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 Stable URL: http://www.jstor.org/stable/2097001 . Accessed: 22/02/2012 22:30
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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 Carolina State University, Raleigh, North Carolina 27695-7617

Thomas Caraco
Departmentof Biological Sciences, State Universityof New York, Albany, New York 12222

INTRODUCTION
Foraging animals confront problems conceptually similar to those facing an economically minded consumer(46, 47), and foragingtheory shares a methodology in common with economics. Indeed, the last 20 years have seen wide application of economic models in biology. A growing consensus suggests thatecological and economic theoriesareultimatelyindistinguishable 30). (6, 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 attributesgenerate higher values are preferredby the consumer over objects generatinglower values. In economics, this index (the 'utility function') is the basic organizing principle (36). Behavioral ecologists use this technique to learn what attributesshould be included in an organism's utility function to determine how various attributes should be combined and weighted, and then to predictchoices by maximizingthe utility functionunder applicable constraints.The organism's utility function is, therefore, both an object of empirical study and a predictive tool. Economic analysis usually stops here, but evolutionary biologists go farther. They assume that the organisms' preferencesare relatedto evolutionaryfitness and thatthe options 371 0066-4162/86/1120-0371$02.00

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REAL& CARACO

more preferredmust lead to greater survival and reproduction.Hence, we hypothesize that the utility function is isomorphic with fitness. This, of course, is an assertion, and one that needs more empirical investigation. The underlyingassumptionsand limitationsof economic optimizationhave been clarified (53), criticized (26), and defended (48). We feel that these techniques, althoughcontroversial,are the best availablefor deducingempirically falsifiable hypotheses based on first principles for behavior. Our theories necessarily examine one (or just a few) phenotypiccharacters in any particular model. Many traits interactively govern survival and reproduction,but we are forced to limit the phenotypic dimensionalityof a of theory if it is to be tested rigorously. However, in our interpretation theory we recognize that single-attributestrategic models concern phenomenaconditioned by other traits and competing selection pressures(11, 42, 53, 59). a Interpreting model for a single trait's adaptivesignificance requiresthat we remainwary of (but not inhibitedby) genetic, environmental,and organismal sources of variation in the characterof interest. We might treat a theory and an organism's behavior like a map and a territory.More formally, we replace a theory's algebraicinterpretation with a probabilisticinterpretation. Many models in behavioralecology, and nearly all models of foraging strategy, can be writtenas questionsof preferenceand choice. In these cases a probabilisticinterpretation a theory means that we of replace a strongutility hypothesiswith a weak utility hypothesis(12, 18, 45). The following example contraststhese alternatives. Suppose an organismmust choose between two options. Let the associated probability densities of benefits be fi and f2. The ecologist constructs a theoretical fitness/utility function W and deduces predictionsby comparing the expected fitnesses E(Wlfi). Letfi Pf2 designatepreferenceforfi overf2. The ecologist seeks to predict preference (or indifference) with the model. If E(WIf,) : E(W If2),then an algebraicinterpretation the model yields a of strong utility hypothesis of the form:
E(W|fi) > E(Wjf2) -* Pr(fi P f2)
=

1.

1.

The strong utility interpretation predicts 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 that the stochasticnatureof selection processes, interactions with other traits, and other factors renderthe organism's behavior less than perfect. The model W still distinguishesany differencebetweenf, andf2, but the predictedresponseto the difference(the traitof interest)is bettertreatedas of probabilistic.This interpretation the model yields a weak utility hypothesis of the form:

RISK-SENSITIVEFORAGING

373 2.

E(WIf,) : E(WIf2)

-*

Pr(fI Pf2) :

1/2.

Iff1 advances fitness more than does f2, there should be a tendency to prefer fl. As the difference between the E(W) values increases, preferencefor the more profitableoption presumablyincreases. The weak utility interpretation maintainsa distinctionbetween the model and the organismand more realistically describesthe consequencesof selection thandoes the determinismof the strong utility interpretation. In this paper we review some models for foraging decisions in stochastic environments.To do so, we must examine both the natureof the stochasticity and the way in which the forager might efficiently respond.

CLARIFYINGRISK
Economists often distinguish between two types of decision-making(2). In the first type of decision the economic agent knows the objective probability distributionscharacterizingoutcomes for feasible actions correspondto conditions 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, organisms with no such knowledge, (or an organism possessing only subjectiveestimates of the distributions)face conditions of 'uncertainty.'To predict behavior we must assume some form of underlying probabilistic structure.Thus, economists analyze uncertaintyin the same manner as conditions of risk. However, the conditions are quite distinct; some aspects of economic behaviorarguablyresult from uncertainty but not from risk (38). From a biological perspective, we emphasize that natural selection operates on objective probabilities, but the organism may still be deciding subjectively (at least during an initial sampling period). The ecological literaturementions differentkinds of risk, and some confusion 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 that a discrete, randomoutcome (the individual survives or is killed by a predator)is replaced by the population's average mortality hazard due to predation. The model organism responds not to of but probabilitydistributions to fixed attributes patches, habitats,etc. In any our discussion of risk concernsan organism'spreferencesover probabilcase, ity distributions. As indicated above, a forager in a stochastic environmentmay face two distinct but complementary problems(23, 69). First, the organismmust learn the reward probability distributionsassociated with different behaviors (a problemof information),and then it must select a strategyfor exploiting those distributions(a problem of risk).

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Informationproblemsare usually analyzedwith Bayesian models in which the organism modifies its estimates of probabilitiesbased on its experience while foraging. For example, Green (27, 28) assumes that a bird searches a 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 probability that a bit contains a prey item), total prey per patch is a binomial variate. Patch quality itself is a Beta randomvariable. The optimal Bayesian bird leaves a patch when it has found only k prey after sampling tk differentbits. The Bayesian dimensionis explicit since the decision to leave a patch dependson experiencethereandthe overallpatternof patchquality(27, 28, 49, 51). Analyses of problems of information have generated a variety of new hypotheses differing qualitatively from the results of corresponding deterministicmodels. For example, consider Clark& Mangel's (21, 22) theory for the evolution of group foraging, or Real's (62) model for habitatselection in fish. Houston et al (31) and Krebs et al (40) have reviewed the theory for problems of information.Experimentalresearchon questions of 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 subjected to a reasonablenumber of tests.

RISK-SENSITIVITYAND FORAGINGBEHAVIOR
Most theories for risk-sensitive foraging propose decision criteria that explicitly or approximatelyinvolve an interactionbetween the mean and variance of food consumed or the time spent acquiringrequiredenergy (8, 9, 32, 50, 57, 58, 59, 69). These criteriaarise naturallywhen the relevantprobability distributions are functions of two independent parameters. However, maximizing the expectationof a randomvariable(withoutexplicit consideration of the variance) will be appropriatein certain simple problems (13). Suppose the randomoutcome of a foraging decision follows a one-parameter distribution,so that all cumulativeprobabilitiesare specified by the parameter's value. If fitness is maximal when the probabilityof starvation(or other penalty) is minimal, rankingthe means can be sufficientto solve the problem. Let the i-th option imply that identical food items will be consumed at constantprobabilisticrate Ai. If T is the time available, andX is the total food consumption (a discrete, nonnegative random variable), then choice of the i-th option means that X will be a Poisson variate with expectation AiT. Suppose the foragerstarvesor fails to reproduceif X ? R. We hypothesize that selection favors minimizingPr(X? R), so thatfitness is a step functionof total food consumption. The best strategy chooses Ai according to:

RISK-SENSITIVE FORAGING
R

375

min Pr(X ? R1A)

min e

-A

(AiT)xlX!

3.

= minr(R + 1, AiT)/R!, where

F(R + 1, AiT) =
fAT

4.

e-ttRdt.

5.

Equation (5) indicates the equivalence between minimizing Pr (X? R) and maximizing AiT = E(X) in this simple example. A useful generalizationof this sort of probleminvokes the orderrelationship'stochasticallylarger' (13, 65). Let XI and X2 be discrete nonnegative random variables where XI is stochasticallylargerthanX2 (denotedXI ' ST X2). Then, by definition (65):
Pr(XI > R) ? Pr(X2 > R) for all R. 6.

Taking complements in (6), we have

Pr(XI ? R) ? Pr(X2 ?R) for all R. 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 outcomes Xi can be rankedby the order relationshipstochastically larger, the chance of starvationcannot increase (and usually 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 intake follows a normal distribution, the probabilityof starvationdepends on combinedeffects of both mean and variance. Consequently, a useful theory for risk-sensitive foraging requires more than ranking strategic options by their associated averages. effects, let W(X)map energy intakeinto fitness. To examine mean-variance In theory, some W specifies present and expected future survival and for reproduction any X, but we requiremore tangiblecurrenciesfor 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

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nonbreedingseason. Therefore, we need not always projectvery far into the future when hypothesizing a form for W(X). For some organisms, W can be taken as survivalover a single day (18, 19, 57, 67, 69). Let X now represent total daily energy intake, a continuous duringthe randomvariable.X is a sum acquiredover n foragingopportunities normalityby time availablefor feeding. For sufficientlylarge n, X approaches the central-limittheorem (8, 67). We let E(X) = , and let V(X) = (J2, and take Pr(X - R) as the probabilityof starvation. Stephens & Charnov(69) assume selection acts to minimizethe probability of starvation,and they identify the consequences in a useful manner.Since X
approaches normality, the distribution of z [where z = (X - p)Io-] approaches

normal. Then minimizingPr(X 2 R) is equivalentto minimizing: the standard

Pr[z ' (R - O)IMi
=

4(ZR)

9.

Hence the z-score model. Equation9 reveals that dJ(zR)hd9p < 0. For given or, an increase in mean deviation rewardwill obviously be favored. The effect of varyingthe standard depends on the difference between the requiredand expected intake, R - ,. If , > R, the foragercan expect to surpassits requirement,so that its energy budget is positive (10, 12). In this case do(zR)ld/o > 0; for a given , an increase in rewardvarianceincreasesthe chance of starvation.Consequently, we anticipaterisk-aversionwhen ,u > R (10, 18, 19, 32, 57, 69). If , < R, 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-proneresponse to benefit variancewhen ,t < R (12, 19, 57, 69). Suppose two alternativeforaging options yield respective total benefits X1 and X2. The Xi are random variables with V(X1) < V(X2). A risk-average forager will prefer X1, because its variance is lower, unless E(X2) is sufficiently largerthan E(X1). A risk-proneforagerwill preferthe more variable X2, unless E[X1] is sufficiently larger than E[X2]. The preceding analysis predicts that a forager's expected energy budget governs its response to risk physiological requirement,and that when the animalmust satisfy a short-term reward mean and variance both will influence choice over two-parameter distributions of 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-score model predicts decreasing risk-sensitivity (see below), so that the way in which mean and variancecollectively govern preferencedepends not only on the sign of (, R), but also on the value of ,u. When W(X) is survival over a single day, all values of X such thatX > R

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 continuous fitness 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, survivorshipshould always increase with energy intake, so we assume W' > 0. This assumptionshould hold unless excess weight imposes a mortalityhazard(44). Survivingwintercould imply thatthe a foragermonitorsan averagedaily requirement; reasonablepossibility is that energy intake balances expected 24-hour expenditures (19). We let R* a representthe averagedaily requirement; total energy intakeof at least yR*is required over y days (-y > 1). For X well below R*, survival is low (but R*, immediate starvationneed not be certainsince y > 1). As X approaches survivorshipincreaseswith increasingrapidity.Therefore,W is convex (W" > 0) for X < R*. Above R* each additionalamount of energy quite likely decreases in value to an adequatelyfed animal (58), but energy consumed beyond R* can be carriedover to the next day (68). Therefore,W is concave (W" < 0) for X > R*. As discussed below, this form for the fitness function predictsrisk-pronepreferencesfor X < R*, and risk-aversepreferencesfor X > R*. When fitness cannot be approximatedby the individual's short-termsurvival or reproductivesuccess, the convex-concaveform for W may not apply. For example, colony-level fitness in social insects might suggest that W(X)is strictly concave for the individual forager, since individual physiological requirementsare presumably less 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 that body size in birds and mammalsshould correlatepositively with the length of time an individual can survive without food (7, 25). Therefore, the time horizon (-ydays) over R* which the average requirement is defined could easily increase with 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 theoretical objective becomes maximizationof the expected time until starvationoccurs. Given a set of assumptionsconcerningprey profitabilitiesand encounterswith prey, they find that a foragershould always take a prey item if it yields an increase in total stored energy. Under certain conditions, this strategy might imply strict risk-aversion (Houston, personal communication). Therefore, larger animals might adhereto risk-aversion,providedthat largerbody size tends to energetic requirements.If the shape of W(X) free the foragerfrom short-term does indeed depend predictably on body size, then the regulatory models proposed by Staddon(66) may prove valuable to both ecologists and operant psychologists.

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REAL& CARACO

Returningto foragers with short-termrequirements,suppose that W(X) is convex-concave with an inflection point at X = R*. If we hypothesize an analytical form for W, the expected fitness associated with the i-th strategic option is:
Ei[W(X)]
=

f W(X)f1(X) dx,

10.

wherefi(X) is the probabilitydensity of energy intakeresultingfrom choice of the i-th option. The best decision maximizes expected fitness. However, we often will want a more general procedurethat does not require specifying W(X) analytically. A simple alternativeis expanding W(X) about A with a Taylor series approximation(1, 34, 58). Expanding through the third derivative and then taking expected values, we have: E[W(X)]
W(g) + (1/2) W" (i)
c.2

+ (1/6) W'.'(..)

3,

11.

symmetricallyabout where 3 is the skew of X, E[(X - 3]. If X is distributed 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 contributionto 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 enhance expected fitness. The second term in Expresto (I) o-2. If ,u < R*, then W" > 0 and expected sion 11 is proportional W" fitness increases as reward variance increases [by Jensen's inequality: (8, 24)]. Hence, the forager should be risk-pronewhen expecting an energetic deficit. If ,u > R*, then WI" < 0 and expected fitness decreases as o-2 increases. Therefore, risk-aversionfollows from an expected energetic surplus. Note that the simplerstep functionmodels generateessentially the 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 risksensitivity as constantor variable.For simplicity, we restrictour discussionto risk-aversion;for a broadertreatmentsee Caraco & Chasin (15). Constantrisk-aversionfollows when a given o-2 depressesexpected fitness by the same amountat any level of ,u, meaning that W" does not depend on X. Decreasing risk-aversionfollows when the negative effect of a given -2 decreases as ,u increases, implying that WI"(,) declines as , increases. For I increasingrisk-aversiondW"(g)/ld > 0, and a given o 2 exerts the opposite

FORAGING 379 RISK-SENSITIVE effect on expected fitness. Decreasing risk-aversionhas the greatestintuitive appeal. We can portrayconstantand variablerisk-aversionvia Pratt's(55) index of 'local risk-aversion':p(X) = - WI/W'I. Since W' > 0, p(X)>0 for all forms of risk-aversion.Under constantrisk-aversion,dp(X)/dX= 0. For decreasing risk-aversion, dp(X)/dX < 0; for increasing risk-aversion, dp(X)/dX > 0. 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, from Equation12, to determine the sign of WI'I and, hence, the effect of skew on expected fitness. Caraco& Chasin (15) show that positive skew tends to advance expected fitness when risk-aversionis either constantor decreasing. Skew in X may arise from rare events or from uniformlyskew rewardsat individualforagingbouts (15). An efficient forager might respond to reward skew, but responses to mean and variance presumablydominate in nature. If we truncateExpression 11 at the second moment, we have a variance discounting formula:E(W) W(,u) + (1/2) W" (,) o-2. Without specifying W(X), we might take WI'/2 as a 'constantof risk-aversion'(60, 64). That is, of we might predictconstantrisk-aversionby assumingW" is independent X. to However, as an approximation a postulatedanalyticalform for the fitness function, variance discounting can accommodateconstant or variable risksensitivity. For instance, if we assume that W(X) = log X and evaluate this function accordingto the Prattmeasureof local risk-aversion,we see that the coefficient of risk diminishes: p(X)
p'(X)
= = -

W"/W' = X > 0 1/X2 < 0.

If we assume that W(X) is quadratic, i.e. W(X) = aX - bX2, then the organism will show increasingrisk-aversion.Alternatively,for W(X) = a e-bX [a form used by Caraco (8)] then risk-aversionwill be constant. Pratt (55) catalogs a variety of different utility/fitnessfunctions that will generate different types of risk aversion. Analysis of the indifference curves for the different fitness functions will reveal the implicit response to increasing expectation (Figure 1). Curves bending upward correspond to fitness showing diminishing risk-aversion. Straight lines correspond to constant risk-aversion. Strictly concave indifference curves indicate increasing risk-aversion. The Taylor Series (Equation 11) can be used to approximateany of these

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REAL & CARACO

a
(N

Mean

(,u)

Figure 1 Generalizedindifference curves for three different specified fitness functions W(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, showing diminishingrisk-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 approximation the second moment at requires either (a) the variables are normally distributed, or (b) W(X) is quadratic.The approximation only be exact then if we admitthe seemingwill ly unreasonableassumptionof increasing risk-aversion. Nonetheless, as an approximationthe variance discount model 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 variance discount approximationwould be:

RISK-SENSITIVEFORAGING E[W(X)] = log , 1/2 o-24lr2,

381

which clearly has a diminishing coefficient of risk. Ourreview of risk-sensitivityhas mentionedonly staticmodels. If a forager can switch among available options during the 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 switching between two options with identical mean rewardratesbut with differentlevels of rewardvariability.The foragershould use the option with the lesser variability as long as the animal expects to surpass its daily requirement.However, if the forager's energetic condition ever indicates that a deficit is more probablethan an excess, the animal then should immediately switch to the more variable option. The best dynamic policy shows a strong similarity to 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 theoretical predictions in light of empirical results.

EMPIRICALRESULTS
To investigate risk-sensitive foraging experimentally, the investigator controls the rewarddistributions availableto an animal. One class of experiments examines preferenceover rewardvariance when mean rewardsare fixed. A second class tests predictedtrade-offsbetween mean and varianceby simultaneously changing both parameters.

Responses to Variance with Fixed Means

The most direct test for risk-sensitivity lets a forager choose between two resources or feeding stations. One resource is held constant. The other resourcevaries randomlyover space or time, but its expected value equals the constant reward. The organism selects the amountof time or effort allocated to each resource. The null hypothesisis indifference;any significantdeviation from equal use of the two resources demonstratesrisk-sensitivity. Real (60) constrained bumblebees (Bombus sandersoni) to an artificial patch where an equal number of yellow and blue flowers were arrayed randomlyon a large grid. A known quantityof 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, and the rest contained6 ,il of nectar. Approximately85% of all visits were to the constantreward,a responseindicatingrisk-aversion.The bees still preferred the constant reward when all flowers contained at least 0.5 ,ul.

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REAL& CARACO

Hence the observed risk-aversionis clearly more than avoidance of a floral type that sometimes provides no reward. Real (60) also found that wasps (Vespula maculifrons) foraged riskaversively in the same patch of artificialflowers. But the wasps' preference for the constant reward appeared weaker than that observed in the bees. Unlike bumblebees, the wasps are carnivorousand do not requirenectar for reproduction.The difference in choice probabilitiescould mean that organisms are more sensitive to variancein those resourcesmore criticallylinked to reproduction. Waddingtonet al (71) demonstratedrisk-aversionin a second species of bumblebee, Bombus edwardsii. In these experimentsreward variation was imposed temporally; bumblebees apparently respond to both spatial and temporal patternsof reward variance in a risk-averse manner. Wunderle & O'Brien (74) studied hand-rearedBananaquits (Coereba flaveola) foraging on artificial flowers of two different colors. 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 experiencedbirds chose the constantreward more than other subjects did. In a second experiment,Wunderle& O'Brien (74) showed thatthe Bananaquits respondedsimilarly when resourcequality, ratherthan quantity,varied randomly. Wunderle & O'Brien filled every flower of both types with the same volume of nectar and made sugar concentrationthe random variable. The birds again preferredlesser variance, and measuresof their risk-aversion did not differ significantly from those observed in the manipulation nectar of quantity. Risk-sensitivity in small granivorousbirds has been explored extensively by Caraco(10, 11, 12, 14, 19). A birdis confined in a large aviarywhere two feeding stations are separatedby a partition. At each experimentaltrial the bird leaves a perch on the aviary's centerline and visits one of the feeding stations where the animal obtains a known numberof millet seeds (Panicum miliaceum). The subject's expected daily energy budget can be manipulated by adjustingthe length of preexperimental deprivationand the average feeding rate which the bird experiences during an experiment. The daily physiological requirement(the food intake balancing all energetic costs) is estimated from analyses of oxygen consumption or food intake under ad lib availability. Caraco et al (19) examined risk-sensitivityin yellow-eyed juncos (Junco phaeonotus) at both positive and negative expected energy budgets. The birds faced choices between a constant numberof seeds and a randomnumberof seeds; the mean of the variable reward equalled the constant reward. The juncos preferredthe constantrewardwhen their energy budget was positive

FORAGING 383 RISK-SENSITIVE but switched to preferencefor the variablerewardwhen their energy budget was negative. The shift between risk-averseand risk-pronepreferenceswas independentof the order of treatmentsan individual experienced. Similar experimentswith dark-eyedjuncos (Junco hyemalis) yielded similar results;energy budgetspredictedpreferenceover rewardvariance(10). In addition, Caraco found that indifference to reward variance was the most common result for 'balanced' energy budgets. This was an intermediate condition where the feeding rate during an 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 experiments that revealed risk-aversionin juncos. White-crowned sparrowsweigh 50% more than dark-eyedjuncos, but their preference behavior did not reveal a significant interspecific difference in risk-aversion. Most small birds are constrainedby daily energy requirements during the winter, so that similar responses to 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 variation in the time horizon over which foragers attemptto regulate energy intake relative to expenditures. Experimentsreviewed to this point all involve choice between a constant and a variablereward. But animalsmust discriminateamong, and strategically use, differentvariablerewardsif risk-sensitivityis to influence behaviorin a significant way. Caraco (12) reports that white-crowned sparrows chose between two variable rewards (random numbers of millet seeds) with the same expected value. The birds preferredthe smaller or largerreward standard deviation according to their expected energy budget. The transitionfrom risk-averseto risk-pronepreferenceshas been observed in two other experimentalsystems. 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;expected rewards were identical. When the shrews were fed at a rate below their physiological requirement, they preferredvariability. However, they were risk-averse at positive energy budgets and chose the constant reward on 74% of the experimental trials. In a clever extension of their work, Barnard& Brown (4) presented the same choices to shrews under conditions of apparentresource competition. competitor,since the When a competitorwas introduced(actuallyan apparent introducedanimalwas not allowed to feed), subjectshrewswere indifferentto reward variance. Competitioneliminated evidence of risk preferencein the shrews, but the adaptivesignificance (if any) remainsa mystery. Kagel et al (35) suggest an economic interpretation.

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Moore & Simm (52) linked a switch between risk-averse and risk-prone foraging preferences to the annual cycle of the migratory yellow-rumped warbler (Dendroica coronata). Energy requirementspeak during the premigratoryperiod. The birds must deposit fat sufficientto satisfy the demands of migratory travel. 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. birds not in premigratorydisposition) were risk-averse when presented the very same choices. Furthermore,the migratorybirds' preferences changed from riskprone to risk-averse after they reached maximal body size. Note that the warblers' behavior showed both preferencefor and aversion to rewardvariance, but their daily energy budgetwas never negative. That is, the transition in risk-preferencewas based on more than a comparisonof daily intake and daily expenditure.When the birds' weight was less than the migratorylevel, they preferredthe variable reward. But they became risk-averse when they to attained the weight appropriate the physiological requirementsof migration. In terms of our hypotheticalW(X), this suggests that the average daily requirement(R* in the discussion above) varies seasonally in yellow-rumped warblers in accordancewith the demands of their annual cycle. Daily energy budgets predict the nature of risk-sensitivity in organisms whose fitness should be proportional to short-term survivorship: small, nonbreedingbirds and mammals. But some other results indicate that risksensitivity is a more complex phenomenon,and we summarizethose observations here. Recall that Barnard& Brown (4) found that common shrews' sensitivity to risk depended on their expected energy budget, but their risk-sensitivity disappearedwhen an apparentcompetitor was introduced. Shrews usually forage solitarily, but the result may suggest that direct competitive interferenceor dominance interactionscould influence foraging preferencesin nature. K. D. Waddington,B. Heinrich, & L. Real independentlyhave attempted to induce risk-pronebehaviorby deprivingbumblebeesof food, but the bees remainedrisk-aversetowardvariancein rewardsize (personalcommunication and personal observation). As we indicated above, an individualbee's food intake may always map into colony fitness in a concave manner(promoting risk-aversion). A second adaptive explanationproposes that bumblebees reduce their energetic expendituresby lowering their metabolicrate when food is scarce, so that risk-pronenessoffers no strategicadvantage.Of course, the mechanical rule 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 resources with large reward variances. For still anotherview, see Wells & Wells (73).

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Battalio et al (5) found thatlaboratory exhibitedrisk-aversepreferences rats over randomly sized rewardswhether their energy budgets were positive or negative. As previously discussed, a large animal's survival is seldom constrainedby immediateenergy requirements,and risk-aversionbecomes more likely as the time horizon for regulating food consumption lengthens with increases in body size. Large animals can depend on energy stores to moderate the influence of temporal fluctuationsin food availability. Therefore, their risk-sensitivityneed not be attuneddirectly to 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 provides the same fixed rewardsize. One alternativerewards the animal after a fixed delay elapses between choice and consumption;the other alternativeimposes a variable delay (with expected value equal to the fixed delay). Most results indicate strong preference for the variable delay (23, 29, 37, 56). The subjects (usually pigeons, Columbia livia) were deprived 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 manner from reward size. If foragers discount future rewards, the economic model analyzed by Kagel et al (35) predicts that a variable delay will always be preferredover its mean. For anotherdiscussion of responsesto energeticvalues vs responsesto delays, see Staddon (66).

Mean-Variance Trade-offs
The models discussed above predict an interactionbetween the expectation and variance of a reward distribution. For example, a risk-averse forager prefers large means and small variances, so that its preferenceswill reveal a trade-offbetween mean and varianceunderappropriate conditions. The exact natureof the predictedtrade-offis model specific, but most work in this area has realistically been limited to a comparisonof constant and variable risksensitivity. Caraco et al (19) studied certaintyequivalents for rewarddistributionsin foraging yellow-eyed juncos. That is, they located the constant reward for which a bird was indifferentbetween that constant number of seeds and a given variable reward. Under risk-aversion, the certainty equivalents were 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 decreasing risk-aversion.Stephens & Paton (70) have demonstrated decreasing risk-aversionin rufoushummingbirds (Selasphorusrufus). Via an indirect

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statistical method, Battalio et al (5) interpretlaboratoryrats' preferences as examples of decreasing risk-aversion. The way a risk-averseforagertradesoff mean and variancecan be studied by constructing indifference curves in the mean-varianceplane. However, only two such studies have been conducted to date. Real et al (64) estimated mean-variance indifference curves from the foraging preferencesof captive bumblebees (Bombuspennsylvanicus). In an artificial patch, flowers of one color provideda constantnectarvolume. The variance of the other floral type was fixed, and its mean was increased or decreaseduntil individualbees were indifferent(i.e. until the constantreward became a certaintyequivalentfor the variablereward). Next, the varianceof the variable reward was increased and its mean then was adjusteduntil the bees' foraging choices showed indifference again. For a single constant reward, the procedureidentifies three sets of responses to variablerewards:a set with each element preferredover the constant reward, a set where the constant rewardis preferredover each element, and an indifference set with elements preferredequally to the constantreward.Regression analysis of the of trade-off indifferenceset reveals the slope and curvature the mean-variance (17, 64). Real et al (64) completed four experiments of this sort. In three experiments, they detected a significant trade-off between mean reward and characterof the trade-offwas sensitive to rewardvariability.The quantitative a variety of ecological attributes,including the patchiness and color of the floral types. Two of the three significant trade-offs indicated constant riskaversion; the third significant result suggested either constant or decreasing
risk-aversion.

Caraco& Lima (17) performedsimilarexperimentswith dark-eyedjuncos. In each of two series of experiments, they found a significant trade-off between mean reward and rewardvariability. Both constant and decreasing risk-aversionaccounted equally well for the estimated indifference curves. The experiments discussed in this section collectively reveal that riskaverse foragers clearly do trade off reward variance against mean reward. emerges as the domiHowever, neitherconstant-nor variable-risk-sensitivity nant response. Recalling our earlier comments on algebraic vs probabilistic interpretationof a theory, we feel that a qualitative demonstrationof a trade-off is the biologically significant result. Both theoreticaland empiricalwork on risk-sensitiveforagingbegan only a few years ago. But there alreadyhas been a healthyexchange between model and experiment,resulting in a variety of new ideas (63). Our models need to be refined; we also need field tests and a greater understandingof the mechanisms involved. What is encouragingis that when we look at resource variance, it nearly always influences foraging behavior. The details of risk-

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

IMPLICATIONS
The concepts of risk-sensitivedecision-makingcurrentlyare being applied to 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 strategicobjective. In an environmentwhere two prey types are encounteredsequentially and independently,the preferencerankingof the prey types, 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 generalize depend on the forager's energy reserve, means and variancesof food items' energetic values, and the amount of time left in the day. Caraco& Gillespie (16) analyze choice of foragingmode as a problemwith risk. The model attempts to explain variation in mobility among certain female orb-weaving spiders during the reproductiveseason. When foraging to sites vary both temporallyand spatially,risk-aversioncorresponds a mobile correspondsto the strategy(changingweb site each night), andrisk-proneness sit-and-waitstrategy(staying at the same site). The option yielding the greater dependson the difference between the probabilityof successful reproduction expected prey consumptionand the intake requiredfor 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). When food is distributedin patches, the variancein the time an individualspends searchingfor food can vary inversely with group size. Similarly, larger groups may reduce the variancein daily food intakewhen food is found in patchesand foragingtime is constrained(20). Caraco& Brown (14) investigatedthe evolutionof food-sharingin stochastic environments. In certain communal species, nonrelated reproductives foster both their own and each other's dependentoffspring. Sharingfood can reduce the variancein the time spent providingthe young theirrequiredfood. But sharingwill be an evolutionarilystable strategyonly when food density is high, foraging time constraintsare sufficiently relaxed, and mortalityhazard due to predationis positively correlatedamong the young. The implicationsof risk-sensitiveforaging for the dynamics and evolution of interactionsare obvious. The distribution nectarrewards of plant-pollinator can influence both the frequencyof floral visitation and the patternof pollen dispersal (61, 72).

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L. Real (personal observation) finds that pollinators' risk-sensitivity can depend on the scaling of rewardsizes. The significance of risk-sensitivityin insect pollinators rests critically on the correlationof mean reward and its variance across floral species. Ott et al (54) show thatrisk-sensitivityinfluencespollinator-mediated gene flow. Bumblebees (Bombus pennsylvanicus) increased the distance moved between floral visits as the variancein nectarvolume increasedabout a fixed mean volume. Additionally, the variance in flight distance increased as reward variance increased. By equating the variance in flight distance with that variancein gene dispersal, Ott et al (54) demonstrated neighborhoodsize increases linearly as reward variance increases. Hence, risk-sensitivity in pollinators may be an importantfactor regulatinggene flow among plants. We hope that we have provideda simple introduction both the concepts to underlying theories of risk-sensitive foraging and the experimental work designed to test those theories. Of course, the most importantevaluationsof the theory will come from the results of field studies, many of which arejust
beginning.
ACKNOWLEDGMENTS

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