdf/i1548-8659-111-3-255.

pdf Online ISSN: 1548-8659 Print ISSN: 0002-8487 DOI: 10.1577/1548-8659(1982)111<255:PIBLBA>2.0.CO;2 American Fisheries Society

TRANSACTIONS
AMERICAN

of the
May 1982
VOLUME 111 3 NUMBER

FISHERIES SOCIETY
Transactions of the American Fisheries Society 111:255-266,1982 Copyright by the American Fisheries Society 1982

Predator-Prey Interaction betweenLargemouthBass and Bluegills as Influenced by Simulated, Submersed Vegetation


JACQUELINE F. SAVINO
OhioCooperative Fishery Research Unit
RoY A. STEIN

Department of Zoolo TheOhioStateUniversity, Columbus, Ohio43210


Abstract

Datafromtheliterature suggest thatpredatory success declines ashabitat complexity increases. To explainthis phenomenon, we studiedthe predator-prey interaction between largemouth

bass Micropterus salmoides andbluegills Lepomis macrochirus in four laboratory pools (2.4-3.0m
diameter,0.7 m deep),eachwith a different density (0, 50, 250, 1,000stems/m e) of artificial plantstems. Behavior was quantified for bothpredator andpreyduringlargemouth bass feeding bouts lasting 60 minutes. Predation success (number of captures) by largemouth bass was similar at 0 and 50 stems/m 2, thendeclined to near zeroat 250 and 1,000stems/m 2. As stemdensity increased, predatoractivity declined due to a decrease in behaviors associated withvisual contact with prey.Reduced predation success by largemouth bass in habitats of increased complexity apparently is relatedto increases in visual barriers provided by plantstems aswellasto adaptive
changes in bluegillbehavior.

Littoral zones,with their associated vegetation, are importantareasof fishproduction in north temperate aquatic communities. In particular, theseareasprovidehabitatfor many fishes, including members of thesunfish family,
Centrarchidae (DiCostanzo 1957; Hall and Werner 1977; Werner et al. 1977; Keast 1977,

pomis macrochirus shouldmove out of the vegetated littoralzoneinto open waterand feed on Daphniaduring much of the summer.Because

bluegills smallerthan 100 mm total lengthdo not move offshore as predicted, Mittelbach
(1981) suggested that fish of this sizeremain in

the vegetationto avoid predation by large1978; Laughlinand Werner 1980). mouth bass Micropterus salmoides. This is a reaJuvenile sunfishes mightlivein vegetation for sonable hypothesis because a varietyof studies at leasttwo reasons: availability of forage or suggest that prey vulnerability decreases asenavoidance of predators. Basedon relativehab- vironmental complexity increases (Huffaker itat profitabilities measured in a naturallakeand 1958; Glass1971; Steinand Magnuson 1976; optimal-foragingconsiderations, Mittelbach Saiki and Tash 1979). However, no one has (1981) predictedthat all sizesof bluegillsLe- demonstrated explicitly that vegetation reduces vulnerability of bluegills. To test this assumption, we completed a series of experiments that betweenpredation The Unit isjointlysponsored by theUnitedStates quantifiedthe relationship Fishand Wildlife Service, Ohio Departmentof Nat- mortalityand vegetation density, usinglargeural Resources, and The Ohio StateUniversity. mouthbass as predators and bluegills as prey.
255

256

SAVINO AND STEIN

If vulnerabilityof bluegillsdeclineswith in-

remained flexible, allowing largemouth bass

creasing structural complexity, selection of this habitatby bluegills, even in the face of poor foragingreturn, couldbe explainedon the basisof highersurvival in vegetation than in open
water.

freedom of movement through thepool. Each


poolcontained a differentdensity of theserope
strands(0, 50, 250, 1,000 stems/m2), hereafter

referred toaszerol low, medium, andhigh stem

density.Inter-stemdistances were about 14, 6, A variety of mechanisms might be involved and 3 cm for low, medium,and high stemdenThese densities were chosen in reducing prey vulnerability in complex hab- sity, respectively. itats. For example, vulnerability could be re- to reflect the range of macrophyte densities ducedin vegetation simplybecause randomvi- found in natural communities (Ozimek et al. sualencounters between predatorand prey are 1976; Sheldonand Boylen1977;Crowderand to estimate reduced (Cooperand Crowder 1979). Alter- Cooper1979).To permit observers in the pools, we laid colored stones 0.3 natively, behavioral responses of thepreyto the distances were predatorcouldalter the probability of prey de- m aparton the sandbottom.Experiments tection and capture. And certainly,predator run only in the morning to eliminatetime-ofbehaviorcould be modifiedby vegetation. To day effects. distinguish amongthesecompeting hypotheses Largemouth bassused in our experiments in our experiments, we quantifiedthe behav- were collectedfrom RossLake, RossCounty, ioral interactions betweenlargemouthbass and Ohio,aridrangedfrom 33 to 37 cmtotallength. bass wereused,one inbluegillswith increasing stem density.If the In all, five largemouth usedranged random modelexplains our results, then these dividualper experiment.Bluegills data could be generalizedto many predator- from 35 to 44 mm total length and were obprey interactions in the vegetation. However, tained from localpondsand Hebron National if prey vulnerability is strongly influenced by Fish Hatchery, Ohio. Bluegillsof this sizecombehavioralinteractions, then our resultsmay be monly are found within the littoral vegetation

specific to thisparticular predator-prey system. of natural lakes (Hall and Werner 1977; Mittelbach 1981), and thus should be most affected
Methods

We conducted1-hour observational experiments in a shaded outdoor area during two summers. Four circular,plasticpools(3 m diameter,0.7 m deep)with dark insidewallswere usedthe firstyear,whereas circular,steelpools (2.4 m diameter,0.7 m deep)with whiteinside walls, whichfacilitated viewing of fish,wereused Search:moving,but not orientingto the prey. during the secondyear. Water temperatures Follow: moving, and orienting to particular

by changes in stemdensity. Largemouth bass and bluegillbehaviorcategorieswere determinedfrom preliminaryobservations.Largemouth bassbehaviorswere separated into six mutually exclusive categories:

rangedfrom 16 to 24 C during the study,but fluctuated only2 C duringany24-hourperiod. Between experiments, water was circulated through a sand-floss filter to improve water clarityand maintaindissolved oxygenconcentrations at about7 mg/liter.Algalblooms were controlled by an algicide(containing monuron, simazine, and atrazine)appliedtwiceper summer.

prey.

Pursue:followingat burstspeed. Attack: strikingat prey. Capture:ingesting prey. Inactive:restingand motionless. Bluegillbehaviorand position in experimental poolswascategorized as follows:
Behavior

individualsaggregated and moving Lengths of yellowpolypropylene rope (4 mm Schooled: about as a unit. diameter,0.5 m long) simulated natural plant strongly stems.Periphyton coveredtheserope strands Dispersed:individualsnot associating after a few weeks,causingthem to resemble with one another.

aquatic macrophytes. Ropeends werefastened,


in a uniform distribution, to wire mesh that was Position
floated to the water surface. Attached

covered withsandon the poolbottom;free ends Top edge: upper 0.25 m of the water column strands and within 0.3 m of the pool side.

PREDATOR--PREY INTERACTIONSALTEREDBY COVER

257

Bottomedge: lower0.25m of thewatercolumn and within 0.3 m of the pool side. Top center:upper 0.25 m of the watercolumn and beyond0.3 m from the pool side.
Bottom center: lower 0.25 m of the water col-

gillswereremoved and counted. Modifications in bluegillbehavioracross stemdensitycould be influenced either by the presenceof the largemouth bass predatoror stemdensity itself.
To distinguish between these twoeffects, we also

quantifiedthe behaviorof bluegills without a predator at all stemdensities. of largemouthbass and bluegillbeExperiments generally consisted of observing Analysis of the different types feedingbehaviorof largemouth bass and anti- haviorsdiffered because predatorbehavior of bluegills in the four stem of data collected for each fish: that is, contindensities. In eachexperiment,one largemouth uous versus instantaneous observations. We basswas combinedwith 35 prey. Before any analyzed predatordataon the basis of number experiment, largemouth bass were acclimated of occurrences and time spentin eachactivity of the percentof to the experimental poolfor 2 to 7 days.Indi- and bluegilldata on the basis vidualswere considered acclimated when they individuals participating in each behavior at each fed regularlyin the presence of an observer. observation. Walshaverages were usedto calLargemouth bass werestarved for 24 hoursbe- culate medians and 95% confidence intervals for fore eachexperiment. Immediately beforetest- behaviors and positions (Hollanderand Wolfe ing, bluegills (previously untested) wereadded 1973). and isolated from the predatorby a smallwireTo providefor replication we testedat least meshcage(1 m diameter)for 5 minutes. When two differentlargemouth bass a totalof seven the cagewasremoved,experiments beganand timesat eachstemdensity. For bluegills, each continued for 60 minutes. At the end of 60 treatmentwasreplicatedat leastfive timeswith minutes, largemouth basseither were satiated a predatorand two timeswithouta predator. or had quit trying to captureprey.Observations About60%of the replicates for thelargemouth wererun in the first year; all replicates of weremadefrom 2-m-highladders placednext bass treatmentwere run in the secto the pools.The first year, only predatorbe- the low-density havior was recorded;the next year, a second ond year. Results obtainedin the 2 yearswere observer documented antipredator behavior of not significantly different (P > 0.05) nor were bluegills. Largemouth bass behaviors werecod- the three major behaviors amongindividual ed directlyinto a Datamyte900 (Electro/Gen- largemouth bass (two-way layout): eral Corporation,Minnetonka,Minnesota).An Behavior Years (P) Individuals (P) entrywasmadeeachtime the largemouth bass Captures(number) 0.11 0.26 exhibited a change in behavior. The Datamyte Activity (minutes) 0.28 0.82 records time of eachentry, therebyproviding Visual contact (minutes) 0.15 0.38 a record of time spent in each behaviorand somefish were used in experiments number of occurrences during each experi- Because ment. Bluegillbehaviorwasrecorded on coded more often than others, we tested each individdata sheets at 5-minuteintervals, providingin- ual against the others (combined asa group)to stantaneous observations of their behavior determineif any one of them might biasour no individuals twelvetimesduring eachexperiment.At each results.In thesecomparisons, weredifferentfrom the group(P > 0.05, observation,we recorded the percentageof tested bluegills either schooledor dispersedand in two-waylayout). Furthermore,we added data each of the four locations. At the same time, from preliminaryexperiments (in whichwe rebehaviors in a slightly differentfashion) distances between the largemouth bass and the corded bluegill closest to it were recorded. Behavior, to the group of final experimentsand again behavior of single fish with that of location, and initial distance from the predator compared of single fish wererecorded for bluegills attacked during ex- the group.Asbefore,thebehavior periments.From thesedata, we comparedbe- did notdiffer from that of the group(P > 0.05, layout).Thus, datafrom bothyears for havior of bluegills attacked with thosenot at- two-way tacked.After an experiment, largemouth bass individual largemouthbasswere lumped for and analysis. were permittedcontinuedaccess to the remain- presentation To relate our findingsto a more natural siting bluegills for 24 hours;after 24 hours,blueumn and beyond0.3 m from the pool side.

258

SAVINO AND STEIN

6O 4O
z

L 95% MEDIAN, CONFIDENCE INTERVAL A

6O

MEDIAN, 95% CONFIDENCE INTERVAL B


(7) (7)

(8)

(7)
z
--

20 0 6O 4O 20 0 20 0

20
0

(8) )
SEARCH= O 50

250

IOO0

L EL
Ld

60
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FOLLOW. 0 50 20

I000

m_ 20
co

P-

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FF

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0

PURSUE

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iooo

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CAPTURES AFTER 60 MINUTES: 0 50 250 IOO0

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AFFACK. 500
ATTACK'

250

Iooo

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20
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0 50 250

-r

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CAPTURE.

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0 50 250

, ,,[
IOO0

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ACTIVE.

0 50

250

IOO0

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2O
CAPTURES AFTER 24 HOURS o 50 25O iooo

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50

250

I000

I0

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I000

STEM DENSITY (NUMBER PER M+ 1)


FIGUr 1.(A) Number oftimes each ofseveral largemouth bass behaviors occurred with increasing stem density during an experiment. (B) Time spent in each behavior bylargemouth bass with increasing stem density during an experiment. Visual contact was the sum of time the predator spent motionless while observing bluegills, and following, pursuing,

attacking, and capturing bluegills. Medians not significantly different from each other are underlined (Kruskal-Wallis test, P > 0.05).Sample sizes (inparentheses) for each treatment for all behaviors aregiven in the top panel, except
where indicated differently.

uation,we compared the amountof coverpro- lated to the amount of visual isolation between and prey,percent cover should providedby polypropylene linewiththatprovided predhtor by a natural aquaticmacrophyte Potamogetonvide somemeasureof protectionavailableto natans, by quantifyingthe percentcoverpro- prey at any given stem density.To measure cover, we photographed from the side videdbyeach at the same stem density. Percent percent cover was defined as the percentvertical area a 0.5-m strip(extending12.5cm into an aquaror natural)at of the water column occupiedby vegetation ium) of eachstemtype (artificial densities. Photographs (artificialor natural). If refuge for prey is re- the three experimental

PREDATOR--PREY INTERACTIONS ALTERED BY COVER

259

(7)

100

95% CONFIDENCE INTERVAL

MEDIAN,

8o

6o

4o

2o
ATTACKS PER FOLLOW:
I000

50

250

o Ioo

8o

6o

CAPTURES PEr ATTACK: -T-

o 250 50
4o
I I I i II

I
I I II

I0

50

250

Iooo

STEM DENSITY (NUMBERPER M2 + 1)


FIGURE 2.-Percent ofattacks onbluegills per followand percent ofcaptures perattack in an experiment withlargemouth baas under conditions ofincreasing stem density. Number ofexperiments pertreatment isindicated inparentheses. Medians
notsignificantly different (KruskaI-Wallis test, P > O.05) from each other are underlined. No attacks were obseroed at highstem density.

then were digitized(Hewlett-Packard Digitizer, currences of the behaviors, declined as stem Model 9874) and percent coverwascalculated density increased (Fig. 1A). As thesebehaviors for eachstemdensity. decreased, so did the numberof bluegills captured by largemouthbass, during both 1-hour
Results

and 24-hourfeedingbouts. Consistent with the

Changesin stem densitymodified the pred- results of Glass (1971),increasing stemdensity atory tactics of largemouthbass.Predator be- reduced the predatory ability of largemouth havior,asmeasured by numberof occurrences bass. or time spent,did not change from zero to low Time spentin eachpredatorbehavior did not density, nor did it change from mediumto high reflect the number of its occurrences. Search (Fig. 1). However,nearly all predatorybehav- time remained constant whereas follow time iors declined significantlyas stem density in- decreased as stemdensity increased (Fig. lB).
creased from zero to medium or from low to

When active,largemouthbassspentmost of

high, suggesting that thesebehavioralpatterns their time searching and following.Pursuing, were modified between densities of 50 and 250 attacking, and capturing contributed little to

totalfeeding times at zeroandlowstem density. Participationby largemouthbassin preda- As thesebehaviorsdeclinedand approached tory behaviors, asmeasured by numberof oc- zero at mediumand high stemdensity, signif-

stems/m 2.

260

SAVINO AND STEIN

-
o o

100

MEDIAN, 95% CONFIDENCE INTERVAL


80
0

_
o
z

40
z0

I0

50

250

I000

STEM DENSITY(NUMBER PER M2 + 1)


FCURE 3.--Percent schooling of bluegills withand without a largemouth bass present, in relation to stem density. Significant differences (Kruskal-Wallis test, P < 0.05) between thepercentages of schooling withandwithout largemouth bass within a treatment aredesignated byan asterisk (*).

occurred between zero-low and begun,attacks led to captures about70% of the medium-high stem densities.Becauseswim- time in a total of 476 attacks.Even given this ming speedand metabolicrate are exponen- result,more attacks were requiredper capture tially related(Glass1971),the contribution of at low than at zerodensity. Numberof captures pursuit,attack,and capture(behaviors that in- were similar between these two densities; howvolvefastswimming) to costs of predation may ever,energyrequiredper capturewasprobably be substantial,even though these behaviors higher at low than at zero stemdensity. make up a small portion of the time budget. Bluegillbehavior wasmodifiedby both stem

icant differences

Time spent active by largemouth bassdecreased with increasing stemdensities; predatots did not appearto compensate for reduced captures by increased searching or following. Largemouthbasscould not capturebluegills at high stemdensity because theycouldnot find or followthemthroughtheartificial vegetation. Visual contact betweenpredatorand prey declined precipitously with increasing stemdensity(Fig. lB). Both the total numberof follows (Fig. 1A) and the percentof followsleadingto an attack(Fig. 2) decreased with increased stem dbnsity,therebydecreasing the possible number of attacks.However, the percent of captures resultingfrom an attackdid not change withstem density (Fig.2), a resultsupported by the work of Glass (1971).Thus, the abilityof a largemouth bassto follow and attack was instrumental in determining capturesuccess. Once

densityand the presence of largemouth bass. Generally, bluegill behaviorwas lessvariable when largemouthbasswere present. At each stemdensityexceptthe highest, the percentof fish schooling was similar, whether a predator waspresentor not (Table 1; Fig. 3). At high density, predator presencesignificantlyreducedthe percent of bluegills schooling. Of the bluegillsattackedby largemouthbassat zero,
low, and medium stem densities, few were

schooling (mean= 6.0%; Clopper-Pearson 95%


confidence interval = +_2.7%; N = 302; Hollander and Wolfe 1973). The ratio of attacks

on schooled to dispersed bluegillswas similar


across these three treatments (binomial test: P > 0.14; N = 302; Hollander and Wolfe 1973). Thus, because so few schools were attacked,

schooling wasadvantageous at thesedensities. Yet, at high stemdensity,no bluegills were at-

PREDATOR--PREY INTERACTIONS ALTERED BY COVER

261

T ^BI 1.--Null probabilities a of changes in behavior anddistribution of bluegills across stem densities withandwithout co-occurring largemouth bass. Plusandminus signs inparentheses indicate whether a behavior ofbluegill was enhanced (+) or depressed (-) asstem density increased. Probabilities arefrom distribution-free multiple comparisons based on Kruskal-Wallis ranksums (Hollander and Wolfe1973). Within-treatment comparisons canbe foundon the figures
referenced.
Plantdensities (stems per m2)
0 0 0 50 50 250

Bluegillbehavior
or distribution

Figure
reference

versus
50

versus
250

versus
1,000

versus
250

versus
1,000

versus
1,000

Schooling (%) With bass


Without bass

3
__b
--

__
--

*** (_)
--

*** (-)

*** (-)

Top edge(%)
With bass Without bass

4
*** (-) 0.22 (+) *** (+) -*** (+) ----

0.06 (-) -0.10 (-) 0.36 (+) *** (+)


--

-0.15 (-)

0.34 (+) ** (-) *** (-) *(+) *** (+)

** (+) -*** (-) -*** (+)

Bottomedge(%)
With bass Without bass

4
*** (+) --

Top center(%)
With bass
Without bass

4
---

Bottom center (%) With bass Without bass


Distanceto bass(m) Closestschooled School attacked

4 --5 * (+) * (+) 0.39 (+) -** (+)


-c

** (+) --

*** (+) 0.22 (-)

*** (+)

*** (+)

*** (+)

0.48 (+)
c

Closest dispersed Dispersed attacked


ap <. 0.05; ** 0.01; *** 0.001.

-0.49 (+)

-0.39 (+)

0.07 (-) c

*** (-)
e

*** (-)
e

All dashes designate P >0.5.


No attacks on bluegills by largemouth bass occurred at high stemdensity.

tacked and only schooling bluegillswere followed.Apparently,bluegills reducedtheir susceptibilityto the predator by dispersing among the stemsat high densityand schooling at low
densities.

slightpreferencefor attackingbluegills at the top edge(binomial test: P = 0.05;mean= 57%; N = 169).Giventhat sofew bluegills werefound at the top edge (Fig. 4) and about50% of the predatorattacks occurredthere, the probability
that an individual at the surface would be eaten

Bluegill distribution was also modified by stem densityand predators.In the absence of predators,bluegillsmoved throughoutthe pool, althoughtheyshowed someaffinityfor edges (Fig. 4). When a largemouthbass waspresent,bluegills stayednear pool edges(especially bottom edges),except at high densitywhen they dispersedthroughoutthe pool. Largemouthbass responded to this distribution by exclusively attackingindividualsat the edge in the three lowest stemdensities; only 1%of all attacks (N = 302) were on bluegills in the center.Center attacksexcluded,largemouthbass did not differentially attack bluegills at the topor bottomedge (binomial test: P > 0.12;N = 129)except at low density,in which largemouthbassshoweda

washigh. Thus, bluegillsreducedtheir vulnerabilityto a predatorby congregating near bottom edges in all pools. Typically, bluegills stayed in areas of discontinuity, either air-water or sediment-water interfaces, at the pool edge. In this way,bluegills were protected from two attack directions:dorsallyand laterally or ventrally and laterally.Bluegills movedonlyto center pool when stem densitywashigh enough

(1,000 stems/m 2) to provide protectionfrom


predation. Occurrenceof an attack depended on distancesbetweenlargemouthbassand bluegills.

Largemouthbassgenerallyattackedbluegills within about0.5 m from the predator;bluegills

262

SAVINO

AND

STEIN

TOP EDGE
ILl 80

+ MEDIAN,

95% CONFIDENCE INTERVAL

if' 4o
o

,,- WITHBASS

>58 OBSERVATIONS)
(N=24 OBSERVATIONS)

. WiH::T 'sAs...S'' 1' '" .. ,.. ,.;,..


BOTTOM CENTER

4o

.J

TOP CENTER
I I0 50 250 I000

I0

50

250

I000

STEM DENSITY (NUMBER PER M2+1)


FOUR[, 4.-Distribution of blueglls withina poolwithincreasing stem densities, withand without a largemouth bass present. sggncant differences (KtuakaI-Wallis test, P 0.05) between bluegrill distributions withandwithout a predatar in each location withina treatment aredesignated byan asterisk (*).

were mostcommonly farther than 0.5 m from the predator(Fig. 5). Generally, schooled bluegills remainedfarther from largemouthbass than dispersed ones(not attacked; Fig. 5). As stem densityincreased, schools stayedfarther fromlargemouth bass, whereas individuals were closer.Largemouth bassattacked from about the samedistance regardless of stemdensity or dispersion patternof bluegills (Fig. 5). Our comparison of artificialwith natural cover showedthat Potamogeton natansprovided more coverthan artificialvegetation at similar densities (Fig. 6). From this relationship, we wouldpredictthat naturaldensities ofP. natans of 130 stems/m z (about 250 artificialstems/m z) or greater wouldmodifypredatory behavior of largemouth bass and antipredator behavior of bluegills.
Discussion

betweenstructuralcomplexity and prey numbers (DiConstanzo1957; Saikiand Tash 1979) and an inverserelationshipbetweenpredation rate and structural complexity--assumptions supported by our results and by those of other

investigators(Huffaker 1958; Glass 1971; Crowder and Cooper 1979; Saiki and Tash
1979). However, rather than a linear relation-

ship, we found a break in capturerate occur-

Recent work suggeststhat intermediate structural complexity withina habitatproduces optimum conditions for predator growth, becauseit ensures a long-termsupplyof prey

(Glass 1971;Cooperand Crowder1979).This predictiondepends on a positive relationship 1977; Werner et al. 1977; Saikiand Tash 1979).

ring at a moderately high structural complexity (greaterthan 15% cover),beyondwhichlargemouth bass predators of greaterthan 300 mm were severely limited. This limitationwasproducedby a combination of factors, including the antipredatorresponse of prey and a reduction in visualcontact of prey by predators caused by an increasing numberof barriers. Largemouth bass alsochanged their tactics with changes in structural complexity; at low densities theywere active searchers whereas at highdensities, they became "sit and wait" or ambush predators. These behavioralshiftsmay operate to minimize energycosts requiredfor prey capture. Vulnerable prey often seek cover to avoid predation (Stein and Magnuson1976; Stein

PREDATOR--PREY INTERACTIONS ALTERED BY COVER

263

MEDIAN, 95% CONFIDENCE INTERVAL () CLOSEST SCHOOL

(28) I /

SAMPLE SIZE
0.5

.- ...

'
0
1.0

SCHOOL ATTACKED

-(4) . CLOSEST INDIVIDUAL tc,

(49)

0.5

' --INDIVIDUAL ATTACKED


0
I I0 50 250 I000

STEM DENSITY (NUMBERPER M2 + 1)


FIGU.E 5.--Distances between largemouth bass andbluegills (both schooled anddispersed) withincrearing stem density. Bluegills that were attacked arecompared with those that were closest tothe predator but not attacked Signcant differences (Kruakal-Wallis test, P < 0.05) between bluegills attacked andnotattacked within a treatment aredesignated byan asterisk (*). Theclosest schooled bluegill (notattacked) was significantly farther fromthelargemouth bass (P <0.05) than the closest dispersed bluegill (not attacked) in all treatments except for 0 stems/m e.Sample sizes indicate the number of times each behavior wasobserved.

Immobilizationor "freezing" (Smythe 1970; Curio 1976) combines with crypticcoloration (Endler 1980) to permit prey to blend in with their background and avoid detection. Although percent cover increased linearly with stem density,it did not afford protectionfor dispersed bluegills in our experiments until high
stem densitieswere reached (about 40% cover).

ertoire to reduce their susceptibility Schooling

canreducethe probability of captureof a given


individual, for as the number of individuals in

a group increases, predationsuccess and probability of encounter with a predator decline (Brockand Riffenburgh 1960; Hamilton 1971;

Neill and Cullen 1974; Taylor 1976; Major


1978; Shaw 1978). Furthermore, imitation of

At high coverdensities, bluegills may well be difficult to detectowingto their barred color patterns. Thesecolorpatterns combine with the antipredatortacticof becoming completely motionless in the presence of a predatorto reduce substantially the vulnerabilityof bluegills,even within strikingrangeof largemouth bass.

neighbors in defense movements enables schooling prey to respondto an attack more rapidly than solitaryprey (Radakov1973). As group size increases,it becomesincreasingly difficult for a predator to singleout and attack

an individual(Neill and Cullen 1974;Seghers 1974;Major 1978).In fact,few schooled blueAt stem densities less than 250 stems/m2, gillsin our studywere attacked,perhapsowing in difficultyof capturing schooled bluegillsexhibiteda different behavioralrep- to the increase

264

SAVINO AND STEIN

(4)

nO

60

+MEDiAN, RAN6E
SZE (3) t
/(6,)

Y=4.93 + O.06X
/ (4)

(D
z

40

. P. natans

r2=0.97
/

.. -. -- -'" 1

(D

2_0

.... -- -- -'
r 2 = 0.96

EL

0 -'"
0

(T
200 400

Y=2.68 +0.04 X
600 800 I000

STEM DENSITY (NUMBER PERM2 +1)


FIGURE 6.--Percent cover provided bydifferent densities of Potamogeton natansandsingle strands ofpolypropylene
line (4 mmdiameter, 0.5 m long).

overdispersed prey or to the abilityof schooled prey to respondand stayfarther from largemouth bass than dispersed prey. Increased structural complexityalso increasedthe distanceschools couldmaintainfrom largemouth bass.However, bluegills eventuallyswitched their strategyfrom primarily schooling at low stemdensities to dispersing at the highest density,in response to advantages associated with dispersal. At high density dispersed prey could hide effectively; thusfeweradvantages accrued to schooling individuals. Indeed, schooling may be disadvantageous at thisdensity asit provided groups largeenough for largemouth bass to find
and follow.

Optimal foragingtheory predictsthat strategies will be selected for maximizing net energy intake (providing lowestcosts per benefit to a predator:Pykeet al. 1977). Costoften is measuredastime spentin activeforagingbehaviors (Werner 1974). Predator activitymay be influencedby the relativecosts in searching for, pursuing,and capturingprey (Griffiths 1980). If prey attackand capture is energetically inexpensive, then predators canafford to adoptan activeforagingstrategy--increasing time spent in searchand pursuit. Given that prey attack and captureis energetically costly, then predators shouldminimizeenergyexpenditures in other activities(suchas pursuit) and become

ambushpredators.Our resultssuggest that predators switch strategies aspreyvulnerability changes;largemouthbasswere far-ranging predators at low stemdensities in whichprey werehighlyvulnerable, but ambush predators at high stemdensities, whenpreyvulnerability waslow. Thus, webelievethat predatorytactics of largemouth bass maybea function of habitat as well as a species-specific characteristic (such asbodyshape). Clearly, piscivores thattypically associate themselves with inshoremacrophytes (largemouthbass;northern pike Esoxlucius) would be ambush predators, whereasopenwater species (white crappiePomoxis annularis; white bassMoronechrysops) would be active, searching predators. Fromour perspective, the largemouth bass is probably flexiblein its predationstrategies. Whetherthisspecies isan ambushor an actively searching predatordepends on the complexity of the habitat in whichit (or its prey) happens to live. In additionto usingdifferent tactics in different stemdensities, largemouth bass alsoreduced costs by attackingonly prey with the greatest chance of being captured. Almostalways, these preyweredispersed withina rather shortstrikingdistance. Oncethe predatorattacked, capture was nearlyassured; success rates werehigh--70-80%---corresponding to the 90% rate measured by Nyberg (1971).The mosten-

PREDATOR--PREY INTERACTIONS ALTERED BY COVER

265

ergy-costly behaviors are probablypursuit, attack, and capture, and these behaviorswere directed at prey within a shortdistancefrom largemouth bass. With this strategy, costs per
unit of benefit were minimized.

This studydemonstrates that vegetationis ence 32:19-34. effectiveas coverin reducingpredationmorJ. A. 1980. Natural selection on color pattality of juvenilebluegills. Therefore,we have ENDLER, terns in Poecilia reticulata. Evolution 34:75-91. at leastpartlyexplained the distribution of juvenile centrarchids in natural communities on

vision,AmericanFisheries Society, SpecialPublication6, Bethesda, Maryland,USA. Cwmo,E. 1976.The ethology of predation. Springer-Verlag, New York, New York, USA. DCosTANZO, C.J. 1957. Growthof bluegill,Lepomis macrochirua, andpumpkinseed, L. gibbosus, of Clear Lake, Iowa. Iowa State CollegeJournal of Sci-

continual

tation or areasprovidingsimilaramountsof York, New York, USA. D. 1980.Foraging costs andrelative prey cover.The resultant reduction in vulnerability GRIFFITHS, size. American Naturalist 116:743-752. can be explainedby increases in the number of D. J., ANDE. E. WERNER. 1977. Seasonal disvisual barriers (or percent cover), aswellasby HALL, tribution and abundance of fishes in the littoral modifications in prey behavior. The randomzone of a MichiganLake. Transactions of the encountermodel is supportedin part by the AmericanFisheries Society 106:545-555.
decline in encounter rates as stem

GLASS, N. R. 1971. Computeranalysis of predation energetics in the largemouth bass. Pages 325-363 the basisof predationpressures, which cause in B. C. Patten,editor.Systems analysis and simprey to moveinto relatively safeareasof vegeulationecology, volume1. Academic Press, New

HAMILTON, W. D. 1971.Geometry for theselfish herd.

density increases. In addition, preymodifytheir Journalof Theoretical Biology31:295-311. M., ANDD. A. WOLFE. 1973. Nonparabehavior (decreased schooling) in the presence HOLLANDER, metricstatistical methods. JohnWileyand Sons, of predators, further reducingtheir visibility New York, New York, USA. and susceptibility.
Acknowledgments
We thank Vanessa Murchake for her untir-

HUFFAKER, C. B. 1958. Experimental studies on predation:dispersion factors and predator-prey oscillations. Hilgardia 27:343-383.

KEAST, A. 1977.Mechanisms expanding nichewidth

and minimizingintraspecific competition in two ing assistance and enthusiasm in the faceof tecentrarchid fishes.Evolutionary Biology 10: dious behavioralobservations, and B. L. John333-395. son, R. F. Carline, J. F. Downhower, L. B. KEAST, t. 1978.Feeding interrelations between ageCrowder,D. L. Johnson, and K. Laub for progroupsof pumpkinseed (Lepomis gibbosus) and comparisons with bluegill(L. macrochirua). Jourvidingcritical, highlyconstructive reviews of this nal of the Fisheries Research Board of Canada manuscript. This research wassupported in part 35: 12-27. by funds from the Federal Aid in Fish Resto- LAUGHLIN, D. R., AND E. E. WERNER. 1980. Resource rationAct under Dingell-Johnson ProjectF-57partitioning in two coexisting sunfish: pumpkin-

R, the National Science Foundation (DEB77-

16167),and the Department of Zoology.


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