Ecological Entomology (1988) 13,107-118

Egg laying decisions by the bean maculatus

KENNETH WILSON Department of Zoology, University of Sheffield

ABSTRACT. 1. Previous work has shown that female Callosobruchus maculatus (F.) (Coleoptera: Bruchidae) can accurately assess the number of eggs on a and use this information to produce a near uniform distribution of egg-loads, so minimizing larval competition within hosts. 2. The decision to lay on a particular seed may be based on one of two possible rules: (i) a ‘relative’ rule, which compares the number of eggs on the present seed with that on previously encountered ; and (ii) an ‘absolute’ rule, which takes into account the current egg-load alone. 3. This paper describes an experimental study of oviposition behaviour which concludes that an absolute measure of egg-load probably deter- mines egg-laying decisions. The implications of this result are discussed.

Key words. Callosobruchus, Bruchidae, oviposition behaviour, egg-load, .

Introduction mechanism by which this is achieved by testing two models for making egg-laying decisions. Organisms which supply their progeny with a Bruchids are pests of cultivated legumes and limiting resource after birth must make choices dried pulses. Although they infest crops in the regarding division of the resource between field their impact here is minimal when com- offspring. For internally-feeding granivorous pared with the severe and costly damage they such as the bean weevil Callosobruchus cause to seeds in stores (Southgate, 1978, 1979; maculatus (F.) (Coleoptera: Bruchidae), a Jackai & Daoust, 1986). Females lay their eggs single ovipositing female will maximize her fit- singly onto the surface of appropriate host seeds. ness by dispersing her eggs over the available After a few days the first instar larva hatches out seeds so as to minimize the effects of larval com- of the egg and burrows into the seed, where it petition between her offspring, provided that feeds and develops into a sexually mature adult. the fitness curve is convex at all clutch sizes Individuals remain in the host seed chosen by below the Lack solution. In other words, she their mother until emerging as adults. Adults do should disperse her eggs in an ‘ideal free’ way not feed and so must survive on reserves (Fretwell & Lucas, 1970). Such behaviour will accumulated during larval development. Both result in a near-uniform distribution of eggs over individual survival and emergence weight are the available seeds. This paper examines the negatively correlated with the number of larvae & Correspondence: Mr K. Wilson, Department of per seed even at low larval densities (Smith Zoology, The Alfred Denny Building, The University Lessells, 1985). Heavier females live longer and of Sheffield, Western Bank, Sheffield S10 2TN have higher fertility than lighter females. Thus,

107 108 Kenneth Wilson as the number of larvae already present in a seed between similar-sized egg-laden seeds by com- increases, the gain in fitness to an ovipositing paring the egg-load on the current seed with that female from each additional egg laid. decreases on the last seed encountered. He suggested that (see Smith & Lessells, 1985, for review). The the female should lay on the present seed only if best strategy available to the female, then, is to it had fewer eggs than the last seed encountered. lay first on seeds already bearing the fewest eggs. This is a somewhat crude relative rule, as the so producing a distribution of eggs on seeds comparison the female makes is only between which is more uniform than random. Several the last two seeds visited. Mitchell suggested studies (e.g. Utida. 1943; Avidov er al., 1965; that the were also able to distinguish pers. obs.) have shown that bruchid beetles do between seeds of different weights. However, this. because his experiments were performed at low The female requires a set of rules to decide egg densities he was not able to show whether whether or not to lay on each seed encountered. females made a distinction between seeds with There are two basic types of rules that could be low or high egg-loads, only that they distin- used: (i) a ’relative’ rule. i.e. oviposition rate is guished between egg-laden and pristine seeds. determined by a comparison of the present egg- Mitchell produced a simulation of his rule of load with that of the previous seed(s) encoun- thumb and this compared favourably with data tered. or, (ii) an ‘absolute‘ rule, i.e. oviposition obtained from ovipositing beetles. rate is determined solely by the current seed’s Messina & Renwick (1985a) showed that, in egg-load. choice experiments, female C. maculatus were There are many possible variations on these able to discriminate between very small differ- rules, each producing a different distribution of ences in egg-load (0 eggs v. 1 egg; 1 egg v. 3 eggs; eggs on seeds. For example, the female may and 3 eggs v. 5 eggs) and preferentially laid on oviposit on a seed with a probability that varies the lower egg-density seeds. They also continuously with current egg-load (fine dis- demonstrated, by sequentially offering females crimination), or she may distinguish only batches of low (1 egg); intermediate (3 and 4 between pristine and egg-laden seeds, laying on eggs); or high (5-12 eggs) egg-load seeds for 1 h the latter with the same probability regardless of at a time, that oviposition rate was strongly egg-load (coarse discrimination). influenced by egg-load: females transferred Fig. 1 shows the distribution of egg-loads from seeds with high egg-loads to seeds with generated by computer simulations of a range of lower egg-loads increased their rate of oviposi- possible oviposition rules. In all of the simula- tion whilst the reverse transfer decreased it. tions. seeds are visited at random and indepen- Their experiments demonstrated that egg-load dently of their current egg-load. Only one egg is assessment is not coarse but that the beetles are laid per oviposition visit. The computer simula- ‘counting’ each seed’s egg-load. They appear to tions show that distributions which are more do this using both chemical and tactile stimuli uniform than random can be generated by either (Messina & Renwick, 1985b). The authors absolute or relative oviposition rules. Moreover, pointed out, however, that the rules governing rules in which the probability of laying an egg the decision to oviposit were not clear from their depends only on whether the seed is pristine or results. Ovipositing females may be using a rela- egg-laden, and not on the egg-load of egg-laden tive or an absolute rule. Although their results seeds, also produce more uniform than random could not distinguish between the two strategies, distributions at low final egg densities. Messina & Renwick were able to predict that if a However, as expected, they do not function well memory trace of previously encountered seeds is at higher egg densities. The simulations show used it must go back farther than just the pre- that a range of possible oviposition rules could vious seed, as females laid at a low rate for the be used by a female to achieve a uniform dis- full hour following transfer from low to high egg- tribution of eggs over seeds; the aim of this study load seeds. is to determine which rule is actually being used. Both Mitchell and Messina & Renwick appreciated that the actual egg-laying rule could Previous models only be found through a closer analysis of Mitchell (1975) developed a model based on a searching behaviour during oviposition bouts. In ‘rule of thumb’ in which the chooses this way the number of seeds and the time Egg laying decisions by Cullosobruchus 109

r--, (a ) Absolute rule; coorse discrimination ''1 ''1 II/

(b) Absolute rule; fine discrimination 70 II

(c Relative rule; coarse discrimination r-- 3 ub- L 0

id) Relotive rule, fine discrimination

1 ? 3 ' 4 5 6 ' 7 8 9 I 10' 11' Egg-load per seed FIG. 1. Egg distributions generated by computer simulations of oviposition rules. Distributions were generated by hlonte Carlo simulations of a single female ovipositing on 100 initially pristine seeds. Females visited (arid re-visited) seeds at random, and at each visit laid an egg with a probability that was a function of the egg-load of the current seed, and, in the case of relative rules, of the egg-load of previously visited seeds (see below). Simulations were stopped after either 100 eggs (dashed lines) or 500eggs (solid lines) had been laid. Histograms are examples of generated distributions; continuous curves are the expected (Poisson) distributions, when the decision to lay is independent of the current egg-load. All of the observed distributions, except for the 500-egg distributions in (a) and (c), differ from random (chi-square goodness- of-fit test). The following oviposition rules were used, where p(lay)=the probability of ovipositing on the current seed, c= the current seed's egg-load, m=the mean egg-load at encounter for all seed visits so far, and v=the proportion of seeds which were pristine at encounter for all seed visits so far. (a) If c=O. p(lay)=l. If 00, p(lay)=O.25. (b) p(lay)=exp(-c). (c) If c=0, p(lay)=exp(-v). If 00,p(lay)=0.25exp(-v). (d) p(lay)=exp(-c/(m+l)). (e) If cm, p(lay)=exp(-c/(m+l)). 110 Kenneth u'ilsoti involved in the process of egg-load assessment o1,iposits. declines over time (e.g. Dick & Cred- could be determined. This paper describes an land. 1984). This decline is evident even in the experimental study in which observations of first hour of oviposition (pers. obs.), so where oviposition behaviour were used to test whether necessary it has been controlled for using an absolute or relative rule was being used. analysis of covariance in comparisons between groups. Testing the motlelv Ovipositing females were presented with a Materials and Methods total of sixteen seeds. half of which bore just one egg and the other half a higher number of eggs: Ciiltitre t~trthotis In 'low-density grids' the other half were all The stock cultures of C.rizaculatirs were main- 5-egg seeds. and in 'high-density grids' all were tained on , Vigriia utigiticitlara (L.) 11-egg seeds. Thus the mean number of eggs per Walp, in a constant temperature room at 30°C seed on the low- and high-density grids were 3 35% r.h. with a 16L:8D photoperiod. The cul- and 6. respectively. tures were obtained from Imperial College at It follows from the definitions for the two rules Silwood Park. Berkshire, and were derived from that if egg-load assessment is based upon a rela- the populations used by Bellows (1932). These tive rule. then eggs should be laid on the I-egg have been in culture for at least 100 seeds at a higher rate in the high density grid generations and so can be considered as adapted than on the low. However. if only the present to similar conditions which prevail in seed egg-load is involved in egg-laying decisions (an stores. Egg-loads reached a maximum mean of absolute rule). then the o\iposition rate on the about 15 eggs per seed in culture. I-egg seeds should be the same in the two grids In order to obtain seeds with suitable egg (,Table 1). loads. newly emerged adults (0-12 h old) were It also follows that in both grids oviposition collected from stock cultures 24 h prior to each should be at a higher rate on the 1-egg seeds than series of tests. Varying numbers of these adults on the higher egg-densit!. seeds. and that the (about 16, 80 and 130) were placed in small oviposition rate on Segg seeds should be greater plastic dishes (400 ml) containing approximately than that on 11-egg seeds. The overall oviposi- 100 cowpeas each. and allowed to oviposit for tion rate results from a combination of the rate 24 h. The adults Mere then sieved out and the on the high-density seeds and on the low-density number of eggs on each seed counted until seeds. If an absolute rule is operating then the enough 1-egg. 5-egg and 1 1-egg seeds had been overall oviposition rate will be greater on lotv- collected for that clay's trials. Thus. all eggs used density grids than on the high. However. no such in experiments were less than 36 11 old at the predictions can be made if a relative rule is time they were used. As oviposition markers operating because the overall rate on the two persist after egg shell removal (Messina & Ren- grids is dependent on the exact form of the rule. wick. 1985b) the required egg-loads were As a consequence of a decrease in the female's achieved naturally and not by scraping off motivation to la! and/or of a shortage of mature surplus egg\. eggs (pers. obs. ). the rate at which C.tiincrtlarits Young, virgin females were required for each oviposition trial in order to ensure that no egg- laying had occurred prior to testing. Seeds coii- 'FABLE 1. Prcdiciionh for qg-laying rates in grids of high and low egg-density. taining adults ready to emerge were removed from the stock boxes approximately S h prior to Seed rbpe Dmmn rule

_. ~ __ the first test and placed in individual cells of a Relati\ e A bsol u t e divided petri-dish. After 1 h. adults which had __ - 1-egg seeds H>L H=L emerged during this time were removed and 5/ 1 I -egg seeds L>H 1 >H pairs (one of each sex) placed in 35 ml plastic All seeds LrH pots without seeds and allowed to mate. Thus all H=oviposition rate in high-density grid (mean 6 females used in tests had not previously laid any eggsiseed); L=oviposition rate in low-density grid eggs: were less than 1 h old prior to mating; and (mean 3 eggs/seed). were mated to virgin males of similar age. In Egg laying decisions by Callosobruchw 111 order to ensure enough time for mating to occur when seeds are without eggs (Mitchell, 1975; successfully and for maturation of the eggs pers. obs.), therefore only egg-laden seeds were within the newly emerged females, the pairs used. There was no difference in the mean were left for at least a further 4 h. Preliminary weights of seeds with different egg-loads (as experiments showed this method gave the most shown by random sampling). At the start of each consistent results. Females were not trial the test female was placed, using a small anaesthetized prior to testing, and only the non- paintbrush, into the centre of the grid, and an flying ‘normal’ phase adults were used in experi- inverted 400 ml dish placed over the top to pre- ments. ‘Active’ form females, which emerge at vent escape. high larval densities (Utida, 1972), were The trial began when the female mounted the extremely rare in culture and were discarded, as first seed and for the next hour the ’s were females which failed to lay within the first behaviour was observed and recorded using a 20 min of a trial. BBC microcomputer as a real-time event recorder. Each animal was used for just one Experimental design trial, and trials on the low-density and high- density grids were performed alternately. A Sixteen egg-laden seeds were placed 20 mm maximum of six trials per day was achieved. At apart on a clean filter paper divided into a 4x4 the end of the trial, the number of eggs laid was grid. Each row and each column of the grid confirmed by counting each seed’s egg-load and contained two 1-egg seeds and two 5-egg or comparing this with the figures recorded. There 11-egg seeds. Seed weight may be an important was no significant difference in the mean weights factor in a female’s choice of oviposition site of females in each group.

LOUNGE 6% GROOM 3%

C

B

I INSPECT 27% I I MARCH 20% I A

STILL 2 0 010

I LAYING 9% 1

FIG. 2. An ethogram for ovipositing C.maculatus. Figures given are the mean percentage times spent performing each activity. There were no significant differences in these times between grid types. 112 Kenneth Wilson

Oviposition behaviour ‘Rejection time’ was the time spent on the seed surface in visits which did noiresult in an Eight mutually exclusive behaviours (Fig. 2) oviposition. were defined: Using these definitions, egg-laying propensity Inspect: time spent walking over a new seed was measured in the following four ways: (i) the before either stopping (usually prior to egg-lay- probability of accepting a seed for oviposition: ing) or leaving the seed. acceptance probability; (ii) the time taken to Still: time spent motionless on the seed sur- accept a seed for oviposition or to reject it: face (usually before or after egg-laying). acceptance/rejection times; (iii) the number of Laying: time during which the female’s eggs laid on each accepted seed; (iv) the number ovipositor was more or less permanently of eggs laid per seed encountered. extended. Each of these four variables was calculated March: time spent walking over the surface of separately for the 1-egg seeds and for the higher a seed other than the initial inspect walk. egg-load (5-egg/ll-egg) seeds in both grids. Travel: time spent on the arena floor between Mean values were calculated using the average seeds. from each female for which a mean could be Hike: walking outside the boundary of the determined. Thus the maximum sample size for grid, i.e. on the arena walls. each grid mean (for figures given in Tables 2-6) Lounge: time spent inactive on the sides of the was 16. arena. Groom: time spent cleaning antennae and limbs (usually outside the grid boundary). Results The oviposition behaviour sequence, for the Overall oviposition rate purpose of calculating rates, was defined as the time spent laying plus any time spent motionless Females on both the high- and low-density immediately prior to or following oviposition. grids laid an average of 11 eggs during the 1 h ‘Acceptance time’ was defined as the time trial (Fig. 3), the rate of egg-laying decreasing taken from arriving at a seed to starting oviposi- over the test period (Fig. 4). An analysis of tion behaviour. covariance indicates that there was no significant

Low density

High density

I I 0 10 20 30 40 50 60 Time (min) FIG. 3. Cumulative egg production by C.maculatus on high and low egg-density grids (means calculated using sixteen females for each grid type;. Egg laying decisions by Callosobruchus 113

Low density

High density

0 10 20 30 40 50 60 Time (min)

FIG. 4. Egg-laying rate by C.maculatus on high and low egg-density grids (means calculated using sixteen females for each grid type).

difference between the grids in the relationship series of Fisher Exact Probability Tests, compar- between oviposition rate and time (ANCOVA: ing the proportion of females from each grid- test for homogeneity of slopes: type which oviposited during each 10 min period F(1,380)=0.2762, P>O.l; test of intercepts: of the trial, approached significance. The overall F( 1,381)= 13308, P>O. 1). If an absolute rule probability of acceptance for individual females were being used, a higher overall rate of oviposi- did not differ between the grid densities (Table tion would be expected on the low-density grid 2). It therefore seems safe to conclude that the than on the high. Although the difference is not probability of accepting a I-egg seed for oviposi- significant, the regression line for the low-den- tion is independent of the mean egg density of sity grid is slightly higher than that for the high- the grid. This is consistent with the predictions density grid, therefore the absolute rule cer- based on an absolute rather than a relative rule tainly cannot be discounted at this stage. No (Table 1). prediction can be made for a female using a (b) 5-egglII-egg seeds. The probability of relative rule (see Table 1). accepting 5-egg seeds for oviposition also declines with time (rs= -0.369, N=82, PO.9). In other words there was no consistent bability Test: P

- (a 1 I - egg seeds 0 -

T

Low density ? Hlgh density

i

I (b) 5/11-egg seeds w +':j 08 - M m f 04 "a - - U * 02 * a ,A ,A - Y * r CTlnc, 0 10 20 30 40 50 60 Time [rnin) FIG 5. Acceptance probabilities for seeds in high and low egg-density grids (means calculated using only females which inspected seeds during each 10 min period, therefore sample sizes vary between eight and sixteen for each grid type).

TABLE 2. Probability of accepting a seed for oviposition (mean +SE [sample sue]). Seed egg-load High-density grid Low-density grid 1 0.4620.07 (161 (U=103; NS) 0.5320.13 [16] (U=2; ***) (U=O; ***) 1115 0.02f0.01 [16] (U=77.5; (*)) 0.04f0.01 [16] Mann-Whitney U test: NS, not significant; (*)P

Seed acceptancelrejection times There was no significant difference in the mean 1-egg acceptance times in the two grids. (a) Acceptance time. The time between a This provides further evidence that an absolute female arriving at a seed and her laying an egg on rule may be used by ovipositing females. As that seed did not alter significantly during the predicted by both rules, individuals took signifi- course of each trial in either grid (rsg0.192, cantly longer to accept 11-egg seeds for oviposi- N379, NS). Analysis was therefore performed tion than 5-egg seeds (Table 3). If females used a on the mean acceptance times for individuals relative rule one would predict that they might during each trial. take longer to accept 1-egg seeds on the low- Egg laying decisions by Callosobruchus 115 density grid than on the high-density grid. ences. However, the small sample size for 11-egg Clearly, this didn't happen. seeds should be noted. (b) Rejection time. There was no significant difference between the rejection times for the Mean number of eggs laid per encountered seed four seed types (Table 4). The mean number of eggs laid per encoun- tered seed is the product of the probability of seed acceptance and the number of eggs laid per Number of eggs laid per accepted seed accepted seed. There was no significant differ- The mean number of eggs laid on accepted ence between the mean number of eggs laid on seeds did not alter significantly during the course each 1-egg seed encountered on high- and low- of the trial in either grid (r5~-0.193,Ns79, density grids. However, significantly more eggs NS). The means for individual beetles in the two were laid on 5-egg seeds than on 11-egg seeds, grids were therefore compared. Significantly and more on I-egg seeds than on seeds with more eggs were laid on accepted I-egg seeds higher egg-load (Table 6). This is further evi- than on S-egg seeds in the low-density grids dence for females using an absolute rather than a (Table 5). There were no other significant differ- relative rule.

TABLE 3. Time (s) to accept a seed for oviposition (mean ISE [sample sizel). Seed egg-load ____ High-density grid Low-density grid 1 67.7k8.1[16] (U=120; NS) 60.0k3.9[16] I U=4:*) (U=69.5;NSI 1115 125.3223.4[3] (U=2;*) 71.6+0.01 [16] Mann-Whitney Utest: NS, not significant; (*)P

TABLE 4. Time (s) to reject a seed for oviposition (mean +SE [sample size]). Seed egg-load High-density grid Low-density grid 1 18.154.9 [16](U=84; NS) 22.0f4.4[16] (U=77;NS) (U=71 (*)) 1115 10.5f1.9[16] (U=lOO; NS) 11.7k1.4(161 Mann-Whitney U test; NS, not significant; (*)P

TABLE 5. Number of eggs laid per accepted seed (mean 2SE [sample size]). Seed egg-load High-density grid Low-density grid 1 1.71k0.16[16] (U=105; NS) 1.5120.16 [16] (U=13;NS) (U=34;*) 11/5 1.33k0.34131 (U=12;NSI 1.3020.24 1101 Mann-Whitney Utest; NS. not significant; (*)P

TABLE 6. Number of eggs laid per seed encountered (mean +SE lsamole sizelI. Seed egg-load High-density grid Low-density grid 1 0.8720.20[16] (U=122;NS) 0.84f0.21[16] (U=2;** *) (U=2;** *) 1115 0.02+0.01 [16](U=79; (*)) 0.0610.02[16] Mann-Whitney U test; NS, not significant; (*)P

The trends presented above were determined behavioural observations to solve what are on the assumption that a female’s motivation to essentially behavioural problems. Previous lay is dependent on time rather than the number studies on the oviposition strategies of of eggs already laid. Comparisons have phytophagous insects have concentrated on the therefore been made between groups, in various end result of an oviposition bout to make measures of oviposition rate. in relation to time. inferences about the behavioural mechanisms As a female’s motivation to lay may instead be operating (e.g. Mitchell, lY75: Messina & Ren- dependent on the number of eggs laid. the wick. 1Y85a). In the present study, oviposition analyses were repeated comparing the various rates were derived solely from the time spent measure4 of oviposition rate in relation to the making the appropriate egg-laying decisions, number of eggs laid. No differences were found and hence are a more accurate reflection of between the two analyses: therefore only the C. rnaciclarits egg-laying behaviour. time-dependent analysis is presented above. The results indicate that when assessing egg- load the beetles do not utilize information obtained during the course of the oviposition Discussion boiit concerning mean egg-loads. A number of The results indicate that the overall oviposition models have heen developed in recent years to rate declines over time. but at a similar rate for describe how animals. in a variety of situations, both grid densities. This is due primarily to a should use information about the mean utility of decline in the probability of accepting a seed for their environment to make choices about how to oviposition. ruther than to a lengthening of the behave whilst within resource patches which acceptance time or a decrease in the number of form part of that environment (e.g. Charnov. eggs laid on accepted seeds. 1976; Parker & Stuart, 1976; Cook & Hubbard. The probability of accepting a 1-egg seed for 1979; Smith & Lessells, 1985). Although very oviposition. and the rime taken to accept the few studies to date have explicitly attempted to seed. do not differ between grid densities. test these models. those which have (e.g. Krebs Honever. female\ take longer to accept. and er al., 1974: Hubhard Cyr Cook. 1Y7X; Wange. accept felver. 11-egg seeds than 5-egg seeds. 1979). support the notion that decisions are Oncr a seed has been accepted. the number of dependent upon an assessment of the average eggs a beetle uill lay appears to be negatively utility of the environment (i.c. relative rules are correlated with the current egg-load of the seed. used). However. Charnov tv a/. (1981) The egg-laying rate on the I-egg seeds does demonstrated that the sex ratio of offspring pro- not differ between the two grid types. The ovi- duced by the braconid wasp Hrterospiliy pro- position rate on the 5-egg seeds is significantly sopidis.which lays its eggs on the larvae of bean greater than on the I 1-egg seeds however. These . is dependent upon the age of the current results are consistent with the hypothesis that host but is independent of the proportion of female C.mucrc/arirs are using an absolute rather hosts of that age in the environment. Thus than a relative rule in deciding whether or not to Hrrrrosyilis uses an absolute rule in deciding the lay on a 5eed. that is. only the egg-load of the sex ratio of its offspring. current seed. and not those of previously Therefore. although absolute rules do appear encountered seeds. influences the decision to to operate in nature. they are apparently very oviposit. Not all relative rules are excluded scarce. The reason for this becomes clear when though. For instance, the results do not exclude one considers the simulations described earlier a rule in which the probability of laying on a seed (see Fig. I). At both high and low mean egg- with less than the mean egg-load is con4tant but loads finely-discriminating absolute rules pro- decrease5 monotonically as the current seed’s duce very uniform distributions of eggs. egg-load exceeds the mean forthe environment However, when the average egg-load of seeds is (FIg. le). It would prove her! difficult to per- high. females which use absolute rules spend form the nece\sar! experiments to make all of much time visiting seeds which they subse- the distributions required in order to exclude the quently reject. For example. in simulation (b) possibility of a relative rule kine used by approximately 11 .OOO seeds were visited before ovipositing females. all 500 eggs were laid, compared with about 1100 Thk study demonstrates the usefulness of visits required in simulations (d)and (e). Ilence. Egg laying decisions by Cal[osobruchus 117 the egg-laying rate was slower when using an Bellows, T.S., Jr (1982) Analytical models for labora- absolute rule rather than a relative rule. tory populations of and There are several possible explanations for C.maculatus (Coleoptera. Bruchidae). Journal of Animal Ecology, 51,263-287. why Cmuculutus uses an absolute rule. Firstly, if Charnov, E.L. (1976) Optimal foraging, the marginal high mean egg-loads are uncommon in the value theorem. Theoretical Population Biology. 9, natural environment, then the ability to respond 129-136. to such a situation (and hence to evolve a relative Charnov, EL., Los-den Hartogh. R.L., Jones, W.T. & van den Assem, J. (1981) Sex ratio evolution in a rule), would not necessarily be selected for. patchy environment. Nature, 289, 27-33. However, bruchids have probably been associ- Cook, R.M. & Hubbard, S.F. (1977) Adaptive search- ated with seed stores for several thousand years ing strategies in parasites. Journal ofAnima1 (Southgate, 1978), and so the natural conditions Ecology, 46, 115-125. which this animal faces may be considered as Dick, K.M. & Credland, P.F. (1984) Egg production and development of three strains of similar to those which prevail in culture, where Callosobruchus maculatus (F) (Coleoptera: high egg-loads are the norm rather than the Bruchidae). Journal of Stored Products Research, exception. Secondly, if the cost (in terms of 20, 221-227. time, energy, or egg-equivalents) of travelling Fretwell, S.D. & Lucas, H.L. (1970) On territorial behaviour and other factors influencing habitat dis- between seeds is low compared to the benefits of tribution in birds. Acta Biorheoretica, 19, 16-36. producing a near-uniform distribution, then Hubbard, S.F. &Cook, R.M. (1978) Optimal foraging there would not be strong selection to reduce the by parasitoid wasps. Journal of Animal Ecology, number of unsuccessful seed visits. Thirdly, one 47, 593-604. may speculate that the neural apparatus Jackai, L.E.N. & Daoust, R.A. (1986) Insect pests of cowpeas. Annual Review of Entomology, 31, required for an effective memory trace, a prere- 95-119. quisite for any relative rule. has a greater cost Krebs, J.R., Ryan. J.C. & Charnov, E.L. (1974) than any benefit of using a relative instead of an Hunting by expectation or optimal foraging? A absolute rule. If this is true, then natural selec- study of patch use by chickadees. Animal tion would favour individuals which used the Behaviour, 22, 953964. Messina, F.J. & Renwick, J.A.A. (1985a) Ability of ‘cheaper’ absolute rule. ovipositing seed beetles to discriminate between Further studies are required before general seeds with different egg-loads. Ecological statements can be made regarding the pre- Entomology. 10, 225-230. valence of absolute rules in nature and about the Messina, F.J. & Renwick, J.A.A. (1985b) Mechanism for egg recognition by the weevil sorts of situations in which we might expect them Callosobruchus maculatus. Entomologia Experi- to evolve. mentalis et Applicata, 31, 241-245. Mitchell, R. (1975) The evolution of oviposition tac- tics in the bean weevil, Callosobruchus mnculatus (F.). Ecology, 56, 696-702. Acknowledgments Parker, G.A. & Stuart, R.A. (1976) Animal behaviour as a strategy optimiser: evolution of I would like to thank Kate Lessells for helpful resource assessment strategies and optimal emigra- discussion of my work and for reading numerous tion thresholds. American Naturalist. 110, 1055- earlier drafts of the manuscript. I am also grate- 1076. Smith, R.H. & Lessells, C.M. (1985) Oviposition, ful to Geoff Parker, Alex Kacelnik. Paul Lam, ovicide and larval competition in granivorous Adrian del Nevo and an anonymous referee for insects. Behavioural Ecology: ecological conse- their comments. This research was supported by quences of adaptive behaviour (ed. by R. M. Sibly a studentship from the Natural Environment and R. H. Smith). pp. 423-448. Blackwell Scien- Research Council. tific Publications, Oxford. Southgate, B.J. (1978) The importance of the Bruchidae as pests of grain legumes, their distribu- tion and control. Pests of Grain Legumes: ecology References and control (ed. by S. R. Singh, H. F. van Emden and A. Taylor). pp. 219-229. Academic Press, Avidov, Z., Applebaum, S.W. & Berlinger, M.J. London. (1965) Physiological aspects of host specificity in Southgate, B.J. (1979) Biology of the Bruchidae. the Bruchidae. 11. Ovipositional preference and Annual Review of Entomology, 24, 449-473. behaviour of Callosobruchus chinensis L. Utida, S. (1943) Studies on the experimental popula- Entoniologia Experimentalis et Applicata, 8, tion of the azuki bean weevil, Callosobruchus 9&-106. chinensis (L.). VIII. Statistical analysis of the fre- 115 Kenneth Wilson

quency distribution of the emerging weevils on Waage. J.K. (1979) Foraging for patchily-distributed beans. Memoirs of rhe College of Agriciilrirre, hosts by the parasitoid. Nerneritis cunescerzs. Jow- Kyoro Imperial Ghiiwsiiy. 54, 1-22, rid of Ariimal Ecology, 48, 353-371. Utida. S. (1972) Density-dependent polymorphism in the adult Callosohriichits rnacularus (Coleoptera. Bruchidae). Jortriiul of Stored Proditcis Resewch, 8, 111-126. Accepted 27 June 1987