Interspecific Interactions in Phytophagous Insects: Competition

Annual Reviews www.annualreviews.org/aronline

INTERSPECIFIC INTERACTIONS IN PHYTOPHAGOUSINSECTS: Competition Reexamined and Resurrected

Robert F. Denno Departmentof Entomology,University of Maryland,College Park, Maryland20742

Mark S. McClure TheConnecticut Agricultural Experiment Station, ValleyLaboratory, Cook Hill Road,Box 248, Windsor,Connecticut 06095

James R. Ott Departmentof Biology,Southwest Texas State University,601 University Drive, San Marcos,Texas 78666

KEYWORDS: facilitation, competition-mediating factors, competitive exclusion, niche, . resource partitioning by University of Minnesota- Law Library on 09/17/06. For personal use only. ABSTRACT Annu. Rev. Entomol. 1995.40:297-331. Downloaded from arjournals.annualreviews.org This review reevaluates the importanceof interspecific competitionin the populationbiology of phytophagousinsects and assesses factors that mediate competition. Anexamination of 193 pair-wise species interactions, repre- senting all major feeding guildsl providedinformation on the occurrence, frequency, symmetry,consequences, and mechanismsof competition. Inter- specific competitionoccurred in 76%of interactions, wasoften asymmetric, and wasfrequent in mostguilds (sap feeders, woodand stem borers, seed and fruit feeders) exceptfree-living mandibulatefolivores. Phytophagousinsects weremore likely to competeif they wereclosely related, introduced,sessile, aggregative,fed on discrete resources,and fed on forbs or grasses. Interference 297 0066-4170/95/0101-0297505.00 Annual Reviews www.annualreviews.org/aronline

298 DENNO, McCLURE& OTT

competition was most frequent between mandibulate herbivores living in concealed niches. Host plants mediated competitive interactions more frequently than natural enemies, physical factors, and interspecific competition. Sufficient experimentalevidence exists to reinstate interspecific competition as a viable hypothesis warranting serious consideration in future investigations of the structure of phytophagousinsect communities.

INTRODUCTION

The importance of interspecific competition as a force affecting the distribution, abundance, and communitystructure of phytophagousinsects has experienced a controversial history, to say the least (107, 152, 174). During the 1960s and 1970s, field investigations of interspecific competition amongher- bivorous insects consisted mainly of observational studies of resource partitioning (e.g. 108, 143, 147, 179, 184). The rationale for such studies stemmed from classical competition theory, which predicted that two species could not occupy the same niche and coexist, and that coexistence could be achieved only through divergence in resource use (reviewed in 152). Thus, manyinsect ecologists sought differences in the wayherbivorous insects divided up their host plants or habitats and implicated competition as the cause of such differences when they were found. We also contributed to this fashionable but deductive approach (36, 127), for which the precedent had been set largely vertebrate ecologists (reviewed in 151, 161). During these decades, experimental field studies documentingthe occurrence of interspecific competition in phytophagousinsects were rare (126, reviewed in 26, 153). Nevertheless, there was sufficient experimental support for competition emerging from ma- rine invertebrate and terrestrial vertebrate systems (26, 153) to persuade many insect ecologists to accept interspecific competition as the paradigmfor the organization in phytophagousinsect communities. by University of Minnesota- Law Library on 09/17/06. For personal use only. During the early 1980s, however, the role of competition in structuring

Annu. Rev. Entomol. 1995.40:297-331. Downloaded from arjournals.annualreviews.org phytophagousinsect communities was challenged severely, and within a few years its status fell from a position of prominence to that of a weak and infrequent process (89, 102-104, 106, 107, 174). Twomajor lines of criticism led to this downfall. The first had its roots in a theoretical paper by Hairston et al (74), whoargued that because defoliation was rare, food must rarely limiting for herbivores, and that predators, parasites, and pathogens were largely responsible for maintaining herbivore densities below competitive levels. The few insect studies included in reviews at the time (26, 107, 153, 174) seemedto substantiate this contention. The second avenue of criticism stemmed from analyses of phytophagous insect distributions and cooccurrences. Positive interspecific associations, the failure to find repulsed distributions (19, 102, 170, 171), and the presence Annual Reviews www.annualreviews.org/aronline

COMPETITIONIN PHYTOPHAGOUSINSECTS 299

vacant niches and unsaturated communities(102) led someecologists to ques- tion the importance of competition. Notably few experimental field studies of competition in phytophagousinsects had been added to the literature at this time, and the insect studies responsible for both the deification and demiseof interspecific competition were overwhelmingly observational and pattern rather than process oriented. By the mid 1980s the scientific communityhad responded to a plea for a more experimental approach (26, 153), and more controlled, manipulative investigations of competition betweeninsect herbivores were instigated (e.g. 31, 41, 45, 50, 63, 81, 92, 94, 96, 114, 123, 124, 129, 132, 134, 135, 167). Accompanyingsuch studies has been a growing body of evidence suggesting that herbivorous insects indeed do compete, and recent assessmentsreflect this reversal in thinking (34, 48, 49, 1’69). The focus of this review is to reevaluate the importance of interspecific competition in the population biology of phytophagousinsects and to assess those factors that promoteits occurrence. Previous treatments have emphasized folivores (34, 107), and current perceptions of the importance of competition for phytophagousinsects are based largely on conclusions drawn from this guild. Here, we examine interactions for food and space in all guilds of herbivorousinsects (e.g. folivores, seed feeders, woodborers, gall makers,root feeders) except pollinators. Interactions involvingdetritivores (e.g. 156 in part, 187) are also excluded. Our specific objectives are to: (a) update and expand the database interspecific interactions for phytophagousinsects; (b) compareevidence for and against competition and facilitation within and amongguilds and contrast the occurrence, frequency, symmetry, consequences, and mechanismsof competition; (c) examinefour factors that mediate (promoteor diminish) interspecific competition including host plants, natural enemies, physical factors, and intraspecific competition; (d) determine whether taxonomicrelatedness, vari-

by University of Minnesota- Law Library on 09/17/06. For personal use only. ous life-history traits, diet breadth, and host plant growth form predispose herbivorous insects for competition; (e) establish a link between resource Annu. Rev. Entomol. 1995.40:297-331. Downloaded from arjournals.annualreviews.org partitioning (temporal and spatial), niche shifting, and interspecific competition, and assess the relationship betweenrepulsed distributions and interspecific competition; and (f) examine facilitative interactions between phytophagousinsects and assess their symmetry, causes, and consequences. By using the comparative approach, we address suggestions in the literature that competition occurs more frequently in the Homopteraand Hemiptera(41, 92, 135, 174); is more intense between closely related taxa (133); is more likely betweenspecies feeding on discrete resources (e.g. seeds, fruits, stems) (54, 71, 166); and is more frequent between species in introduced systems, managedhabitats, and concealed feeding niches, which are situations in which the action of natural enemiesis often reduced (28, 72, 73). Annual Reviews www.annualreviews.org/aronline

300 DENNO, McCLURE& OTT

THE DATABASE

Welimit our treatment of phytophagousinsects to those feeding on the living tissues of vascular plants. Thus, insects feeding on rotting fruits or dead wood are not considered. Fromthe remaining literature, we extracted 193 pair-wise interspecific interactions that provided information on competition and facilitation (Table 1). These interactions represented 104 study systems [e.g. the investigations of Addicott & Antolin on fireweed aphids (1-4, 9) constituted one study system and offered one interaction between two species]. Wein- eluded in our analysis only those interactions for which there was direct evidence for or against competition and facilitation. Direct evidence included: (a) experimental demonstrations (41, 92, 114), (b) displacement or exclusion following the introduction of a competitor (84, 123, 124, 125, 130, 158), and (c) observationswith verification of mortality or niche shift [e.g. the dissection of galls or stems with confirmation of competitor death (6, 167), or alterations in gallery construction in the case of bark beetles (138)]. In large part, wedid not include interactions in which competition was assessed indirectly (e.g. nonexperimentalstudies of resource partitioning, niche overlap, or dispersion and density correlation). Somestudies provided direct evidence of competition for somespecies pairs and nonexperimental,distributional evidence for others (e.g. 70, 143). In these cases, we included only those species pairs for which competition was measured directly. Of the 193 pair-wise interactions, 148 were experimental demonstrations, 9 were exclusively examples of competitive displacement, 31 were observational with direct evidence for death or niche shift, and 5 were nonexperimental. Mostpair-wise interactions (166 examples)were studied in the field; however, supplemental laboratory assessments of competition were made in manyof these cases. Studies in which leaves were either naturally or artificially dam- aged in the field and then later assayedin the laboratory for delayedcompetitive

by University of Minnesota- Law Library on 09/17/06. For personal use only. effects were scored as having a field component(e.g. 75, 137, 186). The remaining 27 interactions were appraised exclusively in the laboratory or Annu. Rev. Entomol. 1995.40:297-331. Downloaded from arjournals.annualreviews.org greenhouse. These were included because they provided valuable information on the mechanismor symmetryof competition. Twoof these 27 interactions involved aphids in greenhouses (175, 181), and 6 involved bruchid pests stored beans, whichis their primary habitat (e.g. 71,177). If competition wasfound, regardless of its intensity or frequency, the interaction was scored as competitive (Table 1). If evidence for competition was found, but only at densities above those normallyencountered in the field, the interaction was scored as noncompetitive(e.g. 77). Wealso assessed the frequency (not strength) of the competitive interaction, based on the investigators’ opinions as well as publishedresults~ Competitive interactions wereclassified as frequent, infrequent (occasional to rare), or not Annual Reviews www.annualreviews.org/aronline

COMPETITIONIN PHYTOPHAGOUSINSECTS 301

determined. Competitive interactions resulting in exclusion were scored as frequent (23, 35, 84, 97, 114, 123, 124), as were cases when competition occurred across most seasons or years (6, 31, 41, 47), and during or following frequent herbivory or outbreaks (137, 185). Interactions were also scored frequent if the removalor addition of one species was followed by a significant population changein the other (92, 94, 132, 142, 167). Interactions were scored as infrequent whencompetition occurred only on susceptible plants or clones and not on resistant ones (63, 134, 135), in dense but not in sparse plantings (96), in certain plant patch sizes (70), on stressed but not on healthy plants (85), on somehost plant species but not on others (128, 129), and during following rare defoliations (87, 136, 163). The symmetryof interactions was evaluated and was scored as symmetric, asymmetric,or not determined. Instances of reciprocal deterrence (17, 20, 21, 54), reductions in fitness (85, 126, 165), and population size (175) were scored as symmetric. Strong one-wayeffects on survival (6, 124, 166), fecundity (82, 114), and population size (35, 92, 135, 145) were considered asymmetric, were cases in which previous herbivory influenced the performance of subsequent herbivores (75, 78, 81, 136, 185). If only the competitive effect of one species on another was tested (129, 131, 134), and not the reverse, then the symmetryof the interaction could not be determined. The consequencesof competitive interactions were scored as: (a) competitive exclusion on the geographic or habitat scale, (b) local displacement from the feeding or oviposition site on a plant, or (c) fitness reduction or population change. Consequenceb could result from overt killing, niche preemption, niche shifting, avoidance, or emigration, and c from adverse effects on survival, developmenttime, fecundity, and body size, and from changesin population size in the presence or absence of competitors. Single pair-wise interactions could exhibit various combinationsof these outcomesand were scored accordingly. The mechanismof competition was scored as exploitative, interference, or

by University of Minnesota- Law Library on 09/17/06. For personal use only. both for each pair-wise interaction. Exploitative competition occurs when individuals, by using resources, deprive others of the benefits to be gained Annu. Rev. Entomol. 1995.40:297-331. Downloaded from arjournals.annualreviews.org from those resources (153, 154). Interference competition results whenindi- viduals harmone another directly through fighting and killing, or indirectly by the aggressive maintenanceof territory or the production of chemicals that deter other individuals (153). Exploitative competition maybe direct or indirect and effects maybe felt either immediatelyor at a later time (34). Exploitative interactions mediated throughthe host plant are difficult to categorize. Whena mandibulatedefoliator removes tissue that is no longer available to another species, a direct and immediateadverse effect can result (18, 84). In contrast, sap-feeding Homop- tera can reduce plant nutritional quality, which in turn can have indirect negative effects on cooccurring species (114). The competitive effect may Annual Reviews www.annualreviews.org/aronline

302 DENNO, McCLURE & OTT by University of Minnesota- Law Library on 09/17/06. For personal use only. Annu. Rev. Entomol. 1995.40:297-331. Downloaded from arjournals.annualreviews.org Annual Reviews www.annualreviews.org/aronline by University of Minnesota- Law Library on 09/17/06. For personal use only. Annu. Rev. Entomol. 1995.40:297-331. Downloaded from arjournals.annualreviews.org Annual Reviews www.annualreviews.org/aronline

304 DENNO, McCLURE& OTT

occur immediately or it maybe delayed and carry over to subsequent generations (122; RF Denno & J Cheng, in preparation). Similarly, mandibulate herbivore feeding mayinduce nutritional or allelochemical changes in plants (95), resulting in either immediateor delayed indirect effects on potential competitors (75, 78, 81, 136, 185). Interactions exhibiting interference competition included those involving direct killing (6, 139, 143, 148, 166, 168, 178), aggressive behavior (69, 128, 129), and the production of chemicals (deterrents and pheromones)that hinder colonization (17, 55, 109, 110), feeding (144), or oviposition (53, 54, 71, 99). Avoidanceof previously damagedleaves (46, 47, 79) and tissues modified or fouled by other species (16, 25, 112, 130) were considered interference phenomena.Cases of preemption [the passive occupation of a plant part by one individual that precludes colonization by another latecomer (183)], and space overgrowth by scale insects (114, 122), were scored as interference competition because they contain elements of avoidance. Interactions resulting in selective emigration(43, 88, 175) or the interspecific triggering of migratory forms in wing-polymorphicinsects (41, 100) were regarded as interference competition, as were natural enemy-mediatedinteractions, such as those in which the intensity or outcome of competition between two phytophagous species was influenced by predators or parasitoids (15, 122, 158). Weassigned factors mediating the intensity or outcomeof competition to four major categories: host plants, natural enemies, physical factors, and intraspecific competition. Host plant effects were further partitioned into immediate effects (plant resistance, plant nutrition, and plant phenological events such as bud break), delayed effects (plant damage,or feeding-induced changes in plant nutrition or allelochemistry), and textural effects (plant density, patch size, plant species composition).If any host plant (e.g. 41, 60, 75, 86, 96, 114, 135), natural enemy(e.g. 15, 43, 47, 115, 158), or physical factor (e.g. 64, 126) influenced the intensity or outcomeof the competitive interaction, the by University of Minnesota- Law Library on 09/17/06. For personal use only. factor was scored as mediating. Weconsidered intraspecific competition to be

Annu. Rev. Entomol. 1995.40:297-331. Downloaded from arjournals.annualreviews.org a mediating factor if its effect on a particular herbivore species exceededthat of interspecific competition (e.g. 126). Evidence for and against interspecific competition and its frequency, consequences, symmetry, mechanism,and mediating factors is comparedbetween feeding guilds and niches in Table 1. Feeding niche (e.g. free living, stem borer, gall maker)is nested within two major mouthpartguild types: haustellate and mandibulate. Basedon the concealmentof their feeding niche, mandibulate herbivores are categorized as external feeders (free-living species and leaf tiers and leaf rollers) or internal feeders (stem and woodborers, leaf miners, seed/pod/cone/bract feeders, gall makers, and root feeders). Interactions between mandibulate herbivores in different niches that consisted mostly of interactions betweenexternal and internal feeders (e.g. free-living and leaf- Annual Reviews www.annualreviews.org/aronline

COMPETITIONIN PHYTOPHAGOUSINSECTS 305

miner species) are placed in a separate category for analysis. Wealso established a major interguild grouping that includes interactions betweenhaustellate and mandibulate herbivores (most interactions were between free-living species). Wecompared the occurrence of competition between native and introduced systems (if either herbivore or the host plant was introduced the system was considered introduced), natural and managedhabitats (agricultural, ornamental, and sylvicultural), forb/grass- and tree/shrub-feeding species, monophages (feeding within one genus of plants) and polyphages (feeding on more than one genusof plants), aggregated(feeding in groupsat least during early instars) and solitary species, and sessile and mobile species. To discern if particular life history traits contributed to competitive success, we comparedthe fecundity, body size, voltinism, and dispersal ability of the superior and inferior competitor in each interaction. Published studies are undoubtedly biased toward detecting competition. Biases maystem from: (a) the choice of species pairs most likely to interact, (b) the selection of commonspecies for study, or (c) the failure to publish nonsignificant results (26, 34). Decisionsconcerning the inclusion of particular studies and the scoring of specific parameter states are also subject to bias (34). To minimizethose biases within our control, we limited our assessment to experimentalstudies, established uniformcriteria for scoring all aspects of competition, and scored conservatively. All comparisons were conducted using categorical data analysis of counts [CATMODprogram (58, 149)]. Maximum-likelihood chi-square and probability values are reported for each comparison. Weacknowledge that some comparisons presented herein are not completely independent. For example, introduced species often occur in managedhabitats. Therefore, comparisons of competition between introduced and native species, and between species in managedand natural habitats, must be interpreted with caution. by University of Minnesota- Law Library on 09/17/06. For personal use only.

Annu. Rev. Entomol. 1995.40:297-331. Downloaded from arjournals.annualreviews.org GENERAL PATTERNS OF INTERSPECIFIC INTERACTION

Evidencefor interspecific competition is widespread,occurring throughout all feeding guilds of phytophagousinsects (Table 1). Of the 193 pair-wise interactions we assessed, 147 (76%) showevidence of interspecific competition, 11 (6%) support facilitation, and only 35 interactions (18%)indicate an absence of competition. Although competitive effects were detected in the great majority of cases, their strength and frequency vary considerably. Nonetheless, the paucity of.hard experimental evidence against interspecific competition contrasts sharply with the claims of the traditional view. Anotherrecent review of phytophagousinsects (34) also found that the vast majority of experimental Annual Reviews www.annualreviews.org/aronline

306 DENNO, McCLURE& OTT

studies (91%)provided evidence for interaction (negative or positive) and most studies (67%) detected competitive effects. A comparison between guilds showed that interspecific competition was more prevalent amonghaustellate species (93%) than mandibulate species (78%) 2 = 4.57, P = 0.032), an d th at co mpetition was more co mmon among haustellate species than in interguild interactions between haustellate and mandibulate species (62%) (~2 = 6.90, P = 0.009) (Table 1). Furthermore, competitive interactions were scored as frequent more often for haustellate species (77%) than for mandibulate herbivores (51%) (~2 = 6.47, P = 0.011). Similarly, interactions tended to be frequent more often amongsap feeders (77%) than between sap feeders and mandibulate herbivores, for which most interactions were infrequent (80%) (~2 = 4.80, P = 0.029). These findings consistent with reports that interspecific competition occurs moreoften in the Homopteraand Hemiptera (41, 92, 135, 174). Within mandibulate phytophages, competition occurred more often in interactions between species occupying internal feeding niches (89%) (e.g. stem borers, woodborers, and seed feeders) than in interactions betweenexternally feeding folivores (59%) such as free-living Orthoptera, Lepidoptera, Hymenop- tera, and Coleoptera(22 = 11.90, P = 0.001). Competitionwas also detected more often in interactions between mandibulatefree-living folivores and concealed feeders (100%) (e.g. folivores and leaf miners) than in interactions between free-living folivores themselves(59%) 2 = 5.11, P = 0.024). Also, competitive interactions were more often infrequent between external feeders (79%) than either betweeninternal feeders (40%)(Z2 = 7.02, P = 0.008) or betweenexternal and internal feeders (30%)(~ = 5.93, P = 0.015). Thus, for the major guilds phytophagousinsects, competition was detected least often in free-living, rnandibulate species. Whencompetition occurred in this guild, it was usually scored as infrequent. Oneshould note that the current view regarding the strength and frequency of competition in phytophagousinsects has generally emphasized by University of Minnesota- Law Library on 09/17/06. For personal use only. mandibulatefolivores (e.g. 107), the guild in whichcompetition appears to

Annu. Rev. Entomol. 1995.40:297-331. Downloaded from arjournals.annualreviews.org least likely. Internal feeding guilds (seed and fruit feeders and woodborers), whichthere is abundant evidence for competition (Table 1), have been inexpli- cably excluded from most previous treatments. Wefound that most competitive interactions (84%) are asymmetric (amen- salistic) (Table 1), a result consistent with the findings of previous critiques (105, 106, 174). Althoughamensalism prevailed in most guilds, nearly half the interactions amonghaustellate sap feeders (44%) were symmetric. Aneven greater frequency of symmetrical interactions (53%) occurred amongthe free- living sap feeders, especially the Cicadellidae and Aphididae(82, 85,126, 158, 165, 175). The frequency of symmetrical interactions between sap feeders (44%) was significantly higher than that observed within mandibulate herbivores (5%) 2 = 20.50, P = 0.001). Nodifferences in symmetry were observed Annual Reviews www.annualreviews.org/aronline

COMPETITIONIN PHYTOPHAGOUSINSECTS 307

betweenmandibulate herbivores with internal feeding niches, external feeding niches, or betweeninternal and external feeders (P > 0.05), and all interactions were strongly asymmetric. The few cases of symmetric competitive interactions in mandibulate herbivores involved bark beetles in which inhibitory pheromonesreciprocally deterred the simultaneous colonization of pine trees (17, 30, 31, 55, 110, 138, 182). Certain guilds appearedto be consistently out-competedin interactions with others. For example, root feeders were adversely affected in all reported interactions with folivores (52, 84, 91, 111, 135). Also, leaf miners were usually less successful on leaves previously damagedby chewing herbivores (46, 47, 50, 51, 185), although free-living chewers mayavoid feeding on mined leaves (79). Haustellate herbivores, however, appeared to prevail in interactions with mandibulate species (113, 129), as often as they succumbed(18, 57, 92, 94). Clearly, morestudies are neededto verify these trends. The consequencesof competition also differ amongcertain guilds (Table 1). For instance, the frequencyof large-scale competitiveexclusion, local displacement, and fitness reduction/population changediffered betweenhaustellate and mandibulateherbivores (Z~ = 6.04, P = 0.049), a difference largely attributable to a higher incidence of competitiveexclusion (11 vs 3%)for sap feeders, and higher frequency of local displacement (49 vs 37%)for mandibulateherbivores. The consequencesof competition also differed significantly betweenmandibulate herbivores feeding in internal and external niches (Z2 = 8.49, P = 0.014). Local displacements occurred muchmore frequently amongspecies in concealed feeding niches than in external feeders (59 vs 26%respectively). The high incidence of local displacement observed for mandibulate herbivores in concealed niches was associated with interference competition (direct killing in many cases), a mechanism that predominated for internal compared with external feeders (~2 = 32.10, P = 0.001; Table 1). Interference competition was also moreprevalent amonginternal feeders than in interactions betweeninternal

by University of Minnesota- Law Library on 09/17/06. For personal use only. and external feeders (Z2 = 9.12, P = 0.011). Surprisingly, the frequency of exploitative and interference competition does Annu. Rev. Entomol. 1995.40:297-331. Downloaded from arjournals.annualreviews.org not differ significantly betweenhaustellate and mandibulateguilds (~2 = 3.58, P = 0.167; Table 1). However,the nature of the interference mechanismdoes seem to differ. Overt killing and chemically mediated deterrence are more characteristic of mandibulateherbivores (e.g. 17, 139, 144, 166, 178), while emigration stimulated by bodily contact and space preemption are more com- monfor sap feeders (e.g. 41, 88, 100, 114, 123, 124).

FACTORS MEDIATING INTERSPECIFIC COMPETITION

Host plant-related factors, natural enemies, physical factors, and intraspecific competition are all thought to maintain herbivore densities at low levels where Annual Reviews www.annualreviews.org/aronline

308 DENNO, McCLURE& OTT

interspecific competition is rare (107). Recent reviews of competition have also emphasized the importance of plant resources and natural enemies as significant factors mediatinginterspecific interactions (34, 48, 49, 83, 140). this section, we explore howthese factors mediate the intensity and outcome of interspecific competition. In the assessed studies, host plant factors (immediate,delayed, and textural effects combined)mediate moreinterspecific interactions (n = 77) than natural enemies (n = 24), physical factors (n = 15), and intraspecific competition = 29). A comparisonbetween haustellate sap feeders (n = 68) and mandibulate phytophages (n = 72) shows that mandibulate herbivore interactions are mediated by host plant-related factors more frequently than are interactions between sap feeders (67% vs 38%); natural enemies influence these groups approximately the same extent (15% vs 18%), and physical factors (6% 16%) and intraspecific competition (12% vs 28%) mediate mandibulate her- bivore2 interactions less often than they affect those of haustellate insects (X -- 12.63, P = 0.006). This pattern, however, mayin part reflect the current flurry of research on the effects of induced changes in plant nutrition or chemistry on the Performanceof later-feeding mandibulate species (57, 75, 78, 79, 81, 136, 137, 185), a phenomenonseldom studied with sap feeders (but see 114; RF Denno& J Cheng, in preparation). Host Plants Manyinterspecific interactions between phytophagousinsects can be intensified through induced changesin plant nutrition or allelochemistry (75, 81, 111, 114, 145, 185). Induced changes mayoccur immediately and affect the performanceof cooccurring species (short-term effect), or they maypersist and adversely alter the fitness of potential competitors in subsequent generations or seasons (delayed effect). Abundantevidence indicates that competitive interactions betweensap feed-

by University of Minnesota- Law Library on 09/17/06. For personal use only. ers intensify as heavy feeding causes host plants to rapidly deteriorate and

Annu. Rev. Entomol. 1995.40:297-331. Downloaded from arjournals.annualreviews.org plant nutrition to decrease (41, 114). Under such conditions, aphid survival and population growth decline dramatically (82, 88, 175) and emigration (walking) to neighboringplants increases (9, 43, 88, 175). Large-scale dispersal also occurs in aphids, whenalate formsare selectively producedin inter.specific aggregations (100). Similarly, for planthoppers interspecific crowing with Prokelisia dolus triggers the production of migratory forms in Prokelisia marginata, which results in the selective emigration of P. marginata from shared habitats (41). For both aphids and planthoppers, the triggering of migratory forms is mediated in part by feeding-induced changes in host-plant chemistry (37, 39, 41). Short-term induced changes in host-plant nutrition and allelochemistry mediate interactions betweenscale insects and adelgids as well. For example, Annual Reviews www.annualreviews.org/aronline

COMPETITIONIN PHYTOPHAGOUSINSECTS 309

contemporaneousfeeding by nymphsof the scale Fiorinia externa significantly reduces the nitrogen available in young hemlockfoliage, which in turn dramatically decreases the survival of the scale Nuculaspis tsugae (114). Also, heavy feeding by the adelgid Pineus boerneri causes resinosis on the bark of pines, whichforces it to feed on needles, whereit displaces Pineuscoloradensis (116, 117, 123). Short-term induced changes in plant nutrition also mediate interspecific interactions between mandibulate herbivores. Examplesinclude leaf mining by the agromyzid Chromatomyiasyngenesiae that reduced plant nitrogen and decreased the growth rate of the root-feeding chafer Phyllopertha horticola (111), and plant fertilization that diminished competition betweenthe grasshoppers Arphia conspersa and Pardalophora apiculata (145). Feedingby early-season folivores can also induce long-term changes in plant quality that can influence the choice of feeding and oviposition sites and hence the performanceof free-living herbivores that feed later during the season. For example, when fed birch leaves that were artificially damagedto simulate feeding by the spring defoliator Epirrita autumnata, free-living Lepidoptera and sawflies exhibited reduced growth rates and/or survival (75, 81, 136), probably as a result of induced phenolics (81). Spring-damagedleaves tended to adversely affect the performanceof mid-seasonherbivores to a greater extent than late-season herbivores (75). Similarly, the growth rate (186), survival (137), fecundity (78), and density (57) of several other species of free-living herbivores declined following the damage-induceddeterioration of foliage. Changesin leaf quality can also mediate interactions betweenfree-living folivores and late-season leaf miners (48, 49). Early-season feeding on oaks caterpillars of Operophterabrumata and Tortrix viridana (natural and simulated damage)reduced leaf nitrogen, which adversely affected the survival of Phyl- lonorycter spp. leaf miners (185). Larvae of several species of free-living Lepidoptera consistently avoided the mined leaves of birch but showedvariable

by University of Minnesota- Law Library on 09/17/06. For personal use only. responses to chewedleaves (79). However,larval feeding preferences in this

Annu. Rev. Entomol. 1995.40:297-331. Downloaded from arjournals.annualreviews.org study were not related in any simple wayto induced changesin leaf chemistry. Survival and development of late-season leaf miners on oak were also negatively influenced on previously damagedleaves (47-49). Although induced leaf chemistry was implicated in delayed development (46, 49), important source of mortality for leaf miners was parasitism, which was significantly higher on damagedcompared with intact leaves (46-48, 50, 51). Although parasitoids maybe selectively attracted to damage-related changes in leaf chemistry, structural damagealone affected rates of leaf miner attack (50). Nonetheless, some leaf miner species avoid ovipositing on previously damagedleaves, apparently because rates of development,leaf abscission, and parasitism are elevated (46, 47, 49). Delayedplant-mediated interspecific interactions also occur for sap feeders, Annual Reviews www.annualreviews.org/aronline

310 DENNO, McCLURE& OTT

but these are less well studied. Previous feeding by the scale insect F. externa dramatically reduced the performance of the next generation of N. tsugae feeding on the same tree (114). The same result occurred for the planthopper Prokelisia marginata, whose fitness was diminished when plants were fed upon by previous generations of Prokelisia dolus (RF Denno & J Cheng, in preparation). In both of these systems, feeding-related reductions in plant quality intensified competition. Interactions between phytophagous insects can also be mediated through herbivore-producedmodifications in plant parts that alter the ability of other herbivores to utilize those structures. For example, the scolytid beetle Cono- phthorus resinosae severed the vascular system of pine cones, rendering them unsuitable for attack by the conewormDioryctria disclusa (112). Flower-bud feeding by the cecidomyid Arcivena kiehneyerae altered the stamens so as to preclude subsequent feeding by the weevil Anthonornusbiplagiatus (25), and larvae of the fly Urophoraaffinis prevented seed heads from attaining a size suitable for oviposition by Urophoraquadrifasciata (16). Similarly, stem galls of the sawfly Euura lasiolepis reduced new leaf production, which decreased the availability of oviposition sites for other sawfly species (63). Foraging larvae of O. brumatainterfered with the leaf-rolling ability of T. viridana, whichresulted in the latter species’ desiccation and death (87). Plant phenological events can also mediate interactions between phytophagous insects. Synchrony of O. brumata larval eclosion with bud break drives the population dynamics of this oak-feeding lepidopteran (86). Thus, despite its superior competitive ability over T. viridana, stochastic variation in bud break dictates the intensity of the competitive interaction betweenthese two species (86, 87). Herbivorous insects feeding in the bracts of Heliconia spp. plants have a very narrow windowof opportunity for oviposition (155, 156). Thus, the extent to which these insects compete is dictated by the probability of simultaneous colonization (155, 156). by University of Minnesota- Law Library on 09/17/06. For personal use only. Genetic and environmental variability in plant resistance can also mediate

Annu. Rev. Entomol. 1995.40:297-331. Downloaded from arjournals.annualreviews.org the intensity and frequency of competitive interactions. For example,the leaf- galling aphid Hayhurstia atriplicis drastically affected the survival of the root-feeding aphid Pemphigusbetae, but only on susceptible plant genotypes (135). The intensity of competition amongseveral species of gall-making sawflies depended on host plant clone (60). The presence of balsam aphids (Mindarus abietinus) reduced the survival of budworms(Choristoneurafumif- erana) but only on fir trees susceptible to aphid attack (113). Similarly, the fecundity of the sawfly Neodiprion edulicolis was reduced in the presence of the stem wormDioryctria albovitella, but only on pine genotypes susceptible to attack from stem worms(134). Only on stressed trees in ornamental plantings (85, 119), and on trees at the edge of their natural range(I 18), did densities of several homopteransreach competitive levels. Annual Reviews www.annualreviews.org/aronline

COMPETITIONIN PHYTOPHAGOUSINSECTS 311

Vegetation texture (plant spacing, patch size, and species composition) can also dictate interactions betweenphytophagous insects. Followingthe removal of Phyllotreta crucifreae, competitive release of Phyllotreta striolata was observed, but only in dense plantings in which these collard-feeding flea beetles could easily moveamong plants (96). Interactions between two aphid species (genus Uroleucon) were more intense on small patches of Solidago altissima than on single stems (43). With the removal of the bug Neacoryphus bicrucis, several sap-feeding and mandibulate species exhibited a short-term competitive release, which lasted longer in small than in large patches of Senecio smallii because bugs recolonized small patches more slowly (129). Finally, the survival of the bug Megalocerarecticornis was reduced by another bug, Notostira elongata, but the competitive effect was removedin the presence of an alternate host plant species that acted as a refuge for the inferior competitor (70).

Natural Enemies Natural enemies are frequently espoused as maintaining populations of phytophagous insects below competitive levels (9, 106, 107, 148, 173, 174). The few experimentalstudies that bear on this hypothesis, however,offer conflict- ing evidence. Edson (43) experimentally removedinvertebrate predators from patches of S. altissima and found that the densities of two aphid species (Uroleucon)increased as did interspecific competition. Similarly, the exclusion of parasitoids resulted in increases in normally low-density populations of hemlockscale insects and in interspecific competition (119). In contrast, Karban(92-94) showedthat populations of three folivores on Erigeron glaucus were each affected strongly by only one biotic factor: spittlebugs by interspecific competition, plume moths by vertebrate predation, and thrips by clonal variation. Because the factor that was most important for each herbivore species did not interact with the other biotic factors, it wouldbe difficult to by University of Minnesota- Law Library on 09/17/06. For personal use only. conclude that predation mediated competitive interactions (94). Miller (131,

Annu. Rev. Entomol. 1995.40:297-331. Downloaded from arjournals.annualreviews.org 132), by experimentally removing combinations of competitors and natural enemies, showed that interspecific competition accounted for 51%of the mortality in bark beetle (Ips calligraphus) populations, whereas enemies accounted for only 38%of mortality. In this instance, foraging by the major wood-boring cerambicid competitor (Monochamustitillator) also killed the nonmobile natural enemies of L calligraphus. Exclusion of natural enemies did not temper the adverse effect of previous herbivory on the performanceof several birch-feeding herbivores (57). Similarly, predators and parasitoids did not prevent intense interspecific competition amongthe insect herbivores feeding on the flower heads of thistles (188). Introduced herbivores are often deficient of natural enemies as are pest species in managedhabitats as a result of control practices (28, 72). Thus, Annual Reviews www.annualreviews.org/aronline

312 DENNO,McCLURE & OTI"

higher incidence of competition between introduced species or species in managedhabitats mayprovide indirect support for the hypothesis that natural enemies diminish competitive interactions. In support of this hypothesis, we detected interspecific competition morefrequently in introduced systems (91% of 45 interactions) than in systems comprised of native herbivores (77% 136 interactions) (X2 = 3.88, P = 0.049). Interactions betweenscale insects and adelgids on hemlock(114, 115, 119, 122) and pine (120, 121, 124), studied in their native Japan and in eastern North America where they have been introduced, provide a striking exampleof the mediatingrole of natural enemies. In Japan, natural enemies usually maintain densities belowcompetitive levels. In contrast, in North Americawhere specialized natural enemies are largely ineffective, these insects fiercely competeto the point of competitive exclusion in regions of overlap. Similarly, severe competitive interactions often take place betweenherbivorous insects that have been serially introduced without natural enemies to control noxious weeds (84). Competition, however, was more frequent in managed(90% of 42 interactions) than in natural habitats (78%of 139 interactions) (;~2 = 3.17, P = 0.075). Alternatively, novel host plant associations for introduced herbivores may foster increased densities and competitive interactions. For example, introduced homopteransattain high densities and compete on new hosts but rarely competeon native hosts with which they have had a long-standing association (119, 124). Also, mandibulate herbivores in concealed feeding niches experience a higher incidence of interspecific competition than free-living herbivores in exposed niches (Z2 = 11.90, P = 0.001; Table 1) with presumably more enemy-relatedmortality (73). This observation is consistent with the view that natural enemies can moderate interactions between some phytophagous insects. Besides influencing the intensity of interspecific competition, natural ene- by University of Minnesota- Law Library on 09/17/06. For personal use only. mies mayalso alter the outcomeof competition between two species. Whether

Annu. Rev. Entomol. 1995.40:297-331. Downloaded from arjournals.annualreviews.org enemies promote coexistence or accelerate exclusion appears to depend on which herbivore suffers most from attack. Increased enemy attack on the inferior competitor mayhasten its reduction or exclusion. For instance, the shift of a bivoltine shared parasitoid to the secondgeneration of the scale insect N. tsugae accelerated its exclusion by the univoltine and competitively superior F. externa (115, 122). Likewise, elevated attack of yellow scale Aonidiella citrina by shared parasitoids hastened its exclusion from citrus orchards by California red scale Aonidiella aurantii, ~vhich is the better competitor (35). A shared parasitoid also tipped the competitive balance between two leafhopper species with similar competitive abilities (158). The replacement of Eu- rythroneura elegantula by Eurythroneura variabilis in the vineyards of California resulted from selective attack on E. elegantula eggs, which were Annual Reviews www.annualreviews.org/aronline

COMPETITIONIN PHYTOPHAGOUSINSECTS 313

inserted closer to the leaf surface and consequently experienced greater parasitism (158). Furthermore, the aphid Panaphisjuglandis experienced dramatic density increases in commercialwalnut orchards following suppression of the competitive dominant Chromaphisjuglandicola by a parasitoid (130). Whenthe bark beetles Dendroctonusponderosae and Ips pini were experimentally forced to simultaneously colonize pine trees, D. ponderosaesuffered directly from competition for phloemresources but also incurred greater mortality from parasitoids and predators, someof whichwere normally associated with and attracted by the pheromonesof L pini (15). In this case, interspecific competition and enemies acted in concert. Natural enemies also indirectly intensify interactions betweenearly season folivores and late season leaf miners. For example, rates of leaf miner parasitism were higher on chewedleaves than on intact ones (46, 47, 50, 51), which resulted from parasitoid attraction to physical damage(50) and perhaps leaf chemical cues as well (49). Evidencealso suggests that someaphids competefor the services of tending ants, which increase aphid persistence by deterring invertebrate predators (3, 4, 32). Thus, mutualistic ants can have a positive effect on aphid population size, thereby increasing the potential for interspecific competition(4). Physical Factors Weather-related factors mediate competitive interactions more frequently between sap feeders (16% of 68 interactions) than between mandibulate herbivores (6%of 72 interactions). The disproportionate susceptibility of sap feeders to physical factors maybe related to their relatively small size and exposed feeding niches. For instance, heavy rain and wind reduced the densities of Eurythroneura leafhoppers on sycamore below competitive levels (126, 127). Sap feeders mayalso be more sensitive to plant stress resulting from adverse weather (101). by University of Minnesota- Law Library on 09/17/06. For personal use only. Differential temperature tolerance can also dictate competitive outcome.

Annu. Rev. Entomol. 1995.40:297-331. Downloaded from arjournals.annualreviews.org Tropical species of rice-feeding Nephotettix leafhoppers out-competed temperate species under warmrearing conditions, but the reverse occurred when they were raised under cooler conditions (180). The psyllid Arytaina spartii undergoes egg diapause and is morecold tolerant than its competitively superior congener A. genistae (183). However,the early hatch of A. spartii eggs in spring allows nymphsto preempt buds before the superior competitor is active: For mandibulate herbivores, subtle changes in physical conditions can also shift the competitive result. Becausedevelopmental optima differ, the bruchid Callosobruchus chinensis excludes Callosobruchus maculatus at 30°C, but a 2°C increase completely reverses the outcome(64). The subtropical fruit fly Dacusdorsalis readily out-competed the subtemperate Dacuscapitata in cooc- Annual Reviews www.annualreviews.org/aronline

314 DENNO,McCLURE & O’Iq"

cupied fruits at low elevations in Hawaii, but D. capitata dominatedat higher elevations (97). Similarly, the buprestid Agrilus hyperici persisted in only shaded habitats where the chrysomelid Chrysolina quadrigemina, the superior competitor in sunny sites, was at a developmentaldisadvantage (84).

lntraspecific Competition Evidence supporting the view that intraspecific competition diminishes the intensity of interspecific competition is mixed(44, 126). For example,in only 40%of the 70 species for which data were available was intraspecific greater than interspecific competition. Interspecific competition equaled or exceeded intraspecific competition for 8 (11%) and 35 (50%) species, respectively. However,there was a slight tendencyfor intraspecific competition to be greater than or equal to interspecific competition morefrequently for sap feeders (60% of 42 interactions) than for mandibulatespecies (39%of 28 interactions) = 2.71, P = 0.099). In somesap feeders, intense intraspecific competition seems able to moderate interspecific interactions. The best evidence comes from Eurythroneura leafhoppers on sycamore and Eupteryx leafhoppers on nettles, in which strong intraspecific competition diminished but did not preclude interspecific interactions (126, 165). Additional evidenceindicates that intraspecific competition is a moreimportant mortality source for leaf miners than interspecific competition (19, 51). However,in the Homoptera(41, 114, 123, 124, 183) and chewing insects (31, 87) strong intraspecific competition in the competitive dominant often does not deter extreme adverse affects on the competitive subordinate. For instance, 14 of the 15 species we were able to evaluate experienced a higher degree of intraspecific competition than interspecific competition, yet the adverse effects of each species were greater on its competitor than on itself. Perhaps the extent to which intraspecific competition tempers interspecific interactions depends on the symmetryof the interspecific interaction. If the by University of Minnesota- Law Library on 09/17/06. For personal use only. interactions are symmetric, as was the case for the two leafhopper systems

Annu. Rev. Entomol. 1995.40:297-331. Downloaded from arjournals.annualreviews.org (126, 165), then strong intraspecific effects maydampen interspecific ones. However,if interspecific interactions are very asymmetric,as is the case for most phytophagousinsects (Table i), then strong intraspecific effects in the superior competitor maynot preclude a significant interspecific impact on the inferior competitor. It has often been assumedthat intraspecific competition is a prerequisite for interspecific competition (see 174). In one instance, however, spittlebugs actually benefited from conspecifics, but suffered badly in the presence of plume mothcompetitors (94). Furthermore, in our analysis, interspecific competition was far moreimportant than intraspecific competition for 27 of 28 species for which data were available. In fact, 14 of these species experienced regional or local competitive exclusion (8, 18, 71, 84, 97, 114, 123-125). Also, for Annual Reviews www.annualreviews.org/aronline

COMPETITIONIN PHYTOPHAGOUSINSECTS 315

herbivores that competevia interference mechanisms(aggression or deterrent chemicals), interspecific competition mayoccur despite abundant food resources and diminished intraspecific competition (17, 54, 55, 71, 109, 110, 143, 166, 178). These examples cast doubt on the premise that intraspecific competition is a necessary requirement for interspecific competition. Interplay of Factors Mediating Interspecific Competition Given the experimental information available, it is difficult to championone particular factor as mediating competitive interactions or inflicting the most mortality on phytophagousinsects, even within a given system. For example, in the communityof insect herbivores feeding on E. glaucus, no single factor (interspecific competition, natural enemies, or host plant clones) explained the organization of this communitybecause each factor was most important for a different herbivore species (94). For two aphid species on goldenrod, abundance was dictated by the dynamicinteraction of interspecific competition, predation, and dispersal in response to induced changes in plant quality (43). Several two-factor studies also showthat interspecific competition can be the most important source of mortality as often as natural enemiesand host plants. Of the 13 natural systems in which the relative importance of these factors was reported, interspecific competition was most influential in 6 (9, 57, 131, 183, 185, 188), natural enemies were most important in 5 (19, 46, 47, 119, 173), and host plant factors were most consequential in 2 (63, 87). Althoughthe evidence that host plants, natural enemies, and physical factors mediate certain competitive interactions is compelling, sweepinggeneralities concerningtheir impact are often unjustified. Herbivorelife histories can vary widely (e.g. mobility, aggregation, body size, feeding niche), and these differences maybe equally important in arbitrating competitive interactions (see 94). by University of Minnesota- Law Library on 09/17/06. For personal use only. LIFE HISTORIES AND FEEDING STYLES THAT Annu. Rev. Entomol. 1995.40:297-331. Downloaded from arjournals.annualreviews.org INFLUENCE COMPETITION

Certain life history traits (mobility or aggregation) and feeding styles (feeding niche, diet breadth, and host plant growthform) mayinfluence the probability for competition in phytophagousinsects. Herbivores that are immobile and have little ability to switch host plants maybe more likely to experience competition (94). Our analysis supported this hypothesis. Sessile herbivores competed in 89%of 71 interactions, whereas mobile herbivores competed in only 76%of 111 interactions 0~2 = 4.54, P = 0.033). This pattern was strongest for mandibulate herbivores, in which competition was detected in 89%of 56 interactions involving sessile species (e.g. leaf miners, woodborers, root feeders), but in only 69%of 68 interactions involving mobile herbivores such as Annual Reviews www.annualreviews.org/aronline

316 DENNO, McCLURE& OTT

free-living grasshoppersand caterpillars (~2 = 6.76, P = 0.009). Similarly, for mandibulatespecies that develop within a discrete resource (fruit, seed, cone, inflorescence, stem, gall, or leaf), competition was detected more frequently (86%of 43 interactions) than it was for their less confined counterparts (free- living folivores and woodborers; 68%of 65 interactions) (Z2 = 4.41, P = 0.036). Although aggregation in the superior competitor is thought to promote coexistence by providing refuges for the inferior competitor (10), aggregation in the sameniche for reasons related to plant quality mayfacilitate interspecific interactions (41, 114, 124). Under these circumstances, contact amongindi- viduals is frequent and the group maymodify plant nutrition or induce plant chemistry in waysthat intensify plant-mediated interactions (41, 114). Indeed, we found that competition occurred more frequently for pair-wise interactions involving aggregated herbivores (89%of 83 interactions) than it did for interactions involving only solitary species (74%of 35 cases) (~2 = 3.99, P = 0.046), a pattern documentedpreviously (34). The aggregated distributions of sap feeders and woodborers contributed heavily to this result. Phenotypic trade-offs betweenlife history traits such as dispersal and fecundity (40) maypreclude an herbivore from being both a successful disperser and a superior competitor if competitive ability depends on fecundity and rapid population growth. Thus, phytophagousinsects exploiting ephemeral habitats maybe destined to competitive inferiority. Evidence from the free-living Homopteraand Hemiptera supports this hypothesis. In 10 of 13 interactions that could be assessed, the relative loser was a better disperser than was the winner (1, 41, 43, 69, 70, 88, 114, 124, 129, 175), and dispersal ability was equivalent in the remaining 3 species pairs. A balance betweendispersal and. competitive ability amongspecies exploiting ephemeral and patchy resources is thought to promote coexistence (10, 160). Coexistence occurs because the inferior competitor can emigrate to unoccupied habitats, a phenomenonwell by University of Minnesota- Law Library on 09/17/06. For personal use only. demonstrated for several homopterans(41, 43, 88, 175). High fecundity, how-

Annu. Rev. Entomol. 1995.40:297-331. Downloaded from arjournals.annualreviews.org ever, was not associated with competitive ability. Across all herbivore guilds, the winner tended to be no more fecund than the loser (winner > loser in 16 cases, and winner < loser in 20 interactions). Bodysize does appear to influence competitive outcome.Across all guilds, the superior competitor was larger than the inferior competitor in 41 interactions, equal in size in 17 interactions, and smaller in size in 20 interactions. This trend was particularly strong for mandibulateherbivores (winner > loser in 32 cases, winner---loser in 5 cases, winner< loser in 10 cases), whereasin sap feeders, size did not appear as important in dictating competitivesuperiority (winner > loser in 6 cases, winner= loser in 12 cases, winner< loser in 7 cases) (Z2 = 13.71, P = 0.001). In manydirect interactions involving mandibulateherbivores, particularly stem borers, seed feeders, and root feeders, the competitivesuccess of larger Annual Reviews www.annualreviews.org/aronline

COMPETITIONIN PHYTOPHAGOUSINSECTS 317

individuals was achieved by overt overpoweringand killing of opponents via aggressive biting behavior (24, 143, 148, 166, 178), or by inadvertent killing while foraging (139, 168). Such behavior is less possible for sap feeders, which mayexplain the poor association between large body size and competitive success in this guild. Nevertheless, there are a few hemipteransand homopterans in which large body size and/or aggressiveness confers competitive superiority in direct interactions (6, 70, 129). One might hypothesize that multivoltinism (independent of body size) could contribute to rapid population growthand competitive superiority, especially for species that interact exploitatively. Wefound no overall support for this hypothesis. The superior competitor underwentmore generations per year than did the inferior competitorin 9 cases, fewer generations in 12 cases, and their voltinism was the samein 82 instances. Several examplesillustrate whyhaving more broods per year is not necessarily a competitive advantage. Anyadvan- tage the bivoltine psyllid Arytaina genistae gains in autumnis offset in spring because the univoltine Arytaina spartii appears first and preemptsmost feeding sites (183). Additionally, the numerical advantage of bivoltinism in the scale insect N. tsugae is offset by increased parasitism froma parasitoid shared with its univoltine competitor F. externa. Whenthe latter scale insect becomesrare in fall, the parasitoid shifts to N. tsugae. Furthermore,the high rate of parasitism accelerates the exclusion of the bivoltine scale from cohabited forests (115, 122). In somecases, however, a second generation mayprovide a refuge for the inferior competitor and promotecoexistence (16, 69). Finally, although having a shorter life cycle and producing more broods per year than one’s competitor confers an advantage under constant conditions, this advantage is less likely to be realized in temperate habitats because life cycles are resyn- chronized every winter (13). Arriving at a resource first allows somespecies to gain the numerical, and consequently, the competitive edge (43, 54, 84, ll0, ll2, 114, 183). Early by University of Minnesota- Law Library on 09/17/06. For personal use only. arrival can result either from advancedseasonal emergence(84, 114, 123, 183)

Annu. Rev. Entomol. 1995.40:297-331. Downloaded from arjournals.annualreviews.org or rapid colonization (54, 110). Early arrival tends to confer competitive superiority whencoupled with rapid population growth and/or the preemption of resources that results from physical exclusion (114, 183) or chemical deterrence (54, 110). Whenthe advantage of early arrival was experimentally removed,the scale insect F. externa lost its competitive superiority (114). The Homopterapossess manylife history traits that promote competitive interactions, including rapid population growth (41, 88, 175), aggregation (reviewed in 41), sessile behavior throughout muchof their life cycle (6, 92,114, 123, 124, 126), and feeding on a commonphloem resource (135). The frequent combination of these traits in the Homopteramay partly explain their over-representation in studies demonstrating competition (41, 92, 135, 174) (Table 1). Annual Reviews www.annualreviews.org/aronline

318 DENNO, McCLURE& OTT

Dietary specialists mayincur increased competition because they do not have the option of switching to alternative host plant species. In contrast, the metabolic costs and foraging styles associated with feeding on a chemically diverse array of plants mayinfluence the competitive ability of polyphagous species. Regardless, we found no evidence to suggest that the frequency of competition differed between monophages(83% of 117 interactions) and polyphages(74% of 65 interactions) (~2 = 2.09, P = 0.148). However,for interactions involving polyphages, competition was tested with only one host plant species present. This caveat is noteworthy because the presence of an alternate host plant species reduced competition between the two hemipterans N. elongata and Megalocerarecticornis (70). Also, competitive interactions betweenpolyphagous grasshoppers resulted in shifts in the proportion of mono- cots and dicots in their diets (145). These examples suggest that polyphagy mayprovide feeding options that diminish competitive interactions for some species. Competitiveinteractions maybe less intense on large, more architecturally diverse plants on which herbivores may be able to escape from one another (see 34). Wefound that the growth form of the host plant did affect the likelihood of competition. Interspecific competition occurs less frequently on trees and shrubs (74%of 100 interactions) than on forbs and grasses (87% 82 interactions) (Z2 = 4.27, P = 0.039).

TAXONOMIC RELATEDNESS AND INTERSPECIFIC COMPETITION

Competitionmay be more likely to occur between closely related taxa because of similarity in feeding niche (133). In support of this hypothesis, interspecific competition was detected in 100%of 44 interactions involving congeneric species pairs. In contrast, competition occurred in only 74%of 137 noncongen- by University of Minnesota- Law Library on 09/17/06. For personal use only. eric interactions 0~2 = 7.07, P = 0.008). However,even though closely related

Annu. Rev. Entomol. 1995.40:297-331. Downloaded from arjournals.annualreviews.org taxa competed more frequently, competition was still commonbetween non- congeneric pairs, 41 of whichwere interordinal interactions.

LINK BETWEEN RESOURCE PARTITIONING, NICHE SHIFTING, AND INTERSPECIFIC COMPETITION

Sharing the same feeding niche is thought to intensify competition between two species. Conversely, spatial and temporal differences in the use of resources maydiminish competitive interactions (151, 152). In support of this classical view, severe competition between phytophagousinsects often occurs whenthey share an identical niche (41, 43, 92, 166, 183). For example,several competitive exclusions involving sap feeders have occurred in species that Annual Reviews www.annualreviews.org/aronline

COMPETITIONIN PHYTOPHAGOUSINSECTS 319

prefer to feed in the samemicrohabitat on the plant (114, 123, 124). Also, four species of aphids on bean plants, the two species sharing the samefeeding site competedmore intensively than those exhibiting microhabitat segregation (82). Regardingthe moderatingeffects of resource partitioning on interspecific interactions, we found substantial evidence that temporal and spatial differences in resource use can dampen,although not necessarily preclude, competition. Here we explore experimental evidence for an association between resource partitioning and reduced competition, and the use of shared resources and niche shifting. The widespread evidence for competitive interactions between early-season and mid- to late-season feeders via altered plant chemistry (57, 75, 78, 79, 81, 136, 137, 185) suggests that temporal displacement does not necessarily prevent competition. However, several manipulative experiments suggest that temporal partitioning mayreduce interspecific competition for somespecies. Leaf miners normally feed later in the season than do manyfree-living leaf chewers (49, 185). By experimentally forcing a generation of the miner Phyl- lonorycter spp. to emergein the spring and thereby cooccur with leaf chewers, the miner’s fitness was muchlower than it was in the naturally occurring summergenerations (185). Despite a more nutritious plant resource in spring, miner survival was adversely affected by leaf damage-relatedinteractions with chewers. Similarly, the bark beetle D. ponderosaeattacks living pines, while L pini usually follows by exploiting dying trees (142). Experimentally forced synchrony of these beetles resulted in drastic reductions in the survival of D. ponderosae, which was attributable to direct competition with I. pini as well as increased mortality from the predators and parasitoids normally associated with L pini (15, 142). The observation that enemypressure can be reduced the temporal partitioning of resources is consistent with the view that herbivores compete for enemy-free space (12, 140).

by University of Minnesota- Law Library on 09/17/06. For personal use only. Reciprocal avoidance of aggregation pheromonesin bark beetles deters colonization and contributes to their spatial segregation both within and among Annu. Rev. Entomol. 1995.40:297-331. Downloaded from arjournals.annualreviews.org trees (17, 20, 22, 55, 109, 110, 138, 182). Furthermore, in the absence of competitor, bark beetles occupy broader niches than they do in mixed species populations (30, 138, 142). Notably, when beetles that normally partition resources are forced to interact experimentally, severe competition can ensue (110, 142). During oviposition, females of Callosobruchus maculatus beetles mark beans with a chemical that inhibits oviposition by Callosobruchusrhodesien- sis, forcing them to place eggs elsewhere (71). Whenthese two bruchid species are confined together in mixed culture, C. ~naculatusexcludes C. rhodesiensis (71). Similarly, on large-sized beans, Callosobruchusanalis feeds in the center of the bean and Callosobruchusphaseoli feeds near the outside surface; this Annual Reviews www.annualreviews.org/aronline

320 DENNO, McCLURE& OTT

microhabitat segregation allows these bruchids to coexist (178). Whenthese species are reared together on small beans, partitioning of the bean is precluded, and C. analis excludes C. phaseoli (177, 178). In contrast, the spatial segregation of the host plant by manysap-feeding insects does not appear to preclude interspecific competition (1, 82, 88, 123, 175). In these cases, competition may result from the sharing of a common phloemresource, because even foliar-feeding and root-feeding sap feeders can competeintensively (135). Similarly, mandibulatefolivores mayinduce chemical changes in plants that adversely impact other species, especially immobile ones, elsewhere on the plant (34). Wefound numerouscases of niche shifting in the presence of a competitor (or previous damage), wherebya species was relegated to a poor feeding site (114, 123, 124, 134, 157), a different feeding or oviposition site (17, 20, 47, 52, 54, 71, 79, 91, 99, 109, 112, 138, 144, 163), a different host plant species (70, 145), or a different portion of the habitat (35, 41, 97, 100, 130). In one case, the presence of a competing bruchid species promotedthe rapid adaptation of another bruchid species to a novel host plant species (176). several of the above cases, niche shifting was mediated by chemicals (interference mechanism)produced by one herbivore that deterred colonization (17, 20, 109, 138), feeding (144), or oviposition by another (52, 54, 71, 91, Another commonresponse to interspecific crowding is emigration to nearby plants (9, 43, 69, 82, 88, 129, 163) or distant habitats (41, 100). Emigration triggered by heterospecifics is better documentedfor sap feeders (13 cases) than it is for mandibulateherbivores (1 case). Emigrationdeters local exclusion in aphids because as mixed species aggregations contribute to the rapid demise of the current plant, the inferior competitor colonizes neighboring healthy plants (88). Although emigration allows an insect to escape the effects interspecific crowding, enemy-related risks maybe associated with movement (146).

by University of Minnesota- Law Library on 09/17/06. For personal use only. Eventhough interspecific competition results in niche constriction or shift-

Annu. Rev. Entomol. 1995.40:297-331. Downloaded from arjournals.annualreviews.org ing for somephytophagous insects, for others the niche does not change in the absence of competitors. For instance, the distribution of Mordellistena splen- dens within stems did not differ between populations with and without an important competitor (166). Similarly, the distribution of Eriosomaspp. gall aphids on the leaves of elm did not differ between regions of allopatry and sympatry with a major competitor (6). Such observations have been used suggest that niche divergence does not necessarily result from interspecific competition (6). Wehave presented substantial evidence that supports the classical view that species sharing the same niche compete most severely, and that resource partitioning can often moderate, but not necessarily preclude, interspecific competition. Several studies have demonstrated that when normally displaced Annual Reviews www.annualreviews.org/aronline

COMPETITIONIN PHYTOPHAGOUSINSECTS 321

herbivores are experimentally forced to eooeeur, intense competition results. However,our analysis also suggests that traditional views of the relationship between resource partitioning and competition must be modified to include cases in which spatially segregated sap feeders compete via a shared phloem resource, and cases in whichtemporally or spatially displaced folivores compete through herbivore-induced changes in plant physiology.

INTERSPECIFIC COMPETITION AND REPULSED DISTRIBUTIONS

Repulsed distributions of herbivores in the field have been used as evidence for interspecific competition (36, 127, 184). Conversely,positive associations have been called on to challenge the importance of competition (102, 170, 171). Here we present data for and against the relationship betweeninterspe- cific competition and herbivore distribution. Onthe interplant scale, 25 of the species pairs we studied were negatively associated. Of these, 10 were sap feeders (2, 35, 43, 114, 123, 124, 128, 130, 135, 158); 7 were stem borers (143, 166); 2 were woodborers (110, 142); were fruit/cone feeders (97, 112); and 4 were involved interguild interactions (31, 94, 128). For 13 of these species pairs, strong experimental evidence linked interspecific competitionto repulsed distribution (31, 43, 94, 110, 114, 123, 124, 128, 135, 142, 166). In contrast, competition was not demonstrated between thrips and plume moths, yet they showeda negative association in the field; differences in habitat selection caused their lack of cooccurrence(93). Other species were positively associated despite the occurrence of interspecific competition (43, 61, 138, 182). Positive associations betweenpotential competitors mayresult from both species respondingsimilarly to host plant variation (e.g. nutrition) for feeding or oviposition (19, 61). For somephytophagous insects, evidence also suggests

by University of Minnesota- Law Library on 09/17/06. For personal use only. that feeding and oviposition sites are not chosen on the basis of competitor presence or absence (9, 139). Together, these observations emphasize the Annu. Rev. Entomol. 1995.40:297-331. Downloaded from arjournals.annualreviews.org weaknessinherent in inferring interspecific competition from insect distributional data (see 27, 80, 150).

FACILITATIVE INTERACTIONS BETWEEN PHYTOPHAGOUS INSECTS

Wefound 11 interactions betweenphytophagous insects that were facilitative (Table 1). Four of these cases involved aphid species that showedincreased survival, developmentrate, or body size when in close proximity to another herbivore species (56, 67, 98, 159). In three of these instances, one aphid species selected the most nutritious feeding site on the plant, which happened Annual Reviews www.annualreviews.org/aronline

322 DENNO, McCLURE& OTT

tO be adjacent to the nutrient sink created by an aggregation of a previously established aphid species (56, 98, 159). Also, feeding by one folivore (Lepidoptera) maystimulate plant regrowth, which benefits other herbivores that feed later in the season (33, 186). How- ever, an increase in the intensity of herbivory may change the herbivore interaction from facilitation to competition. For instance, moderateherbivory by the western tent caterpillar, Malacosomacalifornica, had positive effects on the fall webwormHyphantria cunea, but heavy defoliation conferred adverse effects on performance(186). Similarly, Ips avulsus is attracted to trees under attack by other bark beetle species, and the mixed species attack can increase the probability of all the species securing oviposition sites as they mutually defeat resin-based tree defenses (55, 138, 182). However,this initial benefit does not preclude intense competitive interactions amongspecies for the best developmentsites (55, 138, 182). Thus, for somecases of facilitation, positive effects are transient and give waylater to competitivesituations. Most facilitative interactions were very asymmetric, with only one species gaining an advantage. In one unusual interaction between the leaf miner C. syngenesiae and the root-feeding chafer P. horticola, the leaf miner benefited from root feeding whereas the root feeder was disadvantaged by foliar feeding (111). Fewif any of the aforementionedfacilitative interactions represent tightly coevolvedrelationships. However,some ant-tended lycaenid butterflies ensure protection of their offspring by specifically ovipositing on plants with ants already tending homopterans(11, 162). Finally, some studies demonstrating facilitation between herbivores and detritivores have been incorrectly included in assessments of interspecific interaction between"phytophagous insects" (26, 107). For example, the elegant experimental studies of Seifert & Seifert (156) on the insect inhabitants Heliconia bracts actually involved several species that are detritivores (155,

by University of Minnesota- Law Library on 09/17/06. For personal use only. 156). All cases of facilitation reported in this communityrepresented interactions betweenan herbivore and a detritivore, whichis not surprising whenone Annu. Rev. Entomol. 1995.40:297-331. Downloaded from arjournals.annualreviews.org species increases food resources for another. The only two herbiVore-herbivore interactions studied were both weakly competitive.

SUMMARY AND PROSPECTUS

This review has reexaminedthe importance of interspecific competition in the population biology of phytophagousinsects. Our analysis of a greatly expanded database, selected from all feeding guilds, demonstrates widespread evidence for interspecific competition betweenphytophagous insects (76%of 193 pair- wise interactions). Of all the guilds examined,competition was most frequently detected amongsap feeders, stem borers, woodborers, and seed and fruit Annual Reviews www.annualreviews.org/aronline

COMPETITIONIN PHYTOPHAGOUSINSECTS 323

feeders. Interspecific competitionwas least likely to occur betweenfree-living, mandibulate folivores. Most interspecific competitive interactions were mark- edly asymmetric. This asymmetrymay explain the lack of a general tendency for intraspecific competition to diminish interspecific interactions. Host plant factors mediated far more interspecific interactions than did natural enemies, physical factors, and intraspecific competition combined.An important consequenceof variation in host plant chemistry maybe the con- centration of herbivores at optimal feeding sites, thereby predisposing them to competitive interactions. The extent to which natural enemies direct competitive interactions depends on whichcompetitor is attacked. Selective attack of the inferior competitor can promotecompetitive exclusion; concentrated attack on the superior competitor maypromote coexistence; and heavy attack on both herbivore species maydeter competition altogether. Exploitative and interference mechanismswere equally frequent when all herbivore species were considered as a whole. However,interference competition was more commonin mandibulate herbivores living in concealed niches (e.g. stem borers and seed feeders) comparedwith free-living species. For mandibulate herbivores, but not sap feeders, competitive superiority was very strongly associated with large body size and aggressive behavior. Phytophagous insects were more likely to compete if they were closely related (congeners), introduced, sessile, aggregative, and fed internally on discrete resource (e.g. seed, fruit, or stem) or fed on forbs or grasses as opposed to trees or shrubs. Interspecific competition betweenherbivores occurred with similar frequencies in managedand natural habitats. Despite the widespread evidence for interspecific competition presented here, a demonstration of the overall importance of interspecific competition in the population and communityecology of phytophagous insects remains a challenge. Several experimental studies in natural systems have specifically addressedthe relative importanceof interspecific competition, natural enemies,

by University of Minnesota- Law Library on 09/17/06. For personal use only. and host plant factors. The results of these studies indicate that competition was as important as natural enemies and host plant factors in structuring the Annu. Rev. Entomol. 1995.40:297-331. Downloaded from arjournals.annualreviews.org communityof herbivores (92-94), or that herbivore abundance was dictated by the dynamicinteraction of interspecific competition, predation, and dispersal in response to induced changes in plant quality (43). Two-factor comparisons in natural systems have also shownthat interspecific competition can be the most important source of mortality (9, 57, 131,183, 185, 188), as often natural enemies (19, 46, 47, 119, 173) and host plants (63, 87). These parative studies, coupled with the paucity of experimental evidence against interspecific competition(only 18%of 193 interactions), provide little support for the claim that competition is a weakand infrequent force in phytophagous insect communities. To the contrary, the existing experimental evidence for this assertion is itself weakand infrequent. Annual Reviews www.annualreviews.org/aronline

324 DENNO, McCLURE& OTI"

Given the experimental data currently available, we conclude that there is far more justification for retaining competition as a potentially important factor than for dismissing it. Other recent assessments have drawn similar conclusions regarding the potential importance of interspecific competition in phytophagous insect communities (34, 48, 49, 94, 169). We argue, as have others (34, 48, 49, 94), for the collective assessment of both intra- and intertrophic- level factors in studies investigating the distribution and abundance of phytophagous insects. Toward this end, sufficient evidence exists to call for the resurrection of interspecific competition as a viable hypothesis warranting serious consideration in future investigations of the structure of phytophagous insect communities.

ACKNOWLEDGMENTS Hans Damman, John Losey, Charles Mitter, Susan Mopper, and Merrill Pe- terson critiqued an earlier draft of this review and provided many helpful suggestions. Tim Paine, Douglas Ferguson, Tom Henry, Ronald Hodges, and David Smith confirmed the diet breadth and various life history traits for several species of Hemiptera, Coleoptera, Lepidoptera, and Hymenoptera. John McAllister and Andie Huberty assisted with the monumental literature chase. Ches Zeeb helped condense and catalogue host plant data and offered constant direction. Weare most appreciative to all of these colleagues for their assis- tance and support. This research was supported in part by National Science Foundation Grants BSR-8614561 to RFD and DEB-9209693 to RFD and JRO. This is Scientific Article Number A-6564, Contribution Number 8776 of the Maryland Agricultural Experiment Station, Department of Entomology.

AnyAnnual Review chapter, as well as anyarticle cited in an AnnualReview chapter, maybe purchasedfrom the AnnualReviews Preprints and Reprints service. 1-800-347-8007;415-259-50171 emaih [email protected] by University of Minnesota- Law Library on 09/17/06. For personal use only.

Annu. Rev. Entomol. 1995.40:297-331. Downloaded from arjournals.annualreviews.org Literature Cited

1. AddicottJF. 1978.Niche relationships 5. AkimotoS. 1981. Gall formation by amongspecies of aphids feeding on Eriosomafundatrices and gall parasit- fireweed. Can. J. Zool. 56:18837-41 ism in Eriosoma yangi (Homoptera, 2. Addicott JF. 1978. The population dy- Pemphigidae).Kontyu 49:426-36 namics of aphids on fireweed: a com- 6. AkimotoS. 1988. Competition and parison of local ’ populations and niche relationships amongEriosoma metapopulations.Can. J. Zool. 56:2554- aphids occurring on the Japaneseelm. 64 Oecologia75:44-53 3. AddicottJF. 1978.Competition for mu- 7. AkimotoS. 1988.The evolutionof gall tualists: aphidsand ants. Can.J. Zool. parasitism accompaniedby a host shift 56:2093-96 in the gall aphid, Eriosomayangi (Ho- 4. Addicott JF. 1979. A multispecies moptera: Aphidoidea).Biol. Z Linnean aphid-ant association: density depend- Soc. 35:297-312 enceand species-specificeffects. Can. 8. Allotey J, KumarR. 1985. Competition J. Zool. 57:558-69 between Corcyracephalonica (Stain- Annual Reviews www.annualreviews.org/aronline

COMPETITION IN PHYTOPHAGOUS INSECTS 325

ton) and Ephestia cautella (Walke0 in colonization: regulation of inter- and cocoa beans, Insect £cL Appl, 6:627-32 interspecific competition, J, Chem. 9. Antolin MF, Addicott JF. 1988. Habitat Ecol. 10:861-77 selection and colony survival of 23. Chen C. 1978. Epidemiology of rice Macrosiphumvaleriani Clarke (Homop- yellow dwarf. TalchungDist. Agric. lm- tera: Aphididae). Ann. Entomol. Soc. prov. Sin. Rep. pp. 139-66 Am. 81:245-51 24. Clark JD, Potter DA.1986. Competition 10. Atkinson WD,Shorrocks B. 1981. Com- between and relative feeding impact of petition on a divided and ephemeral masked chafer and Japanese beetle resource: a simulation model. J. Anim. grubs: confoundingeffects of a parasite. Ecol. 50:461-71 Ky. Turfgrass Res. Prog. Rep. 303:34- 11. Atsatt PR. 1981. Ant-dependent-food 35 plant selection by the mistletoe butterfly 25. Clark WE, Martins RP. 1987. An- Orgyris amaryllis (Lycaenidae). Oe- thonomus biplagiatus Redtenbacher cologia 48:60-63 (Coleoptera: Curculionidae), a Brazilian 12. Atsatt PR. 1981. Lycaenid butterflies weevil associated with Kielmeyera and ants: selection for enemy-free- (Guttiferae). Coleopterists Bull. 41:157- space. Am. Nat. 118:72-82 13. Bellows TS, Hassell MP. 1984. Models 26. Connell JH. 1983. On the prevalence for interspecific competition in labora- and importance of interspecific compe- J.tory Anim. populations Ecol. 53:831-48 of Callosobruchusspp. tition: evidence from field experiments. Am. Nat. 122:661-96 14. Belovsky G. 1986. Generalist foraging 27. Connor EF, Bowers MA. 1987. The and its role in competitive interactions. spatial consequences of interspecific Am. Zool. 26:51-69 competition. Ann. Zool. Fenn. 24:213- 15. Bergvinson DJ, Borden JH. 1991. 26 Glyphosate-induced changes in the at- 28. Cornell I-IV, HawkinsBA. 1993. Accu- tack success and development of the mulation of native parasitoid species on mountain pine beetle and impact of its introduced herbivores: a comparison of natural enemies. Entomol. Exp. Appl. hosts as natives and hosts as invaders, 60:203-12 Am. Nat. 141:847-65 16. Berube DE. 1980. Interspecific compe- 29. Coulson RN, Mayyasi AM, Foltz JL, tition between Urophoraaffinis and U. HahnFP. 1976. Interspecific competi- quadrifasciata (Diptera: Tephritidae) tion between Monochamustitillator and for ovipositional sites on diffuse knap- Dendroctonusfrontalis. Environ. Ento- weed (Centaurea diffusa: Compositae). tool. 5:235-47 Z. Angew. Entomol. 90:299-306 30. Coulson RN, Pope DN, Gagne JA, 17. Birch MC,Svihra P, Paine TD, Miller Fargo WS, Pulley PE, et al. 1980. Im- JC. 1980. Influence of chemically me- pact of foraging by Monochamustitil- diated behavior on host tree colonization lator (Col.: Cerambycidae) on within- by four cohabiting species of bark bee- tree populations of Dendroctonusfron- ties. J. Chem. Ecol. 6:395-414 talis (Col.: Scolytidae). Entomophaga 18. Blakley N, Dingle H. 1978. Butterflies 25:155-70 eliminate milkweedbugs from a Carib- 31. CrawleyMJ, Pattrasudhi P. 1988. Inter-

by University of Minnesota- Law Library on 09/17/06. For personal use only. bean island. Oecologia 37:133-36 specific competition between insect 19. Bultman TL, Faeth SH. 1985. Patterns herbivores: asymmetric competition be-

Annu. Rev. Entomol. 1995.40:297-331. Downloaded from arjournals.annualreviews.org of intra- and interspecific association in tween cinnabar moth and the ragwort leaf-mining insects on three oak species. seed-head fly. Ecol. Entomol. 13:243- Ecol. Entomol. 10:121-29 49 20. Byers JA, WoodDL. 1980. Interspecific 32. CushmanJA, Addicott JF. 1989. Intra- inhibition of the response of the bark and interspecific competition for mutu- beetles, Dendroctonus brevicomis and alists: ants as a limited and limiting Ips paraconfusus. J. Chem.Ecol. 6:149- resource for aphids. Oecologia 79:315- 64 21 21. Byers JA, WoodDL. 1981. Interspecific 33. DammanH. 1989. Facilitative interac- effects of pheromoneson the attraction tions between two lepidopteran herbi- of the bark beetles, Dendroctonusbre- vores of Asimina. Oecologia 78:214-19 vicomis and Ips paraconfusus in the 34. DammanH. 1993. Patterns of herbivore laboratory. J. Chem. Ecol. 7:9-18 interaction amongherbivore species. In 22. Byers JA, WoodDL, Craig J, Hendry Caterpillars: Ecological and Evolution- LB. 1984. Attractive and inhibitory ary Constraints on Foraging, ed. NE pheromonesproduced in the bark beetle, Stamp, TM Casey, pp. 132-69. New Dendroctonus brevicomis, during host York: Chapmanand Hall Annual Reviews www.annualreviews.org/aronline

326 DENNO, McCLURE & OTT

35. DeBach P, Hendrickson RM, Rose M. Schultz, pp. 135-71. NewYork: Aca- 1978. Competitive displacement: ex- demic tinction of the yellow scale, Aonidiella 49. Faeth S. 1988. Plant-mediated interac- citrina (Coq.) (Homoptera:Diaspididae) tions between seasonal herbivores: by its ecological homologue, the Cali- enoughfor evolution or coevolution? In fornia red scale, Aonidiella aurantii ChemicalMediation of Coevolution, ed. (Mosk.) in southern California. Hil- KCSpencer, pp. 391-414. New York: gardia 46:1-35 Academic 36. Denno RF. 1980. Ecotope differentia- 50. Faeth S. 1990. Structural damageto oak tion in a guild of sap-feeding insects on leaves alters natural enemyattack on a the salt marsh grass, Spartina patens. leafminer. Entomol. Exp. Appl. 57:57- Ecology 61:702-14 63 37. DennoRF. 1985. The role of host plant 51. Faeth S. 1992. Interspecific and intra- condition and nutrition in the migration specific interactions via plant responses of phytophagous insects, In The Move- to folivory: an experimental field test, ment and Dispersal of Agriculturally Ecology 73:1802-13 Important Biotic Agents, ed. DRMac- 52. Finch S, Jones TH. 1987.. Interspecific Kenzie, pp. 151-72. Baton Rouge: Clai- competition during host plant selection tor by insect pests on cruciferous crops. In 38. Deleted in proof Insects--Plants, ed. V Labeyrie, G 39. Denno RF, Douglass LW, Jacobs D. Fabres0 D Lachaise, pp. 85-90. Dor- 1985. Crowdingand host plant nutrition: drecht, The Netherlands: W. Junk environmental determinants of wing- 53. Finch S, Jones TH. 1989. An analysis form in Prokelisia marginata. Ecology of the deterrent effect of aphids on 66:1588-96 cabbage root fly (Delia radicum) egg- 40. Denno RF, Olmstead KL, McCloudES. laying. Ecol. Entomol. 14:387-91 1989, Reproductivecost of flight capa- 54. Fitt GP. 1984. Ovipositi0n behavior of bility: a comparisonof life history traits two tephritid fruit flies, Dacustryoni in wing dimorphic planthoppers. Ecol. and Dacusjarvisi, as influenced by the Entomol. 14:31-44 presence of larvae in the host fruit. 41. Denno RF, Roderick GK. 1992. Den- Oecologia 62:37-46 sity-related dispersal in planthoppers: 55. FlammRO, Wagner TL, Cook SP, Pul- effects of interspecific crowding. Ecol- ley PE, Coulson RN, McArdle TM. ogy 73:1323-34 1987. Host colonization by cohabiting 42. Drbel HG, Denno RF. 1993. Preda- Dendroctonusfrontalis, lps avulsus, and tor-planthopper interactions. In Plan- I. calligraphus (Coleoptera: Scolytidae). thoppers: Their Ecology and Man- Environ. Entomol. 16:390-99 agement, ed. RF Denno, JT Perfect~ 56. Forrest JMS. 1971. The growth of Aphis pp. 325-99, NewYork: Chapman and fabae as an indicator of the nutritional Hall advantage of galling to the apple aphid 43. Edson JL. 1985. The influences of pre- Dysaphis devecta. Entomol. Exp. AppL dation and resource subdivision on the 14:447-83 coexistence of goldenrod aphids. Ecol- 57. Fowler SV, MacGarvin M. 1986. The ogy 66:1736-43 effects of leaf damageon the perform- by University of Minnesota- Law Library on 09/17/06. For personal use only. 44. Evans EW.1989. Interspecific interac- ance of insect herbivores on birch, tions among phytophagous insects of Betula pubescens. J. Anim. Ecol. 55: Annu. Rev. Entomol. 1995.40:297-331. Downloaded from arjournals.annualreviews.org tallgrass prairie: an experimental test. 565-73 Ecology 70:435-44 58. Freeman DH. 1987. Applied Categori- 45. Evans EW.1992. Absence of interspe- cal Data Analysis. NewYork: Marcel cific competition amongtallgrass prairie Decker grasshoppers during a drought. Ecology 59. Deleted in proof 73:1038~J,4 60. Fritz RS. 1990. Variable competition 46. Faeth S. 1985. Host leaf selection by betweeninsect herbivores on genetically leaf miners: interactions amongthree variable host plants. Ecology71:20008- trophic levels. Ecology 66:870-75 11 47. Faeth S. 1986. Indirect interactions be- 61. Fritz RS, Gaud WS, Sacchi CF, Price tween temporally separated herbivores PW.1987. Patterns of intra- and inter- mediated by the host plant. Ecology specific association of gall-forming 67:479-94 sawflies in relation to shoot size on 48. Faeth S. 1987. Communitystructure and their willow host plant. Oecologia folivorous insect outbreaks: the role of 73:159-69 vertical and horizontal interactions. In 62. Fritz RS, Price PW. 1990. A field test htsect Outbreaks, ed. P Barbosa, JC of interspecific competition on oviposi- Annual Reviews www.annualreviews.org/aronline

COMPETITION IN PHYTOPHAGOUS INSECTS 327

tion of gall-forming sawflies on willow. biological control. Environ. Entomol. Ecology 71:99-106 20:1217-27 63. Fritz RS, Sacchi CF, Pdce PW. 1986. 74. Hairston NG, Smith FE, Slobodkin LB. Competition versus host plant pheno- 1960. Communitystructure, population type in species composition: willow control, and competition. Am. Nat. sawflies. Ecology 67:1608-18 44:421-25 64. Fujii K. 1967. Studies on the interspe- 75. Hanhim~ikiS. 1989. Induced resistance cies competition between the azuki bean in mountainbirch: defence against leaf- weevil, Callosobruchus chinensis, and chewinginsect guild and herbivore com- the southern cowpea weevil, C. macu- petition. Oecologia 81:242-48 latus. II. Competition under different 76. Harris P. 1980. Establishment of Uro- environmental conditions. Res. Popul. phora affinis Frfld. and U. quadrifas- Ecol. 9:192-200 ciata (Meig.) (Diptera: Tephritidae) 65. Fujii K. 1969. Studies on the interspe- Canada for the biological control of cies competition between the azuki bean diffuse and spotted knapweed. Zeit. weevil and the southern cowpeaweevil. Angew. Entomol. 89:504-14 IV. Competition between strains. Res. 77. Harrison JO. 1964. Factors affecting the Pop. EcoL 11:84-91 abundance of lepidoptera in banana 66. Fujii K. 1970. Studies on the interspe- plantations. Ecology 45:508-19 cies competition betweenthe azuki bean 78. Harrison S, Karban R. 1986. Effects of weevil, Callosobruchus chinensis, and an early-season folivorous moth on the the southern cowpea weevil, C. macu- success of a later-season species, medi- latus. V. The role of adult behavior in ated by a change in the quality of the competition. Res. Pop. Ecol. 12:233-42 shared host, Lupinus arboreus Sims. 66a. Fujii K, Gatehouse AMR,Johnson CD, Oecologia 69:354-59 Mitchell R, Yoshida T, eds. 1990. 79. Hartley SE, Lawton JH. 1987. Effects Bruchids and Legumes: Economics, of different types of damage on the Ecology and Coevolution. Boston, MA: chemistry of birch foliage, and the re- Kluwer Academic sponses of birch feeding insects. Oe- 67. Gange AC, Brown VK. 1989. Effects cologia 74:432-37 of root herbivory by an insect on a 80. Hastings A. 1987. Can competition be foliar-feeding species, mediatedthrough detected using species co-occurrence changes in the host plant. Oecologia81: data? Ecology 68:117-23 38-42 81. Haukioja E, Niemel~i P. 1979. Birch 68. Gibson CWD.1976. The importance of leaves as a resource for herbivores: sea- food plants for the distribution and abun- sonal occurrence of increased resistance dance of some Stenodemini (Heterop- in foliage after mechanical damage of tera: Miridae) of limestone grassland. adjacent leaves. Oecologia 39:151-59 Oecologia 25:55-76 82. Hendi A. 1975. Untersuchungen iiber 69. Gibson CWD.1980. Niche use patterns intra- und interspezifische Konkurrenz among some Stenodemini (Heteroptera: bei vier Blattlausarten an Vicia faba. Miridae) of limestone grassland, and an PhDdissertation. Justus Liebig-Univer- investigation of the possibility of inter- sit,it Giessen, Germany.62 pp. specific competition between Notostira 83. Holt RD.1984. Spatial heterogeneity, by University of Minnesota- Law Library on 09/17/06. For personal use only. elongata Geoffroy and Megaloceraea indirect interactions, and the coexistence recticornis Geoffroy. Oecologia 47: of prey species. Am. Nat. 124:377-406 Annu. Rev. Entomol. 1995.40:297-331. Downloaded from arjournals.annualreviews.org 352-64 84. Huffaker CB, Kennett CE. 1969. Some 70. Gibson CWD,Visser M. 1982. Inter- aspects of assessing efficiency of natural specific competition between two field enemies. Can. Entomol. 101:425-47 populations of grass-feeding bugs. Ecol. 85. Hunter CE, Yeargan KV. 1989. Devel- Entomol. 7:61-67 opment, reproduction, and competitive 71. Giga DP, Smith RH. 1985. Oviposition interactions betweentwo sympatric leaf- markers in Callosobruchus maculatus hopper species (Homoptera: Cicadelli- F. and Callosobruchus rhodesianus Pic. dae) on redbud trees. Environ. Entomol. (Coleoptera, Bruchidae): asymmetry 18:127-32 interspecific responses. Agric. Ecosyst. 86. Hunter MD.1990. Differential suscep- Environ. 12:229-33 tibility to variable plant phenologyand 72. Greathead DJ. 1986, Parasitoids in clas- its role in competition betweentwo in- sical biological control. In Insect Parasi- sect herbivores on oak. Ecol. Entomol. toids, ed. J Waage, D Greathead, pp. 15:401-8 289-318. London: Academic 87. Hunter MD, Willmer PG. 1989. The 73. Gross P. 1991. Influence of target pest potential for interspecific competition feeding on success rates in classical between two abundant defoliators on Annual Reviews www.annualreviews.org/aronline

328 DENNO, McCLURE & OTT

oak: leaf damage and habitat quality. of bracken herbivores at sites on two Ecol. Entoraol. 14:267-77 continents. J. Anita. Ecol. 51:573-95 88. It6 Y. 1960. Ecological studies on popu- 103. Lawton JH. 1984. Non-competitive lation increase and habitat segregation populations, non-convergent communi- amongbarley aphids. Bull, Natl. Inst. ties, and vacant niches: the herbivores Agric. Sci. Set. C 11:45-130 of bracken. See Ref. 174a, pp. 67-100 89. Jermy T. 1985. Is there interspecific 104. Lawton JH. 1984. Herbivore community competition between phytophagous in- organization: general models and spe- sects? Z. Zool. Syst. Evolutionsforsch. cific tests with phytophagousinsects. In 23:275-85 A New Ecology--Novel Approaches to 90. Joern A. 1986. Experimental study of Interactive Systems, ed. PWPrice, CN avian predation on coexisting grasshop- Slobodchikoff, WSGaud, pp. 329-52. per populations (Orthoptera: Acrididae) NewYork: John Wiley in a sandhills grassland. Oikos 46:243- 105. Lawton JH, Hassell MP. 1981. Asym- 49 metrical competition in insects. Nature 91. Jones TH, Cole RA, Finch S. 1988. A 289:793-95 cabbage root fly oviposition deterrent 106. LawtonJH, Hassell MP. 1984. Interspe- in the frass of garden pebble mothcat- cific competitionin insects. In Ecologi- erpillars. Entomol. Exp. Appl. 49:277- cal Entomology, ed. CB Huffaker, RL 82 Rabb, pp. 451-95. New York: John 92. Karban R. 1986. Interspecific competi- Wiley tion betweenfolivorous insects on Erig- 107. Lawton JH, Strong DR. 1981. Commu- eron glaucus. Ecology 67:1063-72 nity patterns and competitionin folivor- 93. KarbanR. 1987. Effects of clonal various insects. Am. Nat. 118:317-38 ation of the host plant, interspecific 108. Le Quesne WJ. 1977. Studies on the competition, and climate on the popu- coexistence of three species of Eupteryx lation size of a folivorous thrips. Oe- (Hemiptera, Cicadellidae) on nettle. cologia 74:298-303 Entomol. Ser. A 47:37-44 94. Karban R. 1989. Communityorganiza- 109. Light DM,Birch MC.1982. Bark beetle tion of Erigeron glaucus folivores: ef- enantiomeric chemoreception: greater fects of competition, predation, and host sensitivity to allomone than pheromone. plant. Ecology 70:1028-39 Naturwissenschaften 69:243-45 95. Karban R, Myers JH. 1989. Induced 110. Light DM, Birch MC, Paine TD. 1983. plant responses to herbivory. Annu. Rev. Laboratory study of intraspecific and Ecol. Syst. 20:331-48 interspecifie competition within and be- 96. Kareiva P. 1982. Exclusion experiments tween two sympatric bark beetle spe- and the competitive release of insects cies, lps pini and L paraconfusus. Z. feeding on collards. Ecology 63:696- Angew. Entomol. 96:233-41 704 111. Masters GJ, Brown VK. 1992. Plant- 97. Keiser I, Kobayashi RM,Miyashita DH, mediated interactions between two spa- Harris EJ, Schneider EL, ChambersDL. tially separated insects. Funct. Ecol. 6: 1974. Suppression of Mediterranean 175-79 fruit flies by Oriental fruit flies in mixed 112. Mattson WJ. 1986. Competition for food infestations in guava. J. Econ. Entomol. between two principle cone insects of by University of Minnesota- Law Library on 09/17/06. For personal use only. 67:355-60 redtomol. pine, 15:88-92 Pinus resinosa. Environ. En- 98. Kidd NAC, Lewis GB, Howell CA. Annu. Rev. Entomol. 1995.40:297-331. Downloaded from arjournals.annualreviews.org 1985. An association between two spe- 113. Mattson WJ, Haack RA, Lawrence RK, cies of pine aphid, Schizolachnus pineti Herms DA. 1989. Do balsam aphids and Eulachnus agilis. Ecol. Entomol. (Homoptera:Aphididae) lower tree sus- 10:427-32 ceptibility to spruce budworm?Can. 99. Klijnstra JW. 1985. Interspecific egg Entomol. 121:93-103 load assessment of host plants by Pieris 114. McClure MS. 1980. Competition be- rapae butterflies. Entomol. Exp. AppL tween exotic species: scale insects on 38:227-31 hemlock. Ecology 61:1391-1401 100. Lamb RJ, MacKayPA. 1987. Acyrtho- 115. McClure MS. 1981. Effects of volt- siphon kondoi influences alata produc- inism, interspeciflc competition and tion by the pea aphid, A. pisum. parasitism on the population dynamics Entomol. Exp. Appl. 45:195-98 of the hemlockscales, Fiorinia externa 101. Larsson S. 1989. Stressful times for the and Tsugaspidiotus tsugae (Homoptera: plant stress-insect performancehypothe- Diaspididae). EcoL Entomol. 6:47-54 sis. Oikos 56:277-83 116. McClure MS. 1982. Distribution and 102. Lawton JH. 1982. Vacant niches and damage of two Pineus species (Homop- unsaturated communities: a comparison tera: Adelgidae) on red pine in New Annual Reviews www.annualreviews.org/aronline

COMPETITION IN PHYTOPHAGOUS INSECTS 329

England. Ann. Entomol. Soc. Am. 75: ing by three species of hemipteran her- 150-57 bivores on the basis of host plant den- 117. McClure MS. 1984, Influence of co- sity, Oecologia 48:414-17 habitation and resinosis on site selection 129. MeLain DK, Shure DJ. 1987. Pseudo- and survival of Pineus boerneri Annand competition: interspecifie displacement and P. coloradensis (Gillette) (Homop- of insect species through misdirected tera: Adelgidae) on red pine. Environ. courtship. Oikos 49:291-96 Entomol. 13:657--63 130. Messenger PS. 1975. Parasites, preda- 118. McClure MS. 1985. Patterns of abun- tors and population dynamics. In In- dance, survivorship, and fecundity of sects, Science and Society, ed. D Nuculaspis tsugae (Homoptera: Di- Pimintel, pp. 201-23. NewYork: Aca- aspididae) on Tsuga species in Japan in demic relation to elevation. Environ. Entomol. 131. Miller MC. 1985. The effect of Mono. 14:413-15 chamustitillator (F.) (Col., Cerambyci- 119. McClure MS. 1986. Population dynam- dae) foraging on the emergence of lps ics of Japanese hemlock scales: a com- calligraphus (Germ.) (Col., Scolytidae) parison of endemic and exotic insect associates. Z. Angew. Entomol. communities. Ecology 67:1411-21 100:189-97 120. McClure MS. 1986. Role of predators 132. Miller MC.1986. Within.tree effects of in regulation of endemicpopulations of bark beetle insect associates on the Matsucoccus matsumurae (Homoptera: emergenceof lps calligraphus (Coleop- Margarodidae)in Japan. Environ. Ento- tera: Scolytidae). Environ. Entomol. tool. 15:976-83 15:1104-8 121. MeClure MS. 1987. Potential of the 133. Miller RS. 1967. Pattern and process in Asian predator Harmoniaaxyridis Pal- competition. Adv. Ecol. Res. 4:1-74 las (Coleoptera: Coccinellidae) to con- 134. Mopper S, Whitham TJ, Price PW. trol Matsucoccus resinosae Bean and 1990. Plant phenotypeand interspecific Godwin (Homoptera: Margarodidae) competition between insects determine the United States. Environ. Entomol. sawfly performance and density. Ecol- 16:224-30 ogy 71:2135-44 122. McClure MS. 1988. The armored scales 135. Moran NA, Whitham TG. 1990. Inter- of hemlock. In Dynamicsof Forest In- specific competition betweenroot-feed- sect Populations, ed. AABerryman, pp. ing and leaf-galling aphids mediated by 45-65. New York: Plenum host-plant resistance. Ecology71:1050- 123. McClureMS. 1989. Biology, population 58 trends, and damage of Pineus boerneri 136. NeuvonenS, Hanhim~iki S, Suomela J, and P. coloradensis (Homoptera: Adel- Haukioja E. 1988. Early season damage gidae on red pine. Environ. Entomol. to birch foliage affects the performance 18:1066-73 of a late season herbivore. J. Appl. 124. McClure MS. 1990. Cohabitation and Entomol. 105:182-89 host species effects on the population 137. Niemelii P, TuomiJ, Mannila R, Ojala growth of Matsucoccus resinosae (Hoo P. 1984. The effect of previous damage moptera: Margarodidae) and Pineus bo- on the quality of Scots pine foliage as erneri (Homoptera: Adelgidae) on red food for Diprionid sawflies. Z. Angew. by University of Minnesota- Law Library on 09/17/06. For personal use only. pine. Environ. Entomol. 19:672-76 Entomol. 98:33-43 125. MeClure MS. 1991. Adelgid and scale 138. Paine TD, Birch MC, Svihra P. 1981. Annu. Rev. Entomol. 1995.40:297-331. Downloaded from arjournals.annualreviews.org insect guilds on hemlock and pine. In Niche breadth and resource partitioning Forest Insect Guilds: Patterns of lnter- by four sympatricspecies of bark beetles action with Host Trees. Gen. Tech. Re- (Coleoptera: Scolytidae). Oecologia port NE-153, ed. YN Baranchikov, WJ 48:1-6 Mattson FP Hain, TL Payne, pp. 256- 139. Pettersson MW.1992. Taking a chance 70. Broomall, PA: USDept. Agrie. For. on moths: oviposition by Delia flavi- Serv. Northeast For. Exp. Stn. frons (Diptera: Anthomyiidae) on the 126. McClure MS, Price P,W, 1975. Com- flowers of bladder campion,Silene vul- petition among sympatdc Erythroneura garis (Caryophyllaceae). Ecol. Entomol. leafhoppers (Homoptera: Cicadellidae) 17:57-62 on American sycamore. Ecology 56: 140. Price PW, Westoby M, Rice B, Atsatt 1388-97 PA, Fritz RS, et al. 1986. Parasitic 127. McClure MS, Price PW. 1976. Ecotope mediation in ecological interactions. characteristics of coexisting Eurythro- Annu. Rev. Ecol. Syst. 17:487-505 neura leafhoppers (Homoptera: Cicadel- 141. Qureshi ZA, Hussain T, Siddiqui QH. lidae) on sycamore. Ecology 57:928-40 1987. Interspecific competition of 128. McLainDK. 1981. Resource partition- Dacuscurcurbitae Coq. and Dacuscili- Annual Reviews www.annualreviews.org/aronline

330 DENNO, McCLURE & OTT

atus Loewin mixed infestation of cur- 158. Settle WH,Wilson LT. 1990. Invasion curbits. J. Appl. Entomol. 104:429-32 by the variegated leafhopper and biotic 142. Rankin LJ, Borden JH. 1991. Competi- interactions: parasitism, competition, tive interactions between the mountain and apparent competition. Ecology 71: pine beetle and the pine engraver in 1461-70 lodgepole pine. Can. J. Forest Res. 21: 159. Shearer JW. 1976. Effect of aggrega- 1029-36 tions of aphids (Periphyllus spp.) on 143. Rathcke BJ. 1976. Competition and co- their size. Entomol. Exp. Appl. 20:179- existence within a guild of herbivorous 82 insects. Ecology 57:76-87 160. Shorrocks B, Atkinson W, Chadesworth 144. Raupp MJ, Milan FR, Barbosa P, Leo- P. 1979. Competition on a divided and hardt BA. 1986. Methylcyclopentanoid ephemeral resource. J. Anlra. Ecol. monoterpenes mediate interactions 48:899-908 amonginsect herbivores. Science 232: 161. Shorrocks B, Rosewell J, Edwards K. 1408-10 1984. Interspecific competition is not a 145. Ritchie ME, Tilman D. 1992. Interspe- major organizing force in manyinsect cific competition among grasshoppers communities. Nature 310:310-12 and their effect on plant abundancein 162. Smiley JT, Atsatt PR, Pierce NE. 1988. experimental field environments. Oe- Local distribution of the lycaenid but- cologia 89:524-32 terfly, Jalmenus evagorus in response 146. Roitberg BD, Myers JH, Fraser BD. to host ants and plants. Oecologia 1979. The influence of predators on 76:416-22 the movementof apterous pea aphids 163. Stamp NE. 1984. Effect of defoliation between plants. J. Anim. Ecol. 48:111- by checkerspot caterpillars (Euphydryas 22 phaeton) and sawfly larvae (Macrophya 147. Ross HH. 1957. Principles of natural nigra and Tenthredo grandis) on their coexistence indicated by leafhopper host plants (Chelone spp.). Oecologia populations. Evolution 11:113-29 63:275-80 148. Rothschild GHL.1971. The biology and 164. Stamp NE. 1987. Availability of re- ecology of rice-stem borers in Sarawak sources for predators of Chelone seeds (Malaysian Borneo). J. Appl. Ecol. and their parasitoids. Am. Midl. Nat. 8:287-322 117:265-79 149. SAS. 1990. SAS/STAT User’s Guide. 165. Stiling PD. 1980. Competition and co- Cary, NC: SASInst. existence among Eupteryx leafhoppers 150. Schluter D. 1984. A variance test for (Hemiptera: Cicadellidae) occurring detecting some species associations, stinging nettles ( Urtica dioica). J. Anita. with some example applications. Ecol- Ecol. 49:793-805 ogy 65:998-1005 166. Stiling PD, Strong DR. 1983. Weak 151. Schoener TW.1974. Resource partition- competition among Spartina stem boring in ecological communities. Science ers, by means of murder. Ecology. 64: 185:27-39 770-78 152. Schoener TW. 1982. The controversy 167. Stiling PD, Strong DR. 1984. Experi- over interspecific competition. Am. Sci. mental density manipulation of stem- 70:586-95 boring insects: some evidence for by University of Minnesota- Law Library on 09/17/06. For personal use only. 153. Schoener TW. 1983. Field experiments interspecific competition. Ecology 65: on interspecific competition. Am. Nat. 1683-85 Annu. Rev. Entomol. 1995.40:297-331. Downloaded from arjournals.annualreviews.org 122:240-85 168. Story JM, Boggs KW,Good WR, Harris 154. Schoener TW. 1988. Ecological inter- P, Nowierski RM.1991. Metzneria pau- actions. In Analytical Biogeography,ed. cipunctella Zeller (Lepidoptera: Gele- AAMyers, PS Giller, pp. 255-97. New chiidae), a moth introduced against York: Chapman and Hall spotted knapweed:its feeding strategy 155. Seifert RP. 1982. Neotropical Heliconia and impact on two introduced Urophora insect communities. Q. Rev. Biol. 57:1- spp. (Diptera: Tephritidae). Can. Ento- 28 moL 123:1001-7 156. Seifert RP, Seifert FH. 1976. A com- 169. Strauss SY. 1988. The Chrysomelidae: munity matrix analysis of Heliconia A useful group for investigating herbi- insect communities. Am. Nat. 110:461- vore-herbivore interactions. In Biology 83 of Chrysomelidae, ed. P Jolivet, E Pe- 157. Seifert RP, Seifert FH.1979. Utilization titpierre, THHsiao, pp. 91-105. Boston: of Heliconia (Musaceae) by the beetle Kluwer Academic Xenarescus monocerus (Chrysomelidae: 170. Strong DR. 1981. The possibility of Hispinae) in a Venezuelan forest. Bio- insect communities without competi- tropica 11:51-59 tion: hispine beetles on Heliconia. In Annual Reviews www.annualreviews.org/aronline

COMPETITION IN PHYTOPHAGOUS INSECTS 331

Insect Life History Patterns: Habitat hill rangeland in northeastern Colorado. and Geographic Variation, ed. RF Oecologia 8:276-95 Denno, H Dingle, pp. 183-94. New 180. Valle RR, Kuno E, Nakasuji F. 1989. York: Spfinger-Verlag Competition between laboratory popu- 171. Strong DR. 1982. Harmonious coexis- lations of green leafhoppers, Nephotettlx tence of hispine beetles on Heliconia in spp. (Homoptera: Cieadellidae). Res. experimental and natural communities. Pop. Ecol. 31:53-72 Ecology 63:1039-49 181. Vehrs SLC, Walker GP, Patrella MP. 172. Strong DR.1982. Potential interspecific 1992. Comparisonof population growth competitionand host specificity: hispine rate and within-plant distribution be- beeries on Heliconia. Ecol. Entomol. tween Aphis gossypii and Myzus persi- 7:217-20 cae (Homoptera: Aphididae) reared 173. Strong DR. 1984. Exorcising the ghost potted chrysanthemums.J. Econ. Ento- of competition past: phytophagous in- mol. 85:799-807 sects. See Ref. 174a, pp. 28-41 182. Wagner TL, Flamm RO, Coulson RN. 174. Strong DR, Lawton JH, Southwood 1985. Strategies for cohabitation among TRE. 1984. Insects on Plants. Cam- the southern pine bark beetle species: bridge, MA:Harvard Univ. Press. 313 comparisons of life-process biologies. PP. In Proc. Integrated Pest Management 174a. Strong DR, Simbedoff D, Abele LG, Research Symposium, Gen. Tech. Rep., Thistle AB,eds. 1984. Ecological Com- pp. 87-101. Raleigh, NC: South. For. munities. Princeton, N J: Princeton Univ. Exp. Stn. Press 183. Waloff N. 1968. Studies on the insect 175~ Tamaki G, Allen WW.1969. Competi- fauna on Scotch broom Sarothamnus tion and other factors influencing the scoparius (L.) Wimmer.Adv. Ecol. Res, population dynamics of Aphis gossypii 5:87-209 and Macrosiphoniella sanborni on 184. Waloff N. 1979. Partitioning of re- greenhouse chrysanthemums. Hilgardia sources by grassland leaf hoppers 39:447-505 (Auehenorrhyncha, Homoptera). Ecol. 176. Taper ML. 1990. Experimental charac- EntomoL 4:379-85 ter displacementin the adzuki bean wee- 185. West C. 1985. Factors underlying the vil, Callosobruchuschinensis. See Ref. late seasonal appearanceof the lepidop- 66a, pp. 289-301 terous leaf-mining guild on oak. Ecol. 177. Toquenaga Y. 1990. The mechanisms Entomol. 10:111-20 of contest and scramble competition in 186. Williams KS, Myers JH. 1984. Previous bruchid species. See Ref. 66a, pp. 341- herbivore attack of red alder may im- 49 prove food quality for fall webworm 178. Toquenaga Y, Fujii K. 1990. Contest larvae. Oecologia 63:166-70 and scramble competition in 187. Wise DH. 1981. A removal experiment bruchid species, Callosobruchus analis with darkling ground beetles: lack of and C. phaseoli (Coleoptera: Bruchi- evidence for interspecific competition. dae). I. Larval competition curves and Ecology 62:727-38 interference mechanisms. Res. Popul. 188. Zw61fer H. 1979. Strategies and coun- Ecol. 32:349~i3 terstrategies for space and food in flower by University of Minnesota- Law Library on 09/17/06. For personal use only. 179. Uekert DN, Hansen RM. 1971. Di- heads and plant galls. Fortschr. Zool. etary overlap of grasshoppers on sand- 25:331-53 Annu. Rev. Entomol. 1995.40:297-331. Downloaded from arjournals.annualreviews.org Annu. Rev. Entomol. 1995.40:297-331. Downloaded from arjournals.annualreviews.org by University of Minnesota- Law Library on 09/17/06. For personal use only. Annu. Rev. Entomol. 1995.40:297-331. Downloaded from arjournals.annualreviews.org by University of Minnesota- Law Library on 09/17/06. For personal use only.