Selection of Molting and Pupation Sites by Coleomegilla Maculata (Coleoptera: Coccinellidae): Avoidance of Intraguild Predation

Home , Coleomegilla, Coleomegilla maculata

COMMUNITY AND ECOSYSTEM ECOLOGY Selection of Molting and Pupation Sites by Coleomegilla maculata (Coleoptera: Coccinellidae): Avoidance of Intraguild Predation

1 2 1 E´ RIC LUCAS, DANIEL CODERRE, AND JACQUES BRODEUR

Environ. Entomol. 29(3): 454Ð459 (2000) ABSTRACT Molting and pupating insects are especially vulnerable to natural enemies and one possible component of their defensive strategy is the selection of suitable microhabitats. We hypothesized that larvae of the lady beetle Coleomegilla maculata lengi Timberlake select molting and pupation sites that effectively reduce their susceptibility to intraguild predation. We charac- terized microsites on potato plants and evaluated their associated risk of predation by the lacewing Chrysoperla ruﬁlabris Burmeister (Neuroptera: Chrysopidae), a common intraguild predator. The majority of molts (Ͼ60%) occurred on potato plants in sites similar to those used by mobile coccinellid larvae. In contrast, 90% of the larvae left the plant to pupate. Second, third, and fourth instars selected artiÞcial shelters for both molting and pupation when these were available. Vul- nerability of pupae and newly molted larvae to lacewing larvae depended on plant microsite, with leaves supporting an aphid colony as the most risky sites. Molting and pupating microhabitat selection by coccinellid larvae appears to be a trade-off between the advantages of remaining close to the aphid resource, and the costs of being exposed to intraguild predators.

KEY WORDS Coleomegilla maculata, habitat selection, molt, pupation, intraguild predation, defense

ONTOGENIC TRANSFORMATION PHASES like shedding (am- nough (Ephemeroptera: Ephemerellidae) molt more phibians, reptilians, birds) or molting and metamor- frequently during the daytime when predatory stone- phosis (arthropods) may disrupt physiological, mor- ßies are less active (Soluk 1990). The springtail Iso- phological, and behavioral patterns of animals. Such toma carpenteri Borner (Collembola: Isotomidae) de- disruptions temporarily handicap normal reproduc- lays molting when predation risk by pseudoscorpions tive, foraging, and defensive functions (Soluk 1990). is high (Witt and Dill 1996). For instance, shedding and molting individuals are Pupation is a more complex process than molting, usually more vulnerable to intraspeciÞc (Polis 1981, and involves thorough physiological and morpholog- Crump 1992), intraguild (Dick et al. 1990) and extra- ical transformations, such as genesis of sexual organs guild predation (Soluk 1990) than foraging individu- and wings. Pupae are usually sessile and protected by als. One of the main detrimental effects associated morphological (Hinton 1955, Vo¨lkl 1995), chemical with shedding and molting is reduced locomotion (Edmunds 1974, Bowers 1992, Attygalle et al. 1993), (Wassersug and Sperry 1977). Consequently, sessile and behavioral defenses (Hinton 1955). Prepupating stages cannot display escape or aggressive behaviors stages have been shown to select pupation sites that normally displayed by mobile individuals. lower the probability of predation or of hyperparasit- Holometabolous insects are immobile (or sessile) as ism. For example, Brodeur and McNeil (1989, 1992) eggs and pupae as well as during molting. Molting, a showed that the aphid parasitoid Aphidius nigripes periodic process of shedding the exoskeleton, is di- Ashmead (Hymenoptera: Braconidae) has the ability vided into two phases: exuviation, the shedding of the to induce its host to leave the aphid colony and mum- old cuticule, and postexuviation, the scleriÞcation of mify in microhabitats where the incidence of pupal new teguments. The insect usually remains immobile hyperparasitism is reduced. Tschinkel (1981) ob- during the Þrst phase, whereas it can move during the served that tenebrionid larvae tend to disperse just second. Few studies have evaluated the vulnerability before pupation, to presumably reduce cannibalism. of molting insects to natural enemies. However, it has Also, aquatic larvae of Toxorhynchites sp. (Diptera: been shown that molting individuals may reduce mor- Culicidae) enter a phase of “frenzy killing” at the end tality through avoidance of parasitoids and predators of their larval development and eliminate, without by selecting a less exposed site or by delaying molting. feeding on them, all invertebrate predators they en- Larvae of the mayßy Ephemerella subvaria McDun- counter in the habitat (Corbet and GrifÞths 1963). In this study we assessed the susceptibility to pre- 1 Centre de Recherche en Horticulture, De´partement de Phytolo- dation of molting and pupating of the lady beetle gie, Universite´ Laval, Sainte-Foy, QC, Canada G1K 7P4. Coleomegilla maculata lengi Timberlake to the lace- 2 De´partement des Sciences Biologiques, Universite´ du Que´bec a` Montreál, C.P. 8888 Succ. Centre-ville, Montreál, QC, Canada H3C wing Chrysoperla rufilabris Burmeister (Neuroptera: 3P8. Chrysopidae). Both species are common predators of

0046-225X/00/0454Ð0459$02.00/0 ᭧ 2000 Entomological Society of America June 2000 LUCAS ET AL.: MOLTING AND PUPATION SITE SELECTION BY C. maculata 455 potato aphids (Burke and Martin 1956, Mack and established. It was then compared with the position of Smilowitz 1980, Legaspi et al. 1994) and occur simul- the following molting larva or pupa on the plant (like- taneously in potato Þelds (Obrycki et al. 1983). The lihood ratio G test). The distance-indexes (exuvia- immature coccinellid goes through four larval instars, colony) of the molting larvae and of the pupa were therefore three molts, before pupating (Warren and compared by a MannÐWhitney U test. Tadic 1967). Just before molting and pupating, the Selection of an Artificial Shelter. Tests were per- larva stops feeding and attaches itself to the substrate formed to evaluate the utilization of an artiÞcial shel- by the anal pseudopod (Majerus 1994). As shown by ter (refuge) by molting and pupating coccinellid lar- Lucas et al. (1997, 1998), larvae and pupae of C. macu- vae. A C. maculata larva was placed in a petri dish (5 lata are highly vulnerable to intraguild predation. In by 1 cm) covered with muslin. Each petri dish con- this article, we tested the hypothesis that coccinellid tained a moist cotton wick (1.5 by 0.5 cm), pollen as larvae select molting and pupating sites that lower a food source and a packing clear plastic bubble as a their mortality by natural enemies. We Þrst charac- shelter (3 by 3 cm). Because the plastic shelter was terized and compared the within plant distribution of transparent, light intensity should not be a signiÞcant molting, pupating, and mobile C. maculata larvae. factor in site selection. Four stages (C. maculata L1, Next, we determined how molting and pupation site Þrst molt; L2, second molt; L3, third molt; L4, pupa- selection might reduce the probability of attack by the tion) were tested and the position of exuviae found on intraguild predator C. rufilabris. the petri dish, cotton wick, pollen, or plastic shelter was recorded. Twenty replicates were carried out per treatment. A theoretical randomized distribution of Materials and Methods exuviae on the four sites was calculated based on their Chrysoperla rufilabris and C. maculata were pur- relative surface (petri dish, 77% of total surface; cotton chased from Groupe Biocontroˆle (Sainte-Foy, Can- wick, 2.5%; pollen, 1.6%; and plastic shelter, 18.9%). ada) and reared on the potato aphid Macrosiphum The theoretical and observed distributions of each euphorbiae Thomas at 23 Ϯ 2ЊC and a photoperiod of coccinellid instar for molting/pupating sites were 16:8 (L:D) h. All experiments were carried out under compared using a G test. the same environmental conditions. Vulnerability of Mobile and Molting Larvae. Vul- Distribution of Molting Larvae, Pupae, and Mobile nerability of mobile and molting C. maculata larvae to Larvae. A potato plant with 4Ð6 leaves was placed in C. rufilabris was evaluated on a potato stem (10Ð13 a plastic container (15 cm high by 12 cm diameter), cm), bearing one leaf (6 by 5 cm) at a height of 3Ð5 cm. with a muslin covered lid that prevented insects from Molting larvae were collected from rearing units after escaping. The stem of the plant passed through a hole they had attached to the substrate but before exuvi- in the cage ßoor into a second container Þlled with ation. A mobile (L1, L2, L3, or L4) or a molting larva water. Leaves were identiÞed as follows: the lowest (Þrst, second, or third) of C. maculata was placed in leaf: F1, the second leaf: F2, and so on. An aphid colony the center of the upper surface of the leaf. A third- was established, using clip-cages, on the second leaf instar C. rufilabris, starved for 24 h before the test, was (F2), 24 h before the test. The aphid density was Þxed introduced on the stem with its head facing the leaf. at 20, 30, 40, and 50 aphids (second instar) for C. The experiment ended after the chrysopid killed the maculata L1, L2, L3, and L4, respectively, and main- coccinellid, the coccinellid left the leaf, or 30 min had tained every day. A trial started by introducing a coc- elapsed. A replicate was considered valid when the cinellid larva at the base of the plant, a minimum of lacewing came in contact (face on) with the coccinel- 24 h before molting and terminated once molting or lid. The occurrence of predation during the exuviation pupation occurred. As exuviae remained attached on and postexuviation phases were recorded. The pro- the plant, their position was an accurate indication of portion of fatal contacts was calculated by dividing the transformation sites. Exuviae were recorded as being number of contacts from the chrysopid that caused the found on or off the plant, and for those on the plant, death of the coccinellid by the total number of con- the precise location (F1, F2, F3Ð6, terminal, stem) was tacts between the two predators. Fifteen trials were determined. For mobile larvae, their position on the conducted per treatment. Mortality of mobile larvae plant was recorded every hour over a 24-h period. A and molting larvae, as well as the proportion of fatal minimum of 15 replicates were carried out for each contacts during the exuviation and postexuviation larval instar. A distance-index was attributed for each phases were compared using likelihood ratio G tests. exuvia, based on its position compared with the aphid Risk Associated to Molting Site. Coccinellid vulner- colony position: (1) exuvia on the same leaf, same ability to C. rufilabris during the molting process was leaßet and same surface as the colony; (2) exuvia on evaluated at different sites on the potato plant. Given the same leaf, same leaßet, but on the surface opposite the difÞculty in synchronizing coccinellid molts, we to the colony; (3) exuvia on the same leaf, but on a used second-instar C. maculata larvae pinned by their leaßet other than the colony; (4) exuvia on a leaf other last abdominal segment to the plant and considered than the colony; (5) exuvia off the plant. these to be “pseudomolting larvae.” Pseudomolting Distribution of molting and pupation sites were larvae did not have a superior defensive capacity than compared according to their position (likelihood ratio molting larvae because they were not able to escape G test). The average occurrence of mobile larvae on and because C. maculata second-instar larvae did not each part of the plant or outside of the plant was have efÞcient aggressive defenses against C. rufilabris 456 ENVIRONMENTAL ENTOMOLOGY Vol. 29, no. 3

Fig. 1. Distribution of molting and pupation sites selected by C. maculata larvae on a potato plant (on the left). Corresponding mortality of C. maculata pinned larvae in the presence of a C. rufilabris third-instar larva (on the right). Different letters indicate a signiÞcant difference in C. maculata mortality between sites (G test, P Ͻ 0.05). NA, nonap- plicable. Fig. 2. Distribution of molting and pupation sites selected by C. maculata larvae in a petri dish. The asterisk third-instar larvae (Lucas et al. 1997). In addition, indicates a signiÞcant difference between the two selected Ͼ90% of nonattacked pseudomolting larvae were alive bars (G test, P Ͻ 0.05). after 24 h. Pseudomolting larvae were Þxed in 14 different sites on the plant: on the stem, on the terminal pupa, P Ͻ 0.001; second molt versus pupa, P Ͻ 0.001; portion and on both surfaces, and on the edge and the and third molt versus pupa, P Ͻ 0.001). Different larval center of leaves F1, F2, and F3ϩ. Forty M. euphorbiae instars chose similar distances from the aphid colony second-instar aphid nymphs were introduced on the for molting (MannÐWhitney U, Þrst versus second second leaf (F2) and kept in a clip-cage 24 h before the molt, P ϭ 0.506; Þrst versus third molt, P ϭ 0.225; beginning of the experiment. The test started with the second versus third molt, P ϭ 0.137). introduction of a third-instar C. rufilabris larva on the Selection of an Artificial Shelter. In petri dishes, petiole of the second leaf. Fifteen replicates were molting and pupation sites were similar (G ϭ 16.04, conducted. After 24 h, the mortality of pseudomolting df ϭ 9, P Ͼ 0.050; Fig. 2). Second molt (G ϭ 12.59, df ϭ larvae by the lacewing was determined under a stereo 3, P Ͻ 0.010), third molt (G ϭ 20.81, df ϭ 3, P Ͻ 0.005), microscope. Mortality of pseudomolting larvae was and pupation (G ϭ 9.27, df ϭ 3, P Ͻ 0.050) occurred compared by likelihood ratio G tests according to the more often in the shelter than was predicted based on position on the plant (F1, F2, F3Ð6, terminal, stem), as its surface area (18.90%). well as the surface and the position (edge or center) Vulnerability of Mobile and Molting Larvae. First on the leaf. molting larvae were no more susceptible to lacewing predation than mobile Þrst and second instar larvae (G ϭ 1.23, df ϭ 1, P Ͼ 0.250; Fig. 3). However, older Results molting/pupating stages were more vulnerable to pre- Distribution of Molting Larvae, Pupae, and Mobile dation than mobile large coccinellid larvae (second Larvae. Molting larvae occurred in microhabitats sim- molt versus second and third instar, G ϭ 12.02, df ϭ 1, ilar to those used by foraging mobile larvae (L1 versus P Ͻ 0.005; third molt versus third and fourth instar, G Þrst molting larva, G ϭ 10.83, df ϭ 5, P Ͼ 0.050; L2 ϭ 15.50, df ϭ 1, P Ͻ 0.005). Mortality was similar for versus second molting larva, G ϭ 8.94, df ϭ 5, P Ͼ the three molting larvae (G ϭ 0.901, df ϭ 2, P Ͼ 0.500), 0.100; L3 versus third molting larva, G ϭ 10.48, df ϭ 5, but the proportion of fatal contacts was signiÞcantly P Ͼ 0.050). There was no signiÞcant difference among higher during exuviation than during the postexuvia- sites selected for Þrst, second, and third molting (G ϭ tory phase (Þrst molt, G ϭ 33.67, df ϭ 1, P Ͻ 0.005; 14.11, df ϭ 10, P Ͼ 0.100), most with molts occurring second molt, G ϭ 9.66, df ϭ 1, P Ͻ 0.005; third molt, on the plant. All parts of the plant were used for G ϭ 35.05, df ϭ 1, P Ͻ 0.005; Fig. 4). molting except for the stem (Fig. 1, left). The terminal Risk Associated to Molting Site. Vulnerability of portion was used only by Þrst instars. coccinellid pseudomolting larvae to lacewing preda- Pupation sites differed signiÞcantly from molting tion differed greatly according to the site on the plant sites (G ϭ 47.15, df ϭ 15, P Ͻ 0.001; Fig. 1, left), as 90% (G ϭ 66.49, df ϭ 4, P Ͻ 0.005; Fig. 1, right), the leaf (n ϭ 20) of fourth-instar larvae left the plant to pupate bearing the aphid colony (F2) being the most risky on the cage. Mobile fourth-instar larvae foraged in site for molting/pupating. Leaves without aphids (F1 microhabitats different from sites selected for pupa- and F3ϩ) were the safest microhabitats (G ϭ 4.45, tion (G ϭ 14.27, df ϭ 5, P Ͻ 0.025). The distance df ϭ 1, P Ͻ 0.050). Susceptibility of pseudomolting between the pupation site and the aphid colony was larvae was similar on the different parts of the leaf greater than the distance between the molting site and (G ϭ 0.09, df ϭ 1, P Ͼ 0.750) and also on both surfaces the aphid colony (MannÐWhitney U, Þrst molt versus (G ϭ 0.97, df ϭ 1, P Ͼ 0.250). June 2000 LUCAS ET AL.: MOLTING AND PUPATION SITE SELECTION BY C. maculata 457

metamorphosis stages (Wilbur 1980). Thus, for highly vulnerable transformation phases, the selection of a protected site could be an effective defensive strategy against predation. Our study revealed that microhabitat selection differed signiÞcantly for premolting and prepupating larvae of C. maculata. In fact, the majority of molts occurred on the plant, in sites used by mobile larvae, whereas 90% of fourth instar larvae left the plant to pupate. Premolting and prepupating larvae face the same trade-off: maximizing growth rate versus minimizing mortality caused by natural enemies. Microhabitat selection might have evolved to counterbalance the risks of mortality during prospection for a suitable site (prospection risk), mortality during the molt/pupation stages (site predation risk), and losing the aphid resource (resource-dependency). The extent to which each of these risks modulate microhabitat selection appears to differ for premolting and prepupating larvae of C. maculata. Fig. 3. Mortality of mobile and molting larvae of C. macu- Molts occurred on the plants close to the aphid lata in the presence of a C. rufilabris third-instar larva. The asterisk indicates a signiÞcant difference between molting colony in sites used by mobile larvae. In this instance, and mobile larvae (G test, P Ͻ 0.05). premolting larvae secure their resource-dependency and reduce prospection risk. Starvation is a major factor of mortality for coccinellid larvae once aphid Discussion colonies had collapsed (Majerus 1994). Coccinellid In organisms with complex life cycles such as am- larvae have poor prey detection capacities and it phibians and holometabolous insects, frequent habitat seems that they must come in contact with prey to shifts occur, either during or between larval, adult, and detect them (New 1991). Prospecting for a safe molting site could be dangerous for larvae because it in- creases the probability of fatal encounters, especially if stems are used, as they frequently are, by foraging predators (at least apterous stages and ground-leaving predators) (GrifÞths et al. 1985). When shelters were available near the aphid resource, they were preferred by second and third molting larvae, suggesting that premolting larvae actively search for and choose protected sites when prospection risks are low. Although the siteÐpredation risk is expected to be high in the vicinity of aphid colonies, its relative importance to microhabitat selection by molting coccinellids might be lessened by a time component. The clumped distribution of aphids has been shown to result in an aggregative numerical response of predators in the vicinity of the aphid colony (Frazer 1988), and in a shift from random search to area restricted search patterns by predators (Dixon 1959, Hemptinne et al. 1996). These behaviors would favor encounters among aphidophagous predators (Hassell 1978), thereby increasing site-predation risks for molting coccinellid larvae. However, the period of vulnerability of molting C. maculata larvae is relatively short because the exuviation/postexuviation phase lasts for less than an hour (i.e., Ͻ1% of the total duration of the preimaginal development). For prepupating larvae the selection of pupation sites off the host plant primarily reßects the siteÐ predation risk constraint. Pupation of C. maculata lasts Њ Fig. 4. Percentage of fatal contacts during exuviation and 3.8 d at 26.7 C, which represents 20% of its preimaginal postexuviation of C. maculata in the presence a C. rufilabris developmental time (Warren and Tadic 1967). Pupae third-instar larva. The asterisk indicates a signiÞcant differ- are therefore exposed to natural enemies for a longer ence between open and solid bars (G test, P Ͻ 0.05). period than molting individuals. Selection of a site 458 ENVIRONMENTAL ENTOMOLOGY Vol. 29, no. 3 away from the aphid colony might therefore be an pating larvae could be the main defensive strategy of adaptive response to intraguild predation. However, pupae. further work is needed to evaluate the survival of coccinellid pupae in different microhabitats and to better understand if the observed pattern results from Acknowledgments a search for enemy-free space (Berdegue et al. 1996, We thank S. Demougeot and M. Veilleux for technical Hopkins and Dixon 1997). For instance, pupae located assistance, and C. Cloutier, L.A. Giraldeau and J. McNeil for off the plants may be attacked by ground predators comments. This research was supported by grants from the like carabid beetles (Winder 1990). Prepupating lar- Natural Sciences and Engineering Research Council of Can- vae are not as resource dependent as younger instars ada (NSERC) to D.C. and J.B., and by graduate scholarships because alate imagos emerging from the pupa have a from NSERC, le Fonds pour la Formation de Chercheurs et much greater capacity to disperse and Þnd resources lÕAide a` la Recherche du Que´bec, and the Canadian Pest than larvae. Finally, prospection risks are lower for Management Society to E.L. fourth-instar coccinellids than for younger instars. Large larvae are more mobile, stronger, and less vul- References Cited nerable to predation than younger larvae (Sengonca and Frings 1985; Lucas et al. 1997, 1998). Attygalle, A. B., K. D. McCormick, C. L. Blankespoor, T. Other factors, aside from intraguild predation, may Eisner, and J. Meinwald. 1993. Azamacrolides: A family inßuence the selection of a pupating site away from of alkaloids from the pupal defensive secretion of a la- the host plant. Pupal parasitism by Phalacrotophora sp. dybird beetle (Epilachna varivestis). Proc. Natl. Acad. Sci. (Diptera: Phoridae) of the coccinellid Harmonia U.S.A. 90: 5204Ð5208. Berdegue, M., J. T. Trumble, J. D. Hare, and R. A. Redak. axyridis Pallas occurred more intensely on plants in- 1996. Is it enemy-free space? The evidence for terrestrial fested by aphids than in other pupation sites (Osawa insects and freshwater arthropods. Ecol. Entomol 21: 203Ð 1992). Similarly, the level of pupal cannibalism was 217. higher close to the aphid colony. Extraguild predation Blum, M. S. 1981. Chemical defenses of arthropods. Aca- may also induce the search for a protected pupation demic, New York. site. Some species of caterpillars select pupation sites Bowers, M. D. 1992. The evolution of unpalatability and the based on their related vulnerability to predation cost of chemical defense in insects, pp. 216Ð24. In B. D. (West and Hazel 1982, Hazel et al. 1998). The search Roitberg and M. B. Isman [eds.], Insect chemical ecology: for microclimatic conditions that reduce the duration an evolutionary approach. Chapman & Hall, New York. Brodeur, J., and J. N. McNeil. 1989. Seasonal microhabitat of pupation, and thereby the period of exposure to selection by an endoparasitoid through adaptative mod- natural enemies, can also affect site selection, as hy- iÞcation of host behavior. Science (Wash. D.C.) 244: pothesized for mummies of aphid parasitoids (Hyme- 226Ð228. noptera: Aphidiidae) Brodeur and McNeil 1992). Brodeur, J., and J. N. McNeil. 1992. Host behaviour modi- The simultaneous occurrence of various defensive Þcation by the endoparasitoid Aphidius nigripes: a strat- strategies is common among animals (Edmunds 1974), egy to reduce hyperparasitism. Ecol. Entomol. 17: 97Ð144. and for instance, several defenses used against pred- Burke, H. R., and D.F Martin. 1956. The biology of three ators are not efÞcient against parasitoids (Gross 1993). chrysopid predators of the cotton aphid. J. Econ. Ento- In addition to the predator-avoidance strategy, C. mol. 49: 698Ð700. Corbet, P. S., and A. Griffiths. 1963. Observations on the maculata pupae may also reduce mortality as a result aquatic stages of two species of Toxorhynchites (Diptera: of natural enemies through ßipping behavior, “gin- Culicidae) in Uganda. Proc. R. Entomol. Soc. Lond. A 38: traps” (sclerotized toothed along junctions of movable 125Ð135. abdominal segments; Eisner and Eisner 1992, Hinton Crump, M. L. 1992. Cannibalism in amphibians, pp. 256Ð 1955), warning coloration (Majerus 1994), and the 276. In M. A. Elgar and B. J. Crespi [eds.], Cannibalism, synthesis of toxic alkaloids (Blum 1981). ecology, and evolution among diverse taxa. Oxford Sci- The data reported here suggest that vulnerable ence Publications, Oxford. stages, such as holometabolous pupae that are exposed Dick, J.T.A., D. E. Irvine, and R. W. Elwood. 1990. Differ- for a long period and unable to ßee, may chießy adopt ential predation by males on moulted females may explain the competitive displacement of Gammarus duebeni by G. a primary defensive response (occurring regardless of pulex (Amphipoda). Behav. Ecol. Sociobiol. 26: 41Ð45. predator presence); whereas, stages exposed for a Dixon, A.F.G. 1959. An experimental study of the searching short period, such as most insect molting larvae, may behaviour of the predatory coccinellid beetle Adalia de- modify their response according to their immediate cempunctata (L.). J. Anim. Ecol. 39: 739Ð751. environment (refuge, presence of predators, and so Edmunds, M. 1974. Defence in Animals. Longman, New on). Although it was not possible to evaluate the pre- York. dation risk off the plant, based on several studies (par- Eisner, T., and M. Eisner. 1992. Operation and defensive asitism and cannibalism, Osawa 1992; numerical re- role of “gin traps” in a Coccinellid pupa (Cycloneda san- sponse, Frazer 1988; area-restricted searching, Dixon guinea). Psyche 99: 265Ð273. Frazer, B. D. 1988. Predators, pp. 217Ð230. In A. K. Minks 1959; absence of predation activity off the plant by and P. Harrewijn [eds.], Aphids: their biology, natural chrysopids, M. Canard, personal communication), we enemies and control, vol. B. Elsevier, New York. can expect that the risk was lower off the plant than Griffiths, E., S. D. Wratten, and G. P. Vickerman. 1985. close to the extraguild prey. Therefore, we can con- Foraging by the carabid Agonum dorsale in the Þeld. Ecol. clude that the search for enemy free space by prepu- Entomol. 10: 181Ð189. June 2000 LUCAS ET AL.: MOLTING AND PUPATION SITE SELECTION BY C. maculata 459

Gross, P. 1993. Insect behavioral and morphological de- Osawa, N. 1992. Effect of pupation site on pupal cannibalism fenses against parasitoids. Annu. Rev. Entomol. 38: 251Ð and parasitism in the ladybird beetle Harmonia axyridis 273. Pallas (Coleoptera: Coccinellidae). Jpn. J. Entomol. 60: Hassell, M. P. 1978. The dynamics of arthropods predator- 131Ð135. prey systems. Princeton University Press, Princeton, NJ. Polis, G. A. 1981. The evolution and dynamics of intraspe- Hazel, W., S. Ante, and B. Stringfellow. 1998. The evolution ciÞc predation. Annu. Rev. Ecol. Syst. 12: 225Ð251. of environmentally-cued pupal colour in swallowtail but- Sengonca, C., and B. Frings. 1985. Interference and com- terßies: natural selection for pupation site and pupal co- petitive behaviour of the aphid predators, Chrysoperla lour. Ecol. Entomol. 23: 41Ð44. carnea and Coccinella septempunctata in the laboratory. Hemptinne, J.-L., A.F.G. Dixon, and G. Lognay. 1996. Entomophaga 30: 245Ð251. Searching behaviour and mate recognition by males of Soluk, D. A. 1990. Postmoult susceptibility of Ephemerella the twospotted ladybird beetle, Adalia bipunctata. Ecol. larvae to predatory stoneßies: constraint on defensive Entomol. 21: 165Ð170. armour. Oikos 58: 336Ð342. Hinton, H. E. 1955. Protective devices of endopterygote Tschinkel, W. R. 1981. Larval dispersal and cannibalism in pupae. Trans. Soc. Br. Entomol. 12: 49Ð93. a natural population of Zophabas atratus (Coleoptera: Hopkins, G. W., and A.F.G. Dixon. 1997. Enemy-free space Tenebrionidae). Anim. Behav. 29: 990Ð996. and the feeding niche of an aphid. Ecol. Entomol. 22: Vo¨lkl, W. 1995. Behavioral and morphological adaptations 271Ð274. of the coccinellid, Platynaspis luteorubra for exploiting Legaspi, J. C., R. I. Carruthers, and D. A. Nordlund. 1994. ant-attended resources (Coleoptera: Coccinellidae). Life history of Chrysoperla ruﬁlabris (Neuroptera: Chry- J. Insect Behav. 8: 653Ð670. sopidae) provided sweetpotato whiteßy Bemesia tabaci Warren, L. O., and M. Tadic. 1967. Biological observations (Homoptera: Aleyrodidae) and other food. Biol. Control on Coleomegilla maculata and its role as a predator of the 4: 178Ð184. fall webworm. J. Econ. Entomol. 60: 1492Ð1496. Lucas, E., D. Coderre, and J. Brodeur. 1997. Instar-speciÞc Wassersug, R. J., and D. G. Sperry. 1977. The relationship of defense of Coleomegilla maculata lengi (Coccinellidae): locomotion to differential predation on Pseudacris trise- inßuence on attack success of the intraguild predator riata (Anura: Hylidae). Ecology 58: 830Ð839. Chrysoperla ruﬁlabris (Chrysopidae). Entomophaga 42: West, D. A., and W. N. Hazel. 1982. An experimental test of 3Ð12. natural selection for pupation site in swallowtail butter- Lucas, E., D. Coderre, and J. Brodeur. 1998. Intraguild pre- ßies. Evolution 36: 152Ð159. dation among aphid predators: characterization and in- Wilbur, H. M. 1980. Complex life cycles. Annu. Rev. Ecol. ßuence of extraguild prey density. Ecology 79: 1084Ð1092. Syst. 11: 67Ð93. Mack, T. P., and Z. Smilowitz. 1980. Development of a green Winder, L. 1990. Predation of the cereal aphid Sitobion ave- peach aphid natural enemy sampling procedure. Environ. nae by polyphagous predators on the ground. Ecol. En- Entomol. 9: 440Ð445. tomol. 15: 105Ð110. Majerus, M.E.N. 1994. Ladybirds. Harper-Collins, Toronto. Witt, D. L., and L. M. Dill. 1996. Springtail postmoult vul- New, T. R. 1991. Insects as predators. New South Wales nerability to pseudoscorpion predation: mechanisms and University Press, Kensington, Australia. implications. J. Insect Behav. 9: 395Ð406. Obrycki, J. J., M. J. Tauber, and W. M. Tingey. 1983. Pred- ator and parasitoid interaction with aphid-resistant po- tatoes to reduce aphid densities: a two-year Þeld study. J. Received for publication 14 April 1999; accepted 16 Novem- Econ. Entomol. 76: 456Ð462. ber 1999.