A Fox in Sheep's Clothing: Furtive Predators Benefit from the Communal Defense of Their Prey

Notes

Ecology, 82(11), 2001, pp. 3246±3250 ᭧ 2001 by the Ecological Society of America

A FOX IN SHEEP'S CLOTHING: FURTIVE PREDATORS BENEFIT FROM THE COMMUNAL DEFENSE OF THEIR PREY

EÂ RIC LUCAS AND JACQUES BRODEUR1 Centre de Recherche en Horticulture, DeÂpartement de Phytologie, UniversiteÂ Laval, Sainte-Foy, QueÂbec, Canada G1K 7P4

Abstract. Many animals live in temporary or permanent groups, either as gregarious or social species, to reduce predation risk. The solitary midge, Aphidoletes aphidimyza, preys speci®cally on aphids and spends its entire larval development within a prey colony where it is susceptible to intraguild predation. We hypothesized that midge larvae pro®t from a dilution effect produced by aphids which enhances their chances of survival. We examined the defensive behaviors of aphids in response to foraging midges, and investigated the effect of aphid density on the predation risk of A. aphidimyza by the lacewing Chry- soperla ru®labris. We found that a foraging midge displays furtive hunting behavior which triggers little defensive reaction by aphids, and does not stimulate signi®cant disturbance of the gregarious prey. Within the aphid colony the midge bene®ts from a dilution effect which reduces the incidence of predation by lacewing larvae. However, the effectiveness of such a mechanism is determined by the level of disturbance caused by foraging intraguild predators. Large lacewing larvae tend to dislodge aphids from their feeding sites, thereby eliminating the dilution effect. We conclude that prey not only provide food to midge larvae, but also protection against natural enemies. Key words: aphid; Aphidoletes aphidimyza; Chrysoperla ru®labris; defensive mechanism; dilution effect; ectosymbiosis; furtive behavior; intraguild predation; predatory midge.

INTRODUCTION Aphids are small, sedentary, plant-sucking insects that often form dense aggregations. They are patchily Potential bene®ts of living in groups include in- distributed in most terrestrial ecosystems, and parthe- creased foraging ef®ciency, information transfer nogenetic populations usually have a high potential rate among individuals, mate location, thermoregulation, of increase (Dixon 1998). Aphids are exploited by and defense against natural enemies (Pulliam and Car- many specialist and generalist aphidophagous species aco 1984, Vulinec 1990, Danchin and Wagner 1997). and have evolved a variety of individual and group One form of communal defense is the dilution effect which decreases the individual's probability of being defenses. Individual aphids living in a group may ben- attacked once the prey patch has been detected by pred- e®t from the presence of sterile soldier castes (Aoki ators (Taylor 1977, Inman and Krebs 1987). The di- 1982), the spatial structure of the colony (VoÈlkl and lution effect has been observed in many different or- Stadler 1996), the release of alarm pheromones (Nault ganisms, including zooplankton, spiders, insects, ®sh, et al. 1973), and the dilution effect (Kidd 1982, Turchin birds, and mammals (see Inman and Krebs 1987, Uetz and Kareiva 1989). and Hieber 1994 and references therein). Mixed groups The predatory midge Aphidoletes aphidimyza Ron- of different prey species may also experience the di- dani (Diptera: Cecidomyiidae) is speci®c to aphids in lution effect, as bene®ts are independent of genetic its larval stages. Females lay eggs close to aphid col- relativeness among individuals (Treisman 1975). How- onies and, upon hatching, neonate larvae enter the col- ever, the intriguing case in which predators pro®t from ony (Lucas and Brodeur 1999). The larvae possess spe- the communal defense of their prey has never been cialized mouthparts to pierce the aphid integument, in- reported. ject a paralyzing toxin, and then suck the aphid's body ¯uids. Con®ned within aphid colonies, eggs, and larvae of A. aphidimyza are vulnerable to intraguild predation. Manuscript received 11 October 2000; revised 20 March 2001; However, the incidence of mortality decreases with in- accepted 26 March 2001. 1 Address correspondence to this author. creased aphid density (Lucas et al. 1998). E-mail: [email protected] We hypothesized that midge larvae pro®t from a di-

3246 November 2001 NOTES 3247 lution effect produced by aphids which enhances the as previously described and 30 min prior to the test a predators' chances of survival. In the laboratory, we larva of A. aphidimyza was gently introduced in the ®rst compared patterns of predation behavior of A. center of the aphid colony using a ®ne paintbrush. Tests aphidimyza with that of the lacewing, Chrysoperla ruf- started with the release of a C. ru®labris larva and ilabris Burmeister (Neuroptera: Chrysopidae), a pred- ended when the lacewing either killed the midge or left ator of aphids and other arthropods. We then examined the leaf. There were a minimum of 14 replicates per how aphid density in¯uences the predation risk of A. treatment. We ®rst compared the lacewing capture suc- aphidimyza by C. ru®labris. cess on aphids and midges, de®ned as the total number of successful captures divided by the total number of METHODS attacks, regardless of colony sizes. We then compared Chrysoperla ru®labris was purchased from Groupe (1) midge mortality risk (the number of midges killed BiocontroÃle (Sainte-Foy, QueÂbec, Canada) and A. aphi- by lacewings divided by the total number of midges dimyza from Plant Products (MontreÂal, QueÂbec, Can- tested); (2) frequency of ®rst attack on midges (the ada). Predators were reared on the potato aphid, Ma- proportion of replicates where the midge was the ®rst crosiphum euphorbiae Thomas (Homoptera: Aphidi- prey attacked); (3) time elapsed before midge death in dae). Midge larvae were selected based on size since replicates where midges died; and (4) number of aphids there is a controversy over the number of A. aphidimyza killed prior to midge capture, as a function of aphid larval stages (see Lucas et al. 1998). Only large larvae colony size. Lacewing capture success on aphids and (Ͼ168 h old) were used in our experiments. Lacewing midges, midge mortality risk, and frequency of ®rst larvae were used 24 h after hatching (®rst instar) or 48 attack on midges were compared using G tests (like- h after molting (second and third instar). To establish lihood ratio). These tests were followed by post hoc aphid colonies on potato plants, early second-instar multiple comparisons tests corresponding to the ex- aphids were introduced on the lower surface of a leaf perimentwise error state (Scherrer 1984), which con- 24 h prior to testing. Clip-cages were used to prevent sists of recalculating the alpha signi®cance level (orig- aphids from dispersing and thus favor cohesion among inal ␣ϭ0.05) and comparing the group two by two individuals. All experiments were carried out at 23ЊC, with G tests. Time to midge death and number of aphids 60±70% relative humidity, under a 16:8 h light:dark killed prior to midge capture were analyzed using the photoregime. Kruskal-Wallis procedure. The Student-Newman- To examine defensive behaviors of potato aphids in Keuls test was used to separate means (Snedecor and response to attacks by predators displaying different Cochran 1967). foraging strategies, we used large A. aphidimyza larvae and ®rst instar C. ru®labris, as these two organisms are RESULTS of similar size (Lucas et al. 1998). Following clip-cage Attempted attacks (F1,22 ϭ 0.044, P ϭ 0.836) and removal, tests were started by introducing a predator successful attacks (F1,19 ϭ 0.286, P ϭ 0.599) were sim- larva close (Ͻ1 cm) to a colony of 9±13 aphids. Each ilar for lacewing and midge larvae. Foraging lacewing test lasted 45 min during which aphids were monitored larvae induced signi®cant defensive responses of continuously. As we observed each predator approach, aphids (F2,23 ϭ 24.95, P Ͻ 0.0001; Fig. 1). Most aphids we recorded the number of attempted attacks, the pro- were dislodged from their feeding sites, thereby dis- portion of successful predation events, and the pro- rupting the integrity of the colony. In contrast, midges portion of aphids displaying defensive behaviors. did not elicit strong defensive reactions in the aphids, These were classi®ed as: walking away from the feed- with the incidences of dropping (LSD, P ϭ 0.367) and ing site, dropping off the plant, and swiveling, a typical swiveling (LSD, P ϭ 0.235) being similar to controls. behavior performed in response to the release of alarm However, the incidence of walking was higher in the pheromone and characterized by repeated up and down midge treatment than in the control (LSD, P ϭ 0.014). movements of the abdomen (Dixon 1998). Aphid col- During bioassays, 95% of the A. aphidimyza larvae onies without a predator served as controls. There were were found within the aphid colony. twelve replicates per treatment. Data were analyzed Capture success of lacewing larvae was similar for using a one-way ANOVA. Proportion data (successful aphids and midges (G test; second instar, G5 ϭ 1.37, attack and defensive behavior) were arcsine trans- P Ͼ 0.900; third instar, G5 ϭ 4.73, P Ͼ 0.250), sug- formed prior to the analysis. gesting that differences in prey vulnerability did not To test whether or not A. aphidimyza larvae bene®t interfere with mortality patterns. Mortality of midges from a dilution effect, we examined their susceptibility to second instar C. ru®labris decreased signi®cantly to predation by second and third instar C. ru®labris with an increase in aphid density (G2 ϭ 10.00, P ϭ within aphid colonies of three different sizes: 4, 10, 0.009; Fig. 2A), as did the occurrence of ®rst attack and 20 individuals/colony. Aphid colonies were formed on midges (G2 ϭ 11.04, P ϭ 0.004; Fig. 2B). However, 3248 NOTES Ecology, Vol. 82, No. 11

dimyza had been introduced. These tactics correspond to furtive predation, an unusual form of foraging behavior that allows predators to circumvent detection and defensive responses of their prey. Aphid communities constitute a favorable template for intra- and interspeci®c encounters between natural enemies (Brodeur and Rosenheim 2000). In natural and managed ecosystems, intraguild predation occurs wide- ly among aphidophagous species and may represent an important mortality factor that reduces substantially intraguild prey populations (Rosenheim et al. 1993, MuÈll- er et al. 1999). Lucas et al. (1998) showed that predatory midge larvae were highly vulnerable to intraguild predation because of their small size, low mobility, and feeding speci®city. Consistent with our initial hypoth- FIG. 1. Proportion of Macrosiphum euphorbiae that ex- esis, we found that foraging A. aphidimyza larvae may hibited defensive behaviors in response to attack by Aphi- bene®t from a dilution effect within the aphid colony doletes aphidimyza and Chrysoperla ru®labris. For each behavior, percentages followed by different letters are signi®- that reduces intraguild predation. Thus, the prey not cantly different (ANOVA, P Ͻ 0.05, N ϭ 12). Vertical lines only serves as a food source, but may also provide represent ϩ1 SE. protection against predators. However, the effectiveness of such a mechanism is in¯uenced by the nature of intraguild predators. Most aphids were disturbed and these parameters were not signi®cantly affected by col- eventually dislodged from their feeding sites by large ony size when the lacewing was a third instar, (mor- predators, thereby eliminating the dilution effect. Third tality, G2 ϭ 0.66, P Ͼ 0.5; Fig. 2A: occurrence of ®rst instar lacewing larvae are robust, highly mobile, and attack, G2 ϭ 3.12, P Ͼ 0.1; Fig. 2B). The time to midge voracious active-searching predators. These character- death (Kruskal-Wallis; second instar, H ϭ 7.54, df ϭ istics contribute to magnify the impact a predator might 2, P ϭ 0.023; third instar, H ϭ 11.86, df ϭ 2, P ϭ have on both the structure of an aphid colony and the 0.003) and the number of aphids killed prior to midge predation risk. capture (second instar, H ϭ 17.84, df ϭ 2, P Ͻ 0.001; The bene®ts of living in groups may be negated by third instar, H ϭ 12.68, df ϭ 2, P ϭ 0.002) increased an increased number of attacks on the group (Turner with an increase in aphid density for both predator and Pitcher 1986, Wrona and Dixon 1991, Uetz and larval instars (Fig. 2C, D). Hieber 1994), as natural enemies tend to aggregate at large groups of prey (Taylor 1984). This question was DISCUSSION critically explored for aphids by Turchin and Kareiva A suite of behavioral traits characterized the atypical (1989). Under ®eld conditions, they showed that ag- foraging strategy of A. aphidimyza larvae. During our gregation of conspeci®c ®reweed aphids, Aphis varians experiments, most individuals were found within the Patch, signi®cantly reduced predation risk to individual aphid colony where they remained immobile in the aphids by Hippodamia convergens GueÂrin-MeÂneville, absence of feeding. They also often covered themselves a common ladybird beetle. Although coccinellids ex- with aphid exuvia and dead or paralyzed aphids (E. hibited both strong numerical and functional responses Lucas, personal observation). This may serve as cam- to aphid colonies, the aphid's probability of being killed ou¯age as shown for chrysopid larvae (Eisner et al. was nevertheless reduced through a dilution effect that 1978, Milbrath et al. 1993). Hunting midges were slow- grew with colony size. Such an outcome may be true moving predators: they approached their victim by in- for A. aphidimyza threatened by similar aphidophagous conspicuous creeping movements and subdued aphids guilds; ®eld experiments are needed to determine the by injecting a paralyzing toxin, usually in the aphid's ecological conditions under which predatory midges leg, thereby deactivating behavioral defenses of the may bene®t from exploiting aphid defense. prey (Klingauf 1967). They extracted the aphids' body Our ®ndings are important in three respects. First, contents on site without stimulating any signi®cant in- they provide a unique example of an adaptive process creased in dropping behavior and alarm signaling of in which a predator usurps (sensu Brodeur and Vet the remaining aphids in the colony. Although predatory 1994), for its own bene®ts, the communal defense of midges caused a number of aphids to momentarily stop its prey. Aphids could, therefore, be viewed as a func- feeding and walk away, the overall cohesion among tional component of A. aphidimyza defensive strategy aphids was maintained in most colonies where A. aphi- that contributes to protect developing larvae from in- November 2001 NOTES 3249

FIG. 2. Susceptibility of Aphidoletes aphidimyza larvae to second-instar (open circle) and third-instar (solid circle) larvae of Chrysoperla ru®labris as a function of aphid density: (A) percentage of experimental midge larvae that were killed by the predator, (B) percentage of replicates in which the ®rst attack was directed toward the midge rather than an aphid, (C) time elapsed before midge death in replicates where midges died, and (D) number of aphids killed before midge death. For each predator developmental stage, values followed by different letters are signi®cantly different (C and D, Kruskal-Wallis; A and B, G tests; ϰϭ0.05; N Ͼ 14). Vertical error bars represent ϩ1 SE. traguild predators. Yet the effectiveness of the dilution systems (HoÈlldobler and Wilson 1990). Furtive behav- effect would depend on the nature, number and for- ior might therefore constitute a preadaptation leading aging behavior of predators. to predatory ectosymbiosis. Within the Cecidomyiidae, Second, selective pressures other than those to re- a family characterized by its life history diversity, spe- duce predation risk are likely to have had an important cies may be mycophagous, phytophagous, gall-making, role in shaping furtive behavior of A. aphidimyza. For predator, or parasitic (GagneÂ 1981). One Termitomastus example, furtive predation may constitute a signi®cant species has been shown to develop as an ectosymbiont mechanism for the evolution of prey specialization, or of eusocial termites (Silvestri 1920, cited in Wilson may re¯ect phylogenetic inertia (many Dipteran larvae 1971) and, conceivably, may have originated from a are sluggish). furtive predatory ancestor. Efforts to examine the im- Third, the present ®ndings may have signi®cant im- portance of furtive predation by species that exploit plications for the evolution of ectosymbiosis. Predatory colonial or social prey will contribute to develop a more ectosymbionts of eusocial insects are associated with complete theory of predator±prey associations. the host colony during part of their life cycle. They ACKNOWLEDGMENTS constitute a rich community of species (Kistner 1981) This research was supported by grant and scholarship from that share several biological attributes of furtive pred- the Natural Sciences and Engineering Research Council of ators. Of signi®cance, they live in the vicinity of the Canada to J. Brodeur and E. Lucas, respectively. We thank prey and have the capacity to deactivate prey defensive L. SeÂneÂchal and A. Bouchard for technical assistance, and D. 3250 NOTES Ecology, Vol. 82, No. 11

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