Causes and Consequences of Cannibalism in Noncarnivorous Insects

Home , Agromyza frontella, Anthocharis scolymus, Cannibalism, Milkweed leaf beetle, Nicrophorus vespilloides, Pseudogonia

ANRV397-EN55-03 ARI 1 November 2009 10:14

Matthew L. Richardson,1 Robert F. Mitchell,2 Peter F. Reagel,2 and Lawrence M. Hanks1,2

1Program in Ecology, Evolution, and Conservation Biology, 2Department of Entomology, University of Illinois at Urbana-Champaign, Urbana, Illinois 61801; email: [email protected]

Annu. Rev. Entomol. 2010. 55:39–53 Key Words First published online as a Review in Advance on Insecta, feeding guild, intraguild predation, competition, population August 11, 2009 density The Annual Review of Entomology is online at ento.annualreviews.org Abstract This article’s doi: We review the primary literature to document the incidence of can- Annu. Rev. Entomol. 2010.55:39-53. Downloaded from www.annualreviews.org by University of Illinois - Urbana Champaign on 06/17/13. For personal use only. 10.1146/annurev-ento-112408-085314 nibalism among insects that typically are not carnivorous. Most of the Copyright c 2010 by Annual Reviews. cannibalistic species were coleopterans and lepidopterans, and the can- All rights reserved nibals often were juveniles that aggregate or that overlap in phenology 0066-4170/10/0107-0039$20.00 with the egg stage. Cannibalism can be adaptive by improving growth rate, survivorship, vigor, longevity, and fecundity. It also can play an important role in regulating population density and suppressing population outbreaks, stabilizing host plant–insect relationships, and reducing parasitism rates. Cannibalism often was favored by density-dependent factors for herbivores that feed in concealed feeding situations (such as stem borers, leafminers), but also by density-independent factors (such as high ambient temperature) for herbivores that feed in exposed feeding situations.

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INTRODUCTION differ among feeding guilds. We exclude eusocial insects from our considerations because Cannibalism, the killing and consumption of they have been the focus of earlier reviews, and Cannibalism: the all or part of a conspecific (33, 64), historically many of the causes and consequences of canni- killing and was considered an uncommon and incidental balism are unique to that group (16, 40, 53). consumption of all or phenomenon of little ecological or evolution- part of a conspecific ary significance (22, 33). It often was attributed Feeding guild: a to the unnatural conditions of laboratory envi- METHODS group of species that ronments (38). However, cannibalism may en- We collected data on cannibalism in noncar- exploit an ecological resource in a similar hance fitness of arthropods in natural environ- nivorous insects by searching the primary lit- manner ments by providing access to essential nutrients erature with the databases for Annual Re- (64), minimizing competition (79, 93) and reg- views (3), ISI Web of Knowledge (82), and ulating population density (38, 64). It also may Google Scholar (42) with the broad search ∗ ∗ be detrimental under some circumstances, such terms “insect ” plus “cannibal ” (truncation as when the cannibal is injured by its intended with asterisk specifies the root of the word). ∗ prey (64) or acquires pathogens from prey (93). A second search combined “cannibal ” with Earlier literature reviews on cannibalism in the names of each insect order, but we ex- arthropods usually have been restricted to car- cluded references that mention only orders nivores (31, 93), because of their adaptations that are entirely carnivorous (e.g., Mantodea, for capturing and killing prey. However, in- Odonata, and Neuroptera). We also examined sects of many feeding guilds that typically are the references in each publication to identify not carnivorous (hence noncarnivorous insects) other publications that present information on also can be cannibalistic, including species that cannibalism. feed on plants, algae, bacteria, and detritus, or Our assessment of cannibalism suffers from species that are omnivorous (21, 31, 38, 52, 53, some natural limitations of the data set. For 64, 79). Few, if any, of these groups of insects example, we undoubtedly have missed some have been included in earlier reviews of can- useful articles that do not mention our search nibalism (38, 64), which usually consider only terms, as well as articles in journals not model organisms, such as Tribolium spp. (46, archived in the databases that we used. Speciose 63), social insects (53), or species that display and common groups of insects, such as the certain forms of cannibalism, such as sexual can- Lepidoptera, may more likely be represented nibalism (31). There is some evidence that can- than smaller groups, such as the Dermaptera. nibalism among noncarnivorous insects is con- Groups that are not economically important tingent upon many diverse life-history factors, may be less likely to be studied and so are un- such as sex, age, and developmental asynchrony derrepresented in the data set. Cannibalism also may go unreported if researchers consider it Annu. Rev. Entomol. 2010.55:39-53. Downloaded from www.annualreviews.org within populations, or environmental factors, by University of Illinois - Urbana Champaign on 06/17/13. For personal use only. such as limitations in the quantity or quality of unusual or insignificant. Another problem is food (50, 60). There is some evidence that can- the rarity of negative data: Few authors make nibalism can be adaptive for these insects (2, 7, a point of mentioning that their study species is 45, 78). not cannibalistic, or design experiments specif- Our objective for this review is to document ically to test that hypothesis. the incidence of cannibalism among the noncar- We include in our review all the information nivorous insects, to characterize its taxonomic from our database that is related to cannibalism distribution, to identify environmental factors in noncarnivorous insects, from anecdotal that predispose insects to cannibalize, to assess observations to empirical data. We compile, for the impact that cannibalism has on individuals each insect species, information on the preva- and populations, and to test the hypothesis that lence, causes, and consequences of cannibalism the causes and consequences of cannibalism and note whether the study was conducted

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in the laboratory or field (if specified in the Mean rates of cannibalism ( ± SD) were cal- publication). We categorized study species into culated by averaging the maximum rates that the following feeding guilds: herbivores that were reported in references. Weused χ 2 contin- Density dependent: feed in exposed situations (e.g., folivores), her- gency tests to determine whether cannibalism describes a factor bivores that feed in concealed situations (e.g., in feeding guilds was associated with density- whose influence on a gall formers, leafminers, granivores that feed dependent or density-independent factors and population varies with within seeds, borers in herbaceous or woody whether it improved fitness (the latter were lim- the density of that tissues, and root feeders), and scavengers that ited to exposed and concealed feeding guilds be- population consume dead organic matter. Some of our cause there were too few data for scavengers). Density study species were not easily classified into independent: describes a factor these guilds, including the greater wax moth, ARE THERE ANY PATTERNS? whose influence on a Galleria mellonella L. (Galeriidae; larvae feed population is on wax in honey bee colonies; 27) and the Our search of the primary literature yielded independent of its European mason bee, Hoplitis anthocopoides 178 publications that reported cannibalism density (Schenck) (Megachilidae; adult females feed in 130 species in orders that contain non- SD: standard on nectar and pollen; 30). Eight of the species carnivorous species: Orthoptera, Blattodea, deviation had mixed diets, which placed them in multiple Hemiptera, Coleoptera, Hymenoptera, Lepi- Neonate: an insect in guilds, including three species of tenebrionid doptera, and Diptera (Supplemental Table 1). its first instar of development beetles in the genus Tribolium whose larvae Some studies were conducted in the field (20% may feed externally on grain and seeds or of reports) or both the field and laboratory internally in stored products such as flour, (10%), but most were conducted in the labo- and the noctuid moth Helicoverpa zea (Boddie) ratory (60% of reports). In some cases, canni- whose larvae are polyphagous and often feed balism was attributed to unnatural laboratory externally on host plants as young instars conditions, such as overcrowding, starvation, and internally as older instars (Supplemental and artificial diet (28, 69, 76, 95). We limit our Supplemental Material Table 1; follow the Supplemental Material discussion below primarily to studies that were link from the Annual Reviews home page conducted in the field or to studies in which the at http://www.annualreviews.org). Factors researchers attempted to simulate the natural that promoted cannibalism were categorized as environment in the laboratory. density dependent or density independent per Cannibals usually were juveniles (75% of the assessment of the authors or our interpre- reports across insect orders; Table 1) and often tation of their findings. The consequences of consumed eggs (21% of reports). This behavior cannibalism for individual cannibals were cate- may have originated with consumption of the gorized as increasing fitness, decreasing fitness, egg chorion by neonates (5, 6, 77, 90). In fact, and decreasing competition (with authors not noncarnivorous insects were more likely to lay Annu. Rev. Entomol. 2010.55:39-53. Downloaded from www.annualreviews.org by University of Illinois - Urbana Champaign on 06/17/13. For personal use only. drawing a conclusion about the ultimate effect eggs in masses (i.e., two or more eggs in con- on fitness). The influences of cannibalism tact) than singly (Table 2), which undoubtedly on population density were categorized as increases the chances that conspecifics will en- increasing survivorship, decreasing survivor- counter one another. Cannibals also often con- ship, and improving regulation of population sumed other juveniles (39% of cases), usually of density. We report the number of cannibalistic smaller body size (Table 1). For example, large species for each feeding guild but report the larvae of the bark beetles Scolytus multistriatus total number of unique factors that promoted (Marsham), S. scolytus (F.), and Tomicus piniperda cannibalism and unique consequences of L. consume smaller conspecifics that they cannibalism (in some cases including multiple encounter while boring in phloem (9). Larvae reports that differed in their findings for the of the sawfly Cephus cinctus Norton tend to con- same species; Supplemental Table 1). sume neonate conspecifics that are parasitized,

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Table 1 Insect orders and families with cannibalistic species, with life stage of the cannibal and prey Life stage of cannibal (and prey) Juvenile Juvenile Juvenile Juvenile Adult Adult Adult Adult Taxon (egg) (juvenile) (pupa) (adult) (egg) (juvenile) (pupa) (adult) Orthoptera Acrididae 3a 2 1 2 2 Gryllotalpidae 1 Tettigoniidae 1 25%b 17% 8% 25% 25% Blattodea Blaberidae Blattellidae 1 Blattidae 2 3 17% 33% 50% Hemiptera Cydnidae 1 1 1 Lygaeidae 3 3 1 1 Miridae 1 Pentatomidae 1 1 Rhopalidae 1 1 31% 31% 6% 13% 19% Coleoptera Bostrychidae 1 Bruchidae 2 Buprestidae 1 Cerambycidae 9 Chrysomelidae 4 3 1 3 Coccinellidae 2 2 Cucujidae 1 1 2 1 1 Curculionidae 1 4 1 Dermestidae 1 1 Elmidae 1 1 Nitidulidae 1 Scolytidae 5 1 1 1 1 Annu. Rev. Entomol. 2010.55:39-53. Downloaded from www.annualreviews.org by University of Illinois - Urbana Champaign on 06/17/13. For personal use only. Silphidae 1 2 Tenebrionidae 7 4 10 2 7 2 7 2 16% 32% 14% 3% 16% 5% 10% 3% Hymenoptera Cephidae 2 2 Megachilidae 1 40% 40% 20% Lepidoptera Arctiidae 2 3 2 Dalceridae 1 Galleriidae 1 (Continued )

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Table 1 (Continued ) Taxon Life stage of cannibal (and prey) Juvenile Juvenile Juvenile Juvenile Adult Adult Adult Adult (egg) (juvenile) (pupa) (adult) (egg) (juvenile) (pupa) (adult) Gracillariidae 3 Lithocolletidae 1 Lycaenidae 1 Noctuidae 1 13 2 Nymphalidae 1 Papilionidae 1 1 Phalaenidae 1 Pieridae 11 8 Prodoxidae 1 Pyralidae 2 4 4 Sesiidae 1 Tortricidae 1 30% 55% 15% Diptera Agromyzidae 2 Muscidae 1 Psychodidae 2 1 Simuliidae 1 Tephritidae 1 13% 75% 13%

aNumbers represent total number of unique cases; summarized from Supplemental Table 1. bPercentages of each cannibal-prey relationship are calculated across families within an order.

and cannibalism may reduce the rate of is true of cannibalistic adults (38.0 ± 27 and Supplemental Material parasitism in the next generation (47, 91). 55.6 ± 1.6% of eggs and pupae, respectively). Cannibalism among instars of similar size also Cannibalism is attributed most often to density- is common in many species, such as the desert dependent rather than density-independent locust, Schistocerca gregaria (Forskal)˚ (4), the factors (Table 2). For example, the proportion moth Carmenta hematica (Ureta) (20), and the of eggs that are consumed by larvae of the beetle Annu. Rev. Entomol. 2010.55:39-53. Downloaded from www.annualreviews.org by University of Illinois - Urbana Champaign on 06/17/13. For personal use only. chrysomelid beetle Labidomera clivicollis (Kirby) L. clivicollis is directly correlated with the num- (26). Caterpillars of the Indian meal moth, ber that the female deposits (26). Nevertheless, Plodia interpunctella Hubner,¨ will even consume the probability of cannibalism also can be influ- larger conspecifics if they are weakened by a enced by many density-independent factors, in- granulosis virus (13). Adult insects apparently cluding abiotic environmental conditions such are rarely cannibalized (5.7% of species in as high temperature, low humidity, and precip- Table 1) and usually only when they are in a itation (4, 48); asynchrony with the host plant vulnerable state, such as teneral orthopterans (e.g., when neonates emerge before host plants and blattodeans (74) (Supplemental Table 1). are available; 26, 78); poor nutritional quality of Teneral: a stage Cannibalistic juveniles may consume many the host plant (62); developmental asynchrony immediately following eclosion from the pupa conspecifics (53.6 ± 38, 47.1 ± 32, and within populations (6, 49, 51, 60); the availabil- in which the insect is ± 31.3 41% of eggs, larvae, and pupae, respec- ity of vulnerable conspecifics (e.g., due to dis- pale and soft-bodied tively; Supplemental Table 1), and the same ease, parasitism, injury, or molting; 10, 13); and

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). a genetic or phenotypic predisposition to cannibalize (34, 43, 81). In fact, cannibalism in the Total 8 (25) 5 (16) 26 (31) 57 (69) 77 (53) 69 (47) 32 (55) 11 (19) 15 (26)

19 (59) noctuid moth Mamestra brassicae (L.) may be under the control of a single gene (68). Cannibalism usually has a positive effect on the ﬁtness of the cannibal and can play an im- 1 (25) 3 (75) 5 (71) 2 (29) 1 (25) 2 (50) 1 (25) 0 (0) 0 (0) 2 (100)

Diptera portant role in stabilizing host plant–insect relationships and regulating population density (Table 2). For example, adults of the burying beetle Nicrophorus vespilloides Herbst limit

6 (27) 4 (18) 4 (33) 1 (8) 7 (58) the density of conspeciﬁc larvae in an animal 14 (50) 14 (50) 22 (43) 29 (57) 12 (55)

Lepidoptera corpse by consuming neonates, which in turn may prevent competition among remaining offspring and ensure their survival on the available resource (7). Cannibalism also can be of 0 (0) 0 (0) 0 (0)

3 (75) 1 (25) selective advantage by eliminating from the 3 (100) 0 (0) 1 (100) 0 (0) 0 (0) population conspeciﬁcs that are infected with Hymenoptera pathogens, as is the case with caterpillars of the fall armyworm, Spodoptera frugiperda ( J.E. Smith) (18). Cannibalism of parasitized individ- 8 (25) 1 (4) 1 (7) 4 (27)

24 (75) 32 (70) 14 (30) 14 (56) 10 (40) 10 (67) uals may serve to reduce rates of parasitism in

Coleoptera subsequent generations (47, 71, 91). For example, larvae of the Indian meal moth, P. inter-

Insect order punctella, kill and consume conspeciﬁcs that are parasitized by the ichneumonid wasp Venturia 3 (43) 4 (57) 0 (0) 4 (100) 2 (100) 0 (0) 0 (0) 2 (100) 0 (0) 0 (0) canescens Gravenhorst (67). On the other hand, Hemiptera insects may acquire pathogens by consuming conspeciﬁcs (64, 92), as is the case with caterpillars that are infected with a nuclear polyhedrosis virus (18, 24). 4 (40) 6 (60) 0 (0) 6 (100) 0 (0) 2 (100) 0 (0) 0 (0) 0 (0) 0 (0) Blattodea

ORDERS OF NONCARNIVOROUS INSECTS THAT INCLUDE a CANNIBALISTIC SPECIES 8 (38) 0 (0) 6 (100) 13 (62) 3 (100) 0 (0) 0 (0) 1 (100) 0 (0) 0 (0) Annu. Rev. Entomol. 2010.55:39-53. Downloaded from www.annualreviews.org by University of Illinois - Urbana Champaign on 06/17/13. For personal use only. . Numbers represent total number of unique cases (percentages, in parentheses, are calculated within columns and categories of life-history traits

Orthoptera The Coleoptera and Lepidoptera together accounted for 75.3% of the cannibalistic species in our data set, possibly because these groups are speciose or commonly studied, with many fewer species in the orders Orthoptera, Blattodea, Hemiptera, Hymenoptera, and

Supplemental Table 1 Diptera (Figure 1). Reports of cannibalism for the Orthoptera are limited to seven species of the Acrididae and to one species each of the Gryllotalpidae and Tettigoniidae (Table 1) (Figure 1). Nymphs of the acridid Gastrimargus transversus Thunberg cannibalize even at low Data summarized from Table 2 Life-history traits that are associated with cannibalism, and the consequences of cannibalism Mode of oviposition Single egg Egg mass Relationship with population density Density dependent Density independent Consequences of cannibalism for individuals Fitness of cannibal increased Fitness of cannibal decreased Competition decreased Consequences of cannibalism for populations Survival of population increased Survival of population decreased Improved regulation of density a population densities when food is plentiful, and

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50 Families Species 40

20 Number of taxa

0 Orthoptera Blattodea Hemiptera Coleoptera Hymenoptera Lepidoptera Diptera Insect order

Figure 1 Number of insect families and species of seven orders for which cannibalism has been reported in insects that typically are not carnivorous (summarized from Supplemental Table 1). Sample sizes are 14, 11, 6, 70, 5, 67, and 8 reports from the primary literature, respectively. Supplemental Material

cannibalism in this and another acridid, (L.), and Periplaneta americana (L.) (44). Female Spathosternum prasiniferum Walker, is favored P. americana also may consume males during by high ambient temperatures and low humid- copulation, a form of cannibalism that is com- ity (48, 55). Cannibalism is common among mon in carnivorous insects (31), or when males neonates of S. gregaria and improves their attempt to mate when the female is carrying ability to survive drought (4). Cannibalism also an ootheca (72). Nymphs of B. germanica may can provide an important source of nitrogen avoid being cannibalized by foraging during the for nymphs and adults of S. gregaria (86). The day, when adults are not active, and by produc- risk of cannibalism may in fact select for the ing a pheromone that cues dispersal in adults marching behavior in this species because (36). nymphs that walk the slowest are more likely to Accounts of cannibalism in the Hemiptera be overtaken and consumed by other nymphs were limited to seven species in five families of (8). Nutrient deficiency may lead to cannibal- the Heteroptera, and in most cases nymphs can- Annu. Rev. Entomol. 2010.55:39-53. Downloaded from www.annualreviews.org by University of Illinois - Urbana Champaign on 06/17/13. For personal use only. ism in the Mormon cricket, Anabrus simplex nibalized eggs (Table 1)(Figure 1). Nymphs of Haldeman. Nymphs may compensate for the cydnid Parastrachia japonensis Scott, how- limited availability of dietary salts and proteins ever, kill other nymphs or adults and will en- by eating conspecifics during migration (74). circle the victim and feed as a group just as Cannibalism has been reported for six they do when feeding on fruit (80). Rates of species in three families of the Blattodea cannibalism are density independent among (Table 1)(Figure 1). In most cases, adults can- nymphs of the small milkweed bug Lygaeus nibalized one another, but also nymphs or eggs kalmii Stal,˚ which attack weakened or recently (Table 1). Cannibalism among cockroaches of- molted conspecifics (70), and nymphs of the ten is encouraged by density-independent fac- stink bug Nezara viridula (L.), which canni- tors. For example, high ambient temperatures balize one another if they become active be- are associated with higher rates of cannibal- fore host plants are available (78). Nymphs of ism in Blatta orientalis L., Blattella germanica the milkweed bugs Oncopeltus cingulifer Stal˚ and

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O. unifasciatellus Slater cannibalize eggs that are the rate of parasitism in the next generation parasitized (71). (75). Cannibalism in C. cinctus may have se- Cannibalism was reported for 50 species lected for earlier emergence of adults, prolong- Oviposit: to lay eggs (in insects) of coleopterans in 14 families (Table 1) ing the seasonal activity period to the extent (Figure 1). Larvae of several of these species that larvae have access to novel species of host show behaviors that apparently serve to dis- plants (59). Adult females of the megachilid bee courage cannibalism, such as thrashing and bit- H. anthocopoides invade the nests of conspecifics, ing by the tenebrionid Zophobas rugipes Kirsch consume the eggs, and then oviposit, and their (84), blocking feeding galleries with silk in the offspring develop on the pollen provisions (30). cucujid Cryptolestes ferrugineus (Stephens) (17), Mouthparts of most adult lepidopterans are and producing chirping sounds that prevent en- unsuitable for predation (14), so cannibalism counters among wood-boring larvae of the cer- is limited to larvae (48 species in 15 families) ambycid beetle Monochamus sutor L. (87). Adult (Table 1)(Figure 1). Older larvae usually kill females of the burying beetle Nicrophorus pustu- and consume younger ones (Table 1); however, latus Herschel defend their brood against other larvae of Helicoverpa zea (Boddie) may wound females that will eat the young, but defend older larvae and feed on their hemolymph (25). against males only when the food source has Larvae of Heliothis virescens (F.) are more likely become unsuitable for supporting a new brood to cannibalize one another where they are sym- (83). patric with H. zea, perhaps as a result of elevated Larvae and adults of the flour beetles Tri- aggression in response to interspecific compe- bolium confusum Jacquelin du Val and T. casta- tition (43). Larvae of the moth Utetheisa orna- neum Herbst consume conspecific eggs and pu- trix (L.) and the butterfly Atrophaneura alcinous pae and, more rarely, other juveniles and adults (Klug) benefit from cannibalism by acquiring (63). Cannibalism appears to have a genetic defensive compounds from their prey (11, 12, basis in both species (34, 39, 56). Larvae of 61). Cannibalism serves to regulate population T. confusum apparently can assess the genetic density in other species of lepidopterans (35, relatedness of eggs and prefer to eat nonsib- 73), which may benefit the surviving larvae by lings (88). In many Tribolium species, the life conserving the quality of host plants or reducing stage consumed may be determined by inter- the number of natural enemies that are attracted specific competition or availability of nutrients by host plant volatiles (19). Females of the pierid (1), and cannibalism plays an important role in moth Anthocharis cardamines L. mitigate canni- regulating population density (57, 58). balism by depositing an epideictic pheromone Neonates of the imported willow leaf beetle, while ovipositing on flowers, which discourages Plagiodera versicolora (Laicharting), cannibalize oviposition by conspecific females (23). Only a one another only during the first 24 h after single larva of A. cardamines can complete de- Annu. Rev. Entomol. 2010.55:39-53. Downloaded from www.annualreviews.org by University of Illinois - Urbana Champaign on 06/17/13. For personal use only. hatching and apparently are not capable of kin velopment in a flower head (23). Cannibalism recognition (41). The cannibals may benefit by of eggs by larvae of the pierid A. scolymus (L.) se- reaching a larger body size, but this selective ad- lects for early eclosion of adult females and early vantage may be counterbalanced by the positive oviposition, but this selection may be counter- relationship between the number of neonates balanced by cooler air temperatures that pre- in a feeding group and the survivorship of the vent flight early in the season and thereby hin- group (15). der reproduction (51). These opposing selective There were only a few reports of canni- forces apparently maintain genetic variation in balism in the Hymenoptera (excluding euso- eclosion time within populations of A. scolymus cial species (Table 1)(Figure 1). Larvae of the (51). European wheat stem sawfly, Cephus pygmaeus Cannibalism was reported for seven species (L.), consume eggs and other larvae, along with of dipterans in five families (Table 1) their endoparasitoids, and as a result reduce (Figure 1). The cannibals were larvae in

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every case, and they consumed other larvae or eggs (Table 1). Adult females of the agromyzid Supplemental Material 55 41 12

108 leafminer Agromyza frontella (Rondani) miti- species Total no. gate cannibalism by depositing an epideictic pheromone after ovipositing (65, 66). Lam et al. (54) found that larvae of the house ﬂy, Musca domestica L., beneﬁt from aggregating because 3 (2) 1 (1) 4 (3) 0

Diptera it elevates the temperature and humidity and hinders development of competing fungi. Bac- teria deposited by females during oviposition initially encourage females to oviposit together,

0 but later, after the bacteria have multiplied, they 30 (9) 11 (7) 41 (13) act as a deterrent to oviposition. The bacteria Lepidoptera therefore serve to narrow the age distribution of larvae, minimizing the rate of cannibalism. 2 (1) 2 (1) 0 0 FEEDING GUILDS OF INSECTS

Hymenoptera THAT ARE ASSOCIATED WITH CANNIBALISM Most of the cannibalistic species in the exposed herbivore category were lepidopterans, 5 (3) 10 (4) 24 (7)

39 (12) while the concealed herbivore category was

Coleoptera dominated by coleopterans (Table 3). The few species in the scavenger feeding guild included

Insect order those in the Blattodea, Coleoptera, and Diptera (Table 3). The feeding guilds differed in ovipo- 7 (5) 7 (5) 0 0 sition behavior (categories differ in percentages 2 Hemiptera of cases; contingency test χ = 52.8, d.f. = 2, P < 0.001): Most scavengers and exposed herbivores oviposited in masses, but this behavior was less common among concealed herbivores 6 (3) 6 (3)

0 0 (Table 4). Cannibalism was density dependent

Blattodea for most of the concealed herbivores, density independent for most of the exposed herbivores, Annu. Rev. Entomol. 2010.55:39-53. Downloaded from www.annualreviews.org by University of Illinois - Urbana Champaign on 06/17/13. For personal use only. but not clearly associated with density in scav- χ 2 = a engers (Table 4; contingency test 32.8, d.f. = 2, P < 0.001). 1 (1) 9 (3) 8 (2) 0 Cannibalism usually improved the ﬁtness Orthoptera of the cannibals for species in the exposed herbivore category and decreased competition

Supplemental Table 1 . Insect families are counted only once in the total row but may be counted in more than one feeding guild. for species in the concealed herbivore category (Table 4; contingency test χ 2 = 75.1, d.f. = 2, P < 0.001). It enhanced the ﬁtness of exposed herbivores by improving nutrition, growth rate, vigor, fecundity, pupation success, and longevity (Table 4)(Supplemental Data summarized from Table 3 Numbers of cannibalistic species (and number of families) by insect order and feeding guild Feeding guild Exposed herbivore Concealed herbivore Scavenger Total a Table 1). Cannibalism among juveniles of some

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Table 4 Mode of oviposition and consequences of cannibalism Feeding guild Exposed Concealed herbivore herbivore Scavenger Total Mode of oviposition Single egg 7 (20)a 13 (54) 1 (10) 21 (30) Egg mass 28 (80) 11 (46) 9 (90) 48 (70) Relationship with population density Density dependent 27 (39) 35 (78) 8 (50) 70 (54) Density independent 42 (61) 10 (22) 8 (50) 60 (46) Consequences of cannibalism for individuals Fitness of cannibal increased 18 (74) 6 (29) 0 (0) 24 (49) Fitness of cannibal decreased 5 (22) 2 (10) 3 (75) 10 (20) Competition decreased 1 (4) 13 (62) 1 (25) 15 (31) Consequences of cannibalism for populations Survivorship of population increased 7 (58) 1 (10) 0 (0) 8 (33) Survivorship of population decreased 2 (16) 2 (20) 0 (0) 4 (17) Improved regulation of density 3 (25) 7 (70) 2 (100) 12 (50)

aNumbers represent total number of unique cases (percentages, in parentheses, are calculated within columns; summarized from Supplemental Table 1).

species of concealed herbivores minimizes com- 56, 94). It may arise nevertheless when food is Supplemental Material petition and so can be an important density- in short supply or of low quality, which may be dependent factor in regulating population due to asynchrony with host plants, or when density, even limiting densities to a single indi- encouraged by abiotic environmental factors. vidual in host plants of small dimensions, such Finally, individuals of some species may have as single seeds, fruits, or leaves (35, 37, 45, 89). a genetic predisposition to cannibalize (34, 39, 43, 81, 88). There was some support for our hypothe- CONCLUSIONS sis that feeding guilds of insects would differ in the causes of cannibalism. For example, can- Cannibalism in noncarnivorous insects is tax- nibalism often is favored by density-dependent onomically widespread, having been docu- factors in concealed herbivores but by density- mented in species that range from phylogenet- independent factors in exposed herbivores. ically primitive to advanced. These insects are Annu. Rev. Entomol. 2010.55:39-53. Downloaded from www.annualreviews.org

by University of Illinois - Urbana Champaign on 06/17/13. For personal use only. Cannibalism in many herbivorous species re- most likely to cannibalize smaller conspecifics, duces population density, thereby minimizing as also is true for carnivorous species (64), but competition for limited resources and improv- may attack conspecifics of similar or larger size ing the fitness of the cannibal. that are in an inactive developmental stage (e.g., eggs, pupae, or molting) or that are infected with pathogens, parasitized, or injured. Rates of cannibalism often are determined simply by FUTURE RESEARCH the availability of vulnerable conspecifics (38, Cannibalism can have important implications 84, 85). Cannibalism can be averted to some for the natural history of insects but neverthe- extent by adaptations that serve to reduce the less is rarely studied directly. Many reports of density of juveniles, narrow their age distribu- cannibalism for species in our data set were tion, or provide a behavioral or chemical de- merely incidental observations or were based fense against conspecific predators (7, 17, 29, on laboratory studies. There is a great need for

48 Richardson et al. ANRV397-EN55-03 ARI 1 November 2009 10:14

empirical research on cannibalism in diverse on the incidence of cannibalism; (e) the genetic insect species, especially in natural environ- basis of cannibalism and the evolution of canni- ments, to document its role in life history. Issues balistic behaviors; ( f ) the influence of genetic that should be addressed in future research are relatedness among conspecifics on the propen- (a) the taxonomic distribution of cannibalism; sity to cannibalize; ( g) the role of cannibal- (b) the dietary qualities of conspecific prey; ism on population density and dynamics; and (c) the behaviors that limit or promote cannibal- (h) the influence of cannibalism on the struc- ism; (d ) the influence of artificial environments ture of communities.

SUMMARY POINTS 1. Cannibalism in insects that are typically noncarnivorous is not limited to the unnatural conditions of laboratory environments and may have important consequence(s) for insects in their natural habitats. 2. Cannibalistic insects typically consume smaller conspeciﬁcs but attack those of similar or larger size that are vulnerable owing to their developmental stage or those that are infected with pathogens, parasitized, or injured. 3. The propensity to cannibalize may be inﬂuenced by many density-dependent and density- independent factors, including developmental asynchrony with host plants, sex or genetic relatedness of the participants, limitations in the amount or quality of food, and abiotic environmental factors such as humidity and high temperature. 4. Cannibalism may be averted by defensive behaviors or other adaptations that serve to reduce the local density of juveniles or equalize their age distribution. 5. Cannibalism often serves to regulate population density and decrease competition and can be advantageous to the cannibal by improving nutrition, growth rate, vigor, fecundity, pupation success, and longevity. It also can serve to eliminate parasitized and diseased individuals from the population. It may act as a selective force that alters the phenology of an insect species. On the other hand, it can be deleterious to the cannibal when it reduces population size below the optimal density or results in transfer of pathogens from victim to cannibal.

FUTURE ISSUES Annu. Rev. Entomol. 2010.55:39-53. Downloaded from www.annualreviews.org by University of Illinois - Urbana Champaign on 06/17/13. For personal use only. 1. How important and widespread is cannibalism as a mechanism for regulating densities of insects? 2. How does cannibalism arise in populations? Is it a genetic trait, or is it determined by ecological factors? 3. There is a great need for empirical research that is focused on cannibalism in a diversity of insect species, especially in natural habitats.

DISCLOSURE STATEMENT The authors are not aware of any afﬁliations, memberships, funding, or ﬁnancial holdings that might be perceived as affecting the objectivity of this review.

www.annualreviews.org • Causes and Consequences of Cannibalism in Noncarnivorous Insects 49 ANRV397-EN55-03 ARI 1 November 2009 10:14

ACKNOWLEDGMENTS We thank M.R. Berenbaum for constructive comments on an early draft of the manuscript, and M.H. Lee, D.K. Rahe, and M.G. Swecker for assistance with data collection. The authors grate- fully acknowledge funding support from the Alphawood Foundation and the National Research Initiative of the USDA Cooperative State Research, Education and Extension Service under grant number 2006-35302-17457 (to LMH).

LITERATURE CITED 1. Alabi T, Michaud JP, Arnaud L, Haubruge E. 2008. A comparative study of cannibalism and predation in seven species of flour beetle. Ecol. Entomol. 33:716–26 2. Al-Zubaidi FS, Capinera JL. 1983. Application of different nitrogen levels to the host plant and cannibalistic behavior of beet armyworm Spodoptera exigua (Lepidoptera: Noctuidae). Environ. Entomol. 12:1687–89 3. Annual Reviews. 2009. http://www.annualreviews.org/. Palo Alto, CA 4. Ashall C, Ellis P. 1962. Studies on numbers and mortality in field populations of the desert locust (Schis- tocerca gregaria Forskal).˚ Anti-Locust Bull. No. 38, London: Anti-Locust Res. Cent. 59 pp. 5. Barros-Bellanda HCH, Zucoloto FS. 2001. Influence of chorion ingestion on the performance of Ascia monuste and its association with cannibalism. Ecol. Entomol. 26:557–61 6. Barros-Bellanda HCH, Zucoloto FS. 2005. Egg cannibalism in Ascia monuste in the field; opportunistic, preferential and very frequent. J. Ethol. 23:133–38 7. Bartlett J. 1987. Filial cannibalism in burying beetles. Behav. Ecol. Sociobiol. 21:179–84 8. Bazazi S, Buhl J, Hale JJ, Anstey ML, Sword GA, Simpson SJ, Couzin ID. 2008. Collective motion and cannibalism in locust migratory bands. Curr. Biol. 18:735–39 9. Beaver RZ. 1974. Intraspecific competition among bark beetle larvae (Coleoptera: Scolytidae). J. Anim. Ecol. 43:455–67 10. Bhatia DR, Singh C. 1959. Cannibalism in locusts. Indian J. Entomol. 21:210–13 11. Bogner F, Eisner T. 1991. Chemical basis of egg cannibalism in a caterpillar (Utetheisa ornatrix). J. Chem. Ecol. 17:2063–75 12. Bogner F, Eisner T. 1992. Chemical basis of pupal cannibalism in a caterpillar (Utetheisa ornatrix). Experientia 48:37–42 13. Boots M. 1998. Cannibalism and the stage-dependent transmission of a viral pathogen of the Indian meal moth, Plodia interpunctella. Ecol. Entomol. 23:118–22 14. Borror DJ, Triplehorn CA, Johnson NF. 1989. An Introduction to the Study of Insects. New York: Saunders. 875 pp. 6th ed. 15. Breden F, Wade MJ. 1987. An experimental study of the effect of group size on larval growth and survivorship in the imported willow leaf beetle, Plagiodera versicolora (Coleoptera: Chrysomelidae). Environ. Entomol. 16:1082–86 Annu. Rev. Entomol. 2010.55:39-53. Downloaded from www.annualreviews.org by University of Illinois - Urbana Champaign on 06/17/13. For personal use only. 16. Camargo CAD. 1982. Longevity of diploid males, haploid males, and workers of the social bee Melipona quadrifasciata (Hymenoptera: Apidae). J. Kans. Entomol. Soc. 55:8–12 17. Campbell A, Sinha RN. 1990. Analysis and simulation modelling of population dynamics and bioenergetics of Cryptolestes ferrugineus (Coleoptera: Cucujidae) in stored wheat. Res. Popul. Ecol. 32:235–54 18. Chapman JW, Williams T, Escribano A, Caballero P, Cave RD, Goulson D. 1999. Age-related cannibalism and horizontal transmission of a nuclear polyhedrosis virus in larval Spodoptera frugiperda. Ecol. Entomol. 24:268–75 19. Chapman JW, Williams T, Martinez AM, Cisneros J, Caballero P, et al. 2000. Does cannibalism in Spodoptera frugiperda (Lepidoptera: Noctuidae) reduce the risk of predation? Behav. Ecol. Sociobiol. 48:321– 27 20. Cordo HA, DeLoach CJ, Ferrer R, Briano J. 1995. Bionomics of Carmenta haematica (Ureta) (Lepidoptera: Sesiidae) which attacks snakeweeds (Gutierrezia spp.) in Argentina. Biol. Control 5:11–24 21. Crespi BJ. 1992. Cannibalism and trophic eggs in subsocial and eusocial insects. See Ref. 32, pp. 176–213 22. Dawkins R. 1976. The Selfish Gene. Oxford: Oxford Univ. Press. 368 pp.

50 Richardson et al. ANRV397-EN55-03 ARI 1 November 2009 10:14

23. Dempster JP. 1997. The role of larval food resources and adult movement in the population dynamics of the orange-tip butterfly (Anthocharis caramines). Oecologia 111:549–56 24. Dhandapani N, Jayaraj S, Rabindra RJ. 1993. Cannibalism on nuclear polyhedrosis virus infected larvae by Heliothis armigera (Hubn.) and its effect on viral infection. Insect Sci. Appl. 14:427–30 25. Dial CI, Adler PH. 1990. Larval behavior and cannibalism in Heliothis zea (Lepidoptera: Noctuidae). Ann. Entomol. Soc. Am. 83:258–63 26. Dickinson JL. 1992. Egg cannibalism by larvae and adults of the milkweed leaf beetle (Labidomera clivicollis, Coleoptera: Chrysomelidae). Ecol. Entomol. 17:209–18 27. Dindo ML. 1987. Comparison of effects of partial starvation and parasitization by Pseudogonia (Wied.) on the cannibalistic behavior and mortality of Galleria mellonella L. (Dipt. Tachinidae – Lep. Galleriidae). Boll. Ist. Entomol. Univ. Stud. Bológna 41:315–24 28. Dodds KJ, Graber C, Stephen FM. 2001. Facultative intraguild predation by larval Cerambycidae (Coleoptera) on bark beetle larvae (Coleoptera: Scolytidae). Environ. Entomol. 30:17–22 29. Dougherty MJ, Hamilton JGC. 1996. A biologically-active compound from pupae of the sandfly Lutzomyia longipalpis (Diptera: Psychodidae) and its possible role in defense. Bull. Entomol. Res. 86:11–16 30. Eickwort G. 1975. Gregarious nesting of the mason bee Hoplitis anthocopoides and the evolution of parasitism and sociality among megachilid bees. Evolution 29:142–50 31. Elgar MA. 1992. Sexual cannibalism in spiders and other invertebrates. See Ref. 32, pp. 128–55 32. Elgar MA, Crespi BJ, eds. 1992. Cannibalism: Ecology and Evolution Among Diverse Taxa. Oxford: Oxford Univ. Press. 361 pp. 33. Elgar MA, Crespi BJ. 1992. Ecology and evolution of cannibalism. See Ref. 32, pp. 1–12 34. Englert DC, Thomas WH. 1970. The influence of the homeotic mutation, “antennapedia,” on egg cannibalism in Tribolium castaneum. Trans. Ill. State Acad. Sci. 63:51–56 35. Faeth SH. 1990. Aggregation of a leafminer Cameraria sp. nov. (Davis): consequences and causes. J. Anim. Ecol. 59:569–86 36. Faulde M, Fuchs M, Nagl W. 1990. Further characterization of a dispersion-inducing contact pheromone in the saliva of the German cockroach Blattella germanica L. (Blattodea: Blattellidae). J. Insect Physiol. 36:353–60 37. Fava A, Springhetti A. 1991. Egg distribution of Sitophilus granarius L. (Coleoptera: Curculionidae) in Triticum aestivum caryopses. J. Appl. Entomol. 111:406–11 38. Fox LR. 1975. Cannibalism in natural populations. Annu. Rev. Ecol. Syst. 6:87–106 38. Reviews the causes 39. Giray T, Luyten YA, MacPherson M, Steven L. 2001. Physiological bases of genetic differences in can- and consequences of nibalism behavior of the confused flour beetle Tribolium confusum. Evolution 55:797–806 cannibalism across 40. Gobin B, Ito F. 2003. Sumo wrestling in ants: major workers fight over male production in Acanthomyrmex animal taxa and how ferox. Naturwissenschaften 90:318–21 cannibalism influences demographic structure 41. Goff PW, Stevens L. 1995. A test of Hamilton’s rule: cannibalism and relatedness in beetles. Anim. and population-level Behav. 49:545–47 processes. 42. Google Scholar. 2009. http://scholar.google.com/ 43. Gould F, Holtzman G, Rabb RL, Smith M. 1980. Genetic variation in predatory and cannibalistic ten- Annu. Rev. Entomol. 2010.55:39-53. Downloaded from www.annualreviews.org by University of Illinois - Urbana Champaign on 06/17/13. For personal use only. dencies of Heliothis virescens strains. Ann. Entomol. Soc. Am. 73:243–50 44. Guthrie DM, Tindall AR. 1968. The Biology of the Cockroach. New York: St. Martin’s Press. 408 pp. 45. Hanks LM, Paine TD, Millar JG. 2004. Influence of the larval environment on performance and adult body size of the wood-boring beetle Phoracantha semipunctata. Entomol. Exp. Appl. 114:25–34 46. Hastings A, Costantino RF. 1991. Oscillations in population numbers: age-dependent cannibalism. J. Anim. Ecol. 60:471–82 47. Holmes ND, Nelson WA, Peterson LK, Farstad CW. 1963. Causes of variations in effectiveness of Bracon cephi (Gahan) (Hymenoptera: Braconidae) as a parasite of the wheat stem sawfly. Can. Entomol. 95:113–26 48. Iqbal M, Aziz SA. 1976. Cannibalism in Spathosterum parasiniferum (Walker) (Orthoptera: Acridoidea). Indian J. Zool. 4:43–45 49. Jasienski´ M, Jasienska´ G. 1988. Parental correlates of the variability in body mass at hatching in Arctia caja larvae (Lepidoptera: Arctiidae). Entomol. Gen. 13:87–93 50. Kakimoto T, Fujisaki K, Miyatake T. 2003. Egg laying preference, larval dispersion, and cannibalism in Helicoverpa armigera (Lepidoptera: Noctuidae). Ann. Entomol. Soc. Am. 96:793–98

www.annualreviews.org • Causes and Consequences of Cannibalism in Noncarnivorous Insects 51 ANRV397-EN55-03 ARI 1 November 2009 10:14

51. Kinoshita M. 1998. Effects of time-dependent intraspecific competition on offspring survival in the butterfly Anthocharis scolymus (L.) (Lepidoptera: Pieridae). Oecologia 114:31–36 52. Kirkpatrick TW. 1957. Insect Life in the Tropics. London: Longmans. 311 pp. 53. Kukuk BJ. 1992. Cannibalism in social bees. See Ref. 32, pp. 214–37 54. Lam K, Babor D, Duthie B, Babor E, Moore M, Gries G. 2007. Proliferating bacterial symbionts on house fly eggs affect oviposition behavior of adult flies. Anim. Behav. 74:81–92 55. Majeed Q, Aziz SA. 1977. Cannibalism in Gastrimargus transversus (Orthoptera: Acrididae). J. Entomol. Res. (New Delhi) 1:164–67 56. McCauley DE. 1978. Demographic and genetic responses of two strains of Tribolium castaneum to a novel environment. Evolution 32:398–415 57. Mertz DB. 1969. Age-distribution and abundance in populations of flour beetles. I. Experimental studies. Ecol. Monogr. 39:1–31 58. Mertz DB. 1972. The Tribolium model and the mathematics of population growth. Annu. Rev. Ecol Syst. 3:51–78 59. Morrill W, Kushnak G. 1996. Wheat stem sawfly (Hymenoptera: Cephidae) adaptation to winter wheat. Environ. Entomol. 25:1128–32 60. Nakamura K, Ohgushi T. 1981. Studies on the population dynamics of a thistle feeding lady beetle Henosepilachna pustulosa in a cool temperate climax forest. II. Life tables, key factor analysis, and detection of regulatory mechanisms. Res. Popul. Ecol. 23:210–31 61. Nishida R, Fukami H. 1989. Ecological adaptation of an Aristolochiaceae-feeding swallowtail butterfly, 63. Reviews and tests Atrophaneura alcinous, to aristolochic acids. J. Chem. Ecol. 15:2549–64 hypotheses about 62. O’Rourke PK, Hutchison WD. 2004. Developmental delay and evidence for reduced cannibalism in corn cannibalistic earworm (Lepidoptera: Noctuidae) larvae feeding on transgenic Bt sweet corn. J. Entomol. Sci. 39:294–97 interactions among life 63. Park T, Mertz DB, Grodzinski W, Prus T. 1965. Cannibalistic predation in populations of flour stages of Tribolium beetles. Phys. Zool. 38:289–321 confusum and T. castaneum. 64. Polis GA. 1981. The evolution and dynamics of intraspecific predation. Annu. Rev. Ecol. Syst. 12:225–51 65. Quiring DT, McNeil JN. 1983. Evidence of an oviposition-deterring pheromone in the alfalfa blotch 64. Reviews the causes leafminer, Agromyza frontella (Rondani) (Diptera: Agromyzidae). Environ. Entomol. 12:990–92 and consequences of 66. Quiring DT, McNeil JN. 1984. Exploitation and interference intraspecific larval competition in dipteran cannibalism across leaf miner Agromyza frontella. Can. J. Zool. 62:421–27 animal taxa and the evolution of 67. Reed DJ, Begon M, Thompson MJ. 1996. Differential cannibalism and population dynamics in a host- cannibalism. parasitoid system. Oecologia 105:189–93 68. Richter P. 1986. Inheritance of cannibalism behavior in noctuid larvae: a single gene hypothesis. Biol. Zbl. 105:615–19 69. Rock GC. 1968. Growth of Argyrotaenia velutinana by egg cannibalism. Ann. Entomol. Soc. Am. 61:1034 70. Root RB. 1986. The life of a Californian population of the facultative milkweed bug Lygaeus kalmii (Heteroptera: Lygaeidae). Proc. Entomol. Soc. Wash. 88:201–14 Annu. Rev. Entomol. 2010.55:39-53. Downloaded from www.annualreviews.org by University of Illinois - Urbana Champaign on 06/17/13. For personal use only. 71. Root RB, Chaplin SJ. 1976. The life-styles of tropical milkweed bugs, Oncopeltus (Hemiptera: Lygaeidae), utilizing the same hosts. Ecology 57:132–40 72. Roth LM, Willis ER. 1960. The Biotic Associations of Cockroaches. Washington, DC: Smithson. Inst. 470 pp. 73. Sigsgaard L, Greenstone MH, Duffield SJ. 2002. Egg cannibalism in Helicoverpa armigera on sorghum and pigeonpea. Biocontrol 47:151–65 74. Simpson SJ, Sword GA, Lorch PD, Couzin ID. 2006. Cannibal crickets on a forced march for protein and salt. Proc. Natl. Acad. Sci. USA 103:4152–56 75. Smith RW. 1959. Status in Ontario of Collyria calcitrator (Grav.) (Hymenoptera: Ichneumonidae) and of Pediobius beneficus (Gahan) (Hymenoptera: Eulophidae) as parasites of the European wheat stem sawfly, Cephus pygmaeus (L.) (Hymenoptera Cephidae). Can. Entomol. 91:697–700 76. Sokoloff A, Albers JC, Cavataio P, Mankau SK, McKibben S, et al. 1980. Observation of populations of Tribolium brevicornis (Le Conte) (Coleoptera, Tenebrionidae).I. Laboratory observations of domesticated strains. Res. Popul. Ecol. 22:1–12

52 Richardson et al. ANRV397-EN55-03 ARI 1 November 2009 10:14

77. Sotherton NW, Wratten SD, Vickerman GP. 1985. The role of egg predation in the population dynamics of Gastrophysa polygoni (Coleoptera) in cereal fields. Oikos 43:301–8 78. Stam PA, Newsom LD, Lambremont EN. 1987. Predation and food as factors affecting survival of Nezara viridula L. (Hemiptera: Pentatomidae) in a soybean ecosystem. Environ. Entomol. 16:1211–16 79. Stevens L. 1992. Cannibalism in beetles. See Ref. 32, pp. 156–77 80. Tachikawa S, Schaeffer CW. 1985. Biology of the Parastrachia japonensis (Hemiptera: Pentatomoidae? -idae). Ann. Entomol. Soc. Am. 78:387–97 81. Tarpley MD, Breden F, Chippendale GM. 1993. Genetic control of geographic variation for cannibalism in the southwestern corn borer, Diatraea grandiosella. Entomol. Exp. Appl. 66:145–52 82. Thomson Scientific. 2009. ISI Web of Knowledge. Stamford, CT: Thomson 83. TrumboST, Valletta RC. 2007. The costs of confronting infanticidal intruders in a burying beetle. Ethology 113:386–93 84. Tschinkel WR. 1978. Dispersal behavior of the larval tenebrionid beetle Zophobas rugipes. Physiol. Zool. 51:300–13 85. Tschinkel WR. 1981. Larval dispersal and cannibalism in a natural population of Zophobas atratus (Coleoptera: Tenebrionidae). Anim. Behav. 29:990–96 86. van Huis A, Woldewahid G, Toleubayev K, Van Der Werf W. 2008. Relationships between food quality and fitness in the desert locust, Schistocerca gregaria, and its distribution over habitats on the Red Sea coastal plain of Sudan. Entomol. Exp. Appl. 127:144–56 87. Victorsson J, Wikars L. 1996. Sound production and cannibalism in larvae of the pine-sawyer beetle Monochamus sutor L. (Coleoptera: Cerambycidae). Entomol. Tidskr. 117:29–33 88. Wade MJ. 1980. An experimental study of kin selection. Evolution 34:844–55 89. Wang R, Kok LT. 1986. Life history of Megacerus discoideus (Coleoptera: Bruchidae), a seedfeeder of hedge bindweed (Calystegia sepium), in southwestern Virginia. Ann. Entomol. Soc. Am. 79:359–63 90. Watanabe M, Yamaguchi H. 1993. Egg cannibalism and egg distribution of two Pieris butterflies, Pieris rapae and P.melete (Lepidoptera, Pieridae), on a host plant, Rorippa indica (Cruciferae). Jpn. J. Ecol. 43:181– 88 91. Weaver DK, Nansen C, Runyon JB, Sing SE, Morrill WL. 2005. Spatial distributions of Cephus cinctus Norton (Hymenoptera: Cephidae) and its braconid parasitoids in Montana wheat fields. Biol. Control 34:1–11 92. Williams T, Hernandez O. 2006. Costs of cannibalism in the presence of an iridovirus pathogen of Spodoptera frugiperda. Ecol. Entomol. 31:106–13 93. Wise DH. 2006. Cannibalism, food limitation, intraspecific competition, and the regulation of 93. Reviews the types of spider populations. Annu. Rev. Entomol. 51:441–65 cannibalism in spiders, 94. Wool D. 1969. The effect of larval age range on survival of two Tribolium castaneum strains in mixed and its influence on cultures, through pupal cannibalism. Res. Popul. Ecol. 11:40–44 population dynamics and trophic interactions. 95. Zucoloto FS. 1993. Adaptation of a Ceritis capitata population (Diptera, Tephritidae)to an animal protein- based diet. Entomol. Exp. Appl. 67:119–27 Annu. Rev. Entomol. 2010.55:39-53. Downloaded from www.annualreviews.org by University of Illinois - Urbana Champaign on 06/17/13. For personal use only.

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Annual Review of Entomology Contents Volume 55, 2010

Frontispiece Mike W. Service ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppxiv The Making of a Medical Entomologist Mike W. Service pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp1 Ecology of Herbivorous Arthropods in Urban Landscapes Michael J. Raupp, Paula M. Shrewsbury, and Daniel A. Herms pppppppppppppppppppppppppp19 Causes and Consequences of Cannibalism in Noncarnivorous Insects Matthew L. Richardson, Robert F. Mitchell, Peter F. Reagel, and Lawrence M. Hanks pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp39 Insect Biodiversity and Conservation in Australasia Peter S. Cranston pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp55 Ekbom Syndrome: The Challenge of “Invisible Bug” Infestations Nancy C. Hinkle ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp77 Update on Powassan Virus: Emergence of a North American Tick-Borne Flavivirus Gregory D. Ebel ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp95 Beyond Drosophila: RNAi In Vivo and Functional Genomics in Insects Xavier Bell´es ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp111 Annu. Rev. Entomol. 2010.55:39-53. Downloaded from www.annualreviews.org by University of Illinois - Urbana Champaign on 06/17/13. For personal use only. Dicistroviruses Bryony C. Bonning and W. Allen Miller ppppppppppppppppppppppppppppppppppppppppppppppppppp129 Olive Fruit Fly: Managing an Ancient Pest in Modern Times Kent M. Daane and Marshall W. Johnson ppppppppppppppppppppppppppppppppppppppppppppppppp151 Insect Silk: One Name, Many Materials Tara D. Sutherland, James H. Young, Sarah Weisman, Cheryl Y. Hayashi, and David J. Merritt ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp171 Bayesian Phylogenetics and Its Inﬂuence on Insect Systematics Fredrik Ronquist and Andrew R. Deans ppppppppppppppppppppppppppppppppppppppppppppppppppp189 Insect Fat Body: Energy, Metabolism, and Regulation Estela L. Arrese and Jose L. Soulages pppppppppppppppppppppppppppppppppppppppppppppppppppppp207

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Sex Differences in Phenotypic Plasticity Affect Variation in Sexual Size Dimorphism in Insects: From Physiology to Evolution R. Craig Stillwell, Wolf U. Blanckenhorn, Tiit Teder, Goggy Davidowitz, Charles W. Fox pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp227 Facultative Symbionts in Aphids and the Horizontal Transfer of Ecologically Important Traits Kerry M. Oliver, Patrick H. Degnan, Gaelen R. Burke, and Nancy A. Moran ppppppppp247 Honey Bees as a Model for Vision, Perception, and Cognition Mandyam V. Srinivasan pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp267 Invasion Biology, Ecology, and Management of the Light Brown Apple Moth (Tortricidae) D.M. Suckling and E.G. Brockerhoff pppppppppppppppppppppppppppppppppppppppppppppppppppppp285 Feeding Mechanisms of Adult Lepidoptera: Structure, Function, and Evolution of the Mouthparts Harald W. Krenn pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp307 Integrated Management of Sugarcane Whitegrubs in Australia: An Evolving Success Peter G. Allsopp ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp329 The Developmental, Molecular, and Transport Biology of Malpighian Tubules Klaus W. Beyenbach, Helen Skaer, and Julian A.T. Dow ppppppppppppppppppppppppppppppppp351 Biorational Approaches to Managing Stored-Product Insects Thomas W. Phillips and James E. Throne ppppppppppppppppppppppppppppppppppppppppppppppppp375 Parallel Olfactory Systems in Insects: Anatomy and Function C. Giovanni Galizia and Wolfgang Rössler pppppppppppppppppppppppppppppppppppppppppppppppp399 Integrative Taxonomy: A Multisource Approach to Exploring Biodiversity Annu. Rev. Entomol. 2010.55:39-53. Downloaded from www.annualreviews.org by University of Illinois - Urbana Champaign on 06/17/13. For personal use only. Birgit C. Schlick-Steiner, Florian M. Steiner, Bernhard Seifert, Christian Stauffer, Erhard Christian, and Ross H. Crozier ppppppppppppppppppppppppppppp421 Evolution of Plant Defenses in Nonindigenous Environments Colin M. Orians and David Ward ppppppppppppppppppppppppppppppppppppppppppppppppppppppppp439 Landscape Epidemiology of Vector-Borne Diseases William K. Reisen ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp461 Role of Adhesion in Arthropod Immune Recognition Otto Schmidt, Kenneth Söderhäll, Ulrich Theopold, and Ingrid Faye pppppppppppppppppppp485 Physical Ecology of Fluid Flow Sensing in Arthropods Jérôme Casas and Olivier Dangles ppppppppppppppppppppppppppppppppppppppppppppppppppppppppp505

viii Contents AR397-FM ARI 12 November 2009 9:17

Managing Invasive Populations of Asian Longhorned Beetle and Citrus Longhorned Beetle: A Worldwide Perspective Robert A. Haack, Franck H´erard, Jianghua Sun, and Jean J. Turgeon ppppppppppppppppp521 Threats Posed to Rare or Endangered Insects by Invasions of Nonnative Species David L. Wagner and Roy G. Van Driesche ppppppppppppppppppppppppppppppppppppppppppppppp547 Malaria Management: Past, Present, and Future A. Enayati and J. Hemingway ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp569 Regulation of Midgut Growth, Development, and Metamorphosis Raziel S. Hakim, Kate Baldwin, and Guy Smagghe pppppppppppppppppppppppppppppppppppppp593 Cellulolytic Systems in Insects Hirofumi Watanabe and Gaku Tokuda pppppppppppppppppppppppppppppppppppppppppppppppppppp609

Indexes

Cumulative Index of Contributing Authors, Volumes 46–55 ppppppppppppppppppppppppppp633 Cumulative Index of Chapter Titles, Volumes 46–55 pppppppppppppppppppppppppppppppppppp638

Errata

An online log of corrections to Annual Review of Entomology articles may be found at http://ento.annualreviews.org/errata.shtml Annu. Rev. Entomol. 2010.55:39-53. Downloaded from www.annualreviews.org by University of Illinois - Urbana Champaign on 06/17/13. For personal use only.

Contents ix