Using Food for Different Purposes: Female Responses to Prey in the Predator Coccinella Septempunctata L. (Coleoptera: Coccinellidae)

Ecological Entomology (2004) 29, 27–34

Using food for different purposes: female responses to prey in the predator Coccinella septempunctata L. (Coleoptera: Coccinellidae)

EDWARD W. EVANS, DOUGLAS R. RICHARDS andANUPAMA KALASKAR Department of Biology, Utah State University, Logan, U.S.A.

Abstract. 1. Although predatory insects often feed on diverse prey, their reproductive activity may be linked most strongly to a more restricted range of prey. The propensity of adult females of the ladybird beetle, Coccinella septempunctata L., to attack two natural prey species, pea aphids [Acyrthosiphon pisum (Harris)] and alfalfa weevil larvae [Hypera postica (Gyllenhal)], was compared, and the degree to which ladybird egg production depends on consumption of aphids vs. weevils was assessed. 2. Coccinella septempunctata females more readily attacked aphids than weevil larvae. This was true regardless of whether females had fed previously on aphids or on weevil larvae. 3. When females were provided with few to many aphids daily, or few aphids plus an excess number of weevil larvae, their rates of egg production depended primarily on the number of aphids consumed. 4. Addition of weevil larvae to diets of limited numbers of aphids increased egg production, but only modestly. Thus, consumption of weevil larvae may have served mostly for self-maintenance, thereby enabling females to use for egg production more of the nutrients and energy obtained from limited consumption of aphids. 5. The females’ linkage of egg production primarily to aphid rather than weevil consumption may be adaptive, as their offspring are much less able as larvae to survive and mature on a diet of weevils rather than aphids. Key words. Aphidophagous, Coccinellidae, diet, oviposition, predation, prey quality, reproductive strategy.

Introduction duction) and alternative prey (those that in the absence of essential prey, serve simply as a source of energy and nutri- Although many predatory insects appear to be opportunis- ents to maintain the predator). Focusing on adult preda- tic generalists in their diets, the suitability of different prey tors, Dixon (2000) further distinguished between nursery for the predator’s growth and reproduction can vary widely prey, patches of which may elicit predator oviposition, (e.g. Strohmeyer et al., 1998; Eubanks & Denno, 2000; and the broader category of food prey consumed by the Michaud, 2000; Stamp, 2001). Thus Hodek (1962) distin- predators to sustain themselves. guished broadly between essential prey (those that support These distinctions are well-illustrated by ladybird beetles both immature growth and development, and adult repro- (Coleoptera: Coccinellidae) that prey especially on aphids (e.g. Hodek, 1973; Gordon, 1985; Hodek & Honeˇk, 1996; Dixon, 2000). Although some species in this group have Correspondence: E. W. Evans, Department of Biology, Utah State relatively broad diets and reproduce readily upon consum- University, Logan, UT 84322-5305, U.S.A. E-mail: ewevans@ ing non-aphid prey (e.g. Putnam, 1957; Schanderl et al., biology.usu.edu 1988; Hazzard & Ferro, 1991; Munyaneza & Obrycki,

# 2004 The Royal Entomological Society 27 28 Edward W. Evans, Douglas R. Richards and Anupama Kalaskar

1997; Phoofolo & Obrycki, 1997), others appear more nar- (1962). In this case, the maximum benefit of consuming rowly tied to aphids and reproduce little if at all unless weevils would be the release from maintenance to egg pro- aphids are present in their diet (e.g. see reviews by Hagen, duction of the full amounts of nutrients and energy pro- 1987; Hodek & Honeˇk, 1988). Adults of the genus vided by the small number of aphids also consumed. Coccinella, for example, consume larvae of Coleoptera Overall, these two experiments with differing levels of and Lepidoptera, but females become reproductively aphid and weevil availability for the predators enabled the inactive when these prey serve as the sole diet (Richards & determination of whether egg production by C. septempunctata Evans, 1998; Evans, 2000). Reproduction by these preda- depends primarily on the rate of aphid consumption even tors is enhanced, however, when a diet of aphids in limited when other prey are also available. supply is supplemented with larvae of the alfalfa weevil [Hypera postica (Gyllenhal)] (Evans et al., 1999). Here it is examined how the availability of alfalfa weevil Materials and methods larvae influences the reproductive output of females of Coccinella septempunctata L. This Palearctic species has Insects now also become abundant throughout North America (e.g. Schaefer et al., 1987; Maredia et al., 1992; Elliott Overwintered adults of C. septempunctata were collected et al., 1996). Both in North America (e.g. Evans & England, from alfalfa fields near Logan, Utah, in May 2000 during 1996) and its native range (e.g. Yakhontov, 1934; Honeˇk, the latter part of the first crop of alfalfa. They appeared free 1980), it occurs commonly in alfalfa fields where it feeds on of disease and were unparasitised (rates of parasitism of this larvae of the alfalfa weevil as well as on pea aphids species in these fields in May 1998–1999 were estimated at [Acyrthosiphon pisum (Harris)]. Larvae of the univoltine less than 1%; E. W. Evans, unpubl. data). Thereafter the alfalfa weevil are most abundant in spring and early sum- adults were maintained on a diet of pea aphids in an incu- mer. Adult ladybirds can be observed frequently in the field bator at cool temperature (13 C, LD 14:10 h) for two to feeding on the larvae at this time, although such prey use several weeks before being used for experiments. Pea aphids may arise largely from opportunistic attacks upon encoun- were collected from broad bean (Vicia faba L.) grown in the ter as the predators search alfalfa primarily for aphid prey. greenhouse. Alfalfa weevil larvae as well as aphids were The propensity of adult females of C. septempunctata to used in experiments; the weevils were collected in alfalfa attack alfalfa weevil larvae vs. pea aphids is assessed here fields in late May and early June, and refrigerated until use. first; the contribution of weevil consumption to egg production by this predator when aphid availability is limited is assessed thereafter. Weevil consumption may either indir- Behavioural observations ectly or directly enhance egg production. It may do so indirectly by enabling a female to meet her nutrient and To prepare for observations of individual predators energy needs for self-maintenance (as suggested by Hodek, exposed to prey, females were removed from the incubator 1962 and Dixon, 2000). This would free her from devoting with cool temperature and placed as paired individuals in to such needs nutrients and energy obtained from consum- Petri dishes (9 cm diameter) in a second incubator at 22 C, ing a limited number of aphids; instead she could produce LD 14:10 h. For the next 3 days, they were provided with more eggs to the extent set by the quantity of aphids con- either pea aphids of mixed ages, or weevil larvae (fourth sumed. Alternatively, aphids in the diet may serve to stimu- instar). In either case, prey were provided in excess. Prey late ladybird reproductive physiology (e.g. by providing were then withheld from all predators for one additional specific nutrients not present in alternative prey such as day. Thereafter, females were observed after placing them weevils). Once such is stimulated, however, a female may individually in Petri dishes (5 cm diameter) that had been consume other prey not only to meet her maintenance stocked immediately before with five prey individuals. One needs, but also to increase directly her egg production. female of each pair was placed randomly with five adult pea In previous experiments (Evans et al., 1999), these differ- aphids, and the other female with five weevil larvae (fourth ent possibilities were not distinguished. In the two experi- instar). Thus, females were observed attacking prey for four ments presented here, these possibilities were assessed treatment combinations of prey (aphids or weevils) pro- by comparing egg production among females of vided prior to observations prey (aphids or weevils) pro- C. septempunctata L. provided with few to many aphids, or vided during observations. One hundred and twenty few aphids but also an excess supply of weevil larvae. If females (i.e. 30 females for each treatment combination) consumption of weevils serves to promote egg produc- were selected initially for the experiment. Two females tion directly as well as indirectly (i.e. by contributing to died, however, while being fed aphids prior to observations. self-maintenance), females may lay as many or more eggs Thus, only 29 females were observed for the treatment com- when provided with few aphids but numerous weevils, as binations: aphids provided prior to observations aphids when provided with many aphids. On the other hand, or weevils provided during observations. females that consume few aphids may produce relatively Predator–prey encounters were observed under ambient few eggs regardless of whether weevils are also available, if conditions (21–24 C) on a laboratory bench exposed to the latter prey serve merely as alternative prey sensu Hodek windows and daylight. Each female was observed for a

# 2004 The Royal Entomological Society, Ecological Entomology, 29, 27–34 Ladybird responses to prey 29 maximum of 10 min as she searched, and the number of ations that attacked a prey during 10 min of observation. encounters with prey (i.e. instances in which the predator For females that attacked a prey, the number of encounters physically contacted the prey) was recorded. Many encoun- with prey that occurred before the predator attacked, and ters were brief; the predator moved away from the prey the time that the predator spent feeding on the prey, were within 2 s or less (if the predator physically contacted an examined with two-way ANOVA (with Type III sums of individual prey after she had previously contacted and squares for unbalanced design) for effects of prey (aphids moved away from that prey, this was scored as another or weevils) provided prior to vs. during observations, and encounter). Predators that made a clear effort to attack for their interaction (SAS Institute, 1998). To homogenise the prey (i.e. predators that remained with the prey and variances among treatment combinations, the number of attacked it for at least two seconds) were observed for up encounters was transformed by taking the square root to 10 min once the attack began. prior to analysis. The number of eggs produced on differing diets in the two experiments was examined by using multivariate Egg production on varied diets repeated measures analysis following square root transform- ation (SAS Institute, 1998). For each experiment, egg Two experiments were conducted with C. septempunctata counts were combined into five 3-day periods (e.g. the first adults kept as mixed pairs (male and female) in Petri dishes to third day) prior to analysis (this was done to retain (9 cm diameter) at 22 C, LD 14:10 h. Pairs were placed in sufficient degrees of freedom in the analysis; Von Ende, these conditions 1 week prior to the start of an experiment, 1993). Data were omitted for females that died during and were fed pea aphids in excess daily during this week. By experiments. In the first experiment, these individuals the start of the experiment, all females had mated and were included one female from a pair provided with five aphids actively producing eggs. plus weevils each day, and two females from pairs provided The first experiment began 2–3 weeks after adults had with 10 aphids each day. In the second experiment, they been collected from the field. Ten pairs of C. septempunctata included one female from a pair provided with 10 aphids were assigned systematically to each of four diets provided each day, and two females from pairs provided with daily during the experiment: (1) five aphids (predators were 10 aphids plus weevils each day. Because the design was provided with adults of the pea aphid in this and other therefore unbalanced, Type III sums of squares were used treatments), (2) five aphids plus 20 alfalfa weevil larvae in analyses. (fourth instar), (3) 10 aphids, or (4) 20 aphids. Females were paired with males throughout the experiment to promote a high level of reproductive activity. Females of Results C. septempunctata eat greater quantities of prey than do males but the two sexes are similar in their relative con- Behavioural observations sumption rates of aphids and weevil larvae (E. W. Evans, unpubl. data). Each pair of C. septempunctata was trans- When C. septempunctata females were exposed to prey for ferred to a new Petri dish each morning, and provided with 10 min, a higher percentage of individuals attacked a pea new prey. The numbers of eggs laid by females were aphid than attacked a weevil larva (Fig. 1a). This was espe- recorded three times throughout each day for 15 days cially evident for females that had previously fed on aphids (based on casual observations made before and during the (Fig. 1a; w2 ¼ 15.82, P < 0.0001). A similar but less pro- experiment, it was assumed that eggs were fertile). In the nounced pattern was evident for females that had fed pre- few instances in which cannibalism occurred, the number of viously on weevil larvae (Fig. 1a; w2 ¼ 6.67, P ¼ 0.001). A eggs consumed by adults was determined (and included in higher percentage of females attacked the prey (both weevils the total count) from the egg remains or yellow spot left and aphids) when they had previously fed on weevil larvae behind. Males (but not females) that died during the experi- rather than on aphids. This was most striking when weevils ment were replaced. were offered as prey (Fig. 1a; w2 ¼ 14.34, P ¼ 0.0002). A The second experiment began 5–6 weeks after adults were similar but less striking pattern occurred when aphids collected from the field. Procedures identical to those of the were offered as prey (Fig. 1a; w2 ¼ 5.65, P ¼ 0.017). first experiment were used, except that pairs were provided Among females that attacked a prey, fewer encounters with more aphids. Thus, 10 pairs of C. septempunctata were tended to occur with aphids than with weevils before the assigned systematically to each of the following four diets predator attacked; this was true both when predators had provided daily: (1) 10 aphids, (2) 10 aphids plus 20 alfalfa fed previously on aphids and when they had fed previously weevil larvae (fourth instar), (3) 20 aphids, or (4) 30 aphids. on weevil larvae (Fig. 1b; two-way ANOVA, effect of prey type offered: F1,83 ¼ 3.44, P ¼ 0.067; interaction of effects of prey type offered and prey type consumed previously: Statistical analyses F1,83 ¼ 0.33, P ¼ 0.56). For a given type of prey (aphid or weevil), more encounters with the prey occurred before an Chi-square analyses (Daniel, 1978) were used to compare attack when the predator had previously been fed aphids percentages of females from different treatment combin- than when the predator had previously been fed weevil

# 2004 The Royal Entomological Society, Ecological Entomology, 29, 27–34 30 Edward W. Evans, Douglas R. Richards and Anupama Kalaskar

100 weevils before abandoning them). Females that attacked (a) aphids and females that attacked weevils spent similar Aphids 80 amounts of time feeding on the prey; this was true both of Weevils females that had fed previously on aphids and of females that had fed previously on weevils (Fig. 1c, two-way ANOVA, 60 effect of prey type offered: F1,83 ¼ 0.63, P ¼ 0.43; interaction of effects of prey type offered and prey type consumed 40 previously: F1,83 ¼ 0.19, P ¼ 0.66). Females that had fed previously fed on weevils, however, spent longer consuming 20 prey (aphids or weevils) than females that had fed pre- % of predators attacking viously on aphids (Fig. 1c, two-way ANOVA, effect of prey 0 type consumed previously: F1,83 ¼ 13.02, P ¼ 0.0005). Aphids Weevils Prey provided previously 7 Egg production on varying diets (b) 6 Pairs of C. septempunctata adults in both experiments Aphids 5 consumed all aphids (or on rare occasions, almost all Weevils aphids) provided each day (the dry weight of an aphid was 4 0.6–0.7 mg). Those pairs that were also provided with weevil 3 larvae consumed these prey as well; pairs killed a mean (þ SE) of 5.9 þ 0.5 weevils per day in the first experiment, 2 and 5.8 þ 0.8 weevils per day in the second experiment (the 1 dry weight of a weevil larva was 2.2–2.6 mg; predators usually did not consume fully the entire carcass of weevils No. of encounters before attack of encounters before No. 0 killed, however). Egg production in the first experiment Aphids Weevils dropped rapidly to very low levels when pairs were provided Prey provided previously with five aphids daily, especially when this diet was not 600 supplemented with weevils (Fig. 2). Egg production when (c) Aphids pairs were provided with 10 aphids daily also dropped after 500 Weevils the first 3 days, but remained much higher for the remainder of the experiment than that of pairs provided with five 400 aphids plus weevils. Egg production was high throughout 300 the experiment for pairs provided with 20 aphids daily. These differences in egg production among females led to 200 a significant interaction between treatment and time (multivariate repeated measures analysis, interaction of treat- 100 ment time: Wilks’ l ¼ 0.337, F12,79 ¼ 3.38, P < 0.001).

Time (seconds) spent feeding Several females of pairs provided with only five aphids 0 daily (with or without weevils) laid no or almost no (only Aphids Weevils one or two) eggs after the first day (when egg production Prey provided previously likely was highly influenced by aphid consumption prior to Fig. 1. Results of encounters with prey when females of Coccinella the experiment). Of the remaining females, those fed weevils septempunctata that had fed previously on pea aphids or alfalfa as well as five aphids daily laid significantly more eggs from weevil larvae were placed with five pea aphids (fully shaded bars) the second day on than did those fed only five aphids daily or five weevil larvae (dappled bars). (a) Percentage of females that (x þ SE: 54.5 þ 10.6 vs. 26.3 þ 7.4 eggs; F1,13 ¼ 6.39, attacked an aphid or a weevil larvae within 10 min after being P ¼ 0.025). Even those reproductively active females that placed with the prey. (b) Mean number of encounters with prey were fed weevils as well as aphids, however, produced (þ 1 SE) that occurred before a female attacked an aphid or a many fewer eggs from the second day on than did females weevil larva for those females attacking within the first 10 min. (c) of pairs provided 10 aphids per day (x þ SE: 54.5 þ 10.6 vs. Mean length of time (in seconds, þ1 SE) that females that attacked 139.9 þ 34.9 eggs; F ¼ 7.26, P ¼ 0.017). spent feeding on aphids or weevil larvae. 1,14 Egg production in the second experiment again rapidly declined when pairs were fed only 10 aphids daily, particu- larvae (two-way ANOVA, effect of prey type consumed pre- larly when this diet was not supplemented with weevils viously, F1,83 ¼ 20.39, P < 0.0001). (Fig. 3). Females of pairs fed 20 aphids daily consistently In all but two cases, attacking predators succeeded in produced substantially more eggs than females of pairs fed subduing the prey and consuming it for at least 20 s (in the 10 aphids plus weevils, and the disparity in egg production two exceptions, females spent only 5 and 11 s attacking between these two treatments increased over time. Females

# 2004 The Royal Entomological Society, Ecological Entomology, 29, 27–34 Ladybird responses to prey 31

45 45 5A 10A 40 40 5A + W 10A + W 20A 10A 35 35 20A 30A 30 30 25 25 20 20 15 15 10 10 Number of eggs laid per day Number of eggs laid per day 5 5 0 0 D1–3 D4–6 D7–9 D10–12 D13–15 D1–3 D4–6 D7–9 D10–12 D13–15 Fig. 3. Mean number of eggs laid per day by a female (þ 1 SE) Fig. 2. Mean number of eggs laid per day by a female (þ 1 SE) when paired adults of Coccinella septempunctata were provided 10 when paired adults of Coccinella septempunctata were provided five (‘10A’), 20 (‘20A’), or 30 (‘30A’) adult pea aphids daily, or 10 such (‘5A’), 10 (‘10A’), or 20 (‘20A’) adult pea aphids daily, or five such aphids and an excess supply of weevil larvae (‘10A þ W’). Mean aphids and an excess supply of weevil larvae (‘5A þ W’). Mean daily egg production is presented for successive 3-day periods daily egg production is presented for successive 3-day periods throughout the 15-day experiment [e.g. the mean number of eggs throughout the 15-day experiment [e.g. the mean number of eggs laid per day during the first 3 days (‘D1–3’) of the experiment]. laid per day during the first 3 days (‘D1–3’) of the experiment]. aphidophagous ladybirds to consume more aphids than of pairs fed 30 aphids daily produced greatest numbers of non-aphid prey when given the choice (e.g. Hussain, 1975; eggs throughout the experiment. As in the first experiment, Ouayogode & Davis, 1981; Lucas et al., 1997; but see also these differences in egg production among females led to a Gagne´et al., 2002, who found that larvae of Coleomegilla significant interaction between treatment and time (multi- maculata lengi Timberlake prefer conspecific eggs over aphids). variate repeated measures analysis, interaction of treat- In the present study, greater percentages of C. septempunctata ment time: Wilks’ l ¼ 0.49, F12,79 ¼ 2.04, P ¼ 0.03). females attacked aphids than attacked weevil larvae, and fewer The most dramatic drop in egg production by females of encounters with aphids vs. weevil larvae occurred before pairs provided 10 aphids daily with or without weevils attack. This was true even when females were maintained on occurred early in the second experiment (Fig. 3). Several a weevil diet prior to observations. Thus, previous feeding females in these two treatments laid no or almost no (four experience did not affect the predators’ basic tendency to or fewer) eggs after the first 3 days. Of the remaining attack aphids more readily than weevils. Similarly, Hagler females, females fed weevils as well as 10 aphids daily laid and Cohen (1991) found that prey preferences of the big-eyed significantly more eggs from the fourth day on than did bug Geocoris punctipes (Say) did not vary between field- females fed only 10 aphids daily (x þ SE: 81.2 þ 19.9 vs. captured individuals and individuals reared in the lab on 31.6 þ 7.2 eggs; F1,11 ¼ 6.85, P ¼ 0.026). These reproduct- artificial diet. Hattingh and Samways (1992) also found that ively active females that were fed weevils as well as aphids, feeding history did not influence food choice of the coccine- however, produced far fewer eggs from the fourth day on llids Chilocorus nigritus (Fabricius) and C. bipustulatus (L.), than did females of pairs provided with 20 aphids per day although these species showed no strong preference in any (x þ SE: 81.2 þ 19.9 vs. 204.7 þ 24.8 eggs; F1,13 ¼ 8.59, case. P ¼ 0.012). Previous feeding experience influenced the tendency of C. septempunctata females to attack prey of both types in the experiment reported here. Thus females that were main- Discussion tained on a weevil vs. aphid diet prior to observations more readily attacked both weevils and aphids, and fed on both Although they may attack diverse kinds of prey, predatory longer. Previous experience in attacking weevils may have insects often show distinct prey preferences in both feeding increased the propensity of females to attack this prey type (e.g. Digweed, 1993; Eubanks & Denno, 2000; Stamp, 2001) (e.g. Bergelson, 1985; Barron, 2001); fourth instar weevils and reproduction (e.g. Hoelmer et al., 1993; Richards & often thrashed in defence when touched and this may have Evans, 1998; Spieles & Horn, 1998). Coccinella septempunctata deterred inexperienced females especially from attacking. in particular is a member of a group of ladybirds that That the females also attacked aphids more readily, how- feed on many kinds of prey but appear to specialise in ever, suggests that hunger played a part. Thus females that preying upon aphids (Gordon, 1985; Hagen, 1987; Hodek had been provided previously with weevils were likely less & Honeˇk, 1996; Dixon, 2000). Previous studies have shown satiated during observations than females that had been

# 2004 The Royal Entomological Society, Ecological Entomology, 29, 27–34 32 Edward W. Evans, Douglas R. Richards and Anupama Kalaskar provided previously with aphids. Overall, the behavioural of Coccinella spp. become reproductively inactive when results reflect the aphidophagous nature of C. septempunctata limited solely to non-aphid diets of larvae of Coleoptera females in indicating that these predators have greater pro- and Lepidoptera (Richards & Evans, 1998; Evans, 2000)? pensity to attack aphids vs. weevils, particularly when they Aphids may possess specific nutrients required for ladybird have ample access to aphids. reproduction that are lacking or present only in small The aphidophagous nature of C. septempunctata females amounts in alternative prey (e.g. see Hagen, 1987). Further- is also apparent in the experimental results for egg produc- more, as noted by Dixon (2000) in his discussion of nursery tion on varying diets. Thus, in both experiments, the num- prey, the behaviour of female ladybirds in this regard may ber of eggs produced by a female depended primarily on the be adaptive. Larvae of C. septempunctata are much less able number of aphids consumed. Females provided with abun- to survive and mature on a diet of weevil larvae than on a dant weevil larvae in addition to limited numbers of aphids diet of pea aphids (Kalaskar & Evans, 2001). By not produ- produced relatively few more eggs than females provided cing large numbers of eggs through consumption of weevil only with limited numbers of aphids. In the first experiment, larvae when only few aphids are present, a female may provision of weevils delayed the rapid collapse in egg pro- avoid placing her offspring in an unfavourable environ- duction when pairs were placed on a diet of only five aphids ment. In contrast, by setting her rate of egg production each day. Thereafter, females became so inactive reproduct- primarily by her rate of consumption of aphids, a female ively when pairs were provided with only five aphids daily, may succeed in placing her offspring in environments that that consumption of weevil larvae provided little benefit for are relatively well-suited for their development. Her ability egg production. Previous studies have similarly documented to do so is further enhanced by her tendency to become less a minimum rate of consumption or density of aphids to active as her rate of aphid consumption increases (e.g. support active reproduction in this and related species Banks, 1956; Dixon, 1959; Frazer & Gill, 1981; Nakamuta, (e.g. Honeˇk, 1978, 1980; Ives, 1981a). The existence and 1987). Thus, a female that encounters and consumes aphids level of such a minimum rate likely reflects the basic at low rates may continue to disperse through the environ- trade-off between reproduction and longevity; female lady- ment in search of suitable oviposition sites even as she is birds may be adapted to survive well at low prey densities in maturing small numbers of eggs (e.g. Ives, 1981b; Ives et al., part by reducing their reproductive effort (e.g. Valicente & 1993; van der Werf et al., 2000). In contrast, at higher aphid O’Neil, 1995). densities and rates of consumption, flight activity of females Females remained more active in egg production drops markedly and they lay eggs locally at high rates throughout the second experiment when pairs were pro- (Honeˇk, 1985; Takahashi, 1993; but see also Hemptinne vided with a minimum diet of 10 aphids daily. Consumption et al., 1992; Dixon, 1997). of weevil larvae modestly enhanced egg production as the Thus the relative specialisation of lady beetles such as second experiment progressed. In neither experiment, how- C. septempunctata on aphid prey, as reflected both in the ever, did females produce as many eggs when abundant greater propensity of females to attack aphids vs. weevils weevil larvae and a limited number of aphids were provided and in the primacy of aphid consumption in promoting egg as when twice as many aphids (but no weevils) were pro- production, may have its ultimate basis particularly in fac- vided. The modest increase in egg production when weevils tors and constraints associated with larval foraging (e.g. see were available may reflect that females consumed these prey Dixon, 1959, 1970; Wratten, 1973). In attacking prey such primarily to gain nutrients and energy for self-maintenance. as weevil larvae, adults may use the energy and nutrients They then could devote to egg production more nutrients gained primarily for self-maintenance. They may thereby and energy as set by aphid consumption than could females also reap a modest benefit indirectly in egg production whose limited diet of aphids was not supplemented with when such is limited by aphid availability. weevils. Both predator and prey condition likely influenced absol- ute rates of egg production in the two experiments. Females Acknowledgements of pairs fed 10 and 20 aphids daily laid fewer eggs in the second experiment than in the first. This may reflect adverse We thank Andrew Nelson for maintaining aphid cultures effects of prolonged storage at cool temperature prior to the and assisting with experiments, and two referees and the start of the second experiment, or greater age of the females associate editor for commenting on the manuscript. (e.g. Dixon & Agarwala, 2002). When pairs were provided Financial support was provided by the U.S.D.A.-N.R.I. with 30 adult pea aphids daily, rates of egg production were (99-35302-8104) and the Utah Agricultural Experiment similar to those reported previously for C. septempunctata Station. (Hodek & Honeˇk, 1996) but nonetheless may have reflected that pea aphids reared on broad beans are less nutritious for C. septempunctata than pea aphids reared on alfalfa (see References Giles et al., 2002). Why do C. septempunctata females not use the opportun- Banks, C.J. (1956) The distribution of coccinellid egg batches and ity to produce more eggs when aphid numbers are low but larvae in relation to numbers of Aphis fabae Scop. on Vicia faba. weevils are abundantly available? Similarly, why do females Bulletin of Entomological Research, 47, 47–56.

# 2004 The Royal Entomological Society, Ecological Entomology, 29, 27–34 Ladybird responses to prey 33

Barron, A.B. (2001) The life and death of Hopkins’ host-selection Hazzard, R.V. & Ferro, D.N. (1991) Feeding responses of adult principle. Journal of Insect Behavior, 14, 725–737. Coleomegilla maculata (Coleoptera: Coccinellidae) to eggs of the Bergelson, J. (1985) A mechanistic interpretation of prey selection by Colorado potato beetle (Coleoptera: Chrysomelidae) and green Anax junius larvae (Odonata: Aeshnidae). Ecology, 66, 1699–1705. peach aphids (Homoptera: Aphididae). Environmental Entomol- Daniel, W.W. (1978) Applied Nonparametric Statistics. Houghton ogy, 20, 644–651. Mifflin, Boston, MA. Hemptinne, J.-L., Dixon, A.F.G. & Coffin, J. (1992) Attack Digweed, S.C. (1993) Selection of terrestrial gastropod prey by strategy of ladybird beetles (Coccinellidae): factors shaping their Cychrine and Pterostichine ground beetles (Coleoptera, Cara- numerical response. Oecologia, 90, 238–245. bidae). Canadian Entomologist, 125, 463–472. Hodek, I. (1962) Essential and alternative food in insects. Dixon, A.F.G. (1959) An experimental study of the searching Transactions of the XIth International Congress of Entomology, behaviour of the predatory coccinellid beetle Adalia decempunc- Vol. 2 (ed. by H. Strouhal and M. Beier), pp. 697–698. tata (L.). Journal of Animal Ecology, 28, 259–281. Organisationalskomittee des XI Internationalen Kongress fu¨r Dixon, A.F.G. (1970) Factors limiting the effectiveness of the Entomologie, Vienna. coccinellid beetle, Adalia bipunctata (L.), as a predator of the Hodek, I. (1973) Biology of Coccinellidae. Czechoslovak Academy sycamore aphid, Drepanosiphum platanoides (Schr.). Journal of of Science, Prague. Animal Ecology, 39, 739–751. Hodek, I. & Honeˇk, A. (1988) Sampling, rearing, and handling of Dixon, A.F.G. (1997) Patch quality and fitness in predatory aphid predators. Aphids: Their Biology, Natural Enemies and ladybirds. Ecological Studies: Analysis and Synthesis, 130, 205–233. Control, Vol. 2B (ed. by A. K. Minks and P. Harrewijn), Dixon, A.F.G. (2000) Insect Predator–Prey Dynamics. Ladybird pp. 311–321. Elsevier, Amsterdam. Beetles and Biological Control. Cambridge University Press, Hodek, I. & Honeˇk, A. (1996) Ecology of Coccinellidae. Kluwer Cambridge, U.K. Academic Publishers, Dordrecht, The Netherlands. Dixon, A.F.G. & Agarwala, B.K. (2002) Triangular fecundity Hoelmer, K.A., Osborne, L.S. & Yokomi, R.K. (1993) Reproduc- function and ageing in ladybird beetles. Ecological Entomology, tion and feeding behavior of Delphastus pusillus (Coleoptera, 27, 433–440. Coccinellidae), a predator of Bemisia tabaci (Homoptera, Elliott, N.C., Kieckhefer, R.W. & Kaufmann, W. (1996) Effects of Aleyrodidae). Journal of Economic Entomology, 86, 322–329. an invading coccinellid on native coccinellids in an agricultural Honeˇk, A. (1978) Trophic regulation of postdiapause ovariole landscape. Oecologia, 105, 537–544. maturation in Coccinella septempunctata (Col. Coccinellidae). Eubanks, M.D. & Denno, R.F. (2000) Health food versus fast Entomophaga, 23, 213–216. food: the effects of prey quality and mobility on prey selection Honeˇk, A. (1980) Population density of aphids at the time of by a generalist predator and indirect interactions among prey settling and ovariole maturation in Coccinella septempunctata species. Ecological Entomology, 25, 140–146. (Col.: Coccinellidae). Entomophaga, 25, 427–430. Evans, E.W. (2000) Egg production in response to combined Honeˇk, A. (1985) Activity and predation of Coccinella septempuncta- alternative foods by the predator Coccinella transversalis. ta adults in the field (Col.: Coccinellidae). Zeitschrift fu¨r Entomologia Experimentalis et Applicata, 94, 141–147. angewandte Entomologie, 100, 399–409. Evans, E.W. & England, S. (1996) Indirect interactions in Hussain, M. (1975) Predators of the alfalfa weevil, Hypera postica,in biological control of insects: pests and natural enemies in western Nevada – a greenhouse study (Coleoptera: Curculionidae). alfalfa. Ecological Applications, 6, 920–930. Journal of the New York Entomological Society, 83, 226–228. Evans, E.W., Stevenson, A.T. & Richards, D.R. (1999) Essential Ives, P.M. (1981a) Feeding and egg production of two species versus alternative foods of insect predators: benefits of a mixed of coccinellids in the laboratory. Canadian Entomologist, 113, diet. Oecologia, 121, 107–112. 999–1005. Frazer, B.D. & Gill, B. (1981) Hunger, movement, and predation Ives, P.M. (1981b) Estimation of coccinellid numbers and move- of Coccinella californica on pea aphids in the laboratory and in ment in the field. Canadian Entomologist, 113, 981–997. the field. Canadian Entomologist, 113, 1025–1033. Ives, A.R., Kareiva, P. & Perry, R. (1993) Response of a predator Gagne´, I., Coderre, D. & Mauffette, Y. (2002) Egg cannibalism by to variation in prey density at three hierarchical scales: lady Coleomegilla maculata lengi neonates: preference even in the beetles feeding on aphids. Ecology, 74, 1929–38. presence of essential prey. Ecological Entomology, 27, 285–291. Kalaskar, A. & Evans, E.W. (2001) Larval responses of aphido- Giles, K.L., Madden, R.D., Stockland, R., Payton, M.E. & phagous lady beetles (Coleoptera: Coccinellidae) to weevil larvae Dillworth, J.W. (2002) Host plants affect predator fitness via versus aphids as prey. Annals of the Entomological Society of the nutritional value of herbivore prey: investigation of a America, 94, 76–81. plant–aphid–ladybeetle system. Biocontrol, 47, 1–21. Lucas, E., Coderre, D. & Vincent, C. (1997) Voracity and feeding Gordon, R.D. (1985) The Coccinellidae (Coleoptera) of America preferences of two aphidophagous coccinellids on Aphis citricola north of Mexico. Journal of the New York Entomological and Tetranychus urticae. Entomologia Experimentalis et Applicata, Society, 93, 1–912. 85, 151–159. Hagen, K.S. (1987) Nutritional ecology of terrestrial insect Maredia, K.M., Gage, S.H., Landis, D.A. & Scriber, J.M. (1992) predators. Nutritional Ecology of Insects, Mites, Spiders and Habitat use patterns by the seven-spotted lady beetle (Coleoptera: Related Invertebrates (ed. by F. Slansky and J. G. Rodriquez), Coccinellidae) in a diverse agricultural landscape. Biological pp. 533–577. John Wiley and Sons, New York. Control, 2, 159–165. Hagler, J.R. & Cohen, A.C. (1991) Prey selection by in vitro-reared Michaud, J.P. (2000) Development and reproduction of ladybeetles and field-reared Geocoris punctipes. Entomologia Experimentalis (Coleoptera: Coccinellidae) on the citrus aphids Aphis spiraecola et Applicata, 59, 201–205. Patch and Toxoptera citricida (Kirkaldy) (Homoptera: Aphidi- Hattingh, V. & Samways, M.J. (1992) Prey choice and substitution dae). Biological Control, 18, 287–297. in Chilocorus spp. (Coleoptera, Coccinellidae). Bulletin of Munyaneza, J. & Obrycki, J.J. (1997) Reproductive response of Entomological Research, 82, 327–334. Coleomegilla maculata (Coleoptera: Coccinellidae) to Colorado

# 2004 The Royal Entomological Society, Ecological Entomology, 29, 27–34 34 Edward W. Evans, Douglas R. Richards and Anupama Kalaskar

potato beetle (Coleoptera: Chrysomelidae) eggs. Environmental Lymatriidae) predator Calosoma sycophanta (Coleoptera: Cara- Entomology, 26, 1270–1275. bidae). Environmental Entomology, 27, 458–462. Nakamuta, K. (1987) Diel rhythmicity of prey-search activity and Stamp, N.E. (2001) Effects of prey quantity and quality on its predominance over starvation in the lady beetle, Coccinella predatory wasps. Ecological Entomology, 26, 292–301. septempunctata bruckii. Physiological Entomology, 12, 91–98. Strohmeyer, H.H., Stamp, N.E., Jarzomski, C.M. & Bowers, M.D. Ouayogode, B.V. & Davis, D.W. (1981) Feeding by selected (1998) Prey species and prey diet affect growth of invertebrate predators on alfalfa weevil larvae. Environmental Entomology, predators. Ecological Entomology, 23, 68–79. 10, 62–64. Takahashi, K. (1993) Daily behavior of adult Coccinella Phoofolo, M.W. & Obrycki, J.J. (1997) Comparative prey septempunctata brucki (Coleoptera, Coccinellidae). Japanese suitability of Ostrinia nubilalis eggs and Acyrthosiphon pisum Journal of Entomology, 61, 839–845. for Coleomegilla maculata. Biological Control, 9, 167–172. Valicente, F. & O’Neil, R.J. (1995) Effects of host plants and Putnam, W.L. (1957) Laboratory studies on the food of some feeding regimes on selected life history characteristics of Podisus coccinellids (Coleoptera) found in Ontario peach orchards. maculiventris (Say) (Heteroptera: Pentatomidae). Biological Canadian Entomologist, 96, 1149–1155. Control, 5, 449–461. Richards, D.R. & Evans, E.W. (1998) Reproductive responses of Von Ende, C.N. (1993) Repeated-measures analysis: growth and aphidophagous lady beetles (Coleoptera: Coccinellidae) to non- other time-dependent measures. Design and Analysis of Eco- aphid diets: an example from alfalfa. Annals of the Entomological logical Experiments (ed. by S. M. Scheiner and J. Gurevitch), Society of America, 91, 632–640. pp. 113–137. Chapman & Hall, New York. SAS Institute (1998) User’s Manual, Version 7.0. SAS Institute, van der Werf, W., Evans, E.W. & Powell, J. (2000) Measuring and Cary, North Carolina. modelling the dispersal of Coccinella septempunctata (Coleoptera: Schaefer, P.W., Dysart, R.J. & Specht, H.B. (1987) North Coccinellidae) in alfalfa fields. European Journal of Entomology, American distribution of Coccinella septempunctata (Coleoptera: 97, 487–493. Coccinellidae) and its mass appearance in coastal Delaware. Wratten, S.D. (1973) The effectiveness of the coccinellid beetle, Environmental Entomology, 16, 368–373. Adalia bipunctata (L.), as a predator of the lime aphid, Schanderl, H., Ferran, A. & Garcia, V. (1988) L’e´levage de deux Eucallipterus tiliae L. Journal of Animal Ecology, 42, 785–802. coccinelles Harmonia axyridis et Semiadalia undecimnotata a` Yakhontov, V.V. (1934) The alfalfa weevil Phytonomus (Phytono- l’aide d’oeufs d’Anagasta kuehniella tue´s aux rayons ultraviolets. mus variabilis Hbst.). Review of Applied Entomology Series A, 22, Entomologia Experimentalis et Applicata, 49, 235–244. 334–336. Spieles, D.J. & Horn, D.J. (1998) The importance of prey for fecundity and behavior in the gypsy moth (Lepidoptera: Accepted 28 July 2003

# 2004 The Royal Entomological Society, Ecological Entomology, 29, 27–34