hyperparasitism: multitrophic ecology and behavior · p1: ars/spd p2: ars/ary qc: ars november 4,...

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November 4, 1998 12:39 Annual Reviews AR074-12

Annu. Rev. Entomol. 1999. 44:291–315Copyright c© 1999 by Annual Reviews. All rights reserved

HYPERPARASITISM: MultitrophicEcology and Behavior

Daniel J. SullivanDepartment of Biological Sciences, Fordham University, Bronx, New York 10458;e-mail: [email protected]

Wolfgang VolklDepartment of Animal Ecology, University of Bayreuth, 95440 Bayreuth, Germany;e-mail: [email protected]

KEY WORDS: biological control, facultative, heteronomous, habitat specificity, sex ratio,foraging behavior

ABSTRACT

Hyperparasitoids are secondary insect parasitoids that develop at the expenseof a primary parasitoid, thereby representing a highly evolved fourth trophiclevel. This review evaluates multitrophic relationships and hyperparasitoid ecol-ogy. First, hyperparasitoid communities of various taxa of phytophagous andpredacious insects are described. Second, specific patterns of hyperparasitoidcommunity organization and hyperparasitoid ecology are described in detail, us-ing the aphid-parasitoid–hyperparasitoid food web as a model system. Aphidhyperparasitoid communities consist of ecto- and endohyperparasitoids, with ec-tohyperparasitoids being less host specific than endohyperparasitoids. Lifetimefecundity and intrinsic rate of increase of hyperparasitoids are generally lowerthan those of their primary hosts. Aphid ectohyperparasitoids search randomly forhosts and do not use specific cues, whereas endohyperparasitoids gain informationthat originates from host plants or hosts for long-range search. Interactions withadult primary parasitoids do not influence hyperparasitoid searches, but aphid-attending ants typically prevent successful hyperparasitoid foraging. Impact ofhyperparasitism on biological control is reviewed.

2910066-4170/99/0101-0291$08.00

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292 SULLIVAN & V OLKL

PERSPECTIVES AND OVERVIEW

Multitrophic ecology and the related behavior of the phytophagous and ento-mophagous insects interacting as a food-web “community” was pioneered byAskew & Shaw (4, 5). Many ecologists such as Price et al (86) have continuedthis exciting research over more than 30 years. In emphasizing the “bottom-up”effects of hosts on their parasitoids, the first trophic level shows that both inter-and intraspecific plant variation can influence the ecology and behavior of thesecond trophic level of phytophagous insects, which, in turn, is one of the majordeterminants of the third trophic level of insect parasitoids (21). Insect “hyper-parasitism” can be defined as a highly evolved fourth trophic level relationshipthat exists between entomophagous insects. It refers to the development of asecondary insect parasitoid or hyperparasitoid at the expense of a primary insectparasitoid. The primary parasitoid attacks an insect host that is usually phy-tophagous, but which could also be a predator or scavenger. Hence, an insecthyperparasitoid attacks another insect that is or was developing in or on anotherinsect host, and this sometimes impacts on biological control of a pest insect.

Hyperparasitoids may have a considerable influence on the “top-down” con-trol of terrestrial herbivorous arthropod populations by parasitoids (90), andtheir action may have shaped the evolution of parasitoid foraging strategies(61, 118, 129). The structure of hyperparasitoid communities, representing thefourth trophic level, has been studied for a representative spectrum of phy-tophagous hosts (39, 41), and the degree of resource utilization in the field isknown for most systems of economic importance. In contrast, there is onlylimited knowledge of life-history parameters and of foraging behaviors of hy-perparasitoids. Both factors are of crucial importance for the understanding ofthe role of hyperparasitism in natural populations as well as in pest control (104).Information about hyperparasitoid life history may help in understanding basicinteractions and may give rough estimates about their general capability to influ-ence primary parasitoid populations (15a, 104). The analysis of hyperparasitoidforaging behavior may give us an idea of the factors that influence the hyperpar-asitoid’s foraging success and may thus contribute explanations for the levelsof hyperparasitism observed in the field. There are two multitrophic systemswith a well-studied hyperparasitoid ecology: (a) the heteronomous hyperpar-asitoids of the genusEncarsiaattacking scale insects and whiteflies (33) and(b) the aphid-parasitoid-hyperparasitoid community (104, 105, 120). In bothsystems, the involved phytophages are worldwide pests. Furthermore, they areeasy to keep in the laboratory, and the knowledge of hyperparasitoid ecology isof basic importance for the design of biological control programs. However, inheteronomous hyperparasitoids or adelphoparasitoids, only males develop ashyperparasitoids, attacking females of their own or another parasitoid species

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HYPERPARASITISM: ECOLOGY–BEHAVIOR 293

(33, 68, 82, 84, 104, 117, 134, 136). But aphid hyperparasitoids generallydevelop as obligate hyperparasitoids (104, 105). In this review, we first re-port on the structure of hyperparasitoid communities in various taxa of hostparasitoid systems and on levels of resource utilization. Concerning ecologyand behavior, we focus on obligate hyperparasitoids. We use the aphid hyper-parasitoid community as a model system to show typical patterns of selectedlife-history aspects and foraging strategies at the fourth trophic level.

TERMINOLOGY

“Obligate” hyperparasitoids are always secondary parasitoids: Their progenycan develop only in or on a primary parasitoid. A subcategory includes both“true” hyperparasitoids, which attack the primary parasitoid through the her-bivore, and “pseudohyperparasitoids,” which attack the primary parasitoid inthe cocoon stage after it has emerged from the host (39). “Facultative” hy-perparasitoids have progeny that can develop either as primary or as secondaryparasitoids. Endophagous hyperparasitoids have larvae that feed inside the host,whereas ectophagous species feed externally. Another feeding-related distinc-tion is between koinobionts, which allow their hosts to continue developmentafter oviposition, and idiobionts, which paralyze or kill their hosts in the processof oviposition (4, 29). “Direct” hyperparasitoids attack the primary parasitoiddirectly by ovipositing in or on it. “Indirect” hyperparasitoids attack the primaryparasitoid’s phytophagous host and thus only attack the parasitoid itself indi-rectly. In this case, the female hyperparasitoid oviposits into the phytophagoushost whether it is parasitized or not (31).

EVOLUTION

Hyperparasitism has evolved in only three insect orders: Hymenoptera (17families) and perhaps in a few species of Diptera and Coleoptera (33). OnlyHymenoptera are treated here.

Evolution of Hyperparasitism in HymenopteraPRIMARY PARASITISM The recent review by Whitfield (131) suggested thatparasitism arose once, in the common ancestor of the Orussoidea (parasiticwood wasps) and the monophyletic Apocrita (narrow-waisted wasps). The ori-gin of the Apocrita, and therefore parasitism in the Hymenoptera, dates to theJurassic period, about 135 million years ago (88). This precursor specializedin larval feeding within tunnels in wood and at least partly upon fungi (intro-duced and/or promoted by secretions from the adult female wasp at the time ofoviposition). Ectoparasitism probably evolved before endoparasitism, with the

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parasitoid egg deposited near or perhaps on the host rather than in it. Hence,these ectoparasitoids usually attacked concealed hosts, often within galleriesin wood or plant galls. The use of venom apparently developed very early andproduced physiological changes in the host. While the venom of the more an-cestral ectoparasitoids resulted in idiobiosis (permanent paralysis or death), thevenom of the more specialized endoparasitoids tended toward koinobiosis (tem-porary or nonlethal paralysis). However, it is not clear whether endoparasitismpreceded koinobiosis or vice versa (33). Of related interest is the evolutionof teratocytes or “giant cells” with nutritive and secretory functions that some-times cause pathologies, then viruses and virus-like particles that can overcomeimmune responses, and finally polyembryony, in which many embryos developfrom a single egg.

HYPERPARASITISM According to Godfray (33), “facultative” hyperparasitismperhaps evolved from ectoparasitism because no special adaptations are neededto oviposit and feed on a primary parasitoid as well as the primary’s host.“Obligate” hyperparasitism has a wide taxonomic distribution and could haveevolved in at least two ways: (a) via facultative hyperparasitism as an oppor-tunistic trade-off to utilize primary or secondary hosts, and/or if the hyper-parasitic species frequently encounters already parasitized hosts; or (b) by ahost shift from a primary parasitoid of one host to a secondary parasitoid ofanother species. This host transfer is facilitated if the old primary and newsecondary hosts share physiological and/or ecological attributes. Finally, somehyperparasitoids are ectoparasitic whereas others are endoparasitic, and someare idiobionts whereas others are koinobionts (10).

NON-APHID HYPERPARASITISM

This section reviews hyperparasitism in insect hosts other than aphids and ispresented in descending order of literature citations by major taxa with selectedexamples of current research on more common multitrophic relationships andinteresting behaviors, with special reference to the impact of hyperparasitismon biological control.

LepidopteraGYPSY MOTH Lymantria dispar(Lymantriidae) is an exotic insect defoliatorof trees in North America, against which classical biological control has beenused over many years. It is attacked by a number of introduced hymenopterousprimary parasitoids, such asCotesia(=Apanteles) melanoscela(Braconidae),Brachymeria intermedia(Chalcididae), andOoencyrtus kuvanae(Encyrtidae).In the case ofC. melanoscela, their cocoons in turn are attacked by as manyas 16 indigenous hyperparasitoid species, sometimes resulting in an average of

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50–90% primary mortality, which can interfere with biological control (11, 24).A nondiapausing Asian strain decreases its exposure time and, hence, reducesits vulnerability to hyperparasitism (78, 132, 133). A tachinid fly,Ceranthiasamarensis(Diptera:Tachinidae), was imported into Canada from Europe andis the predominent parasitoid in low-density populations of gypsy moths whilesuffering 7–16% hyperparasitism (69).

LEAFMINERS Phyllonorycter crataegella(Gracillariidae) on pin cherry andPhyllonorycter propinquinellaon black cherry have parasitoid fauna similar tothat of apple leafminers (62). However, of the parasitoids that emerged fromthese leafminers, nine species were primary parasitoids, and seven were facul-tative hyperparasitoids. Both cherry leafminers are alternate hosts for parasitoidspecies that attack economically important apple leafminers, but obligate hy-perparasitoids do not seem to be important.

GREEN CLOVERWORM In the soybean canopy, the green cloverworm,Plathy-pena scabra(Noctuidae), is parasitized byCotesia marginiventris(Hymenop-tera: Braconidae), which is hyperparasitized byMesochorus discitergus(Hyme-noptera: Ichneumonidae). The hyperparasitoid must hang by its tarsi from theedge of the leaf from which the larva is suspended, and then it reels in thecaterpillar by pulling upward on the caterpillar’s silken thread. Hyperparasitoidpupation occurs within the cocoon spun by the primary parasitoid (137a).

CABBAGE BUTTERFLY Pieris rapae(Pieridae) is attacked by the gregariousparasitoid,Cotesia glomerata(Hymenoptera: Braconidae). Emergence of adulthyperparasitoids,Eurytomasp. (Hymenoptera: Eurytomidae), from the oldestcocoon clusters was found to be strongly male biased, while the sex ratio fromyoung cocoons was in favor of females (108).

SPRUCE BUDWORM An extensive study was done by Huber et al (48) on 28genera representing 10 families of at least 50 chalcidoid parasitoids and hy-perparasitoids recorded fromChoristoneura fumiferana(Tortricidae) and otherChoristoneuraspp. in New Brunswick, Canada. Primary parasitoids belongingto the Ichneumonidae, Braconidae, and Tachinidae were recorded from 10 ofthe 16 NearcticChoristoneuraspp., but chalcidoid hyperparasitoids were fromonly 4 of the 16 species.

STEM BORERS Tetrastichus howardi(Hymenoptera: Eulophidae) is a gregar-ious endoparasitoid introduced into South Africa as a biological control agentagainst stem borers.Chilo partellus (Pyralidae) andHelicoverpa armigera(Noctuidae) were preferred byT. howardiand so behaved as a polyphagousfacultative hyperparasitoid rather than as an obligate hyperparasitoid on theirprimary parasitoids. When one lepidopteran pupa was parasitized by a single

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T. howardi female, about 55 progeny emerged, of which 94% were females(70, 71).

EUCALYPTUS MOTH In South Australia,Uraba lugens(Noctuidae) on severalspecies of eucalyptus was attacked by 11 primary parasitoids and 10 hyperpar-asitoids (one of which was facultative). Of these hyperparasitoids, many weregregarious and polyphagous, and all but one species parasitized the pupae of theprimary parasitoids. Hyperparasitism and the presence of many polyphagousprimary parasitoids in the complex perhaps contributed to the low levels ofparasitism ofU. lugens(2).

TRIGONALYID WASPS Weinstein & Austin’s (127, 128) studies of the relation-ship of the enigmatic trigonalyid wasps (Hymenoptera: Trigonalyidae) withtheir hosts indicated that most species appear to oviposit on a wide variety ofplants. Their eggs are ingested in most cases by lepidopteran or sawfly larvae,and they then develop as obligatory hyperparasitoids in tachinid or ichneumonidprimary parasitoids or in vespid or eumenid wasp larvae. Vespidae are the mostcommonly recorded secondary hosts, perhaps via lepidopteran primary hostsprovisioned into nests.

TUFTED APPLE BUD MOTH Platynota idaeusalis(Tortricidae), a pest in appleorchards, has 41 primary parasitoids, withExochus atriceps(Hymenoptera:Ichneumonidae) as the most common. Only two hyperparasitoid species emer-ged with no major impact noted (9).

SCALE INSECTS AND WHITEFLIES Scale insects and whiteflies are phytopha-gous pests in the order Homoptera. They are often hosts in an unusual relation-ship of multitrophic ecology and behavior unique to the hymenopterous familyAphelinidae, which had been reviewed by Viggiani (116).

HETERONOMOUS HYPERPARASITISM Heteronomous hyperparasitism is alsocalled facultative autoparasitism and adelphoparasitism. Females develop nor-mally as primary endoparasitoids of Homoptera, whereas males develop hy-perparasitically in primary endoparasitoids, including their own conspecificfemales (68, 117, 134). Abnormal behavior or deviant male ontogeny is as-sociated with sex differentiation in the host relations of some species in suchgenera asAneristus, Coccophagus, Coccophagoides, Euxanthellus, Encarsia,Lounburyia, Physcus, andPrococcophagus. This highly evolved mode of de-velopment results in linkage with progeny sex ratio. Field sex ratios of het-eronomous hyperparasitoids can fluctuate dramatically depending on changesin the relative availability of male and female hosts (136).

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SCALE INSECTS Second instar scales ofFilippia geminaare the preferredhosts for the larvae of the female aphelinidCoccophagus atratus. Late larvalinstars and prepupae of the conspecificC. atratusare the preferred hosts ofmaleC. atratuslarvae. Variable population sex ratios observed inC. atratusapparently result from the behavior of individual females, in which brood sexratios are dependent on the relative availability of hosts for males and hosts forfemales (23).

When another aphelinid,Encarsia tricolor, was offered pupae ofEncarsiainaronor conspecific pupae,E. tricolor showed a distinct preference to exploitE. inaron for male production (134). In complexes of parasitoids containinga heteronomous hyperparasitoid and one or more conventional species, in themajority of cases, the heteronomous hyperparasitoid was the most important anddominant species. Hence, caution is necessary when using such parasitoids inclassical biological control programs (135). Three forms ofEncarsia perniciosiare recognized by Stouthamer & Luck (102) based on their mode of reproductionand host choice: a thelytokous form parasitizing California red scale,Aonidiellaaurantii, and both a thelytokous and an arrhenotokous form parasitizing SanJose scale,Quadraspidiotus perniciosus. The arrhenotokousE. perniciosiis aheteronomous hyperparasitoid, and it had been suggested that the arrhenotokousform would become thelytokous in one generation when cultured under constanttemperatures in the laboratory. However, this was not found to be the case in fourcultures under constant temperatures after 2, 3, 11, and 19 generations (102).

WHITEFLIES A tritrophic model of heteronomous hyperparasitism was usedin a cotton–whitefly-parasitoid system by Mills & Gutierrez (68). Male aphe-linid parasitoids develop at the expense of conspecific females or competingparasitoid species. The unresolved question is whether such heteronomoushyperparasitism is compatible with the goals of biological control. Three aphe-linid parasitoids were considered: (a) a typical primary parasitoid (where bothmales and females develop on whitefly hosts), (b) an obligate autoparasitoid(where males develop only on conspecific females), and (c) a facultative au-toparasitoid (where males develop on all other parasitoids including conspecificfemales). Results indicate that the combination of a primary parasitoid and anobligate autoparasitoid provides the greatest suppression of cumulative whiteflyabundance. In contrast, the addition of a facultative autoparasitoid disrupts thecontrol potential of the other parasitoids. Hence, the indiscriminate introductionof aphelinid parasitoids in biological control programs should be avoided whensome are facultative autoparasitoids.Encarsia formosa(Hymenoptera: Aphe-linidae) is a parasitoid used worldwide for the biological control of whiteflieson vegetables and ornamental plants grown in greenhouses (43). It is hyper-parasitized bySigniphora coquilletti, Encarsia pergandiella, andE. tricolor

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(6, 15, 137). Models suggest that the efficacy of biological control is reduced ifheteronomous hyperparasitoids (such asE. pergandiella, E. tricolor) are usedtogether with primary parasitoids such asE. formosa(69; see also 82, 84; seeAC Bellotti et al, this volume).

MealybugsCASSAVA MEALYBUG The history and success in Africa of a classical biolog-ical control program to protect cassava (Manihot esculenta) from the SouthAmerican mealybug (Phenacoccus manihoti) has been reviewed by Herren& Neuenschwander (42). The most effective of the primary parasitoids wasApoanagyrus(=Epidinocarsis) lopezi(Hymenoptera: Encyrtidae), which wasintroduced from Paraguay into Nigeria in 1981. Even some defensive behaviorby the cassava mealybug involving encapsulation and melanization of the wasp’seggs and larvae did not prevent biological control of this pest (106). At least10 indigenous hymenopterous hyperparasitoids adapted to this new exotic pri-mary in Africa: Chartocerus hyalipennis(Signiphoridae) andProchiloneurusinsolituswere the most common hyperparasitoids, followed byProchiloneurusaegyptiacus(Encyrtidae),Tetrastichussp. (Eulophidae), andMarietta leopar-dina (Aphelinidae) (1, 80). The rate of hyperparasitism varied considerably(20–90%). Yet, in spite of sometimes high hyperparasitism, no detrimental ef-fect on the control efficiency ofA. lopeziwas noticed (51, 79). Special field andlaboratory studies on the biology and impact ofChartocerusandProchiloneu-rus spp. confirmed that these hyperparasitoids did not significantly reduceA. lopezi’s success (34, 35).

MANGO MEALYBUG In the early 1980s, the mango mealybug,Rastrococcusinvadens, was accidentally introduced into Togo, causing serious damage onmango (Mangifera indica), citrus, other fruit, and even shade trees. As part ofa biological control program, a primary parasitoid was introduced from India,Gyranusoidea tebygi(Hymenoptera: Encyrtidae), and became established inTogo and most of West Africa (79). Although, at times, 50–60% ofG. tebygimortality was attributable to eight species of hyperparasitoids, this still did notseem to prevent successful control of the mango mealybug (65).

DIPTERA The recent review of Diptera as parasitoids by Feener & Brown (29)compared them with the Hymenoptera and pointed out that the Diptera usea wider array of hosts (22 orders across five phyla) than any other group ofparasitoids. In contrast, hosts of the more diverse parasitic Hymenoptera arerestricted to 19 orders, all within the single phylum Arthropoda. Most dipteranparasitoids are koinobionts and endoparasitoids. Superparasitism (ovpositionin a host already parasitized by a female of the same species) appears to be bothwidely distributed across dipteran species and common within populations, asreported in Conopidae, Phoridae, and Tachinidae.

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GALL-MAKERS Hawkins & Goeden (40), Hawkins & Sheehan (41), and Craig(21) have pointed out that multitrophic ecology and the related behavior ofthe phytophagous and entomophagous insect community are especially welldemonstrated with dipteran gall-makers. In Florida, Stiling & Rossi (101)studied the dipteran midgeAsphondylia borrichiae(Cecidomyiidae), whichinduces the formation of galls on three different plant species: sea oxeye daisy(Borrichia frutescens), marsh elder (Iva frutescens), and beach elder (Iva imbri-cata). The dipteran gall-maker is attacked by four main species of hymenopteranparasitoids. Two of these parasitoids,Torymus umbilicatus(Torymidae) andGaleopsomyia haemon(Eulophidae), are ectoparasitic and facultatively hy-perparasitic (Figure 1). They were the dominant species because the two otherparasitoids are primaries only and endoparasitic:Rileya cecidomyiae(Euryto-midae) andTenuipetiolus teredon(Eurytomidae). As endoparasitic primaries,they are available for attack by the two ectoparasitoids when behaving as facul-tative hyperparasitoids. However, gall size is also important in the further com-petition between these two ectoparasitic and facultative hyperparasitoids. One

Figure 1 Multitrophic ecology and behavior of the parasitoids and hyperparasitoids associatedwith the dipteran gall-makerAsphondylia borrichiae. Redrawn from Stiling & Rossi (101), withpermission from Oxford University Press.

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of these,G. haemon, displaces the other hyperparasitic species,T. umbilicatus,in small galls. ButT. umbilicatushas a much longer ovipositor thanG. haemon,enabling it to oviposit later as galls grow in size. As a result,T. umbilicatushasa competitive advantage in larger galls.

LEAFMINERS The dipteran honeysuckle leafminer,Chromatomyia suikasurae(Agromyzidae), in a natural forest in Kyoto, Japan, was found to have a com-plex of primary parasitoids, of which 3 were koinobiont (all larval-pupal soli-tary) and 22 idiobiont species (11 larval solitary, 9 pupal solitary, and 2 pupalgregarious). Although competition among these primaries contributed to lowemergence rates of parasitoids at high host densities, these primary parasitoidrates were also reduced at low host densities, probably by inter- and intraspecifichyperparasitism (54).

DROSOPHILIDAE A facultative hyperparasitoid,Pachycrepoideus vindemiae(Hymenoptera: Pteromalidae), attacks both as a primary parasitoid onDroso-phila melanogasterand as a hyperparasitoid on the primaryAsobara tabida(Hymenoptera: Braconidae) (85).

BOMBYLIIDAE Unlike most of the dipteran parasitoids, bombyliids are ec-toparasitoids. Hyperparasitism on dipteran parasitoids as hosts seems uncom-mon, but there are some records of hyperparasitism by bombyliid parasitoids(in genera of Anthracinae) on primary hosts (138). However, all bombyliidsrecorded as hyperparasitoids do not appear to have evolved in any close associa-tion with the primary host and are best termed “pseudohyperparasitoids”—withboth facultative and obligate hyperparasitic behaviors existing.

Wasps and BeesCYNIPID GALL-MAKERS The wasp pestDryocosmus kuriphilus(Hymenoptera:Cynipidae) induces galls in chestnut orchards in Japan. An imported parasitoid,Torymus(=Syntomaspis) sinensis(Hymenoptera: Torymidae), was released in1982 in Kumamoto Prefecture, but disappointingly, the population had not in-creased at the rate expected. As a result, the density of the host cynipid pesthas not yet decreased but instead continues to fluctuate at too high a level. Twofactors were suggested to have delayed the success of the introduced para-sitoid: the low female sex ratio and high mortality rate due to native facultativehyperparasitoids (75, 76).

LEAFCUTTER BEES The fly Physocephala vittata(Diptera: Conopidae) is apest of beneficial pollinating alfalfa leafcutter bees,Megachile rotundata(Hymenoptera: Megachilidae), in the former Yugoslavia. A hyperparasitoid,Habrocytus eonopidarum(Hymenoptera: Pteromalidae), emerged from pupae

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of P. vittata in the laboratory, indicating that biological control of this fly pestis a possibility (67).

SAWFLIES Sometimes sawflies’ primary parasitoids in Australia (127, 128)and in Eurasia (87) are in turn attacked by facultative hyperparasitoids.

PsyllidsPEAR PSYLLA Psylla pyri (Homoptera: Psyllidae) is the key pest in pearorchards in France and many European countries.Trechynites psyllae(Hy-menoptera: Encyrtidae) is the main primary parasitoid regulating the pest fromthe first generation. Hyperparasitism, essentially due toSyrphophagus mami-tus (Hymenoptera: Encyrtidae), appears later on another host species,Psyllapyrisuga, which acts as a relay species for primary parasitoids between thefirst and second generation ofP. pyri. Five other hyperparasitoids appear evenlater. Because hyperparasitism is not recorded on the first generation ofP. pyri,early release of primary parasitoids should be successful in reducing pestpopulations (3).

HAWTHORN PSYLLIDS Ant attendance on larval parasitism was studied inthree species of hawthorn psyllids (Cacopsylla peregtina, Cacopsylla mela-noneura, Cacopsylla crataegi). All three psyllid species had low parasitizationrates by two encyrtid primaries. However, the ant-attendedC. crataegiwasalmost exclusively parasitized by only one primary:Prionomitus mitratus. Thetwo other psyllid species that were not ant attended were attacked mainly byPrionomitus tiliaris. In addition, the dominant hyperparasitoid,Pachyneuronmuscarum(Hymenoptera: Pteromalidae), was most successful on the two psyl-lid species unattended by ants. Hence, the primary parasitoid benefited fromant attendance of its psyllid host,C. crataegi, since honeydew-collecting antsprovided it with protection from hyperparasitoids (81).

ColeopteraCOCCINELLID BEETLES The European ladybird beetle,Coccinella septem-punctata, was introduced into the eastern United States during the 1970s. Theliterature and recent North American collection records indicate that at least 16species of insects (ca 14 Hymenoptera from six families, and 2 Diptera fromtwo families) are now known as primary parasitoids and hyperparasitoids, suchasTetrastichusspp.,Pachyneuronspp., etc (91).

WEEVILS Two weevil stem borers (Curculionidae) onRumex crispusdifferedin their feeding position.Apion miniatuminhabited the lower 10% of the stem,while Apion violaceumoccurred all along the stem, thus exploiting distinctlydifferent feeding positions, partly owing to differences in time of oviposition.

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A. miniatumsuffered less parasitization thanA. violaceumbecause its feedingposition in basal, thick parts of the stem constitutes a refuge as the stem diameterincreases. Koinobiont endoparasitoids attack the weevils before they enter thestem (unlike idiobiont ectoparasitoids), and they benefit from the refuge itselfby avoiding hyperparasitism (32).

BRUCHID BEETLES Two species of beetles,Callosobruchus maculatusandBruchidius atrolineatus(Bruchidae), are attacked by two solitary primary ec-toparasitoids:Dinarmus basalis(Hymenoptera: Pteromalidae) andEupelmusvuilleti (Hymenoptera: Eupelmidae). In behavioral contrast toD. basalis,E. vuilleti concentrates ovipositions on hosts already parasitized by the formerand aggressively kills eggs and larvae ofD. basalisby thrusts of the ovipos-itor, resulting in ovicide and larvicide. However,E. vuilleti can also act as afacultative hyperparasitoid on older larvae ofD. basalis(110).

HYPERPARASITISM IN APHID PARASITOIDS

Primary aphid parasitoids are found in two families of Hymenoptera: the Aphi-diidae (=Braconidae: Aphidiinae) (all genera of this family) and the Aphe-linidae (genusAphelinusand related genera). They in turn are attacked by aspecies-rich community of hyperparasitoids (104, 105). The members of thiscommunity belong to different hymenopteran subfamilies [Cynipoidea (Al-loxystidae:Alloxysta, Phaenoglyphis, Lytoxysta), Ceraphronoidea (Megaspili-dae:Dendrocerus), and Chalcidoidea (Pteromalidae:Asaphes, Pachneuron,Coruna,Euneura; Encyrtidae:Syrphophagus= Aphidencyrtus)] (66, 104, 105,109) and represent various life-history strategies.Alloxysta, Lytoxysta, andPhaenogplyphisspp. develop as koinobiont endohyperparasitoids and para-sitize the primary parasitoid larva within the living aphid (37, 63, 64, 95, 96,104, 105).Syrphophagus(=Aphidencyrtus) aphidivorusdevelops also as akoinobiont endohyperparasitoid, but females display a dual oviposition behav-ior by attacking parasitoid larvae both within living aphids and also inside aphidmummies (53, 105).Dendrocerusspp. and all pteromalid species develop asidiobiont ectohyperparasitoids. Females attack parasitoid prepupae and pupaeinside the empty aphid cuticle, which is called an aphid mummy (8, 10, 16, 55,103, 104).

Reproductive PotentialThe few studies on life-table characteristics of aphid hyperparasitoids suggesta relatively low lifetime fecundity when compared with those of primary par-asitoid species. Singh & Srivastava (97) reported that females ofAlloxystapleuralis, a hyperparasitoid ofTrioxys indicusvia Aphis craccivora, laid on

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average 113 eggs, with a daily maximum of about 30 eggs.Dendrocerus car-penterifemales produced on average 75 offspring, with a daily maximum of 10eggs, withAphidius erviviaAcyrthosiphon pisumbeing the host (125). By con-trast, the fecundity ofAsaphesspecies seems to be somewhat higher.Asaphessuspensusfemales laid on average 432 eggs, with a maximum of 16 mum-mies per day when the host wasAphidius uzbekistanicusvia Sitobion avenae(19). Lifetime fecundity and longevity reported forAsaphes vulgarisvaried fordifferent host species. Estimates range from 51 offspring per female, a dailymaximum of 9 eggs, and an average longevity of 14 days [host:Lysiphlebuscarduivia Aphis fabae(61)] to 265 offspring per female, a daily maximum of10 mummies per day, and an average longevity of 47 days [host:A. uzbekistan-icusvia S. avenae(19)] and 1433 offspring per female, 20 mummies per day,and an average longevity of 46 days [host:Aphidius nigripesvia Macrosiphumeuphorbiae(13)].

Sex Ratio and Offspring Sex AllocationOffspring sex allocation and sex ratio variation was intensively studied forD. carpenteri. Mated females are able to produce “precise” sex ratios by ad-justing the sequence of male (=unfertilized) and female (=fertilized) eggs laidduring a single oviposition bout (18). In laboratory studies, the first egg to belaid was fertilized if the host was of high quality (= large mummies) but un-fertilized if the host was of low quality (=small mummies). The second eggusually had the opposite sex. Later ovipositions varied with host quality, withmore fertilized eggs being laid in high quality hosts (18). This pattern may ex-plain sexual size dimorphism. Although immatures of both sexes gain weightat the same rate, males ofD. carpenteriare generally smaller than females(60, 83). Thus, it should be advantageous forD. carpenterifemales to allocatemore female progeny in large hosts, which provide more resources for develop-ment. Female age had apparently no effect on sex allocation (125). The resultsof these laboratory studies are consistent with field collections, where the pro-portion of females depended also on host size, varying between approximately50% in smallA. pisummummies and 75% in largeA. pisummummies (59).

By contrast, there is only very little information about sex ratios in other aphidhyperparasitoids. Singh & Srivastava (98) reported forAlloxysta pleuralisa sexratio of approximately 60% females, which was independent of the number ofeggs laid. InAsaphes vulgaris, the proportion of male progeny increased withthe age of females (13). Across host species, the sex ratio ofA. vulgarisseemsto be a result of host size. Field studies revealed a female biased sex ratio inlarge host species, while there was an extreme male bias in small host species(Table 1), as has been reported for many other species of Hymenoptera.

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Table 1 Sex ratio (proportion of females) in field samples of the aphid ectohyperparasitoidAsaphes vulgariscollected near Bayreuth, Bavaria, Germanya

Primary parasitoids Aphid species Sex ratio(mummy size) (number mummies) Host plant (females)

SmallLysaphidus arvense Coloradoa tanacetina(89) Tanacetum vulgare 0.12Lysiphlebus cardui Aphis fabae(312) Cirsium arvense 0.14Trioxys angelicae Aphis fabae(122) Evonymus europaeus 0.19Lysiphlebus hirticornis Metopeurum fuscoviride(76) Tanacetum vulgare 0.22Trioxys falcatus Periphyllussp. (38) Acer campestre 0.26

MediumEuaphidius setiger Periphyllussp. (26) Acer platanoides 0.35Aphidius funebris Uroleucon jaceae(116) Centaurea jacea 0.38Aphidius absinthii Macrosiphoniella absinthii(58) Artemisia vulgaris 0.41Aphidius absinthii Macrosiphoniella tanacetaria(77) Tanacetum vulgare 0.45

LargeAphidius rosae Macrosiphum rosae(156) Rosasp. 0.58Aphidius funebris Uroleucon cirsii(56) Cirsium arvense 0.64Aphidius ervi Acyrthosiphon pisum(32) Trifolium pratense 0.69Pauesia picta Cinara pinea(77) Pinus sylvestris 0.83

aPrimary parasitoids are divided according to mummy size into small-, medium-, and large-sized hosts(W Volkl, unpublished data).

Host and Habitat SpecificityGenerally, externally feeding idiobiont ectohyperparasitoid species need lessphysiological adaptations for survival on a living host (such as a mechanismto overcome the host’s immune system) than koinobiont endohyperparasitoidspecies do. Host specificity is much more pronounced in endoparasitic speciesthan in ectoparasitoid species, and species richness is also higher in endopar-asitoids (for reviews, see 33, 39, 88). The aphid hyperparasitoid communitypresents an excellent example for this general pattern and is discussed below.

In Europe, the generaDendrocerus(6 spp.),Asaphes(2 spp.),Pachyneuron(4 spp.),Coruna(1 spp.), andEuneura(2 spp.) comprise altogether 15 speciesdeveloping as ectohyperparasitoids of aphids. Of these, 11 species have a verybroad host range and attack various aphidiid genera and species, independentof the aphid host (22, 30, 36, 99, 105). OnlyPachyneuron gibbiscutaandEuneura laeviusculaare host specific, each of them having been reported upto now from only a single primary parasitoid species (72, 74). Two other species,Dendrocerus liebscheri(the only gregarious aphid hyperparasitoid) andEuneura augarus, seem to be habitat specific, having been reported only fromfield samples of conifer lachnids (30, 57, 77, 99, 120).

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By contrast, endohyperparasitic species are much more numerous: more than50 described species and a number of undescribed or cryptic species, especiallywithin the genusAlloxysta(26, 27, 44). There are only a few species attacking abroad range of unrelated aphid and primary parasitoid hosts, such asAlloxystavictrix andPhaenoglyphis villosa(25). The vast majority of the species, how-ever, seem to be host specific, attacking either a specific aphid host independentof the primary parasitoid or a single primary parasitoid genus independent ofthe aphid host. An example of the first strategy is fromPhaenoglyphis stricta,which is restricted to various aphidiid parasitoids of the genusUroleucononvarious host plants (124). Examples for primary parasitoid–specific alloxystidspecies areAlloxysta circumscripta, a hyperparasitoid of variousPraonspp. ondifferent aphid hosts and host plants;Alloxysta pallidicornis, a hyperparasitoidof Pauesiaspp. viaCinara spp.;Alloxysta darci, a hyperparasitoid ofApheli-nusspp.; andAlloxysta castanea, which attacksPraon volucrevia Hyalopteruspruni (17, 25, 26, 28, 120).

This host specificity is also reflected by the composition of faunistic com-plexes. In native systems, host-specific alloxystid wasps are usually the mostabundant hyperparasitoids, while generalist ectohyperparasitoids, especiallyAsaphesspp. orD. carpenteri, are dominant in exotic systems that have beenestablished after the introduction of a primary parasitoid (73, 100, 107, 111,112, 118, 124, 139–141).

Foraging BehaviorLittle information is available on foraging behavior and the cues involved inhost location. Generally, aphid honeydew may represent an unspecific cue pro-viding information on the presence of aphids on the particular host plant afterthe female’s arrival. Honeydew accumulation leads to increased residence timesin females ofA. victrix, P. villosa, andD. carpenteri(14) and might be respon-sible for an increase in hyperparasitoid foraging effort and foraging success oncontaminated plants.

The majority of the alloxystid species are host specific, and a cue like hon-eydew may provide only limited information. There are two possible strate-gies that might be applied that are not mutually exclusive. First, females maysearch for primary parasitoid females. Indeed, females ofAlloxysta fuscicor-nis (=Alloxysta brassicae) responded positively in olfactometer experimentsto the presence of females of their host,Diaeretiella rapae(89). This strat-egy would assure that females arrive in patches with an available resource butmay confront the alloxystid female with the problem of arriving too early; theprimary’s progeny will be available for oviposition only 3–4 days after ovipo-sition, a time interval exceeding by far the known patch times of alloxystid

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females, both in the presence and absence of primary parasitoid females (121,123). Thus, this foraging strategy by such an endohyperparasitoid might not bevery successful in the field. Second, females may search for host plant volatilesand use them, potentially in combination with the presence of aphid honeydew,as reliable information about the potential occurrence of hosts. After the arrivalin an aphid colony, the female would have to acquire information about (a)the kind of aphid host and (b) the presence of parasitized individuals. Singh& Srivastava (94) showed thatA. pleuralisfemales were attracted to foliageextracts of potential host plants. After the arrival on a host plant, females distin-guished between host (=parasitized) and nonhost aphids by ovipositor contact(93, 95, 96). This strategy might explain some extreme host specificities, suchas inA. castanea, which attacks onlyP. volucrevia H. prunionly on the winterhost, Prunus spinosa. A simple searching strategy restricted to cues arisingfrom the host plant, which is not attacked by other hosts ofP. volucre, mightexplain whyA. castaneadoes not attackP. volucreon reeds, the summer host ofH. pruni.

By contrast, ectohyperparasitoids with a broad host range depend less onspecific cues for foraging, since their hosts may occur on a broad variety ofhost plants.A. vulgarisis obviously using kairomones arising from the silkycocoon of aphidiid primary parasitoids for host finding (20), and probablyfemales may use this cue also for locating mummies on a given host plant.Since larvae of aphelinid species (the other hymenopterous family of aphidprimary parasitoids) do not produce silk for pupation, the low incidence ofhyperparasitism inAphelinusspp. byAsaphesspp. (45) may be explained bythe missing kairomone (20).

D. carpenteri, the most polyphagous aphid hyperparasitoid species, doesnot seem to respond to any cues from hosts or host plants. Females did notrespond to differently colored or differently shaped mummies (18), except forPraonmummies (18a). They searched with the same efficiency during nocturnaland diurnal conditions (122) and were only slightly influenced by insecticideresidues (58). Furthermore, residence times did not differ significantly betweendifferently structured plants without aphid mummies and between mummy-freeand mummy-containing plants, as long as no hosts were found (56, 92). Femalesare searching at random on a host plant, a behavior also known for some otherparasitoid species with a broad host or host plant spectrum (113, 114). Thestrategy of random search might be successful, since the hosts ofD. carpenterimay occur on a broad variety of differently structured host plants where theirdensity and distribution is unpredictable (74).

In petri dishes, hyperparasitoid foraging may also be influenced by encoun-ters with primary parasitoids that are also foraging in aphid colonies (46, 47).

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By contrast, females of the primary parasitoidsAphidius funebrisandL. carduidid change their behavior after encounters withAlloxysta brevis, A. victrix, andD. carpenteriwhen foraging in aphid colonies on plants (but the reverse wasnot observed), which suggests that the proximate effect on oviposition behaviorand resource exploitation of aphidiids is negligible (123). However, as one ofthe most important mortality factors, it is likely that hyperparasitism may havehad an ultimate effect on the evolution of the foraging strategies of aphidiidwasps (7, 61, 129).

Also, the behavior of parasitized aphids to leave the aphid colony beforemummification has been suggested as an example of host manipulation by theprimary parasitoid to reduce the risk of hyperparasitism after mummy formation(12). However, most primary parasitoids suffered less from hyperparasitismwithin aphid colonies than outside (74). Therefore, alternative explanations aremore likely to explain this behavior (33, 74).

Ants and HyperparasitismAphid colonies are often attended by honeydew-collecting ants, which defendtheir carbohydrate source against colony intruders (126). Like many other in-sect species, foraging females of all aphid hyperparasitoid species are heavilyattacked and regularly killed by ant workers (50). The presence of ants leadsto a significant reduction in hyperparasitoid foraging success, thereby providinga kind of “enemy-free” space for the primary parasitoid (81, 119, 120). Thereare several strategies among aphid hyperparasitoids to escape ant aggression.Alloxystid species have evolved a chemical defense, which enables specializedspecies to exploit ant-attended resources to a certain degree.A. brevisreleasesa mandibular gland secretion, which contains 6-methyl-5-hepten-2-one, actini-din, and unidentified iridoids in response to an attack of the antLasius niger(121). This secretion functions both as a measure of self-defense if the female isseized by an ant worker and as a repellent that prevents ant attacks during sub-sequent encounters. It enablesA. brevisfemales to hyperparasitize ant-attendedaphids that constitute a major proportion of their hosts and significantly reducesmortality by ectohyperparasitoids (103, 121).D. carpenterican avoid ant con-tacts by quick and flexible movements, thereby mainly using visual cues. Thisstrategy is very successful againstMyrmica laevinodisbut less effective duringinteractions withL. niger (50). Obviously,D. carpenteriis also able to changeits behavior after an aggressive ant contact. Females that survived an attack byL. niger recognized ant workers by their odor and avoided any contacts withthem during the next few hours (49). The benefit of this “avoidance learn-ing” may be sought in the nocturnal activity of this species, when neitherhyperparasitoid nor ant is able to respond to visual cues in their environment.

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Syrphophagus aphidivorus, Pachyneuron aphidis, A. vulgaris, andEuneurastomaphidispossess jumping ability and were hardly exposed to mortality risksin experimental studies (50, 52).

CONCLUSIONS

Hawkins (39) notes that evolution at the fourth trophic level often measureshyperparasitoid species richness based on the number of species per herbi-vore species. A positive relationship between the numbers of hyperparasitoidspecies and primary parasitoids is not surprising, and species richness at thesetrophic levels is therefore dependent on the biological and ecological charac-teristics of the herbivores. In fact, the difficulty in sampling many ecosystemsprobably results in an underestimation of the hyperparasitoid species. For in-stance, most of the data come from rearings of phytophagous insects, with fewerrearings of field-collected parasitoid cocoons that may have been attacked orwill be attacked by hyperparasitoids. Hence, a hyperparasitoid larva or pupacould be developing in these uncollected cocoons, resulting in an undercountof species diversity. Despite these shortcomings, the emerging patterns suggestthat hyperparasitoid community structure seems to follow the same organiza-tion patterns as primary parasitoid communities. Many parasitoids are attackedby generalist ectohyperparasitoids, and by more host-specific endoparasitoids.Furthermore, host-specific hyperparasitoids seem to be generally more abun-dant than unspecialized generalists, a pattern that is also found in primaryparasitoid communities (33, 39, 41, 88).

In contrast to hyperparasitoid community organization, more information onhyperparasitoid foraging and on oviposition decisions might contribute to a bet-ter explanation of the patterns of resource utilization. Most of our knowledgecomes from studies on a small-scale range, i.e. on patch level (14, 19, 46, 47,49, 56, 83, 93, 121, 123), while there are virtually no studies that analyzedhyperparasitoid foraging on a larger scale, for example, between patches on thesame plant, between plants, or between habitats (91a). Studies on a small-scalerange suggest, together with field data from biological control measures (61,104, 112), that the impact of hyperparasitism on primary parasitoid popula-tion dynamics may be overestimated, although hyperparasitoids can be clearlyidentified as an important host mortality factor (90). Although there is no clearevidence for density dependence at the patch level, we have no informationabout such processes on a larger spatial scale. Studies on this topic should com-bine field studies with an experimental laboratory approach, for example, byusing “microcosmos” systems, and should also include detailed examinationsof the cues involved in habitat and host location and of the importance of in-teractions with adult primary parasitoids and with hyperparasitoid predators at

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the habitat level (61, 90, 104, 120). In general, such an analysis may help tobetter understand individual patterns of resource utilization, which are one keyfactor of hyperparasitoid population dynamics and its role in pest control.

Finally, as was mentioned in a review published in this series in 1987 bySullivan (104), it is standard quarantine procedure in biological control pro-grams to exclude exotic obligate hyperparasitoids. Whether or not exotic fac-ultative hyperparasitoids should be imported and released must be evaluatedseparately for each candidate species depending on the availability of conven-tional natural enemies and the seriousness of the insect pest problem. Mostresearchers urge caution and advise a conservative policy in biological controlprograms in order to exclude exotic facultative hyperparasitoids (130). Indige-nous hyperparasitoids, on the other hand, already exist in the ecosystem andusually cannot be eliminated even if they interfere (in varying degrees) withbiological control by exotic primary parasitoids.

ACKNOWLEDGMENTS

We thank G Hübner, P Kranz, and U Schwörer for sharing unpublished data andP Stiling and AM Rossi (101) for permission to use their drawing (Figure 1),as well as the editors (BA Hawkins and W Sheehan) and Oxford UniversityPress for use of this copyright material. M Romstöck-Volkl, G Hubner, MMackauer, and K Dettner provided helpful comments on the manuscript. TheGerman Research Council provided financial support to WV (DFG Vo 628/3-1).

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Literature Cited

1. Agricola U, Fischer HU. 1991. Hy-perparasitism in two newly introducedparasitoids, Epidinocarsis lopeziandGyranusoidea tebygi(Hymenoptera:Encyrtidae), after their establishment inTogo.Bull. Entomol. Res.81:127–32

2. Allen GR. 1990.Uraba lugensWalker(Lepidoptera: Noctuidae): larval sur-vival and parasitoid biology in the fieldin South Australia.J. Aust. Entomol. Soc.29:301–12

3. Armand E, Lyoussoufi A, Rieux R. 1991.Evolution ofPsylla pyri(L.) andPsyllapyrisuga(Foerster) [Homoptera: Psylli-dae] parasitoid complex in pear orchardsof southeastern France in winter, springand summer.Entomophaga36:287–94

4. Askew RR. 1961. On the biology of theinhabitants of oak galls of Cynipidae

(Hymenoptera) in Britain.Trans. R. En-tomol. Soc. London14:237–68

5. Askew RR, Shaw MR. 1986. Parasitoidcommunities: their size, structure anddevelopment. InInsect Parasitoids, ed.JK Waage, D Greathead, pp. 225–64.London: Academic. 389 pp.

6. Avilla J, Anandon J, Sarasua MJ, AlbajesR. 1991. Egg allocation of the autopar-asitoid Encarsia tricolor at differentrelative densities of the primary host(Trialeurodes vaporariorum) and twosecondary hosts (Encarsia formosaandE. tricolor). Entomol. Exp. Appl.59:219–27

7. Ayal Y, Green R. 1993. Optimal egg dis-tribution among host patches for para-sitoids subject to attack by hyperpara-sitoids.Am. Nat.141:120–38

8. Bennett AW, Sullivan DJ. 1978. Defen-

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ol. 1

999.

44:2

91-3

15. D

ownl

oade

d fr

om w

ww

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ualr

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org

by E

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SUR

- E

l Col

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de

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ront

era

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on 0

9/09

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For

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y.




sive behavior against tertiary parasitismby the larva ofDendrocerus carpenteri,an aphid hyperparasitoid.J. NY Entomol.Soc.86:153–60

8a. Bellotti AC, Smith L, Lapointe S. 1999.Recent advances in cassava pest man-agement.Annu. Rev. Entomol.44:343–70

9. Biddinger DJ, Felland CM, Hull LA.1994. Parasitism of tufted apple budmoth (Lepidoptera: Tortricidae) in con-ventional insecticide and pheromone-treated Pennsylvania apple orchids.En-viron. Entomol.23:1568–79

10. Bocchino F, Sullivan DJ. 1981. Effectsof venoms from two hyperparasitoids,Asaphes lucensand Dendrocerus car-penteri (Hymenoptera: Pteromalidaeand Megaspilidae), on larvae ofAphid-ius smithi(Hymenoptera: Aphidiidae).Can. Entomol.113:887–89 (color plate)

11. Bourchier RS, Nealis VG. 1992. Patternsof hyperparasitism ofCotesia mela-noscela(Hymenoptera: Braconidae) insouthern Ontario.Environ. Entomol.21:907–12

12. Brodeur J, McNeil JN. 1992. Host be-haviour modification by the endopara-sitoid Aphidius nigripes: a strategy toreduce hyperparasitism.Ecol. Entomol.17:97–104

13. Brodeur J, McNeil JN. 1994. Life his-tory of the aphid hyperparasitoidAs-aphes vulgarisWalker (Pteromalidae):possible consequences on the efficacyof the primary parasitoidsAphidius ni-gripesAhsmead (Aphidiidae).Can. En-tomol.126:1493–97

14. Budenberg WJ. 1990. Honeydew as acontact kairomone for aphid parasitoids.Entomol. Exp. Appl.55:139–48

15. Buijs MJ, Pirovano I, van Lenteren JC.1981.Encarsia pergandiella, a possiblebiological control agent for the green-house whitefly,Trialeurodes vaporario-rum. A study on intra and interspecifichost selection.Med. Fac. Landbouww.Rijksuniv. Gent46:465–75

15a. Campbell A, Frazer BD, Gilbert N,Gutierrez AP, Mackauer M. 1974. Tem-perature requirements of some aphidsand their parasites.J. Appl. Ecol.11:431–38

16. Carew WP, Sullivan DJ. 1993. Interspe-cific parasitism between two aphid hy-perparasitoids,Dendrocerus carpenteri(Hymenoptera: Megaspilidae) andAs-aphes lucens(Hymenoptera: Pteromal-idae).Ann. Entomol. Soc. Am.86:794–98

17. Carver M. 1992. Alloxystinae (Hy-

menoptera: Cynipoidea: Charipidae) inAustralia.Invertebr. Taxon.6:769–85

18. Chow A, Mackauer M. 1996. Sequen-tial allocation of offspring sexes in thehyperparasitoidDendrocerus carpen-teri. Anim. Behav.51:859–70

18a. Chow A, Mackauer M. 1998. Host han-dling and specificity of the hyperpar-asitoid wasp,Dendrocerus carpenteri:importance of host age and species.J.Appl. Entomol.In press

19. Christiansen-Weniger P. 1992.Wirt-Parasitoid-Beziehungen zwischen Blatt-laus primar-parasitoiden und den Blatt-laushyperparasitoidenAsaphes vulgarisWlk. undAsaphes suspensus(Nees) (Hy-menoptera: Pteromalidae). PhD thesis.Univ. Kiel, Germany. 96 pp.

20. Christiansen-Weniger P. 1994. Studieson semiochemicals affecting the hostacceptance behaviour ofAsaphes vulga-ris Wlk. (Hymenoptera: Pteromalidae).Norw. J. Agric. Sci.16(Suppl.):277–82

21. Craig TP. 1994. Effects of intraspecificplant variation on parasitoid communi-ties. InParasitoid Community Ecology,ed. B Hawkins, W Sheehan, pp. 205–27.Oxford, UK: Oxford Univ. Press. 516 pp.

22. Dessart P. 1972. Révision des espèceseuropeennes du genreDendrocerusRat-zeburg 1852 (Hymenoptera: Ceraphro-noidea).Mem. Soc. R. Belge Entomol.32:1–312

23. Donaldson JS, Walter GH. 1991. Hostpopulation structure affects field sexratios of the heteronomous hyperpara-sitoid, Coccophagus atratus. Ecol. En-tomol.16:35–44

24. Eichhorn O. 1996. Experimental stud-ies upon the parasitoid complex of thegypsy moth (Lymantria disparL.) (Lep.:Lymantriidae) in lower host populationsin Eastern Austria.J. Appl. Entomol.120:205–12

25. Evenhuis HH. 1976. Studies on Cynip-idae Alloxystinae. 5.Alloxysta citripes(Thomson) andAlloxysta ligustrin. sp.,with remarks on host specifity in the sub-family. Entomol. Ber.36:140–44

26. Evenhuis HH. 1982. A study of Har-tig’s Xystusspecies with type designa-tions and new synonyms.Spixiana5:19–29

27. Evenhuis HH, Barbotin F. 1987. Typesdes espèces d’Alloxystidae (Hymenop-tera: Cynipoidea) de la collection Car-pentier, d’ecrits par J. J. Kieffer, avecsynonymes nouveaux et un nomennovum.Bull. Annls. Soc. R. Belge En-tomol.123:211–24

28. Evenhuis HH, Kiriak IG. 1985. Stud-

Ann

u. R

ev. E

ntom

ol. 1

999.

44:2

91-3

15. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

by E

CO

SUR

- E

l Col

egio

de

la F

ront

era

Sur

on 0

9/09

/11.

For

per

sona

l use

onl

y.




ies on Alloxystidae (Hymenoptera:Cynipoidea). 8.Cynips minuteaZetterst-edt andXystus minutusHartig.Entomol.Ber.45:16–20

29. Feener DH, Brown BV. 1997. Diptera asparasitoids.Annu. Rev. Entomol.42:73–97

30. Ferguson NDM. 1980. A revision of theBritish species ofDendrocerusRatze-burg (Hymenoptera: Ceraphronoidea)with a review of their biology as aphidhyperparasites.Bull. Br. Mus. Nat. Hist(Entomol.).41:255–314

31. Flanders SE. 1943. Indirect hyperpara-sitism and observations on three speciesof indirect hyperparasites.J. Econ. En-tomol.36:921–26

32. Freese G. 1995. Structural refuges in twostem-boring weevils onRumex crispus.Ecol. Entomol.20:351–58

33. Godfray HCJ. 1994.Parasitoids: Beha-vioral and Evolutionary Ecology. Prin-ceton, NJ: Princeton Univ. Press. 473pp.

34. Goergen G, Neuenschwander P. 1990.Biology of Prochiloneurus insolitus(Alam) (Hymenoptera: Encyrtidae), ahyperparasitoid on mealybugs (Homop-tera: Pseudococcidae): immature mor-phology, host acceptance and host rangein West Africa.Mitt. Schweiz. Entomol.Ges.63:317–26

35. Goergen G, Neuenschwander P. 1992. Acage experiment with four trophic lev-els: cassava plant growth as influencd bycassava mealybug,Phenacoccus mani-hoti, its parasitoidEpidinocarsis lopezi,and the hyperparasitoidsProchiloneurusinsolitus. Z. Pflanzenkrankh. Pflanzen-schutz.99:182–905

36. Graham MR de V. 1969. The Pteroma-lidae of North Western Europe (Hyme-noptera, Chalcidoidea).Bull. Brit. Mus.Nat. Hist. Entomol. Suppl.16:1–934

37. Gutierrez AP, van den Bosch R. 1970.Studies on the host selection and hostspecifity of the aphid hyperparasiteCharips victrix (Hymenoptera: Cynip-idae). 2. The bionomics ofCharips vic-trix.Ann. Entomol. Soc. Am.63:1355–60

38. Deleted in proof39. Hawkins B. 1994.Pattern and Process

in Host-Parasitoid Interactions. Cam-bridge, UK: Cambridge Univ. Press. 190pp.

40. Hawkins BA, Goeden RD. 1984. Or-ganization of a parasitoid communityassociated with a complex of galls onAtriplex spp. in southern California.Ecol. Entomol.9:271–92

41. Hawkins BA, Sheehan W, eds. 1994.

Parasitoid Community Ecology. Oxford,UK: Oxford Univ. Press. 516 pp.

42. Herren HR, Neuenschwander P. 1991.Biological control of cassava pests inAfrica. Annu. Rev. Entomol.36:257–83

43. Hoddle MS, Van Driesche RG, Sander-son J. 1998. Biology and use of thewhitefly parasitoidEncarsia formosa.Annu. Rev. Entomol.43:645–69

44. Hoffer A, Stary P. 1970. A review ofbiologies of palaearcticAphidencyrtusspecies (Hym., Chalcidoidea, Encyr-tidae).Stud. Entomol. For.1:81–95

45. Holler C, Borgemeister C, Haardt H,Powell W. 1993. The relationship be-tween primary parasitoid and hyperpar-asitoids of cereal aphids: an analysis offield data.J. Anim. Ecol.62:12–21

46. Holler C, Christiansen-Weninger P, Mi-cha SG, Siri N, Borgemeister C. 1991.Hyperparasitoid-aphid and hyperpara-sitoid-primary parasitoid relationships.Redia74:153–61

47. Holler C, Micha SG, Schulz S, FranckeW, Pickett JA. 1994. Enemy-induceddispersal in a parasitic wasp.Experientia50:182–85

48. Huber JT, Eveleigh E, Pollock S,McCarthy P. 1996. The chalcidoidparasitoids and hyperparasitoids (Hy-menoptera: Chalcidoidea) ofChoristo-neura species (Lepidoptera: Tortrici-dae) in America North of Mexico.Can.Entomol.128:1167–220

49. Hubner G. 1997. Instinktives und erl-erntes Meideverhalten vonDendroce-rus carpenterials Teil einer Verhaltens-strategie bei Ameisenreaktionen.Mitt.Dtsch. Ges. Allg. Angew. Entomol.11:395–99

50. Hubner G, Volkl W. 1996. Behav-ioral strategies of aphid hyperparasitoidsto escape aggression by honeydew-collecting ants.J. Insect Behav.9:143–157

51. Iziquel Y, Le Ru B. 1989. Influence ofhyperparasitism on populations of theencyrtid Epidinocarsis lopezi, a para-sitoid of Phenacoccus manihotiintro-duced in Congo.Entomol. Exp. Appl.52:239–48

52. Kamijo K, Takada H. 1983. A newspecies ofEuneura hyperparasitic onStomaphisaphids.Akitu Kyoto NS55:1–8

53. Kanuck MJ, Sullivan DJ. 1992. Ovi-positional behavior and larval deve-lopment ofAphidencyrtus aphidivorus(Hymenoptera: Encyrtidae), an aphidhyperparasitoid.J. NY Entomol. Soc.100:527–32 (color plate)

Ann

u. R

ev. E

ntom

ol. 1

999.

44:2

91-3

15. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

by E

CO

SUR

- E

l Col

egio

de

la F

ront

era

Sur

on 0

9/09

/11.

For

per

sona

l use

onl

y.




54. Kato M. 1994. Structure, organization,and response of a species-rich parasitoidcommunity to host leafminer populationdynamics.Oecologia97:17–25

55. Keller LJ, Sullivan DJ. 1976. Oviposi-tion behavior and host-feeding ofAs-aphes lucens, an aphid hyperparasitoid(Hymenoptera: Pteromalidae).J. NYEntomol. Soc.84:206–11

56. Kranz P. 1994.Das Fouragierverhaltendes BlattlaushyperparasitoidenDendro-cerus carpenteri(Curtis) (Hymenoptera:Megaspilidae): Untersuchungen zurWirtsfindung und Ressourcennutzung.Diploma thesis. Univ. Bayreuth, Ger-many. 105 pp.

57. Liebscher S. 1972.Zur Taxonomie undBiologie von Dendrocerus-Arten (Hy-menoptera, Ceraphronoidea, Megaspi-lidae) im Hyperparasitenkreis der Lach-nidae (Homoptera, Aphidoidea) aufPinusund Larix. Diploma thesis. Tech.Univ. Dresden. 173 pp.

58. Longley M, Jepson PC. 1996. Theinfluence of insecticides residues onprimary parasitoid and hyperparasitoidforaging behaviour in the laboratory.En-tomol. Exp. Appl.81:259–69

59. Mackauer M, Lardner RM. 1995. Sex-ratio bias in an aphid parasitoid-hyperparasitoid association: a test oftwo hypotheses.Ecol. Entomol.20:118–24

60. Mackauer M, Sequeira R, Otto M. 1997.Growth and development in parasitoidwasps: adaptations to variable host re-sources.Ecol. Stud.130:191–203

61. Mackauer M, V¨olkl W. 1993. Regulationof aphid populations by aphidiid wasps:Does aphidiid foraging behaviour or hy-perparasitism limit impact?Oecologia94:339–50

62. Maier CT. 1988. Parasitoid fauna of twoPhyllonorycterspp. (Lepidoptera: Gra-cillariidae) on wild cherries, and simi-larity to fauna of apple leafminers.Ann.Entomol. Soc. Am.81:460–66

63. Matejko I, Sullivan DJ. 1979. Bionomicsand behavior ofAlloxysta megourae,an aphid hyperparasitoid (Hymenoptera:Alloxystidae).J. NY Entomol. Soc.87:275–82

64. Matejko I, Sullivan DJ. 1984. Interspe-cific tertiary parasitoidism between twoaphid hyperparasitoids:DendroceruscarpenteriandAlloxysta megourae(Hy-menoptera: Megaspilidae and Cynipi-dae).J. Wash. Acad. Sci.74:31–38

65. Matokot L, Reyd G, Malonga P, Le RuB. 1992. Population dynamics ofRas-trococcus invadens(Hom.: Pseudococ-

cidae) in Congo: influence of accidentalintroduction of the asiatic parasitoidGy-ranusoidea tebygi(Hym.: Encyrtidae).Entomophaga37:123–40

66. Menke AS, Evenhuis HH. 1991. NorthAmerican Charipidae: key to genera,nomenclature, species checklists, anda new species ofDilyta Forster (Hy-menoptera: Cynipoidea).Proc. Ento-mol. Soc. Wash.93:136–58

67. Mihajlovic L, Krunic MD, RichardsKW. 1989. Hyperparasitism ofPhysoce-phala vittata(F.) (Diptera: Conopidae)by Habrocytus eonopidarum(Boucek)(Hymenoptera: Pteromalidae), a pestof Megachile rotundata(F.) (Hymenop-tera: Megachilidae) in Yugoslavia.J.Kans. Entomol. Soc.62:418–20

68. Mills NJ, Gutierrez AP. 1996. Prospec-tive modelling in biological control:an analysis of the dynamics of hete-ronomous hyperparasitism in a cotton-whitefly-parasitoid system.J. Appl.Ecol.33:1379–94

69. Mills NJ, Nealis VG. 1992. Europeanfield collections and Canadian releasesof Cernathis samarensis(Dipt.: Tachi-nidae), a parasitoid of the gypsy moth.Entomophaga37:181–91

70. Moore SD, Kfir R. 1995. Host prefer-ence of the facultaive hyperparasitoidTetrastichus howardi(Hym.: Eulophi-dae).Entomophaga40:69–76

71. Moore SD, Kfir R. 1995. Aspects of thebiology of the parasitoid,Tetrastichushowardi (Olliff) (Hymenoptera: Eulo-phidae).J. Afr. Zool.109:455–66

72. Moraal LG. 1990. Some parasitoid com-plexes of aphids on poplar and Scotspine, new to the fauna of the Netherlands(Homoptera: Lachnidae).Entomol. Ber.(Amsterdam)50:109–12

73. Muller C, Adriaanse ICT, Belshaw R,Godfray HCJ. 1998. The structure ofan aphid-parasitoid community.J. Anim.Ecol. In press

74. Muller C, Volkl W, Godfray HCJ. 1997.Are behavioural changes in parasitisedaphids a protection against hyperpara-sitism?Eur. J. Entomol.94:221–34

75. Murakami Y, Gyoutoku Y. 1995. Adelayed increase in the population ofan imported parasitoid,Torymus(Syn-tomaspis) sinensis(Hymenoptera: To-rymidae) in Kumamoto, southwesternJapan.Jpn. J. Appl. Entomol. Zool.30:215–24

76. Murakami Y, Hiramatsu T, Maeda M.1994. Parasitoid complexes of the Chest-nut gall wasp (Hymenoptera: Cynipi-dae) in two localities before introduction

Ann

u. R

ev. E

ntom

ol. 1

999.

44:2

91-3

15. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

by E

CO

SUR

- E

l Col

egio

de

la F

ront

era

Sur

on 0

9/09

/11.

For

per

sona

l use

onl

y.




of Torymus(Syntomaspis) sinensis(Hy-menoptera: Torymidae), with specialreference to predictions.Jpn. J. Appl.Entomol. Zool.38:29–41

77. Murphy ST, Volkl W. 1996. Popula-tion dynamics and foraging behaviourof Diaeretus leucopterusHaliday (Hy-menoptera: Braconidae), and its poten-tial for the biological control of pinedamagingEulachnusspp. (Homoptera:Aphididae).Bull. Entomol. Res.86:397–405

78. Nealis VG, Bourchier RS. 1995. Re-duced vulnerability to hyperparasi-tism in nondiapause strains ofCotesiamelanoscela(Ratzeburg) (Hymenopte-ra: Braconidae).Proc. Entomol. Soc.Ont.126:29–35

79. Neuenschwander P. 1996. Evaluatingthe efficacy of biological control ofthree exotic homopteran pests in tropi-cal Africa.Entomophaga41:405–24

80. Neuenschwander P, Hammond WNO.1988. Natural enemy activity followingthe introduction ofEpidinocarsis lopezi(Hymenoptera: Encyrtidae) against thecassava mealybug,Phenacoccus mani-hoti (Homoptera: Pseudococcidae), insouthwestern Nigeria.Environ. Ento-mol.17:894–902

81. Novak H. 1994. The influence ofant-attendance on larval parasitism inHawthorn psyllids (Homoptera: Psyll-idae).Oecologia99:72–78

82. Nguyen R, Sailer RI. 1987. Facul-tative hyperparasitism and sex deter-mination of Encarsia smithiSilvestri(Hymenoptera: Aphelinidae).Ann. En-tomol. Soc. Am.80:713–19

83. Otto M, Mackauer M. 1998. The deve-lopmental strategy of an idiobiont par-asitoid, Dendrocerus carpenteri: in-fluence of variations in host quality onoffspring growth and fitness.Oecologia.In press

84. Pedata P, Hunter M. 1996. Secondaryhost choice by the autoparasitoidEncar-sia pergandiella. Entomol. Exp. Appl.81:207–14

85. Phillips DS. 1993. Host-feeding andegg maturation byPachycrepoideus vin-demiae. Entomol. Exp. Appl.69:75–82

86. Price PW, Bouton CE, Gross P,McPheron BA, Thompson JN, Weis AE.1980. Interactions among three trophiclevels: influence of plants on interac-tions between herbivores and natural en-emies. Annu. Rev. Ecol. Syst.11:41–65

87. Pschorn-Walcher H. 1988. Parasite com-

munity of European Diprionidae from anecological-evolutionary point of view.Z.Zool. Syst. Evol.forsch.26:89–103

88. Quicke DLJ. 1997.Parasitic Wasps.Cambridge, UK: Chapman & Hall. 470pp.

89. Read DP, Feeny PP, Root RB. 1970.Habitat selection by the aphid parasiteDiaeretiella rapaeand the hyperpara-site Charips brassicae. Can. Entomol.102:1567–78

90. Rosenheim JA. 1998. Higher-orderpredators and the regulation of insectherbivore populations.Annu. Rev. Ento-mol.43:421–47

91. Schaefer PW, Semyanov VP. 1992.Arthropod parasites ofCoccinella sep-tempunctata (Coleoptera: Coccinelli-dae) world parasite list and bibliography.Entomol. News103:125–34

91a. Schooler SS, Ives AR, Harmon J. 1996.Hyperparasitoid aggregation in responseto variations inAphidius ervihost den-sity at three spatial scales.Ecol. Ento-mol.21:249–58

92. Schworer U. 1997.Suchverhalten undRessourcennutzung beim Blattlaushy-perparasitoiden Dendrocerus carpen-teri: Der Einfluß von Pflanzenstruk-tur und Regen. Diploma thesis. Univ.Bayreuth, Germany. 104 pp.

93. Singh R, Srivastava PN. 1987. Fac-tors associated with host-location byAlloxysta pleuralis(Cameron), a hyper-parasitoid ofTrioxys indicusSubba Rao& Sharma (Alloxystidae: Hymenopte-ra/Aphidiidae: Hymenoptera).Entomon12:325–28

94. Singh R, Srivastava PN. 1987. Poten-tial host habitat location byAlloxystapleuralis(Cameron) (Alloxystidae: Hy-menoptera).Z. Ang. Zool.74:337–41

95. Singh R, Srivastava PN. 1987. Bio-nomics ofAlloxysta pleuralis, a cynipoidhyperparasitoid of an aphidiid parasitoidTrioxys indicus. Entomol. Exp. Appl.43:11–15

96. Singh R, Srivastava PN. 1988. Host ac-ceptance behaviour ofAlloxysta pleu-ralis, a cynipoid hyperparasitoid of anaphidiid parasitoidTrioxys indicusonaphids. Entomol. Exp. Appl.47:89–94

97. Singh R, Srivastava PN. 1989. Life-table studies of an aphid hyperparasitoidAlloxysta pleuralis(Cameron) (Hym.,Alloxystidae). J. Appl. Entomol.107:351–56

98. Singh R, Srivastava PN. 1989. Ef-fects of parasitoid density on the func-tional response and sex ratio of a

Ann

u. R

ev. E

ntom

ol. 1

999.

44:2

91-3

15. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

by E

CO

SUR

- E

l Col

egio

de

la F

ront

era

Sur

on 0

9/09

/11.

For

per

sona

l use

onl

y.




cynipoid hyperparasitoidAlloxysta pleu-ralis (Cameron) (Hym: Alloxystidae).Entomophaga34:11–18

99. Stary P. 1977.Dendrocerus—hyper-parasites of aphids in Czechoslovakia(Hymenoptera: Ceraphronoidea).ActaEntomol. Bohemoslov.74:1–9

100. Stechmann DH, V¨olkl W. 1990. Apreliminary survey of aphidophagous in-sects of Tonga, with regards to the bio-logical control of the banana aphid.J.Appl. Entomol.110:408–15

101. Stiling P, Rossi AM. 1994. The windowof parasitoid vulnerability to hyperpar-asitism: template for parasitoid com-plex structure. InParasitoid CommunityEcology, ed. B Hawkins, W Sheehan,pp. 228–44. Oxford, UK: Oxford Univ.Press. 516 pp.

102. Stouthamer R, Luck RF. 1991. Transi-tion from bisexual to unisexual culturesin Encarsia perniciosi(Hymenoptera:Aphelinidae): new data and a reinterpre-tation.Ann. Entomol. Soc. Am.84:150–57

103. Sullivan DJ. 1972. Comparative be-havior and competition between twoaphid hyperparasites:Alloxysta victrixand Asaphes californicus(Hymenop-tera: Cynipidae, Pteromalidae).Envi-ron. Entomol.1:234–44

104. Sullivan DJ. 1987. Insect hyperpara-sitism.Annu. Rev. Entomol.32:49–70

105. Sullivan DJ. 1988. Aphid hyperpara-sites. InAphids, Their Biology, Natu-ral Enemies and Control, ed. AK Minks,P Harrewijn, 2B:189–203. Amsterdam:Elsevier. 382 pp.

106. Sullivan DJ, Neuenschwander P. 1988.Melanization of eggs and larvae of theparasitoid, Epidinocarsis lopezi, (Hy-menoptera: Encyrtidae), by the cas-sava mealybug,Phenacoccus manihotiMatile-Ferrero (Homoptera: Pseudo-coccidae).Can. Entomol.120:63–71

107. Sullivan DJ, van den Bosch R. 1971.Field ecology of the primary parasitesand hyper-parasites of the potato aphid,Macrosiphum euphorbiae, in the EastSan Francisco Bay area.Ann. Entomol.Soc. Am.64:389–94

108. Tagawa J, Fukushima H. 1993. Effectsof host age and cocoon position on at-tack rate by the hyperpaprasitoidEury-toma sp. (Hym.: Eurytomidae) on co-coons of the parasitoidCotesia glom-erata (=Apanteles glomerata) (Hym.:Braconidae).Entomophaga38:69–77

109. Takada H. 1973. Studies on aphid hyper-parasites of Japan. II. Aphid hyperpar-asites of the Pteromalidae occurring in

Japan (Hymenoptera).Insecta Matsum.N.S.2:39–76

110. Van Alebeek FAN, Rojas-Rousse D,Leveque L. 1993. Interspecific competi-tion betweenEupelmus vuilletiandDi-narmus basalis, two solitary ectopara-sitoids of Bruchidae larvae and pupae.Entomol. Exp. Appl.69:21–31

111. van den Bosch R. 1981. Specifity of hy-perparasitoids. InThe Role of Hyperpar-asitism in Biological Control: A Sympo-sium, Priced Publ. 4103, ed. D Rosen,pp. 27–33. Berkeley, CA: Div. Agric.Sci. Univ. Calif.

112. van den Bosch R, Hom R, Matteson P,Frazer BD, Messenger PS, Davis CS.1979. Biological control of the walnutaphid in California: impact of the para-site,Trioxys pallidus.Hilgardia 47:1–13

113. van Roermund HJW, van Lenteren JC.1995. Residence times of the white-fly parasitoidEncarsia formosaGahan(Hym.: Aphelinidae) on tomato leaflets.J. Appl. Entomol.119:465–71

114. van Roermund HJW, van Lenteren JC,Rabbinge R. 1997. Analysis of the forag-ing behaviour of the whitefly parasitoidEncarsia formosaon a plant: a simula-tion study.Biocontr. Sci. Tech.7:131–51

115. Deleted in proof116. Viggiani G. 1984. Bionomics of the

Aphelinidae.Annu. Rev. Entomol.29:257–76

117. Viggiani G. 1987. Biological noteson Encarsia aleurolicisViggiani (Hy-menoptera: Aphelinidae).Boll. Ist. En-tomol. Univ. Stud. Bologna.41:87–92

118. Volkl W. 1990. Fortpflanzungsstrate-gien von Blattlausparasitoiden (Hyme-noptera, Aphidiidae): Konsequenzenihrer Interaktionen mit Wirten und Amei-sen. PhD thesis. Univ. Bayreuth, Ger-many. 130 pp.

119. Volkl W. 1992. Aphids or their para-sitoids: Who actually benefits from ant-attendance?J. Anim. Ecol.61:273–81

120. Volkl W. 1997. Interactions betweenants and aphid parasitoids: patterns andconsequences for resource utilization.Ecol. Stud.130:225–40

121. Volkl W, Hubner G, Dettner K. 1994. In-teractions betweenAlloxysta brevis(Hy-menoptera: Cynipoidea, Alloxystidae)and honeydew collecting ants: how anaphid hyperparasitoid overcomes ant ag-gression by chemical defense.J. Chem.Ecol.20:2621–35

122. Volkl W, Kranz P. 1995. Nocturnal activ-ity and resource utilization in the aphidhyperparasitoid,Dendrocerus carpen-teri. Ecol. Entomol.20:293–97

Ann

u. R

ev. E

ntom

ol. 1

999.

44:2

91-3

15. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

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123. Volkl W, Kranz P, Weisser WW, H¨ubnerG. 1995. Patch time allocation and re-source exploitation in aphid primary par-asitoids and hyperparasitoids searchingsimultaneously within aphid colonies.J.Appl. Entomol.119:399–404

124. Volkl W, Stary P. 1988. Parasitiza-tion of Uroleuconspecies (Homoptera,Aphidiidae) on thistles (Compositae,Cardueae).J. Appl. Entomol.106:500–6

125. Walker GP, Cameron PJ. 1981. The bi-ology of Dendrocerus carpenteri(Hy-menoptera: Ceraphronidae), a parasiteof Aphidiusspecies, and field observa-tions of Dendrocerusspecies as hyper-parasites ofAcyrthosiphonspecies.NZJ. Zool.8:531–38

126. Way MJ. 1963. Mutualism between antsand honeydew-producing homoptera.Annu. Rev. Entomol.8:307–44

127. Weinstein P, Austin AD. 1991. The hostrelationships of trigonalyid wasps (Hy-menoptera: Trigonalyidae), with a re-view of their biology and catalogue toworld species.J. Nat. Hist.25:399–434

128. Weinstein P, Austin AD. 1995. Primaryparasitism, development and adult biol-ogy in the waspTaeniogonalos venato-ria Riek (Hymenoptera: Trigonalyidae).Aust. J. Zool.43:541–55

129. Weisser WW, Houston AI, V¨olkl W.1994. Foraging strategies in solitaryparasitoids: the trade-off between fe-male and offspring mortality.Evol. Ecol.8:587–97

130. White EB, Bernal JS, Gonzlez D, Tria-pitsyn SV. 1998. Facultative hyper-parasitism in Brachymeria pomonae(Cameron) (Hymenoptera: Chalcidi-dae).Eur. J. Entomol.In press

131. Whitfield JB. 1998. Phylogeny and evo-lution of the host-parasitoid relationshipin the Hymenoptera.Annu. Rev. Ento-mol.43:129–51

132. Wieber AM, Cook SP, Webb RE, Rear-don RC, Tatman KM. 1996. Similar-ity of the hyperparasitoid communitiesattacking two strains of a gypsy moth(Lepidoptera: Lymantriidae) primaryparasitoid, Cotesia melanoscela(Hy-menoptera: Braconidae).Ann. Entomol.Soc. Am.89:47–52

133. Wieber AM, Webb RE, Ridgway RL,Thorpe KW, Reardon RC, et al. 1995.Effect of seasonal placement ofCote-sia melanoscela(Hym.: Braconidae) onits potential for effective augmentativerelease againstLymantria dispar(Lep.:Lymantriidae). Entomophaga40:281–92

134. Williams T. 1991. Host selection and sexratio in a heteronomous hyperparasitoid.Ecol. Entomol.16:377–86

135. Williams T. 1996. Invasion and dis-placement of experimental populationsof a conventional parasitoid by a hete-ronomous hyperparaitoid.Biocontr. Sci.Technol.6:603–18

136. Williams T, Polaszek A. 1996. A re-exa-mination of host relations in the aphelini-dae (Hymenoptera: Chalcidoidea).Biol.J. Linn. Soc.57:35–45

137. Woolley JB, Vet LEM. 1981. Postovipo-sitional web-spinning behavior in a hy-perparasiteSigniphora coquellettiAsh-mead (Hymenoptera: Signiphoridae).Neth. J. Zool.31:627–33

137a. Yeargan KV, Braman SK. 1989. Lifehistory of hyperparasitoidMesocho-rus discitergus(Hymenoptera: Ichneu-monidae) and tactics used to overcomethe defensive behavior of the greencloverworm (Lepidoptera: Noctuidae).Ann. Entomol. Soc. Am.82:393–98

138. Yeates DK, Greathead D. 1997. Theevolutionary pattern of host use in theBombyliidae (Diptera): a diverse fam-ily of parasitoid flies.Biol. J. Linn. Soc.60:149–85

139. Zuparko R. 1995.Evalution of the bi-ological control of the linden aphid byTrioxys curvicaudusin Northern Cali-fornia. PhD thesis. Univ. Calif., Berke-ley. 128 pp.

140. Zuparko R, Dahlsten DL. 1993. Surveyof the parasitoids of the tuliptree aphid,Illinoia liriodendri (Hom.: Aphididae)in Northern California.Entomophaga38:31–40

141. Zuparko R, Dahlsten DL. 1995. Para-sitoid complex ofEucallipterus tiliae(Homoptera: Drepanosiphidae) in Nor-thern California.Environ. Entomol.24:730–37

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Annual Review of Entomology Volume 44, 1999

CONTENTSMites in Forest Canopies: Filling the Size Distribution Shortfall? David Evans Walter, Valerie Behan-Pelletier 1

Insects as Food: Why the Western Attitude is Important, Gene R. DeFoliart 21

Emerging and Resurging Vector-Borne Diseases, Norman G. Gratz 51

Insect Pests of Pigeonpea and Their Management, T. G. Shanower, J. Romeis, E. M. Minja 77

The Evolution and Development of Dipteran Wing Veins: A Systematic Approach, Julian Stark, James Bonacum, James Remsen, Rob DeSalle 97

Odor-Mediated Behavior of Afrotropical Malaria Mosquitoes, Willem Takken, Bart G. J. Knols 131

Pathogens and Predators of Ticks and Their Potential in Biological Control, M. Samish, J. Rehacek 159

The Role of Stingless Bees in Crop Pollination, Tim A. Heard 183

Bionomics of the Anthocoridae, John D. Lattin 207

Adaptative Strategies of Edaphic Arthropods, M. G. Villani, L. L. Allee, A. Díaz, P. S. Robbins 233

Assessment of the Application of Baculoviruses for Control of Lepidoptera, Flávio Moscardi 257

Hyperparasitism: Multitrophic Ecology and Behavior, Daniel J. Sullivan, Wolfgang Völkl 291

Density-Dependent Physiological Phase in Insects, S. W. Applebaum, Y. Heifetz 317

Recent Advances in Cassava Pest Management, Anthony C. Bellotti, Lincoln Smith, Stephen L. Lapointe 343

Mate Choice in Tree Crickets and Their Kin, W. D. Brown 371

CONGRUENCE AND CONTROVERSY: Toward a Higher-Level Phylogeny of Diptera, D. K. Yeates, B. M. Wiegmann 397

The Insect Voltage-Gated Sodium Channel As Target of Insecticides, Eliahu Zlotkin 429

Management of Plant Viral Diseases Through Chemical Control of Insect Vectors, Thomas M. Perring, Ned M. Gruenhagen, Charles A. Farrar 457

Influence of the Larval Host Plant on Reproductive Strategies in Cerambycid Beetles, L. M. Hanks 483

Insect P450 Enzymes, René Feyereisen 507

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Risk-Spreading and Bet-Hedging in Insect Population Biology, Keith R. Hopper 535

Nutrition and Culture of Entomophagous Insects, S. N. Thompson 561

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hyperparasitism: multitrophic ecology and behavior · p1: ars/spd p2: ars/ary qc: ars november 4,...

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