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Distinguishing between ‘preference’ and ‘motivation’ in food choice: an example from insect oviposition
Anim . Behav ., 1992,44, 4 6 3 --471
Distinguishing between `preference' and `motivation' in food choice : an example from insect oviposition M . C . SINGER, D . VASCO, C . PARMESAN, C . D . THOMAS* & D . NGt Department of Zoology and Division of Biological Science, University of Texas at Austin, Austin, TX 78712, U .S .A . (Received 12 April 1991 ; initial acceptance 26 April 1991 ; final acceptance 7 December /991 ; MS. number.• A5881)
Abstract . Variation among individuals in acceptance of a second-ranked food resource could be caused either by variation in strength of `preference' for the top-ranked over the second-ranked resource type, or by variation in the general readiness to feed . This distinction is important in models of diet evolution . Of the two traits, preference is the more likely to show additive genetic variation and hence be subject to evolutionary change . In the checkerspot butterfly, Euphydryas editha, changes in readiness to oviposit (abbreviated as oviposition `motivation') mediate the relationship between host preference, host encounter rate, and realized diet, and thereby influence the strength of selection on preference . Definitions of acceptance, preference and motivation are given and applied to oviposition behaviour of herbivorous insects . From these definitions, operational measures of these traits are developed for E. editha . These operational measures are then used to investigate a difference between two E . editha populations in acceptance of a second-ranked host species . The results of this study show that this difference was caused partly by variation of preference and partly by variation of motivation . The difference in motivation probably stemmed from the absence of the most-preferred host from one of the study sites, resulting in prolonged search, reduced frequency of oviposition, and higher mean motivation at this site .
Oviposition decisions by herbivorous insects are food choice decisions . Some attempts to model these decisions have met with scepticism from students of vertebrate foraging . For example, Stephens & Krebs (1986, pp . 126-127) doubted whether Jaenike's (1978) insect-based model used appropriate currency, and suspected that insect oviposition decisions were `only superficially similar to foraging decisions' . To understand insect oviposition better, and to incorporate it into ecological and evolutionary theories of foraging, we need both more explicit insect-based models and clearer definitions of terms that describe insect behaviour . Here, we suggest general definitions of 'acceptance', `preference' and `motivation to oviposit' for herbivorous insects . We then develop and use operational measures of these traits for our own study insect, the checkerspot butterfly, Euphydryas editha . Separation of these three concepts in a
behavioural model allows us to describe and interpret the suite of natural responses to host plants that we see in our study populations . General Definitions Acceptance
When a potential host is encountered, an insect may respond positively by proceeding to the next stage in the sequence of oviposition behaviour, or negatively, by failing to do this . We describe these alternatives as `host acceptance' and `host rejection' (Singer 1986; Courtney et al . 1989 ; Mangel 1989) . Motivation
Because of past controversy (Kennedy 1987 ; McFarland 1987 ; Drickamer & Vessey 1992), `motivation' should be used non-anthropomorphically . We define an insect's oviposition motivation as a non-specific readiness to oviposit . By 'nonspecific' we mean that it is not determined by the nature of the potential hosts that are encountered .
*Present address : NERC Centre for Population Biology, Imperial College, Silwood Park, Ascot, Berkshire SL5 7P1', U .K .
+Present address : Pharmaco, 4009 Banister Lane, Austin, TX 78704, U .S .A . 0003 3472/92!090463+09$08 .00/0
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Although the range of hosts that would be accepted (if encountered) may depend on the insect's current motivational state, we do not describe the insect as possessing separate motivations for each host type . Various authors have suggested that an insect's motivation to oviposit is controlled by an internal factor that tends to increase either with passing time (Singer 1982 ; Roitberg & Prokopy 1983 ; Pilson & Rausher 1988), or with increasing eggload (Fitt 1986; Courtney et al . 1989 ; Odendaal 1989), or with both (Mangel & Roitberg 1989) . However, in no case do we know the nature of this internal factor or the causes of its fluctuations . While this ignorance persists, attempts to develop operational estimates of motivation to oviposit will depend at least partly on untested assumptions . Preference We define an insect's oviposition `preference' as the set of relative likelihoods of accepting particular hosts that are encountered . In many species, the likelihoods of accepting different hosts increase at different rates with rising motivation, i .e. as the insect becomes more likely to oviposit in general . When this occurs, the relative likelihoods of accepting different hosts also change with motivation . Thus, comparisons of preference between different individuals must be made at some known or controlled level of motivation across all test insects (Singer 1986) . In our own work, we estimate preference from the changes in acceptance that occur as motivation rises .
fully, probes with its ovipositor and then holds it motionless and extruded for at least 3 s, its behaviour is recorded as acceptance . Conversely, a rejection is recorded if the test butterfly fails to perform this behavioural sequence after 5 min on the plant . Since several seconds normally elapse between acceptance (as measured here) and actual oviposition, an experimenter can observe acceptance, then remove the insect from the test plant without allowing it to lay eggs . By this means . acceptance can be recorded without the decrease in motivation that would follow actual oviposition . Preference Our operational measure of preference stems from the behaviour of E. editha in our study populations, where each female normally undertakes one oviposition search per day . If the insect fails to encounter an acceptable plant at the beginning of its search, oviposition is delayed . While this delay continues, the range of plants that would be accepted if encountered expands with the passage of time (Singer 1982) . Eventually, oviposition usually occurs and the search ends . If the search is unsuccessful, it recommences on the following day . We divide preference into two components . 'Preference rank' is the order in which plants become acceptable to an insect as time passes . `Specificity of preference', which we abbreviate as `specificity', is the set of strengths of preference for particular hosts . So, if two insects prefer the same hosts, but differ in the strength of preference, they are said to differ in specificity but not in rank (cf. Wiklund 1981) .
Operational measures Acceptance
Preference rank
There are three phases in acceptance of a plant by E. editha . In the first, the insect alights in response to visual stimuli (Mackay 1985) . In the second, it tastes the plant with its specialized fore-tarsi and responds to acceptable taste stimuli by curling its abdomen, and extruding its ovipositor (Singer 1986) . In the third phase, the insect probes with its ovipositor until a surface with acceptable physical characteristics is encountered . In this paper, we are concerned with the response to taste that follows alighting . Euphydryas editha behave naturally when manipulated . Acceptance can be assessed by placing a butterfly on a plant and observing its behaviour. If the test butterfly curls its abdomen
Singer (1982) repeatedly placed female E . editha on two hosts in alternation and prevented them from ovipositing by removing them from plants after each acceptance . Each plant was initially rejected, became acceptable to an insect at a particular time, and then remained acceptable until oviposition actually occurred . However, different plants became acceptable at different times . The following sequences were observed : (1) REJECT plant A ; REJECT B ; ACCEPT A ; REJECT B ; ACCEPT A ; REJECT B ; ACCEPT A ; ACCEPT B . (2) REJECT A, B, A, B, A ; ACCEPT B, A, B, A . Sequences of type (1) gave a direct measure of preference rank, the order in which plants became
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Figure 1 . Changes over time in the probability of accepting two hosts, in three different butterflies that all share the same rank order of preference (A > B) and that are tested simultaneously . Thick lines show times at which the probability of accepting host A is the same as that of accepting host B. DP indicates the discrimination phase when one host is accepted and the other rejected . If host A is really the most-preferred of all possible hosts, then the time period before its acceptance is the refractory phase RP as indicated . These refractory phases extend back to ovipositions on the previous day, the times of which are not shown . Because we do not show entire refractory phases (RPs) we do not imply that RP3 is actually shorter than RPI or RP2 as it appears to be in the figure . acceptable (in this case, A > B) . In those of type (2) the plants became acceptable so close to the same time that it was impossible to tell whether one became acceptable before the other . In this case the insect was classified as without preference, although it may have had a preference too slight to be detected . The manipulative preference-testing technique used in this work depends on the assumption that the current likelihood of accepting each host is not influenced by previous encounters with either the same or a different host. This assumption appears to be justified for E. editha (Singer 1986 ; Thomas & Singer 1987) . In insects that oviposit frequently, preference rank can be determined from relative oviposition rates on different resource types that are presented simultaneously (Wasserman & Futuyma 1981 ; Jaenike & Grimaldi 1983 ; Thompson 1988) . Preference spec f city We estimate specificity from the length of the time interval or 'discrimination phase' during which one host is accepted and the other rejected . Figure 1 depicts two insects that differ in specificity . The existence of such discrimination phases has been predicted theoretically (Jaenike 1978 ; Ward 1987 ; Mangel 1989) . In E. editha, we cannot calculate the exact length of the discrimination phase,
but we can obtain maximum and minimum values (Singer 1982) . In practice, we use the minimum length of the discrimination phase, the time from first acceptance of the higher-ranked plant until the last rejection of the lower-ranked plant . The reason for doing this is that maximum values are only obtained if the lower-ranked plant is actually accepted (Singer 1982) . By requiring maximum (or midpoint) values we would disproportionately exclude data from those insects with high specificity that escaped or died before they accepted the lowerranked plants . This effect is especially important when insects are tested for a fixed period (2 days in the present study) . Measures of minimum discrimination phase are truncated at the length of this fixed period, but use of this minimum value allows inclusion of all insects in the data set . Motivation to oviposit The simplest way to classify motivation would be as a binomial variable : an insect that is motivated to oviposit accepts its most-preferred host, while an unmotivated insect rejects it . However, this would be an over-simplification, because the underlying (and presently unknown) physiological variable is likely to be continuous . If we consider motivation a continuous variable, we can use acceptance of the most-preferred host as an easily-measured reference point by which to compare individuals .
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Drickamer & Vessey (1992, page 292) argue that the `black box' concept of motivation can be discarded when the underlying physiological variables become known . We cannot yet do this with respect to insect oviposition, because we are still ignorant of the physiological basis of changing responsiveness . Here, we discuss two operational measures of motivation that differ in whether the `internal physiological variable' measures the passage of time, or the accumulation of eggs. We use hypothetical data sets, in which the most-preferred host is the same for all butterflies . We designate this mostpreferred host as `host A' and the second-ranked host as `host B' . All our hypothetical test butterflies begin the experiment with a refractory phase during which both host species are repeatedly rejected . At some time, host A is accepted and subsequently remains acceptable . At some later time, host B is also accepted . First, we examine our hypothetical data set using the passage of time as the motivation criterion . The motivation levels of butterflies I and 2 at 1400 hours (Fig . 1) are the same as that of 3 at 1200 hours, when host A is first accepted . We can compare motivation at other times by making the simplifying assumptions that all butterflies respond to time in the same way, and that the rate of increase of motivation is the same in different test butterflies that are being compared simultaneously . These assumptions enable us to classify butterfly 3 of Fig . I as having higher motivation than butterfly 2 throughout the test period because 3 was prepared to lay eggs on the most-preferred host (A) earlier in the day . At 1600 hours the behaviour of butterflies 2 and 3 towards plants A and B is identical . What, then, is the use of classifying 3 as more highly motivated than 2 at this time? Suppose we test a third plant, C, that is ranked below B by both butterflies . Our model predicts that butterfly 3 will be more likely than 2 to accept the new test plant C at 1600 hours, because the time span since acceptance of the firstranked host A is longer for 3 than for 2 . The same model also leads us to classify 1 and 2 in Fig . I as identical in motivation from 1400 hours onwards ; the difference in their time of acceptance of host B is described as a difference of preference specificity . Thus, in our model, insects may differ not simply in preference rank, but also in either preference specificity (butterflies I and 2, Fig . 1) or in motivation (2 and 3), or in both (1 and 3) . Now, consider another model in which the physiological basis of motivation is more closely
related to increasing egg-load than to the passage of time . If insects varied in their egg maturation rates, motivation would increase more rapidly in insects with higher rates of egg maturation, producing shorter discrimination phases . However, we would expect that rapid egg maturation would shorten all discrimination phases by approximately the same proportion in the same individual . This could produce the difference between butterflies I and 2 in Fig . 2 ; if, for example, butterfly 2 matured eggs faster, but both butterflies accepted host A when they had 20 eggs mature, host B with 60 and host C with 70 . If this were so, how should we describe the difference between these two butterflies? Because we measure preference (including specificity) at some specified or controlled motivation level, we must measure specificity in terms of the trait most closely related to motivation . In this case, specificity would be estimated in terms of differences in egg-load rather than differences in time, so we should describe these two insects as showing the same specificity but different rates of change of motivation . If we were to plot acceptances on a figure with egg-load rather than time as the abscissa (like fig . 2a of Courtney et al . 1989), then the behaviour of butterflies 1 and 2 (Fig . 2) would appear to be identical . By the same argument, an insect that first accepts host A when it has 40 eggs mature, and host B when it has 60 eggs mature would be more specific than one that accepts host A with 40 eggs and host B with 45 eggs mature . Operational separation of specificity and motivation is much harder than conceptual separation, because operational separation depends on assumptions about the physiological mechanisms of motivation, of which we have insufficient knowledge . We attempt such an operational separation in this paper by assuming that motivation changes uniformly with time at the same rate in insects tested on the same day . In effect, we assume either that time is the important variable or that our test insects all matured eggs at the same rate . We controlled for changes in egg maturation rate with age by matching our samples for age structure . We suspect that future work will show that motivation responds in a complex fashion to egg-load, time and other factors (Mangel & Roitberg 1989) . Consequences of Failure to Separate Motivation from Specificity Without separate concepts of motivation and specificity, the full diversity of behaviour that we
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Changes over time in the probability of accepting three hosts, in three different butterflies (1, 2 and 3) that all share the same rank order of preference (host A > B > C) and that are tested simultaneously . DP(AB) is the discrimination phase with respect to host types A and B . Figure 2 .
observe in the field and depict in Figs 1 and 2 could not be described . It might seem that the difference between butterflies I and 2 of Fig . 2 could equally well be described as a difference in specificity or as a difference in rate of change of motivation . If this were true, we would need only one of these variables, not both, to describe this difference . However, if we did use only one variable, we would be unable to describe all the variation that we observe in the field . For example, if we eliminate specificity and use only motivation, we could only describe the difference between butterflies 1 and 3 in Fig . 2 by defining separate motivations with respect to each host . This would make motivation synonymous with acceptance . We would then describe butterflies I and 2 in Fig . I as differing in motivation to accept plant B . However, if we did this, we would need to define some new term to describe the difference between butterflies 2 and 3 in Fig . 1 . This example helps to explain why we advocate separation of the concepts of motivation as a general trait that is not host-specific, and preference specificity as a trait that can only be defined with respect to particular plants . In this respect our usage differs from that of Jaenike & Papaj (in press) and Mangel (1989), who use concepts of host-specific motivation, but whose models have insufficient dimensions to describe the behaviour of E . editha .
undisturbed population of E . editha at Colony Meadow in Sequoia National Park with those from a population in a clear-cut at Big Bear Meadow in Sequoia National Forest . Both populations are monophagous . The host of the Colony Meadow population is the perennial hemiparasite Pedicularis semibarbata (Scrophulariaceae), while the host at Big Bear Meadow is the annual Collinsia torreyi (Scrophulariaceae) . The Collinsia was not a suitable host until about 1967 (Singer 1983 ; Moore 1989) . At this time, the U .S . Forest Service cleared and burned several patches of forest in the Generals' Highway region, including Big Bear Meadow . In these clearcuts P . semibarbata was completely removed, since it is parasitic on coniferous trees . Simultaneously, the tilling and fertilization (from burning) extended the lifespan of C . torreyi and rendered it phenologically suitable for oviposition by E. editha . These clearcuts are currently inhabited by E . editha that spend their whole life cycle on C . torreyi, even though a high proportion of them still prefer P . semibarbata for oviposition (Singer 1983) . The undisturbed Colony Meadow study site represents the putative ancestral condition of the disturbed Big Bear Meadow site, in terms of both the plant species composition and the diet of the insects .
METHODS STUDY POPULATIONS Working in the Generals' Highway area of Tulare County, California, we compared insects from an
We used the methods of Ng (1988) to identify a highly acceptable individual P . semibarbata plant and an acceptable C . torreyi clump at our Rabbit
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Meadow test site . We subsequently used these same Table 1 . Sample sizes (number of females) of E. edithu from two populations on different dates plants in all trials, so that variation between insects would not be confounded with variation in acceptability among conspecific plants . We captured 15Date Colony Meadow Big Bear Meadow 20 insects synchronously in each of our two study populations, Colony Meadow and Big Bear 1 5 June 6 0 Meadow . We did this sufficiently late in the day 17 June 2 15 (after 1600 hours) that no further oviposition 18 June 10 12 would have occurred that day if we had left the 19 June 9 7 insects at large . We then transported all insects to 20 June 12 10 21 June 8 8 Rabbit Meadow, numbered them individually and 28 June 15 0 sorted them to give samples of similar age structure from each site . The populations of origin were not known to the persons performing preference trials . Starting at 1100 hours or shortly thereafter, practice, the assumption proved not to be critical we repeatedly placed insects on the single test because the estimated differences in motivation P. semibarbata at 10-min intervals until acceptance between the populations would have been augwas recorded . At least 5 min after this first accept- mented rather than reduced if the assumption were ance (but otherwise as soon as possible), we offered not correct (see Discussion) . each insect the test C. torreyi . We continued to manipulate encounters with C. torreyi at hourly intervals until acceptance was recorded . Insects Data Analysis that still rejected C. torreyi 2 days after accepting P . semibarbata were released at their site of capture . Because it is likely that our estimates of both We estimated the strength of preference for motivation and specificity were sensitive to P. semibarbata over C . torreyi from the minimum weather, we analysed our data in a manner that discrimination phase : the time difference between minimized the influence of day-to-day weather the first recorded acceptance of P . semibarbata and changes. We therefore rejected data from 15 June, the last recorded rejection of C. torreyi . When an when we were only able to test Big Bear Meadow insect accepted P . semibarbata on first preseninsects ; and 28 June, when only Colony Meadow tation, its discrimination phase had already begun, butterflies were tested (see Table 1) . We used all the so we were not able to estimate its length . We did data from 18-21 June, when we were able to obtain not use data from such insects in this calculation . almost equal samples each day . On 17 June we Preference for C . torreyi over P . semibarbata has tested 15 Big Bear Meadow insects but only two been rare in the General's Highway area (Singer insects from Colony Meadow . For analysis we used 1983), and we did not attempt to measure it in this the two Colony Meadow insects and randomly experiment . Because we did not present C . torreyi picked two from the Big Bear Meadow sample . Although discarding data from 15 June, 17 June until after P . semibarbata had become acceptable, we cannot distinguish between insects that preand 28 June reduced our sample sizes, in no case did ferred C . torreyi over P . semibarbata and those with it alter the nature of our findings . Accordingly, we no detectable preference . Our data only allow us to present only the conservative analyses using the place insects into two preference rank categories : restricted data set . those that preferred P. semibarbata and those that We analysed frequency data with continuity did not . corrected chi-squared tests . Comparisons of means Because of the past rarity of preference for were preceded by assessment of normality by visual inspection of residuals plotted against computerC. torreyi, and because we did not measure preference for this host in this experiment, we treated generated normal ranks . Data that were approxiP. semibarbata as the most preferred host of all mately normally distributed were analysed by both insects in our calculations . This assumption could t-tests and Mann-Whitney U-tests; those that have presented problems for interpretation of our were not normal were analysed by Mann-Whitney data, dependent on the nature of our results . In U-tests only .
Singer et al. : Host preference and motivation RESULTS
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(Singer et al . 1988) and between populations (Singer et al . 1991) .
Host Preference (Rank Order) The proportion of individuals preferring P . semibarbata (rejecting C. torreyi after having previously accepted P. semibarbata) was higher among Colony Meadow butterflies (29 of 32 insects) than among Big Bear Meadow butterflies (12 of 30 ; corrected x 2 =15 . 53, df= l, P=0 . 0001) . Only those butterflies that rejected P . semibarbata on the first trial were used in this analysis . Host Preference (Specificity) Among those butterflies that preferred P . semibarbata, the mean discrimination phase was longer (3 . 81 h, N=28) at Colony Meadow than at Big Bear Meadow (2 .09 h, N=11) showing that the Colony Meadow insects that perferred Pedicularis did so more strongly (Mann-Whitney, U=94, P= 0 .03) . Again, we used only those butterflies that rejected P . semibarbata on first presentation . Motivation Females from Big Bear Meadow showed higher mean motivation than those from Colony Meadow . Among all insects, including those that accepted P. semibarbata on the first trial, mean time from 1100 hours until first acceptance of P. semibarbata was 1 . 48 h among the Big Bear Meadow insects (N=37) and 1-94h among those from Colony Meadow (N=39) (t=5 . 7, df=1, P=0 . 027 ; U=586, P=0 . 013).
DISCUSSION Inter-population Variation of Preference Rank The difference in host preference between the two test populations is shown both by the higher proportion of Colony Meadow insects that preferred P. semibarbata and by the greater specificity of those that did show a preference . Since Colony Meadow represents the putative ancestral condition of Big Bear Meadow some 20 years ago, this difference indicates that the preferences of Big Bear Meadow insects have changed in parallel with their change of diet . We do not know whether the change in preference is genetic . Other work on E . editha has shown heritable variation in preference both within
Inter-population Variation of Motivation Mean time to first acceptance of P . semibarbata was longer in Colony Meadow than in Big Bear Meadow insects . Our interpretation of this result as a difference between populations in mean motivation depends on the assumption that P . semibarbata was the most preferred host of all insects in both populations . How likely is it that the existence of preference for other plant species could have confounded our interpretation? There are two possibilities for major error . First, some of the Big Bear Meadow insects may have preferred C . torreyi, like a small minority of those in other C . torrevi-feeding populations (Singer 1983) . For these insects, the mostpreferred plant (C . torreyi) would have become acceptable even earlier than the P . semibarbata that we used as the first test plant . If so, the Big Bear Meadow population would have had a higher mean motivation than we measured, and the difference between the two populations in mean motivation would have been greater than our estimate . The existence of C. torreyi-preferring females at Big Bear Meadow would have caused us to underestimate the difference in motivation between the populations . with no qualitative change in our result . The second possibility is that some Colony Meadow insects preferred a 'mystery plant', and were recorded as rejecting Rabbit Meadow P. semibarbata at times when this other plant would have been acceptable . Since the Colony Meadow population is monophagous on P . semibarbata in an undisturbed situation (Sequoia National Park), preference for a 'mystery plant' is unlikely . If we are correct in deducing a difference in mean motivation between our study populations, what could cause such a difference to develop? We believe that the most likely cause is a difference in frequency of oviposition due to the preference of many insects at Big Bear Meadow for a plant (P. semibarbata) that no longer grows at that site . If mean search time were longer at Big Bear Meadow than at Colony Meadow, then insects at Big Bear Meadow might oviposit less frequently, thereby producing a higher mean motivation level in this population . This type of difference in search time has already been shown in a comparison of the search behaviour patterns of free-flying E. editha at two subpopulations at Rabbit Meadow, about 1 km from Big
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Bear Meadow (Mackay 1985) . As we would expect, Mackay found longer searches in the subpopulation that resembled Big Bear Meadow (in both vegetational composition and host use by E . editha) than in the other subpopulation that resembled Colony Meadow . In summary, our study populations apparently differed both in host preference and in oviposition motivation . The most likely explanation of the increased motivation at Big Bear Meadow is that many insects at this site preferred a plant that no longer existed there . This preference, combined with inefficient search (Mackay 1985), caused some Big Bear Meadow insects to oviposit infrequently and so to become more motivated than insects in the Colony Meadow population . Our data are not ideal, but we hope that the problems of interpretation that we have encountered will assist both ourselves and other workers to design better experiments to separate preference and motivation . Potential Use of Motivation and Specificity in Evolutionary Models Although there may be some genetic variation in the way in which motivation changes with egg-load or time, most of the naturally occurring intrapopulation variation of motivation will not be heritable, but will be due to differences in recent oviposition experience of individual insects . Differences among insects in host acceptance that are due to variation of motivation will usually be temporary, non-heritable differences . In contrast, variation of specificity has the potential to be highly heritable . In E. editha, specificity appears not only to be heritable (Singer et al . 1988), but also to be correlated with offspring performance (Singer et al . 1988, and more clearly in Ng 1988) . Although it may often be difficult to separate motivation from specificity operationally, we recommend their separation in models of the evolution of insect diet . In such a model, variation of specificity would be influenced by some combination of learned and genetic factors (cf. Jaenike & Papaj, inpress), while variation of motivation would depend principally on egg-load of time elapsed since the last oviposition . Because specificity, as defined here, is a quantitative behavioural trait, a calculated optimal value of specificity would not be a calculated optimal diet breadth, but a description of the ways in which diet breadth of some optimal insect would depend on rates of encounter with hosts of particular acceptabilities . Such a model would allow us to
ask more sophisticated questions about host selection behaviour than just how many species should be in the diet . ACKNOWLEDGMENTS We are most grateful to J . J . Bull, S . P. Courtney, D . Crews, L . E . Gilbert, R . Gomulkiewicz, B . A . Hawkins, J . Lanza, A . C . Lewis, K . Marler, M . Morris, C . Penz, H . Petursson, R . Roberts, M . J . Ryan, R . Srygley, W . L . Swisher and P . J . deVries . This work was funded in part by The University of Texas, by National Science Foundation grants BSR 86-15433, 90-06603 and 9107510 to M . C . Singer, and by the authors . REFERENCES Courtney, S . P ., Chen, G . K . & Gardner, A . 1989 . A general model for individual host selection . Oikos, 55, 55-65 . Drickamer, L . C . & Vessey, S . H . 1992 . Animal Behavior : Mechanisms, Ecology and Evolution, 3rd edn . Dubuque, Iowa : W . C . Brown . Fitt G . P. 1986 . The influence of shortage of hosts on the specificity of oviposition behaviour in species of Dar-us . Phys. Entomol.,11, 133-143 . Jaenike, J . 1978 . On optimal oviposition behavior in phytophagous insects . Theor . Pop . Biol ., 14, 350-356 . Jaenike, J . & Grimaldi, D . 1983 . Genetic variation for host preference within and among populations of Drosophila tripunctata . Evolution, 37, 1023-1033 . Jaenike, J . & Papaj, D . R . In press . Learning and patterns of host use by insects . In: Chemical Ecology : an Evolutionary Perspective (Ed . by M. Isman & B . D. Roitberg), London : Chapman & Hall . Kennedy, J . S . 1987 . Animal motivation : the beginning of the end? In : Perspectives in Chemoreception and Behavior (Ed . by R . F . Chapman, E . A . Bernays & J . G . Stoffolano, Jr), pp . 17-31 . New York : SpringerVerlag . McFarland, D . 1987 . Motivation . In : The Oxford Companion to Animal Behaviour (Ed . by D . McFarland), pp . 390-398 . Oxford : Oxford University Press . Mackay, D . A . 1985 . Prealighting search behavior and host plant selection by ovipositing Euphydryas editha butterflies . Ecology, 66, 142-15 1 . Mangel, M . 1989 . An evolutionary interpretation of the motivation to oviposit' . J. evol. Biol., 2, 157-172 . Mangel, M . & Roitberg, B . D . 1989 . Dynamic information and host acceptance by a tephritid fruit fly . Ecol . Entomol ., 14,181-189 . Moore, S . D . 1989 . Patterns of juvenile mortality within an oligophagous insect population . Ecology, 70, 1726-1737 . Ng, D . 1988 . A novel level of interactions in plant-insect systems . Nature, Lond ., 334, 611-612 . Odendaal, F . J . 1989 . Mature egg number influences the behavior of female Battus philenor butterflies . J. Insect . Behav., 2, 15-25 .
Singer et al . : Host preference and motivation Pilson, D . & Rausher, M . D . 1988 . Clutch size adjustment by a swallowtail butterfly . Nature, Land., 333, 361-363 . Roitberg, B . D . & Prokopy, R. J . 1983 . Host deprivation influence on response of Rhagoletis pomonella to its oviposition deterring pheromone . Phys . Entomol ., 8, 69-72 . Singer, M . C . 1982 . Quantification of host specificity by manipulation of oviposition behavior in the butterfly Euphydryas editha . Oecologia (Berl .), 52, 224-229 . Singer, M . C . 1983 . Determinants of multiple host use by a phytophagous insect population . Evolution, 37, 389-403 . Singer, M . C . 1986 . The definition and measurement of oviposition preference . In : Plant-Insect Interactions (Ed . by J . Miller & T . A . Miller), pp . 65-94 . Berlin : Springer-Verlag . Singer, M . C ., Ng, D . & Thomas, C . D . 1988 . Heritability of oviposition preference and its relationship to offspring performance within a single insect population . Evolution, 42,977 --985 .
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Singer, M . C ., Moore, R . A . & Ng, D . 1991 . Genetic variation in oviposition preference between butterfly populations . J. Insect . Behav ., 4, 531--535 . Stephens, D . W . & Krebs, J . R . 1986 . Foraging Theory . Princeton, New Jersey : Princeton University Press . Thomas, C . D . & Singer, M . C . 1987 . Variation in host preference affects movement patterns within a butterfly population . Ecology, 68, 1262-1267 . Thompson, J . N . 1988 . Variation in preference and specificity in monophagous and oligophagous swallowtail butterflies. Evolution, 42, 118-128 . Ward, S . A. 1987 . Optimal habitat selection in timelimited dispersers . Am . Nat ., 129, 568-579 . Wasserman, S . S . & Futuyma, D. J . 1981 . Evolution of host plant utilization in laboratory populations of the southern cowpea weevil, Callosobruchus maculates (Coleoptera : Bruchidae) . Evolution, 35, 605-617 . Wiklund, C . 1981 . Generalist versus specialist oviposition behavior in Papilio machaon (Lepidoptera) and the hierarchy of oviposition preferences . Oikos, 36, 163-170 .
Distinguishing between `preference' and `motivation' in food choice : an example from insect oviposition M . C . SINGER, D . VASCO, C . PARMESAN, C . D . THOMAS* & D . NGt Department of Zoology and Division of Biological Science, University of Texas at Austin, Austin, TX 78712, U .S .A . (Received 12 April 1991 ; initial acceptance 26 April 1991 ; final acceptance 7 December /991 ; MS. number.• A5881)
Abstract . Variation among individuals in acceptance of a second-ranked food resource could be caused either by variation in strength of `preference' for the top-ranked over the second-ranked resource type, or by variation in the general readiness to feed . This distinction is important in models of diet evolution . Of the two traits, preference is the more likely to show additive genetic variation and hence be subject to evolutionary change . In the checkerspot butterfly, Euphydryas editha, changes in readiness to oviposit (abbreviated as oviposition `motivation') mediate the relationship between host preference, host encounter rate, and realized diet, and thereby influence the strength of selection on preference . Definitions of acceptance, preference and motivation are given and applied to oviposition behaviour of herbivorous insects . From these definitions, operational measures of these traits are developed for E. editha . These operational measures are then used to investigate a difference between two E . editha populations in acceptance of a second-ranked host species . The results of this study show that this difference was caused partly by variation of preference and partly by variation of motivation . The difference in motivation probably stemmed from the absence of the most-preferred host from one of the study sites, resulting in prolonged search, reduced frequency of oviposition, and higher mean motivation at this site .
Oviposition decisions by herbivorous insects are food choice decisions . Some attempts to model these decisions have met with scepticism from students of vertebrate foraging . For example, Stephens & Krebs (1986, pp . 126-127) doubted whether Jaenike's (1978) insect-based model used appropriate currency, and suspected that insect oviposition decisions were `only superficially similar to foraging decisions' . To understand insect oviposition better, and to incorporate it into ecological and evolutionary theories of foraging, we need both more explicit insect-based models and clearer definitions of terms that describe insect behaviour . Here, we suggest general definitions of 'acceptance', `preference' and `motivation to oviposit' for herbivorous insects . We then develop and use operational measures of these traits for our own study insect, the checkerspot butterfly, Euphydryas editha . Separation of these three concepts in a
behavioural model allows us to describe and interpret the suite of natural responses to host plants that we see in our study populations . General Definitions Acceptance
When a potential host is encountered, an insect may respond positively by proceeding to the next stage in the sequence of oviposition behaviour, or negatively, by failing to do this . We describe these alternatives as `host acceptance' and `host rejection' (Singer 1986; Courtney et al . 1989 ; Mangel 1989) . Motivation
Because of past controversy (Kennedy 1987 ; McFarland 1987 ; Drickamer & Vessey 1992), `motivation' should be used non-anthropomorphically . We define an insect's oviposition motivation as a non-specific readiness to oviposit . By 'nonspecific' we mean that it is not determined by the nature of the potential hosts that are encountered .
*Present address : NERC Centre for Population Biology, Imperial College, Silwood Park, Ascot, Berkshire SL5 7P1', U .K .
+Present address : Pharmaco, 4009 Banister Lane, Austin, TX 78704, U .S .A . 0003 3472/92!090463+09$08 .00/0
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Although the range of hosts that would be accepted (if encountered) may depend on the insect's current motivational state, we do not describe the insect as possessing separate motivations for each host type . Various authors have suggested that an insect's motivation to oviposit is controlled by an internal factor that tends to increase either with passing time (Singer 1982 ; Roitberg & Prokopy 1983 ; Pilson & Rausher 1988), or with increasing eggload (Fitt 1986; Courtney et al . 1989 ; Odendaal 1989), or with both (Mangel & Roitberg 1989) . However, in no case do we know the nature of this internal factor or the causes of its fluctuations . While this ignorance persists, attempts to develop operational estimates of motivation to oviposit will depend at least partly on untested assumptions . Preference We define an insect's oviposition `preference' as the set of relative likelihoods of accepting particular hosts that are encountered . In many species, the likelihoods of accepting different hosts increase at different rates with rising motivation, i .e. as the insect becomes more likely to oviposit in general . When this occurs, the relative likelihoods of accepting different hosts also change with motivation . Thus, comparisons of preference between different individuals must be made at some known or controlled level of motivation across all test insects (Singer 1986) . In our own work, we estimate preference from the changes in acceptance that occur as motivation rises .
fully, probes with its ovipositor and then holds it motionless and extruded for at least 3 s, its behaviour is recorded as acceptance . Conversely, a rejection is recorded if the test butterfly fails to perform this behavioural sequence after 5 min on the plant . Since several seconds normally elapse between acceptance (as measured here) and actual oviposition, an experimenter can observe acceptance, then remove the insect from the test plant without allowing it to lay eggs . By this means . acceptance can be recorded without the decrease in motivation that would follow actual oviposition . Preference Our operational measure of preference stems from the behaviour of E. editha in our study populations, where each female normally undertakes one oviposition search per day . If the insect fails to encounter an acceptable plant at the beginning of its search, oviposition is delayed . While this delay continues, the range of plants that would be accepted if encountered expands with the passage of time (Singer 1982) . Eventually, oviposition usually occurs and the search ends . If the search is unsuccessful, it recommences on the following day . We divide preference into two components . 'Preference rank' is the order in which plants become acceptable to an insect as time passes . `Specificity of preference', which we abbreviate as `specificity', is the set of strengths of preference for particular hosts . So, if two insects prefer the same hosts, but differ in the strength of preference, they are said to differ in specificity but not in rank (cf. Wiklund 1981) .
Operational measures Acceptance
Preference rank
There are three phases in acceptance of a plant by E. editha . In the first, the insect alights in response to visual stimuli (Mackay 1985) . In the second, it tastes the plant with its specialized fore-tarsi and responds to acceptable taste stimuli by curling its abdomen, and extruding its ovipositor (Singer 1986) . In the third phase, the insect probes with its ovipositor until a surface with acceptable physical characteristics is encountered . In this paper, we are concerned with the response to taste that follows alighting . Euphydryas editha behave naturally when manipulated . Acceptance can be assessed by placing a butterfly on a plant and observing its behaviour. If the test butterfly curls its abdomen
Singer (1982) repeatedly placed female E . editha on two hosts in alternation and prevented them from ovipositing by removing them from plants after each acceptance . Each plant was initially rejected, became acceptable to an insect at a particular time, and then remained acceptable until oviposition actually occurred . However, different plants became acceptable at different times . The following sequences were observed : (1) REJECT plant A ; REJECT B ; ACCEPT A ; REJECT B ; ACCEPT A ; REJECT B ; ACCEPT A ; ACCEPT B . (2) REJECT A, B, A, B, A ; ACCEPT B, A, B, A . Sequences of type (1) gave a direct measure of preference rank, the order in which plants became
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Figure 1 . Changes over time in the probability of accepting two hosts, in three different butterflies that all share the same rank order of preference (A > B) and that are tested simultaneously . Thick lines show times at which the probability of accepting host A is the same as that of accepting host B. DP indicates the discrimination phase when one host is accepted and the other rejected . If host A is really the most-preferred of all possible hosts, then the time period before its acceptance is the refractory phase RP as indicated . These refractory phases extend back to ovipositions on the previous day, the times of which are not shown . Because we do not show entire refractory phases (RPs) we do not imply that RP3 is actually shorter than RPI or RP2 as it appears to be in the figure . acceptable (in this case, A > B) . In those of type (2) the plants became acceptable so close to the same time that it was impossible to tell whether one became acceptable before the other . In this case the insect was classified as without preference, although it may have had a preference too slight to be detected . The manipulative preference-testing technique used in this work depends on the assumption that the current likelihood of accepting each host is not influenced by previous encounters with either the same or a different host. This assumption appears to be justified for E. editha (Singer 1986 ; Thomas & Singer 1987) . In insects that oviposit frequently, preference rank can be determined from relative oviposition rates on different resource types that are presented simultaneously (Wasserman & Futuyma 1981 ; Jaenike & Grimaldi 1983 ; Thompson 1988) . Preference spec f city We estimate specificity from the length of the time interval or 'discrimination phase' during which one host is accepted and the other rejected . Figure 1 depicts two insects that differ in specificity . The existence of such discrimination phases has been predicted theoretically (Jaenike 1978 ; Ward 1987 ; Mangel 1989) . In E. editha, we cannot calculate the exact length of the discrimination phase,
but we can obtain maximum and minimum values (Singer 1982) . In practice, we use the minimum length of the discrimination phase, the time from first acceptance of the higher-ranked plant until the last rejection of the lower-ranked plant . The reason for doing this is that maximum values are only obtained if the lower-ranked plant is actually accepted (Singer 1982) . By requiring maximum (or midpoint) values we would disproportionately exclude data from those insects with high specificity that escaped or died before they accepted the lowerranked plants . This effect is especially important when insects are tested for a fixed period (2 days in the present study) . Measures of minimum discrimination phase are truncated at the length of this fixed period, but use of this minimum value allows inclusion of all insects in the data set . Motivation to oviposit The simplest way to classify motivation would be as a binomial variable : an insect that is motivated to oviposit accepts its most-preferred host, while an unmotivated insect rejects it . However, this would be an over-simplification, because the underlying (and presently unknown) physiological variable is likely to be continuous . If we consider motivation a continuous variable, we can use acceptance of the most-preferred host as an easily-measured reference point by which to compare individuals .
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Drickamer & Vessey (1992, page 292) argue that the `black box' concept of motivation can be discarded when the underlying physiological variables become known . We cannot yet do this with respect to insect oviposition, because we are still ignorant of the physiological basis of changing responsiveness . Here, we discuss two operational measures of motivation that differ in whether the `internal physiological variable' measures the passage of time, or the accumulation of eggs. We use hypothetical data sets, in which the most-preferred host is the same for all butterflies . We designate this mostpreferred host as `host A' and the second-ranked host as `host B' . All our hypothetical test butterflies begin the experiment with a refractory phase during which both host species are repeatedly rejected . At some time, host A is accepted and subsequently remains acceptable . At some later time, host B is also accepted . First, we examine our hypothetical data set using the passage of time as the motivation criterion . The motivation levels of butterflies I and 2 at 1400 hours (Fig . 1) are the same as that of 3 at 1200 hours, when host A is first accepted . We can compare motivation at other times by making the simplifying assumptions that all butterflies respond to time in the same way, and that the rate of increase of motivation is the same in different test butterflies that are being compared simultaneously . These assumptions enable us to classify butterfly 3 of Fig . I as having higher motivation than butterfly 2 throughout the test period because 3 was prepared to lay eggs on the most-preferred host (A) earlier in the day . At 1600 hours the behaviour of butterflies 2 and 3 towards plants A and B is identical . What, then, is the use of classifying 3 as more highly motivated than 2 at this time? Suppose we test a third plant, C, that is ranked below B by both butterflies . Our model predicts that butterfly 3 will be more likely than 2 to accept the new test plant C at 1600 hours, because the time span since acceptance of the firstranked host A is longer for 3 than for 2 . The same model also leads us to classify 1 and 2 in Fig . I as identical in motivation from 1400 hours onwards ; the difference in their time of acceptance of host B is described as a difference of preference specificity . Thus, in our model, insects may differ not simply in preference rank, but also in either preference specificity (butterflies I and 2, Fig . 1) or in motivation (2 and 3), or in both (1 and 3) . Now, consider another model in which the physiological basis of motivation is more closely
related to increasing egg-load than to the passage of time . If insects varied in their egg maturation rates, motivation would increase more rapidly in insects with higher rates of egg maturation, producing shorter discrimination phases . However, we would expect that rapid egg maturation would shorten all discrimination phases by approximately the same proportion in the same individual . This could produce the difference between butterflies I and 2 in Fig . 2 ; if, for example, butterfly 2 matured eggs faster, but both butterflies accepted host A when they had 20 eggs mature, host B with 60 and host C with 70 . If this were so, how should we describe the difference between these two butterflies? Because we measure preference (including specificity) at some specified or controlled motivation level, we must measure specificity in terms of the trait most closely related to motivation . In this case, specificity would be estimated in terms of differences in egg-load rather than differences in time, so we should describe these two insects as showing the same specificity but different rates of change of motivation . If we were to plot acceptances on a figure with egg-load rather than time as the abscissa (like fig . 2a of Courtney et al . 1989), then the behaviour of butterflies 1 and 2 (Fig . 2) would appear to be identical . By the same argument, an insect that first accepts host A when it has 40 eggs mature, and host B when it has 60 eggs mature would be more specific than one that accepts host A with 40 eggs and host B with 45 eggs mature . Operational separation of specificity and motivation is much harder than conceptual separation, because operational separation depends on assumptions about the physiological mechanisms of motivation, of which we have insufficient knowledge . We attempt such an operational separation in this paper by assuming that motivation changes uniformly with time at the same rate in insects tested on the same day . In effect, we assume either that time is the important variable or that our test insects all matured eggs at the same rate . We controlled for changes in egg maturation rate with age by matching our samples for age structure . We suspect that future work will show that motivation responds in a complex fashion to egg-load, time and other factors (Mangel & Roitberg 1989) . Consequences of Failure to Separate Motivation from Specificity Without separate concepts of motivation and specificity, the full diversity of behaviour that we
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observe in the field and depict in Figs 1 and 2 could not be described . It might seem that the difference between butterflies I and 2 of Fig . 2 could equally well be described as a difference in specificity or as a difference in rate of change of motivation . If this were true, we would need only one of these variables, not both, to describe this difference . However, if we did use only one variable, we would be unable to describe all the variation that we observe in the field . For example, if we eliminate specificity and use only motivation, we could only describe the difference between butterflies 1 and 3 in Fig . 2 by defining separate motivations with respect to each host . This would make motivation synonymous with acceptance . We would then describe butterflies I and 2 in Fig . I as differing in motivation to accept plant B . However, if we did this, we would need to define some new term to describe the difference between butterflies 2 and 3 in Fig . 1 . This example helps to explain why we advocate separation of the concepts of motivation as a general trait that is not host-specific, and preference specificity as a trait that can only be defined with respect to particular plants . In this respect our usage differs from that of Jaenike & Papaj (in press) and Mangel (1989), who use concepts of host-specific motivation, but whose models have insufficient dimensions to describe the behaviour of E . editha .
undisturbed population of E . editha at Colony Meadow in Sequoia National Park with those from a population in a clear-cut at Big Bear Meadow in Sequoia National Forest . Both populations are monophagous . The host of the Colony Meadow population is the perennial hemiparasite Pedicularis semibarbata (Scrophulariaceae), while the host at Big Bear Meadow is the annual Collinsia torreyi (Scrophulariaceae) . The Collinsia was not a suitable host until about 1967 (Singer 1983 ; Moore 1989) . At this time, the U .S . Forest Service cleared and burned several patches of forest in the Generals' Highway region, including Big Bear Meadow . In these clearcuts P . semibarbata was completely removed, since it is parasitic on coniferous trees . Simultaneously, the tilling and fertilization (from burning) extended the lifespan of C . torreyi and rendered it phenologically suitable for oviposition by E. editha . These clearcuts are currently inhabited by E . editha that spend their whole life cycle on C . torreyi, even though a high proportion of them still prefer P . semibarbata for oviposition (Singer 1983) . The undisturbed Colony Meadow study site represents the putative ancestral condition of the disturbed Big Bear Meadow site, in terms of both the plant species composition and the diet of the insects .
METHODS STUDY POPULATIONS Working in the Generals' Highway area of Tulare County, California, we compared insects from an
We used the methods of Ng (1988) to identify a highly acceptable individual P . semibarbata plant and an acceptable C . torreyi clump at our Rabbit
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Meadow test site . We subsequently used these same Table 1 . Sample sizes (number of females) of E. edithu from two populations on different dates plants in all trials, so that variation between insects would not be confounded with variation in acceptability among conspecific plants . We captured 15Date Colony Meadow Big Bear Meadow 20 insects synchronously in each of our two study populations, Colony Meadow and Big Bear 1 5 June 6 0 Meadow . We did this sufficiently late in the day 17 June 2 15 (after 1600 hours) that no further oviposition 18 June 10 12 would have occurred that day if we had left the 19 June 9 7 insects at large . We then transported all insects to 20 June 12 10 21 June 8 8 Rabbit Meadow, numbered them individually and 28 June 15 0 sorted them to give samples of similar age structure from each site . The populations of origin were not known to the persons performing preference trials . Starting at 1100 hours or shortly thereafter, practice, the assumption proved not to be critical we repeatedly placed insects on the single test because the estimated differences in motivation P. semibarbata at 10-min intervals until acceptance between the populations would have been augwas recorded . At least 5 min after this first accept- mented rather than reduced if the assumption were ance (but otherwise as soon as possible), we offered not correct (see Discussion) . each insect the test C. torreyi . We continued to manipulate encounters with C. torreyi at hourly intervals until acceptance was recorded . Insects Data Analysis that still rejected C. torreyi 2 days after accepting P . semibarbata were released at their site of capture . Because it is likely that our estimates of both We estimated the strength of preference for motivation and specificity were sensitive to P. semibarbata over C . torreyi from the minimum weather, we analysed our data in a manner that discrimination phase : the time difference between minimized the influence of day-to-day weather the first recorded acceptance of P . semibarbata and changes. We therefore rejected data from 15 June, the last recorded rejection of C. torreyi . When an when we were only able to test Big Bear Meadow insect accepted P . semibarbata on first preseninsects ; and 28 June, when only Colony Meadow tation, its discrimination phase had already begun, butterflies were tested (see Table 1) . We used all the so we were not able to estimate its length . We did data from 18-21 June, when we were able to obtain not use data from such insects in this calculation . almost equal samples each day . On 17 June we Preference for C . torreyi over P . semibarbata has tested 15 Big Bear Meadow insects but only two been rare in the General's Highway area (Singer insects from Colony Meadow . For analysis we used 1983), and we did not attempt to measure it in this the two Colony Meadow insects and randomly experiment . Because we did not present C . torreyi picked two from the Big Bear Meadow sample . Although discarding data from 15 June, 17 June until after P . semibarbata had become acceptable, we cannot distinguish between insects that preand 28 June reduced our sample sizes, in no case did ferred C . torreyi over P . semibarbata and those with it alter the nature of our findings . Accordingly, we no detectable preference . Our data only allow us to present only the conservative analyses using the place insects into two preference rank categories : restricted data set . those that preferred P. semibarbata and those that We analysed frequency data with continuity did not . corrected chi-squared tests . Comparisons of means Because of the past rarity of preference for were preceded by assessment of normality by visual inspection of residuals plotted against computerC. torreyi, and because we did not measure preference for this host in this experiment, we treated generated normal ranks . Data that were approxiP. semibarbata as the most preferred host of all mately normally distributed were analysed by both insects in our calculations . This assumption could t-tests and Mann-Whitney U-tests; those that have presented problems for interpretation of our were not normal were analysed by Mann-Whitney data, dependent on the nature of our results . In U-tests only .
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(Singer et al . 1988) and between populations (Singer et al . 1991) .
Host Preference (Rank Order) The proportion of individuals preferring P . semibarbata (rejecting C. torreyi after having previously accepted P. semibarbata) was higher among Colony Meadow butterflies (29 of 32 insects) than among Big Bear Meadow butterflies (12 of 30 ; corrected x 2 =15 . 53, df= l, P=0 . 0001) . Only those butterflies that rejected P . semibarbata on the first trial were used in this analysis . Host Preference (Specificity) Among those butterflies that preferred P . semibarbata, the mean discrimination phase was longer (3 . 81 h, N=28) at Colony Meadow than at Big Bear Meadow (2 .09 h, N=11) showing that the Colony Meadow insects that perferred Pedicularis did so more strongly (Mann-Whitney, U=94, P= 0 .03) . Again, we used only those butterflies that rejected P . semibarbata on first presentation . Motivation Females from Big Bear Meadow showed higher mean motivation than those from Colony Meadow . Among all insects, including those that accepted P. semibarbata on the first trial, mean time from 1100 hours until first acceptance of P. semibarbata was 1 . 48 h among the Big Bear Meadow insects (N=37) and 1-94h among those from Colony Meadow (N=39) (t=5 . 7, df=1, P=0 . 027 ; U=586, P=0 . 013).
DISCUSSION Inter-population Variation of Preference Rank The difference in host preference between the two test populations is shown both by the higher proportion of Colony Meadow insects that preferred P. semibarbata and by the greater specificity of those that did show a preference . Since Colony Meadow represents the putative ancestral condition of Big Bear Meadow some 20 years ago, this difference indicates that the preferences of Big Bear Meadow insects have changed in parallel with their change of diet . We do not know whether the change in preference is genetic . Other work on E . editha has shown heritable variation in preference both within
Inter-population Variation of Motivation Mean time to first acceptance of P . semibarbata was longer in Colony Meadow than in Big Bear Meadow insects . Our interpretation of this result as a difference between populations in mean motivation depends on the assumption that P . semibarbata was the most preferred host of all insects in both populations . How likely is it that the existence of preference for other plant species could have confounded our interpretation? There are two possibilities for major error . First, some of the Big Bear Meadow insects may have preferred C . torreyi, like a small minority of those in other C . torrevi-feeding populations (Singer 1983) . For these insects, the mostpreferred plant (C . torreyi) would have become acceptable even earlier than the P . semibarbata that we used as the first test plant . If so, the Big Bear Meadow population would have had a higher mean motivation than we measured, and the difference between the two populations in mean motivation would have been greater than our estimate . The existence of C. torreyi-preferring females at Big Bear Meadow would have caused us to underestimate the difference in motivation between the populations . with no qualitative change in our result . The second possibility is that some Colony Meadow insects preferred a 'mystery plant', and were recorded as rejecting Rabbit Meadow P. semibarbata at times when this other plant would have been acceptable . Since the Colony Meadow population is monophagous on P . semibarbata in an undisturbed situation (Sequoia National Park), preference for a 'mystery plant' is unlikely . If we are correct in deducing a difference in mean motivation between our study populations, what could cause such a difference to develop? We believe that the most likely cause is a difference in frequency of oviposition due to the preference of many insects at Big Bear Meadow for a plant (P. semibarbata) that no longer grows at that site . If mean search time were longer at Big Bear Meadow than at Colony Meadow, then insects at Big Bear Meadow might oviposit less frequently, thereby producing a higher mean motivation level in this population . This type of difference in search time has already been shown in a comparison of the search behaviour patterns of free-flying E. editha at two subpopulations at Rabbit Meadow, about 1 km from Big
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Bear Meadow (Mackay 1985) . As we would expect, Mackay found longer searches in the subpopulation that resembled Big Bear Meadow (in both vegetational composition and host use by E . editha) than in the other subpopulation that resembled Colony Meadow . In summary, our study populations apparently differed both in host preference and in oviposition motivation . The most likely explanation of the increased motivation at Big Bear Meadow is that many insects at this site preferred a plant that no longer existed there . This preference, combined with inefficient search (Mackay 1985), caused some Big Bear Meadow insects to oviposit infrequently and so to become more motivated than insects in the Colony Meadow population . Our data are not ideal, but we hope that the problems of interpretation that we have encountered will assist both ourselves and other workers to design better experiments to separate preference and motivation . Potential Use of Motivation and Specificity in Evolutionary Models Although there may be some genetic variation in the way in which motivation changes with egg-load or time, most of the naturally occurring intrapopulation variation of motivation will not be heritable, but will be due to differences in recent oviposition experience of individual insects . Differences among insects in host acceptance that are due to variation of motivation will usually be temporary, non-heritable differences . In contrast, variation of specificity has the potential to be highly heritable . In E. editha, specificity appears not only to be heritable (Singer et al . 1988), but also to be correlated with offspring performance (Singer et al . 1988, and more clearly in Ng 1988) . Although it may often be difficult to separate motivation from specificity operationally, we recommend their separation in models of the evolution of insect diet . In such a model, variation of specificity would be influenced by some combination of learned and genetic factors (cf. Jaenike & Papaj, inpress), while variation of motivation would depend principally on egg-load of time elapsed since the last oviposition . Because specificity, as defined here, is a quantitative behavioural trait, a calculated optimal value of specificity would not be a calculated optimal diet breadth, but a description of the ways in which diet breadth of some optimal insect would depend on rates of encounter with hosts of particular acceptabilities . Such a model would allow us to
ask more sophisticated questions about host selection behaviour than just how many species should be in the diet . ACKNOWLEDGMENTS We are most grateful to J . J . Bull, S . P. Courtney, D . Crews, L . E . Gilbert, R . Gomulkiewicz, B . A . Hawkins, J . Lanza, A . C . Lewis, K . Marler, M . Morris, C . Penz, H . Petursson, R . Roberts, M . J . Ryan, R . Srygley, W . L . Swisher and P . J . deVries . This work was funded in part by The University of Texas, by National Science Foundation grants BSR 86-15433, 90-06603 and 9107510 to M . C . Singer, and by the authors . REFERENCES Courtney, S . P ., Chen, G . K . & Gardner, A . 1989 . A general model for individual host selection . Oikos, 55, 55-65 . Drickamer, L . C . & Vessey, S . H . 1992 . Animal Behavior : Mechanisms, Ecology and Evolution, 3rd edn . Dubuque, Iowa : W . C . Brown . Fitt G . P. 1986 . The influence of shortage of hosts on the specificity of oviposition behaviour in species of Dar-us . Phys. Entomol.,11, 133-143 . Jaenike, J . 1978 . On optimal oviposition behavior in phytophagous insects . Theor . Pop . Biol ., 14, 350-356 . Jaenike, J . & Grimaldi, D . 1983 . Genetic variation for host preference within and among populations of Drosophila tripunctata . Evolution, 37, 1023-1033 . Jaenike, J . & Papaj, D . R . In press . Learning and patterns of host use by insects . In: Chemical Ecology : an Evolutionary Perspective (Ed . by M. Isman & B . D. Roitberg), London : Chapman & Hall . Kennedy, J . S . 1987 . Animal motivation : the beginning of the end? In : Perspectives in Chemoreception and Behavior (Ed . by R . F . Chapman, E . A . Bernays & J . G . Stoffolano, Jr), pp . 17-31 . New York : SpringerVerlag . McFarland, D . 1987 . Motivation . In : The Oxford Companion to Animal Behaviour (Ed . by D . McFarland), pp . 390-398 . Oxford : Oxford University Press . Mackay, D . A . 1985 . Prealighting search behavior and host plant selection by ovipositing Euphydryas editha butterflies . Ecology, 66, 142-15 1 . Mangel, M . 1989 . An evolutionary interpretation of the motivation to oviposit' . J. evol. Biol., 2, 157-172 . Mangel, M . & Roitberg, B . D . 1989 . Dynamic information and host acceptance by a tephritid fruit fly . Ecol . Entomol ., 14,181-189 . Moore, S . D . 1989 . Patterns of juvenile mortality within an oligophagous insect population . Ecology, 70, 1726-1737 . Ng, D . 1988 . A novel level of interactions in plant-insect systems . Nature, Lond ., 334, 611-612 . Odendaal, F . J . 1989 . Mature egg number influences the behavior of female Battus philenor butterflies . J. Insect . Behav., 2, 15-25 .
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