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Risk and Foraging in Stochastic Environments Author(s): Leslie Real and Thomas Caraco Reviewed work(s): Source:

Risk and Foraging in Stochastic Environments Author(s): Leslie Real and Thomas Caraco Reviewed work(s):

Source: Annual Review of Ecology and Systematics, Vol. 17 (1986), pp. 371-390

Published by: Annual Reviews

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Ann. Rev. Ecol. Syst. 1986. 17:371-90 Copyright ? 1986 by Annual Reviews Inc. All rights reserved

RISK AND FORAGINGIN STOCHASTICENVIRONMENTS

Leslie Real

Departmentof Zoology, North CarolinaState University, Raleigh, North Carolina

27695-7617

Thomas Caraco

Departmentof Biological Sciences, StateUniversityof New York, Albany, New York

12222

INTRODUCTION

Foraging animals confrontproblemsconceptuallysimilarto those facing an economically mindedconsumer(46, 47), and foragingtheorysharesa meth- odology in commonwith economics. Indeed,the last 20 yearshave seen wide applicationof economic models in biology. A growing consensus suggests thatecological andeconomictheoriesareultimatelyindistinguishable(6, 30). Economic analyses begin with an economic agent that chooses from alternative objects or activities. The analyst extracts a set of measurable attributesfrom this collection of objects (e.g. energy content, costs, etc) that are combined into a single index. This index has the propertythat objects whose attributesgeneratehigher values are preferredby the consumerover objects generatinglower values. In economics, this index (the 'utility func- tion') is the basic organizingprinciple (36). Behavioralecologists use this techniqueto learnwhat attributesshouldbe includedin an organism'sutility function to determine how various attributes should be combined and weighted, andthento predictchoices by maximizingthe utilityfunctionunder applicableconstraints.The organism'sutility functionis, therefore,both an object of empirical study and a predictivetool. Economic analysis usually stops here, but evolutionary biologists go farther. They assume that the organisms'preferencesarerelatedto evolutionaryfitness andthatthe options

371

0066-4162/86/1120-0371$02.00

372 REAL& CARACO

more preferredmust lead to greatersurvival and reproduction.Hence, we hypothesize that the utility function is isomorphic with fitness. This, of course, is an assertion, and one that needs more empiricalinvestigation. The underlyingassumptionsandlimitationsof economic optimizationhave been clarified (53), criticized (26), and defended (48). We feel that these techniques, althoughcontroversial,arethe best availablefor deducingempir- ically falsifiable hypotheses based on first principlesfor behavior. Ourtheoriesnecessarilyexamine one (orjust a few) phenotypiccharacters in any particular model. Many traits interactively govern survival and reproduction,but we are forced to limit the phenotypicdimensionalityof a theoryif it is to be testedrigorously.However, in ourinterpretationof theory we recognize that single-attributestrategicmodels concernphenomenacon- ditioned by other traitsand competing selection pressures(11, 42, 53, 59). Interpretinga model for a single trait'sadaptivesignificancerequiresthatwe remainwary of (butnot inhibitedby) genetic, environmental,andorganismal sources of variationin the characterof interest. We might treat a theory and an organism's behavior like a map and a territory.More formally, we replacea theory'salgebraicinterpretationwith a probabilisticinterpretation.Many models in behavioralecology, and nearly all models of foragingstrategy,can be writtenas questionsof preferenceand choice. In these cases a probabilisticinterpretationof a theorymeansthatwe replacea strongutilityhypothesiswith a weak utilityhypothesis(12, 18, 45). The following example contraststhese alternatives. Suppose an organismmustchoose betweentwo options. Let the associated probability densities of benefits be fi and f2. The ecologist constructs a theoreticalfitness/utilityfunction W and deduces predictionsby comparing the expected fitnesses E(Wlfi). Letfi Pf2 designatepreferenceforfi overf2. The ecologist seeks to predictpreference(or indifference)with the model. If E(W If,) : E(W If2),thenanalgebraicinterpretationof the modelyields a strong utility hypothesis of the form:

E(W|fi)

> E(Wjf2) -*

Pr(fi P f2)

=

1.

1.

The strong utility interpretationpredicts exclusive choice [or equiprobable choice when E(WIfi) = E(W1f2)].Ecologically significant choice behavior seldom exhibits this sort of deterministicregularity(11, 18, 45). Now suppose thatthe stochasticnatureof selection processes, interactions with other traits, and other factorsrenderthe organism'sbehaviorless than perfect. The model W still distinguishesany difference betweenf, andf2, but the predictedresponseto the difference(thetraitof interest)is bettertreatedas probabilistic.This interpretationof the model yields a weak utilityhypothesis of the form:

E(WIf,) :

E(WIf2) -*

Pr(fI Pf2)

:

RISK-SENSITIVEFORAGING

373

1/2.

2.

Iff1 advancesfitness

more thandoes f2, thereshouldbe a tendency to prefer

fl.

As the difference between the E(W) values increases, preference for the

more profitableoption presumablyincreases. The weak utility interpretation

maintainsa distinctionbetweenthe model andthe organismandmorerealisti- cally describesthe consequencesof selectionthandoes the determinismof the strong utility interpretation. In this paperwe review some models for foragingdecisions in stochastic environments.To do so, we mustexamineboththe natureof the stochasticity and the way in which the foragermight efficiently respond.

CLARIFYINGRISK

Economists often distinguishbetween two types of decision-making(2). In the first type of decision the economic agentknows the objectiveprobability distributionscharacterizingoutcomes for feasible actions correspondto con- ditions of 'risk.' The decision-makerpresumablyknows (via experience or selection on a genetic program)the likelihood (probability)of an event's occurrence. In the second type, organismswith no such knowledge, (or an organismpossessing only subjectiveestimatesof the distributions)face con- ditions of 'uncertainty.'To predictbehaviorwe must assume some form of underlyingprobabilisticstructure.Thus, economists analyze uncertaintyin the same manneras conditions of risk. However, the conditions are quite distinct;some aspects of economic behaviorarguablyresultfrom uncertainty but not from risk (38). From a biological perspective, we emphasize that

naturalselection

still be deciding subjectively (at least duringan initial samplingperiod). The ecological literaturementionsdifferentkinds of risk, and some confu- sion has resulted. For example, the 'risk of predation,' though of obvious importance,is not relatedto risk as we use the term. In fact, most models of predationrisk are 'riskless' in thata discrete,randomoutcome(the individual survives or is killed by a predator)is replacedby the population's average mortality hazard due to predation. The model organism responds not to probabilitydistributionsbutto fixed attributesof patches,habitats,etc. In any case, ourdiscussionof riskconcernsanorganism'spreferencesoverprobabil- ity distributions. As indicated above, a foragerin a stochastic environmentmay face two distinctbut complementaryproblems(23, 69). First, the organismmustlearn the reward probabilitydistributionsassociated with different behaviors (a problemof information),andthenit mustselect a strategyfor exploitingthose distributions(a problem of risk).

operates on objective probabilities,but the organism may

374 REAL& CARACO

Informationproblemsareusually analyzedwith Bayesianmodels in which

the organismmodifies its estimates of probabilitiesbased on its experience

while

patch until it exhausts the patch or decides to leave. Each patch contains n

places, or bits, where a prey item may occur. Given a level of patch quality (the probabilitythat a bit contains a prey item), total prey per patch is a binomial variate. Patchqualityitself is a Beta randomvariable.The optimal Bayesian bird leaves a patchwhen it has found only k prey aftersamplingtk differentbits. The Bayesiandimensionis explicit since the decisionto leave a patchdependson experiencethereandthe overallpatternof patchquality(27, 28, 49, 51). Analyses of problems of informationhave generated a variety of new hypotheses differing qualitatively from the results of correspondingde- terministicmodels. For example, considerClark& Mangel's (21, 22) theory

for the evolution of

groupforaging,or Real's (62) model for habitatselection

in fish. Houstonet al (31) and Krebset al (40) have reviewed the theoryfor

problemsof information.Experimentalresearchon questionsof information has begun only recently in behavioral ecology (39, 43). Therefore, the remainderof this review restricts attentionto problems of risk, where the theory has been subjectedto a reasonablenumberof tests.

foraging. For example, Green (27, 28) assumes that a bird searchesa

RISK-SENSITIVITYAND FORAGINGBEHAVIOR

Most theories for risk-sensitive foraging propose decision criteriathat ex- plicitly or approximatelyinvolve an interactionbetween the mean and vari-

ance of

50, 57, 58, 59, 69). These criteriaarisenaturallywhen the relevantprobabil-

ity distributions are functions of two independentparameters.However, maximizingthe expectationof a randomvariable(withoutexplicit considera-

tion of the variance) will be

Suppose the randomoutcome of a foragingdecision follows a one-parameter distribution,so that all cumulativeprobabilitiesare specified by the parame- ter's value. If fitness is maximalwhen the probabilityof starvation(or other penalty)is minimal,rankingthe meanscanbe sufficientto solve theproblem. Let the i-th option imply that identical food items will be consumed at constantprobabilisticrateAi. If T is the time available,andX is the totalfood

consumption (a discrete, nonnegativerandomvariable), then choice of the i-th option means that X will be a Poisson variatewith expectationAiT.

food consumedor the time spentacquiringrequiredenergy (8, 9, 32,

appropriatein certain simple problems (13).

Supposethe foragerstarvesor fails to reproduceif X ?

R. We hypothesize

thatselection favorsminimizingPr(X ? R), so thatfitness is a stepfunctionof

total food consumption. The best strategychooses Ai accordingto:

min Pr(X

where

?

R1A)

=

min e -A

= minr(R

RISK-SENSITIVE

R

(AiT)xlX!

+

1, AiT)/R!,

FORAGING

375

3.

4.

F(R

+

1,

AiT)

=

fAT

e-ttRdt.

5.

Equation(5) indicates the equivalence between minimizing Pr (X? R) and

maximizing AiT = E(X) in this simple

this sortof probleminvokes the orderrelationship'stochasticallylarger'(13,

65).

example. A useful generalizationof

Let XI and X2 be discrete nonnegative random variables where XI is

stochasticallylargerthanX2 (denoted XI '

Pr(XI >

R)

?

Pr(X2 >

R)

for all R.

Taking complements in (6), we have

Pr(XI

?

R)

?

Pr(X2 ?R)

for all R.

ST X2). Then, by definition(65):

6.

7.

Using (6) again and summing over all possible values of R, we obtain:

E(X1)

=

E

R=O

Pr(XI

>

R)

'

E

R=O

Pr(X2 >

R) = E(X2)

8.

As above, let X be total prey consumptionand let R be the requirementfor survival. Expression (7) indicates that choosing XI cannot lead to a greater probabilityof starvationwhen XI : ST X2- If outcomesXi can be rankedby the order relationshipstochasticallylarger, the chance of starvationcannot increase(andusually will decrease)as E(Xi)increases(13). However, such a simple equivalence between fitness and mean rewards will hold only in special cases. For example, if total energy intakefollows a normaldistribu- tion, the probabilityof starvationdependson combinedeffects of both mean and variance. Consequently, a useful theory for risk-sensitive foraging re- quires more than rankingstrategicoptions by their associated averages. To examinemean-varianceeffects, let W(X)mapenergyintakeintofitness. In theory, some W specifies present and expected future survival and reproductionfor anyX, but we requiremoretangiblecurrenciesfor empirical work. For a nonbreedingforager,W(X)can be survivorshipover a given time interval. McNamara& Houston (50) show that, under certain conditions, lifetime fitness will be proportional to short-term survival during the

376 REAL& CARACO

nonbreedingseason. Therefore,we need not always projectvery far into the future when hypothesizing a form for W(X). For some organisms, Wcan be takenas survivalover a single day (18, 19, 57, 67, 69). Let X now representtotal daily energy intake, a continuous randomvariable.X is a sum acquiredover n foragingopportunitiesduringthe

time availablefor feeding. For sufficientlylargen, X approachesnormalityby

and let V(X) = (J2, and

take Pr(X -

the central-limittheorem (8, 67). We let E(X) = ,

R) as the probabilityof starvation.

Stephens& Charnov(69) assumeselection actsto minimizethe probability

of starvation,andthey identifythe consequencesin a useful manner.SinceX

approaches normality, the distribution of z [where z = (X -

p)Io-] approaches

the standardnormal.ThenminimizingPr(X 2 R) is equivalentto minimizing:

Pr[z '

(R

-

O)IMi =

4(ZR)

9.

Hence the z-score model. Equation9 reveals that dJ(zR)hd9p <

rewardwill obviously be favored.The effect of varyingthe standarddeviation

0. For given or,an increasein mean

dependson the differencebetween the requiredandexpected intake,R -

If

, budget is positive (10, 12). In this case do(zR)ld/o

increasein rewardvarianceincreasesthe chanceof starvation.Consequently,

we anticipaterisk-aversionwhen ,u > R (10, 18, 19, 32, 57, 69). If ,

the forager's expected energy budget is negative and d8 (zR)/doJ < 0. For a given , an increase in benefit variance decreases the chance of starvation.

Therefore,we anticipatea risk-proneresponseto benefit variancewhen ,t <

R (12, 19, 57, 69).

,.

> R, the foragercan expect to surpassits requirement,so thatits energy

>

0; for a given ,

<

an

R,

Suppose two alternativeforagingoptions yield respectivetotal benefitsX1

and X2. The Xi are random variables with V(X1) <

forager will prefer X1, because its variance is lower, unless E(X2) is suf- ficiently largerthanE(X1). A risk-proneforagerwill preferthe morevariable X2, unless E[X1] is sufficiently larger than E[X2]. The preceding analysis predictsthat a forager's expected energy budget governs its responseto risk when the animalmust satisfy a short-termphysiologicalrequirement,andthat reward mean and variance both will influence choice over two-parameter

distributionsof benefits or costs (13, 50, 57, 59, 69). Furthermore,the z-score model suggests an explicit mean-varianceinteraction.By analyzing iso-fitness contours,Caraco& Lima(17) show thatthe z-scoremodelpredicts decreasing risk-sensitivity (see below), so that the way in which mean and variancecollectively governpreferencedependsnot only on the sign of (, - R), but also on the value of ,u. When W(X)is survivalover a single day, all values of X such thatX > R

V(X2).A risk-average

RISK-SENSITIVEFORAGING

377

impart the same fitness. That is, the z-score model hypothesizes a step function for W(X), but other models for risk-sensitive foraging treat con- tinuousfitness functions. Real (58) hypothesizesa concave W(X).Caraco(8) and McNamara& Houston (50) conclude that W(X)will be convex-concave when some sort of short-termrequirementis biologically significant. For a nonbreedingforager, survivorshipshouldalways increasewith ener- gy intake, so we assume W' > 0. This assumptionshouldhold unless excess weight imposes a mortalityhazard(44). Survivingwintercould implythatthe foragermonitorsan averagedaily requirement;a reasonablepossibilityis that energy intake balances expected 24-hour expenditures (19). We let R* representthe averagedailyrequirement;a totalenergyintakeof atleast yR* is requiredover y days (-y > 1). For X well below R*, survival is low (but immediatestarvationneed not be certainsince y > 1). As X approachesR*, survivorshipincreaseswith increasingrapidity.Therefore,W is convex (W"

> 0) for X < R*. Above R* each additionalamountof energy quite likely

decreases in value to an adequatelyfed animal (58), but energy consumed beyondR* can be carriedover to the next day (68). Therefore,W is concave (W" < 0) forX > R*. As discussedbelow, this formfor the fitness function

predictsrisk-pronepreferencesforX < R*, andrisk-aversepreferencesforX

> R*.

When fitness cannot be approximatedby the individual's short-termsur- vival or reproductivesuccess, the convex-concaveformfor Wmay not apply. For example, colony-level fitness in social insects might suggest thatW(X)is strictly concave for the individual forager, since individual physiological requirementsare presumablyless importantselectively than is the energy budget of the more permanentcolony (53). If this is true, risk-aversionat all rewardlevels follows. As a second example, we note thatbody size in birds

andmammalsshouldcorrelatepositively with the lengthof time an individual can survive without food (7, 25). Therefore,the time horizon (-ydays) over which the averagerequirementR* is defined could easily increasewith body size. As a consequence, the convexity of W for X < R* may approach linearity as body size increases. Houston & McNamara (33) consider a forager with an infinite time horizon (-y -* oo);their theoreticalobjective becomes maximizationof the expected time until starvationoccurs. Given a set of assumptionsconcerningprey profitabilitiesand encounterswith prey,

they find thata foragershouldalways take a prey item if it yields an increase

in total stored energy. Under certain conditions, this strategy might

strict risk-aversion (Houston, personal communication). Therefore, larger

animalsmight adhereto risk-aversion,providedthatlargerbody size tendsto free the foragerfrom short-termenergeticrequirements.If the shapeof W(X) does indeed depend predictablyon body size, then the regulatorymodels proposedby Staddon(66) may prove valuableto both ecologists and operant psychologists.

imply

378 REAL& CARACO

Returningto foragerswith short-termrequirements,suppose that W(X)is convex-concave with an inflection point at X = R*. If we hypothesize an analyticalform for W, the expected fitness associatedwith the i-th strategic option is:

Ei[W(X)] =

f W(X)f1(X)dx,

10.

wherefi(X) is the probabilitydensityof energyintakeresultingfromchoice of the i-th option. The best decision maximizes expected fitness. However, we often will want a more general procedurethat does not requirespecifying W(X) analytically. A simple alternativeis expanding W(X) about A with a

Taylor series approximation(1, 34, 58).

rivative and then taking expected values, we have:

Expandingthroughthe third de-

E[W(X)]

W(g)

+

(1/2) W" (i)

c.2

+

(1/6) W'.'(

)

3,

11.

where 3 is the skew of X, E[(X - 3]. If X is distributedsymmetricallyabout its mean, p3 = 0 and Expression 11 then suggests variancediscounting(58, 59). When X has a skewed distribution(i.e. when 3 * 0), g and o-2 generally are dependent(1). However, we can separatelyexamine the con- tributionto expected fitness of mean, variance,and skew, both theoretically and experimentally(15, 41). The first term on the righthand side of Expression 11 is the mean's contribution to expected fitness. Assuming W' > 0, an increased mean rewardordinarilywill enhanceexpected fitness. The second termin Expres- sion 11 is proportionalto W"(I) o-2. If ,u < R*, thenW" > 0 andexpected fitness increases as reward variance increases [by Jensen's inequality: (8,

24)]. Hence,

deficit. If ,u > R*, then WI" <

the forager should be risk-pronewhen expecting an energetic

0 and expected fitness decreases as o-2

increases. Therefore, risk-aversionfollows from an expected energetic sur- plus. Note thatthe simplerstep functionmodels generateessentiallythe same

qualitativepredictionsconcerningresponseto rewardvarianceas do the more realistic convex-concave models. The effect of skew on expected fitness will depend on WI'I (which is assumed to exist). To analyze WI'I, it is convenient to categorize risk- sensitivityas constantor variable.Forsimplicity,we restrictourdiscussionto risk-aversion;for a broadertreatmentsee Caraco& Chasin (15). Constantrisk-aversionfollows when a given o-2 depressesexpectedfitness by the same amountat any level of ,u, meaningthatW" does not dependon

X. Decreasing risk-aversionfollows when the negative effect

decreases as ,u increases, implyingthatWI"(,)

> 0, and a given o 2 exerts the opposite

increasingrisk-aversiondW" (g)/ld

of a given - 2 increases. For

declines as ,

I

RISK-SENSITIVEFORAGING

379

effect on expected fitness. Decreasingrisk-aversionhas the greatestintuitive appeal. We can portrayconstantandvariablerisk-aversionvia Pratt's(55) index of

WI/W'I. Since W' > 0, p(X)>0 for all forms

of risk-aversion.Underconstantrisk-aversion,dp(X)/dX= 0. Fordecreasing risk-aversion, dp(X)/dX< 0; for increasingrisk-aversion,dp(X)/dX> 0.

'local risk-aversion':p(X) = -

Since p(X) =

-W"/W',

d

p(X)/dX

=

[(W'v)2 -

W

' W'] I

(W')2.

12.

Knowing the sign of d p(X)/dXmay allow us, fromEquation12, to determine the sign of WI'I and, hence, the effect of skew on expectedfitness. Caraco& Chasin (15) show thatpositive skew tends to advanceexpected fitness when risk-aversionis eitherconstantor decreasing.Skew in X may arisefrom rare events or from uniformlyskew rewardsat individualforagingbouts (15). An efficient foragermight respondto rewardskew, but responses to mean and variance presumablydominate in nature.

If we truncateExpression 11 at the second moment, we have a variance

discountingformula:E(W)

W(X),we might take WI'/2 as a 'constantof risk-aversion'(60, 64). Thatis,

we mightpredictconstantrisk-aversionby assumingW" is independentof X. However, as an approximationto a postulatedanalyticalform for the fitness function, variance discounting can accommodateconstant or variable risk- sensitivity. For instance, if we assume that W(X) = log X and evaluate this function accordingto the Prattmeasureof local risk-aversion,we see thatthe coeffi- cient of risk diminishes:

W(,u)+ (1/2) W" (,)

o-2. Withoutspecifying

p(X) =

-

W"/W'

=

X

>

0

p'(X)

=

-

1/X2 <

0.

If we assume that W(X) is quadratic, i.e.

organismwill show increasingrisk-aversion.Alternatively,for W(X)= a -

[a form used by Caraco(8)] then risk-aversionwill be constant. Pratt

(55) catalogs a varietyof differentutility/fitnessfunctionsthat will generate different types of risk aversion. Analysis of the indifferencecurves for the differentfitness functions will

reveal the implicit response to increasing expectation (Figure 1). Curves bending upward correspondto fitness showing diminishing risk-aversion. Straight lines correspond to constant risk-aversion. Strictly concave in- difference curves indicate increasingrisk-aversion. The Taylor Series (Equation11) can be used to approximateany of these

e-bX

W(X) =

aX

-

bX2, then the

380 REAL & CARACO

(N

a

b

Mean

(,u)

Figure 1 Generalizedindifferencecurves for threedifferentspecified fitness functionsW(X):

(a) W(X) = aX - bX2, showing increasing risk-aversion,(b) W(X) = a - e-'x, showing constantrisk-aversion,and(c) W(X) = log X, showingdiminishingrisk-aversion.The curvature of the indifference relation reveals the organism's sensitivity to risk with variation in the expectation of the distribution.

functions. However, terminationof the approximationat the second moment requires either (a) the variables are normally distributed,or (b) W(X) is quadratic.The approximationwill only be exactthenif we admitthe seeming- ly unreasonableassumptionof increasingrisk-aversion.Nonetheless, as an approximationthe variancediscountmodel will hold for any function W(X) and need not reflect a given type of variabilityin risk aversion.For example, for W(X) = log X the variancediscount approximationwould be:

E[W(X)] =

log

,

-

1/2 o-24lr2,

RISK-SENSITIVEFORAGING

381

which clearly has a diminishingcoefficient of risk. Ourreview of risk-sensitivityhas mentionedonly staticmodels. If a forager can switch among available options duringthe course of a day, a feedback control policy would decrease (or at least never increase)the probabilityof starvation. Houston & McNamara(32) discuss the optimal control policy when there is no cost to switchingbetween two options with identicalmean rewardratesbutwith differentlevels of rewardvariability.The foragershould use the option with the lesser variabilityas long as the animal expects to surpassits daily requirement.However, if the forager'senergetic condition ever indicatesthata deficit is more probablethanan excess, the animalthen should immediately switch to the more variable option. The best dynamic policy shows a strong similarityto the correspondingstatic model, but the optimal control also suggests predictablechanges in sensitivity to risk. In this section we have treatedrisk-sensitivityin a normativemanner.The next step is, of course, to evaluate the theoreticalpredictions in light of empirical results.

EMPIRICALRESULTS

To investigate risk-sensitive foraging experimentally,the investigatorcon- trolsthe rewarddistributionsavailableto an animal.Oneclass of experiments examines preferenceover rewardvariancewhen mean rewardsare fixed. A second class tests predictedtrade-offsbetweenmeanandvarianceby simulta- neously changing both parameters.

Responses to Variance with Fixed Means

The most direct test for risk-sensitivitylets a foragerchoose between two resources or feeding stations. One resource is held constant. The other resourcevariesrandomlyover spaceor time, butits expectedvalueequalsthe constantreward.The organismselects the amountof time or effort allocated to each resource.The nullhypothesisis indifference;any significantdeviation from equal use of the two resources demonstratesrisk-sensitivity. Real (60) constrainedbumblebees (Bombus sandersoni) to an artificial patch where an equal number of yellow and blue flowers were arrayed randomlyon a largegrid. A knownquantityof artificialnectarwas dispensed into each flower. Flowers of one color always provided 2 ,ul of nectar. Flowers of the other color provided a variable reward: Two thirds were empty, andthe rest contained6 ,il of nectar.Approximately85%of all visits were to the constantreward,a responseindicatingrisk-aversion.The bees still preferredthe constant reward when all flowers contained at least 0.5 ,ul.

382 REAL& CARACO

Hence the observed risk-aversionis clearly more than avoidanceof a floral type that sometimes provides no reward. Real (60) also found that wasps (Vespula maculifrons) foraged risk- aversively in the same patch of artificialflowers. But the wasps' preference for the constant reward appearedweaker than that observed in the bees.

Unlike bumblebees, the wasps are carnivorousand do not requirenectarfor reproduction.The difference in choice probabilitiescould mean that organ- isms aremore sensitiveto variancein those resourcesmorecriticallylinkedto reproduction. Waddingtonet al (71) demonstratedrisk-aversionin a second species of bumblebee, Bombus edwardsii. In these experimentsrewardvariationwas imposed temporally; bumblebees apparentlyrespond to both spatial and temporalpatternsof rewardvariancein a risk-aversemanner. Wunderle & O'Brien (74) studied hand-rearedBananaquits (Coereba flaveola) foraging on artificialflowers of two differentcolors. In their first experiment,one floral type provideda constantvolume of nectar. The other type varied, but its mean volume equalled the constant reward. Foragers generally avoided variance;less experiencedbirdschose the constantreward more than other subjects did. In a secondexperiment,Wunderle& O'Brien(74) showedthatthe Banana- quits respondedsimilarlywhen resourcequality, ratherthanquantity,varied randomly. Wunderle& O'Brien filled every flower of both types with the same volume of nectar and made sugar concentrationthe randomvariable. The birdsagainpreferredlesser variance,andmeasuresof theirrisk-aversion did not differ significantlyfromthose observedin the manipulationof nectar quantity. Risk-sensitivity in small granivorousbirds has been exploredextensively by Caraco(10, 11, 12, 14, 19). A birdis confinedin a largeaviarywheretwo

feeding stations are separatedby

bird leaves a perch on the aviary's centerlineand visits one of the feeding

stationswhere the animalobtainsa known numberof millet seeds (Panicum

miliaceum). The subject's expected daily energy budgetcan be manipulated by adjustingthe length of preexperimentaldeprivationand the averagefeed- ing rate which the bird experiences duringan experiment.The daily physi- ological requirement(the food intake balancing all energetic costs) is es- timated from analyses of oxygen consumptionor food intake under ad lib availability. Caraco et al (19) examined risk-sensitivityin yellow-eyed juncos (Junco phaeonotus)at bothpositive andnegativeexpectedenergybudgets.The birds faced choices between a constantnumberof seeds and a randomnumberof seeds; the mean of the variable rewardequalled the constantreward. The

juncos

a partition.At each experimentaltrial the

preferredthe constantrewardwhen their energy budget was positive

RISK-SENSITIVEFORAGING

383

but switched to preferencefor the variablerewardwhen theirenergy budget was negative. The shift between risk-averseand risk-pronepreferenceswas independentof the order of treatmentsan individualexperienced. Similar experimentswith dark-eyedjuncos (Junco hyemalis)yielded sim- ilarresults;energybudgetspredictedpreferenceover rewardvariance(10). In addition, Caraco found that indifference to rewardvariance was the most common result for 'balanced' energy budgets. This was an intermediate condition where the feeding rate duringan experimentwas just sufficient to meet costs for a bird spending all available time foraging. Caraco (11) next subjected white-crowned sparrows (Zonotrichia leucophrys) to the same experimentsthat revealed risk-aversionin juncos. White-crownedsparrowsweigh 50% more than dark-eyedjuncos, but their preference behavior did not reveal a significant interspecific difference in risk-aversion.Most small birdsare constrainedby daily energyrequirements duringthe winter, so that similarresponsesto risk could be expected. As an independentvariable for predictingrisk-sensitivity,body size (in birds and mammals)may be interestingonly when its variationis sufficient to induce variationin the time horizonover which foragersattemptto regulateenergy intake relative to expenditures. Experimentsreviewed to this point all involve choice between a constant and a variablereward.But animalsmustdiscriminateamong, andstrategical-

ly use, differentvariablerewardsif risk-sensitivityis to influencebehaviorin

a significant way. Caraco (12) reportsthat white-crownedsparrowschose

between two variable rewards (randomnumbersof millet seeds) with the same expected value. The birds preferredthe smalleror largerrewardstan-

dard deviation accordingto their expected energy budget.

The transitionfromrisk-averseto risk-pronepreferenceshas been observed

in two otherexperimentalsystems. Barnard& Brown(3) enclosed individual

common shrews (Sorex araneus) in plastic tanks with two feeding stations where the animals could obtain mealworm segments. One station held a constantrewardwhile the otherprovideda variablereward;expectedrewards were identical. When the shrewswere fed at a ratebelow theirphysiological requirement,they preferredvariability. However, they were risk-averseat positive energy budgets and chose the constantrewardon 74% of the ex- perimentaltrials. In a clever extension of their work, Barnard& Brown (4) presentedthe same choices to shrews under conditions of apparentresourcecompetition. When a competitorwas introduced(actuallyan apparentcompetitor,since the introducedanimalwas not allowedto feed), subjectshrewswere indifferentto rewardvariance. Competitioneliminatedevidence of risk preferencein the shrews, but the adaptivesignificance(if any) remainsa mystery. Kagel et al (35) suggest an economic interpretation.

384 REAL& CARACO

Moore & Simm (52) linked a switch between risk-averseand risk-prone foraging preferences to the annual cycle of the migratoryyellow-rumped warbler (Dendroica coronata). Energy requirementspeak during the pre- migratoryperiod. The birdsmustdepositfat sufficientto satisfy the demands of migratorytravel. When birds in this premigratorystatus were given a choice between a constantand a variableamountof food (with a mean equal to the constantreward),they were risk-prone.Controlbirds(i.e. birdsnot in premigratorydisposition) were risk-averse when presented the very same choices. Furthermore,the migratorybirds' preferenceschanged from risk- prone to risk-averse after they reached maximal body size. Note that the warblers'behavior showed both preferencefor and aversionto rewardvari- ance, but theirdaily energybudgetwas nevernegative. Thatis, the transition in risk-preferencewas based on more than a comparisonof daily intakeand daily expenditure.When the birds' weight was less thanthe migratorylevel, they preferredthe variablereward. But they became risk-aversewhen they attainedthe weight appropriateto the physiological requirementsof migra- tion. In terms of our hypotheticalW(X),this suggests thatthe averagedaily requirement(R* in the discussion above) varies seasonallyin yellow-rumped warblersin accordancewith the demandsof their annualcycle. Daily energy budgets predict the natureof risk-sensitivityin organisms whose fitness should be proportionalto short-term survivorship: small, nonbreedingbirds and mammals. But some other results indicate that risk- sensitivityis a morecomplex phenomenon,andwe summarizethose observa- tions here. Recall thatBarnard& Brown(4) foundthatcommonshrews' sensitivityto risk depended on their expected energy budget, but their risk-sensitivity

disappearedwhen

forage solitarily, but the result may suggest that direct competitive in-

terferenceor dominanceinteractionscould influence foragingpreferencesin nature.

K. D. Waddington,B. Heinrich, & L. Real independentlyhave attempted

to induce risk-pronebehaviorby deprivingbumblebeesof food, but the bees remainedrisk-aversetowardvariancein rewardsize (personalcommunication and personalobservation).As we indicatedabove, an individualbee's food intake may always map into colony fitness in a concave manner(promoting risk-aversion).A second adaptiveexplanationproposes that bumblebeesre- duce theirenergeticexpendituresby loweringtheirmetabolicratewhen food is scarce, so thatrisk-pronenessoffers no strategicadvantage.Of course, the mechanicalrule of thumb(40) used by a foragerneed not involve scaling its expected intake to any requirement.A bumblebee might ordinarilyforage quite efficiently by simply avoiding resourceswith large rewardvariances. For still anotherview, see Wells & Wells (73).

an apparentcompetitor was

introduced. Shrews usually

RISK-SENSITIVEFORAGING

385

Battalioet al (5) foundthatlaboratoryratsexhibitedrisk-aversepreferences over randomlysized rewardswhethertheir energy budgets were positive or negative. As previously discussed, a large animal's survivalis seldom con- strainedby immediateenergy requirements,andrisk-aversionbecomes more likely as the time horizon for regulatingfood consumptionlengthens with increases in body size. Large animalscan dependon energy stores to mod- erate the influence of temporalfluctuationsin food availability. Therefore, theirrisk-sensitivityneed not be attuneddirectlyto daily benefits and costs. Both the theory and experimentswe have reviewed to this point concern randomvariationin eitherresourcequantityor resourcequality. A numberof studies in operantpsychology examine a relatedbut differentproblem.Each of two options providesthe same fixed rewardsize. One alternativerewards the animal after a fixed delay elapses between choice and consumption;the other alternativeimposes a variabledelay (with expected value equal to the fixed delay). Most results indicate strong preferencefor the variable delay (23, 29, 37, 56). The subjects (usually pigeons, Columbialivia) were de- prived to about 80% of their normal body weight, so that risk-proneness deserves considerationas a possible explanation(40). However, foragersmay treat delay times in a very different mannerfrom reward size. If foragers discount futurerewards, the economic model analyzed by Kagel et al (35)

predicts that a variable delay will always be

anotherdiscussionof responsesto energeticvaluesvs responsesto delays, see

Staddon (66).

preferredover its mean. For

Mean-VarianceTrade-offs

The models discussed above predictan interactionbetween the expectation

and

prefers large means and small variances, so thatits preferenceswill reveal a trade-offbetween mean andvarianceunderappropriateconditions.The exact

natureof the predictedtrade-offis

has realisticallybeen limited to a comparisonof constantand variablerisk- sensitivity. Caracoet al (19) studiedcertaintyequivalentsfor rewarddistributionsin foraging yellow-eyed juncos. That is, they located the constantrewardfor which a bird was indifferentbetween that constantnumberof seeds and a given variable reward. Under risk-aversion,the certaintyequivalentswere less than the variable distribution'smean (indicative of the mean-variance trade-off). As the mean of the variable reward increased, the difference between the mean and the certaintyequivalentdeclined. This result suggests decreasingrisk-aversion.Stephens& Paton(70) have demonstrateddecreas- ing risk-aversionin rufoushummingbirds(Selasphorusrufus).Via an indirect

variance of a reward distribution.For example, a risk-averse forager

model specific, but most work in this area

386 REAL& CARACO

statisticalmethod, Battalio et al (5) interpretlaboratoryrats' preferencesas examples of decreasingrisk-aversion. The way a risk-averseforagertradesoff mean andvariancecan be studied by constructingindifference curves in the mean-varianceplane. However, only two such studies have been conductedto date. Real et al (64) estimated mean-varianceindifference curves from the foragingpreferencesof captive bumblebees(Bombuspennsylvanicus).In an artificialpatch, flowers of one color provideda constantnectarvolume. The variance of the other floral type was fixed, and its mean was increasedor decreaseduntilindividualbees were indifferent(i.e. untilthe constantreward became a certaintyequivalentfor the variablereward).Next, the varianceof the variablerewardwas increasedand its mean then was adjusteduntil the bees' foraging choices showed indifference again. For a single constant reward,the procedureidentifiesthreesets of responsesto variablerewards:a set with each element preferredover the constant reward, a set where the constantrewardis preferredover each element, and an indifferenceset with elements preferredequallyto the constantreward.Regressionanalysisof the indifferenceset revealsthe slope andcurvatureof the mean-variancetrade-off (17, 64). Real et al (64) completed four experiments of this sort. In three ex- periments, they detected a significant trade-off between mean reward and rewardvariability.The quantitativecharacterof the trade-offwas sensitiveto

a variety of ecological attributes,including the patchinessand color of the

floral types. Two of the three significanttrade-offsindicatedconstantrisk- aversion;the third significantresult suggested either constantor decreasing

risk-aversion.

Caraco& Lima(17) performedsimilarexperimentswith dark-eyedjuncos. In each of two series of experiments, they found a significant trade-off between mean rewardand rewardvariability.Both constantand decreasing risk-aversionaccountedequally well for the estimatedindifferencecurves.

The

experiments discussed in this section collectively reveal that risk-

averse foragers clearly do trade off rewardvariance against mean reward. However, neitherconstant-norvariable-risk-sensitivityemergesas the domi- nant response. Recalling our earliercommentson algebraicvs probabilistic interpretationof a theory, we feel that a qualitative demonstrationof a trade-off is the biologically significantresult. Both theoreticalandempiricalworkon risk-sensitiveforagingbeganonly a few years ago. But therealreadyhas been a healthyexchangebetweenmodel and experiment,resultingin a varietyof new ideas (63). Ourmodels need to be refined; we also need field tests and a greater understandingof the mechanismsinvolved. Whatis encouragingis thatwhen we look at resource variance, it nearly always influences foragingbehavior. The details of risk-

RISK-SENSITIVEFORAGING

387

sensitive foraging require a great deal of elucidation, but its existence is unquestionable.

IMPLICATIONS

The concepts of risk-sensitivedecision-makingcurrentlyarebeing appliedto

a variety of ecological problems. Our sampling will be brief and hardly

exhaustive. Houston & McNamara(33) present several models for optimal dietary choice when minimizing the probabilityof starvationis the strategicobjec- tive. In an environmentwhere two prey types are encounteredsequentially andindependently,the preferencerankingof the preytypes, in contrastto that in the classical model, is not absolute (40). When net energy per item is a randomvariable, the rankingof the prey types and the decision to specialize or generalizedependon the forager'senergyreserve, meansandvariancesof food items' energetic values, and the amountof time left in the day. Caraco& Gillespie (16) analyzechoice of foragingmode as a problemwith risk. The model attempts to explain variation in mobility among certain female orb-weaving spiders duringthe reproductiveseason. When foraging sites varybothtemporallyandspatially,risk-aversioncorrespondsto a mobile strategy(changingweb site each night), andrisk-pronenesscorrespondsto the

sit-and-waitstrategy(stayingat the same site). The optionyieldingthe greater probabilityof successful reproductiondependson the differencebetween the expected prey consumptionand the intakerequiredfor productionof an egg sac.

A number of authors have noted that risk-sensitivity may help explain

aspects of social foraging(9, 13, 20, 21, 22, 57). Whenfood is distributedin patches, the variancein the time an individualspendssearchingfor food can

vary inversely with group size. Similarly, larger groups may reduce the variancein daily food intakewhen food is foundin patchesandforagingtime is constrained(20). Caraco& Brown(14) investigatedthe evolutionof food-sharingin stochas- tic environments. In certain communal species, nonrelatedreproductives foster both theirown andeach other'sdependentoffspring. Sharingfood can reducethe variancein the time spentprovidingthe young theirrequiredfood. But sharingwill be an evolutionarilystablestrategyonly when food densityis high, foragingtime constraintsare sufficientlyrelaxed, and mortalityhazard due to predationis positively correlatedamong the young. The implicationsof risk-sensitiveforagingfor the dynamicsand evolution of plant-pollinatorinteractionsareobvious. The distributionof nectarrewards can influence both the frequencyof floral visitationand the patternof pollen dispersal (61, 72).

388

REAL& CARACO

L.

Real (personalobservation)finds that pollinators'risk-sensitivitycan

dependon the scaling of rewardsizes. The significanceof risk-sensitivityin insect pollinatorsrests critically on the correlationof mean rewardand its variance across floral species. Ott et al (54) show thatrisk-sensitivityinfluencespollinator-mediatedgene flow. Bumblebees (Bombuspennsylvanicus) increased the distance moved between floral visits as the variancein nectarvolume increasedabouta fixed mean volume. Additionally, the variance in flight distance increased as rewardvarianceincreased. By equatingthe variancein flight distance with variancein gene dispersal,Ottet al (54) demonstratedthatneighborhoodsize increases linearly as reward variance increases. Hence, risk-sensitivity in pollinatorsmay be an importantfactorregulatinggene flow among plants. We hope thatwe have provideda simple introductionto both the concepts underlying theories of risk-sensitive foraging and the experimentalwork designed to test those theories. Of course, the most importantevaluationsof the theorywill come fromthe resultsof field studies, manyof which arejust

beginning.

ACKNOWLEDGMENTS

This researchwas supportedby NSF GrantsBNS 8418714 to ThomasCaraco and BSR 8214599 and BSR 8500203 to Leslie Real.

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