Interactions between the egg and larval parasitoids of a gall-forming midge and their impact on the host

1. The gall‐forming midge Rhopalomyia californica was exposed experimentally to parasitism and predation during only the egg stage, during only the larval stage, during neither stage, or during both stages. 2. The combined action of natural enemies that attack during both the egg stage and the larval stage led to the lowest number of midges and total insects (midges + parasitoids) in the next generation, and the highest percentage parasitism. 3. The larval parasitoid killed a large fraction of hosts without producing new parasitoid offspring, while there is some indication that the egg parasitoid on its own tended to produce the most parasitoid offspring. The contrasting implications of host mortality versus parasitoid production for biological control are discussed. 4. Exposure to larval parasitoids resulted in a reduction in the number of egg parasitoid offspring produced, but exposure to the egg parasitoid did not affect the number of larval parasitoid offspring produced significantly.     

Exploitative competition and coexistence in a parasitoid assemblage

Most insect populations are exploited by a complex of different parasitoid species, providing ample opportunities for competitive interactions among the latter. Despite this, resource-mediated competition (i.e., exploitative competition) among insect parasitoids remains poorly documented in natural systems. Here we propose a novel way to infer the presence of competitive interactions from covariance patterns in parasitism levels, and illustrate the use of this approach on a relatively well-defined and simple host–parasitoid system. The parasitism levels caused by three parasitoid species on a shared host showed a highly consistent negative covariance among samples. With the levels of parasitism by one species increasing, the levels of parasitism attributable to the two others decreased. Importantly, negative covariance between parasitism levels by different species appeared at high abundance, but not at low abundance of the phenologically earlier parasitoid species. This as well as several other lines of evidence indicates the importance of competitive interactions in this system. Feeding biology and phenology of the parasitoids suggest that competition in this parasitoid assemblage is primarily resource-mediated rather than occurring through direct interference. The species attacking earlier stages of the host are competitively superior to those attacking their host later in the season. Better dispersal ability and use of alternative host species by the inferior species could contribute to the coexistence of these competing parasitoids.     

Intrinsic inter-specific competition in a guild of tephritid fruit fly parasitoids: Effect of co-evolutionary history on competitive superiority

Tephritid fruit fly parasitoid guilds are dominated by solitary koinobiont species that attack different host stages, but most emerge as adults from host puparia. Previous studies suggest intrinsic competitive superiority by the egg-attacking parasitoid Fopius arisanus (Sonan) against all larval-attacking parasitoids in Hawaii. In this study, we tested the early-acting competitive superiority prediction in relation to the co-evolutionary history of competition between an egg–larval parasitoid (Fopius ceratitivorus Wharton), and each of three larval parasitoids [Psyttalia concolor (Szépligeti), Diachasmimorpha kraussii (Fullaway), and Diachasmimorpha longicaudata (Ashmead)]. F. ceratitivorus and P. concolor share a common origin (eastern Africa), while D. kraussii is an Australian species, and D. longicaudata is from Southeast Asia. The outcomes of intrinsic competition between the egg-attacking parasitoid and each of the three larval-attacking parasitoids within their common host, the Mediterranean fruit fly Ceratitis capitata (Wiedemann) were compared. F. ceratitivorus invariably eliminated the co-evolved P. concolor through physiological suppression of the later-attacking parasitoid’s egg development, providing evidence that supports the early-acting-superiority hypothesis. However, F. ceratitivorus was unable to suppress development of the two non co-evolved larval parasitoids. Instead, the larvae of both later-acting parasitoid species physically killed F. ceratitivorus larvae inside the host. The results suggest that co-evolutionary history influences competitive superiority. The evolution of inter-specific competition and its implications for biological control are discussed.     

Intrinsic, inter-specific competition between egg, egg–larval, and larval parasitoids of plusiine loopers

Abstract.  1. Intrinsic, inter-specific competition between parasitoid wasp species is a key factor in ecological community dynamics and is particularly important for application in biological control. Here three parasitoid wasp species with overlapping host ranges and differing life history strategies were chosen to examine parasitoid–parasitoid interactions: the egg parasitoid Trichogramma pretiosum, the egg–larval, polyembryonic parasitoid wasp Copidosoma floridanum, and the gregarious larval parasitoid Glyptapanteles pallipes , with the plusiine loopers Acanthoplusia agnata and Trichoplusia ni as hosts.
2.  Copidosoma floridanum has been shown to be an intrinsically superior competitor against larval parasitoids because of their production and increased investment in a soldier larval caste during development, but little is known of their interactions with egg parasitoid species. Trichogramma pretiosum completely dominated intrinsic competition with C. floridanum regardless of oviposition order or sex of the C. floridanum egg.
3. Competition between C. floridanum and G. pallipes , however, depended on the host stage at which parasitism occurred, the sex of the C. floridanum egg, and parasitoid development time. Copidosoma floridanum outcompeted G. pallipes overall, despite the fact that G. pallipes injects a polyDNA virus into the host.
4. The sex of the C. floridanum egg was a significant factor in its ability to shift caste ratios to produce more soldiers in response to G. pallipes competition.
5. Only developing female C. floridanum responded to competition with G. pallipes by increasing the ratio of soldier to reproductive larvae, and this happened only when multiparasitism occurred in the host's 1st and 2nd instar.     

Host Niches and Defensive Extended Phenotypes Structure Parasitoid Wasp Communities

Oak galls are spectacular extended phenotypes of gallwasp genes in host oak tissues and have evolved complex morphologies that serve, in part, to exclude parasitoid natural enemies.Parasitoids and their insect herbivore hosts have coevolved to produce diverse communities comprising about a third of all animal species. The factors structuring these communities, however, remain poorly understood. An emerging theme in community ecology is the need to consider the effects of host traits, shaped by both natural selection and phylogenetic history, on associated communities of natural enemies. Here we examine the impact of host traits and phylogenetic relatedness on 48 ecologically closed and species-rich communities of parasitoids attacking gall-inducing wasps on oaks. Gallwasps induce the development of spectacular and structurally complex galls whose species- and generation-specific morphologies are the extended phenotypes of gallwasp genes. All the associated natural enemies attack their concealed hosts through gall tissues, and several structural gall traits have been shown to enhance defence against parasitoid attack. Here we explore the significance of these and other host traits in predicting variation in parasitoid community structure across gallwasp species. In particular, we test the “Enemy Hypothesis,” which predicts that galls with similar morphology will exclude similar sets of parasitoids and therefore have similar parasitoid communities. Having controlled for phylogenetic patterning in host traits and communities, we found significant correlations between parasitoid community structure and several gall structural traits (toughness, hairiness, stickiness), supporting the Enemy Hypothesis. Parasitoid community structure was also consistently predicted by components of the hosts'' spatiotemporal niche, particularly host oak taxonomy and gall location (e.g., leaf versus bud versus seed). The combined explanatory power of structural and spatiotemporal traits on community structure can be high, reaching 62% in one analysis. The observed patterns derive mainly from partial niche specialisation of highly generalist parasitoids with broad host ranges (>20 hosts), rather than strict separation of enemies with narrower host ranges, and so may contribute to maintenance of the richness of generalist parasitoids in gallwasp communities. Though evolutionary escape from parasitoids might most effectively be achieved via changes in host oak taxon, extreme conservatism in this trait for gallwasps suggests that selection is more likely to have acted on gall morphology and location. Any escape from parasitoids associated with evolutionary shifts in these traits has probably only been transient, however, due to subsequent recruitment of parasitoid species already attacking other host galls with similar trait combinations.     

Influence of plant resistance at the third trophic level: interactions between parasitoids and entomopathogenic fungi of cereal aphids

Host-plant resistance can affect herbivorous insects and their natural enemies such as parasitoids and entomopathogenic fungi. This tritrophic effect acts on interspecific interactions between the two groups of natural enemies distantly related in phylogenetic terms. The intra- and extra-host aspects of the interaction between the cereal aphid parasitoid Aphidius rhopalosiphi and the entomopathogenic fungus Erynia neoaphidis developing on the grain aphid, Sitobion avenae, on resistant and susceptible wheat (Triticum aestivum) cultivars, were studied. The competitive outcome of the intra-host interaction depended on the timing of parasitoid oviposition and fungal infection and was affected by wheat resistance. In particular, survival of the parasitoid was lower on the resistant wheat cultivar than the susceptible wheat cultivar, when the competitive outcome of the interaction was favourable for either parasitoid or fungal development. Before and after this period the influence of plant resistance was not significant. Furthermore, the extra-host interaction was not affected by the wheat cultivar, although an increase in fungal infection of S. avenae was observed when parasitoids foraged in the experimental arena with sporulating aphid cadavers compared with foraging in the absence of sporulating cadavers. Our results showed that the host plant may affect interspecific interactions between parasitoids and fungi and that these interactions depended on the timing of parasitoid oviposition and fungal infection. Received: 16 March 1998 / Accepted: 24 August 1998     

Trichogramma pretiosum parasitism and dispersal capacity: a basis for developing biological control programs for soybean caterpillars

In order to succeed in biological control programs, not only is it crucial to understand the number of natural enemies to be released but also on how many sites per area this releasing must be performed. These variables might differ deeply among egg parasitoid species and crops worked. Therefore, these trials were carried out to evaluate the parasitism (%) in eggs of Anticarsia gemmatalis and Pseudoplusia includens after the release of different densities of the egg parasitoid Trichogramma pretiosum. Field dispersal was also studied, in order to determine appropriate recommendations for the release of this parasitoid in soybean fields. The regression analysis between parasitism (%) and densities of the parasitoid indicated a quadratic effect for both A. gemmatalis and P. includens. The maximum parasitism within 24 h after the release was reached with densities of 25.6 and 51.2 parasitoids per host egg, respectively, for the two pests. Parasitism of T. pretiosum in eggs of P. includens decreased linearly as the distance of the pest eggs from the parasitoid release sites increased. For P. includens, the mean radius of T. pretiosum action and the area of parasitoid dispersal in the soybean crop were 8.01 m and 85.18 m2, respectively. We conclude that for a successful biological control program of lepidopteran pests using T. pretiosum in soybean fields, a density of 25.6 parasitoids per host egg, divided into 117 sites per hectare, should be used.     

Assessment of interspecific interactions among parasitoids on the outcome of inoculative biological control of leafminers attacking chrysanthemum

Indigenous natural enemies occur within field grown crops at varying densities dependent upon a variety of other biotic and abiotic parameters. This natural control often does not provide adequate suppression, which results in the application of other pest management solutions including augmentative biological control. When releasing mass-reared natural enemies into a backdrop of existing natural enemy populations, competitive interactions are likely to occur. To assess the influence of these interspecific interactions on the outcome of such biological control practices studies were conducted in a simulated, field cage grown, cut chrysanthemum production system. Competitive interactions of two commercially available parasitoids were studied both in terms of parasitoid-host population dynamics and the impact of interspecific interactions on crop quality at harvest. The parasitoids Diglyphus isaea and Dacnusa sibirica attacking the leafminer Liriomyza langei were used as the model insect system. Both parasitoids are cosmopolitan and are known to occur in many ornamental production areas. Treatment comparisons included single species releases with complimentary releases of both species either simultaneously or with 2-week time lags, as well as a no release control to measure the background effects of natural mortality. Conclusions drawn from results of population-level studies replicated within and among years were that levels of interspecific competition among parasitoid species were undetectable at leafminer densities typical of field-grown ornamental crops (low densities), and thus, the efficacy of one species released into a backdrop of potentially competing parasitoids did not negatively or positively affect the outcome of the augmentative biological control, nor was there a positive outcome; however, crop quality at harvest was influenced.     

Field collection of egg parasitoids of Pentatomidae and Scutelleridae in Northwest Italy and their efficacy in parasitizing Halyomorpha halys under laboratory conditions

The invasion of Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) has caused severe economic damage in crops in North America and Europe, motivating research to identify its natural enemies, both in native and invaded areas. In its Asian native range, the main natural enemies are egg parasitoids, among which the most effective are Trissolcus japonicus (Ashmead) and Trissolcus mitsukurii (Ashmead) (Hymenoptera: Scelionidae) in China and Japan, respectively. In Europe, biology, host range, and impact of most native scelionid species are not well‐known. The present study aimed to investigate (1) presence and abundance of scelionid species that parasitize native Pentatomidae and Scutelleridae eggs in Northwest Italy, and (2) their ability to develop on H. halys eggs. During 4‐year field surveys, egg masses were collected and reared until bug nymph or adult parasitoid emergence. Then, the obtained scelionid females were tested for their ability to parasitize H. halys eggs in laboratory no‐choice experiments. Egg masses of all collected bug species were parasitized, and Telenomus spp. (Hymenoptera: Scelionidae), Trissolcus belenus (Walker), and Anastatus bifasciatus (Geoffroy) (Hymenoptera: Eupelmidae) were the most common parasitoids. In the laboratory, Trissolcus kozlovi Rjachovskij was the only species to significantly produce offspring from fresh H. halys eggs, whereas all tested Trissolcus species significantly induced host egg abortion (non‐reproductive effects). This study provides knowledge of the parasitoid species associated with native bugs, and represents a starting point to investigate the intricate interactions between native and exotic parasitoids recently found in northern Italy. These egg parasitoids could potentially be effective biocontrol agents of H. halys.     

Biological studies on two neotropical egg parasitoid species: Trichogramma nerudai and Trichogramma sp. (Hymenoptera: Trichogrammatidae)

The main biological attributes of two Neotropical egg parasitoids, the arrhenotokous Trichogramma nerudai and the thelytokous Trichogramma sp., were assessed under controlled laboratory conditions. Developmental time from egg to adult, and parasitoid survival, fecundity and fertility were studied using life tables. Results showed that T. nerudai had a faster developmental time than Trichogramma sp. (13.014±0.4019 and 13.595±0.4931 days, respectively). Both species showed similar life table statistics, r_m was 0.222 and 0.225 for T. nerudai and Trichogramma sp., respectively. Parasitoid survival averaged 95% for both species. The results obtained are discussed in the context of selecting one of these natural enemies as a potential biological control agent for the European pine shoot moth Rhyacionia buoliana (Lepidoptera: Tortricidae) in pine forests and the codling moth Cydia pomonella (Lepidoptera: Tortricidae) in apple orchards in Argentina.     

The colonization of native phytophagous insects in North America by exotic parasitoids

Classical biological control could have a major environmental cost if introduced natural enemies colonize and disrupt native systems. Although quantifying these impacts is difficult for systems already colonized by natural enemies, the a priori condition for such impacts can be evaluated based on the extent to which exotics have acquired native hosts. We use native host records for exotic parasitoids introduced into North America for biological control to document the number of exotic species that have been recorded from at least one native insect species. We also evaluate the ability of six biological and ecological variables to predict whether or not a parasitoid will move onto natives. Sixteen percent of 313 parasitoid species introduced against holometabolous pests are known from natives. Further, the likelihood that a parasitoid had colonized native hosts was largely unpredictable with respect to the independent variables. We conclude that given the quality of the data available either now or in the foreseeable future, coupled with inherent stochasticity in host shifts by parasitoids, there are no rules of thumb to assist biological control workers in evaluating if an introduced parasitoid will colonize native insect communities. Received: 2 July 1997 / Accepted: 3 August 1997     

The influence of feeding and host deprivation on egg load and reproduction of an aphid parasitoid, <Emphasis Type="Italic">Aphidius gifuensis</Emphasis> (Hymenoptera: Braconidae)

With a view to improving the establishment of Aphidius gifuensis Ashmead, a potential natural enemy for suppression of aphids on vegetables, the effects of host deprivation and honey feeding before release on the parasitoid’s egg load and reproduction were studied under laboratory conditions. Host deprivation significantly affected mummy production and survival rate of female parasitoids. A. gifuensis produced more mummies when exposed to a short period (1 and 2 days) of host deprivation, but when host deprivation lasted for 3 days, their mummy production sharply decreased. Offspring produced by parasitoids that had been deprived of hosts for 2 days were much heavier than those produced by parasitoids deprived of hosts for 1 and 3 days. However, host deprivation did not affect emergence rate or offspring sex ratio; the emergence rate was always above 80%, and the offspring sex ratio was always female biased irrespective of whether the host-deprivation period was 1, 2, or 3 days. Honey feeding greatly increased egg load, longevity and decelerated oosorption of A. gifuensis when hosts were absent, and significantly increased parasitoid mummy production in late age. We discuss the results in the context of augmentative biological control, with the view to understanding how to increase parasitoid performance after they are released.     

Can hyperparasitoids cause large‐scale outbreaks of insect herbivores?

Synchronous population fluctuations occur in many species and have large economic impacts, but remain poorly understood. Dispersal, climate and natural enemies have been hypothesized to cause synchronous population fluctuations across large areas. For example, insect herbivores cause extensive forest defoliation and have many natural enemies, such as parasitoids, that may cause landscape‐scale changes in density. Between outbreaks, parasitoid‐caused mortality of hosts/herbivores is high, but it drops substantially during outbreak episodes. Because of their essential role in regulating herbivore populations, we need to include parasitoids in spatial modelling approaches to more effectively manage insect defoliation. However, classic host‐parasitoid population models predict parasitoid density, and parasitoid density is difficult to relate to host‐level observations of parasitoid‐caused mortality. We constructed a novel model to study how parasitoids affect insect outbreaks at the landscape scale. The model represents metacommunity dynamics, in which herbivore regulation, colonisation and extinction are driven by interactions with the forest, primary parasitoids and hyperparasitoids. The model suggests that parasitoid spatial dynamics can produce landscape‐scale outbreaks. Our results propose the testable prediction that hyperparasitoid prevalence should increase just before the onset of an outbreak because of hyperparasitoid overexploitation. If verified empirically, hyperparasitoid distribution could provide a biotic indicator that an outbreak will occur.     

Intraspecific competition and density dependence in an Ephestia kuehniella–Venturia canescens laboratory system

A model host-parasitoid system of Ephestia kuehniella and Venturia canescens was used to examine the influence of host and parasitoid density on host and parasitoid life-history parameters via a two-way factorial experimental design (5 initial host densities×3 parasitoid densities). In the absence of parasitoids, E. kuehniella experienced scramble-type competition with reduced growth, diminished adult size and a subsequent fecundity trade-off for mortality. The mortality that did occur was confined to the late larval and pupal stages. In the presence of parasitoids attacking the late larval stage, competition changed from scramble for food to contest for enemy-free space, with hosts escaping parasitism being small with low fecundity and reduced egg size, and with parasitoid adult size inversely dependent on host density. Total insect emergence (host+parasitoid), a measure of the influence of host resource competition on survivorship, exhibited a threshold effect as a function of initial host density; the threshold value was increased to a higher initial host density in the presence of parasitoids. Models of host self-limitation were fitted to the data, with the generalized Beverton-Holt model that incorporates a threshold effect providing the best fit, and the Ricker model with no threshold providing a very poor fit to the data.     

Long-term seasonal fluctuations of lepidopteran cereal stemborers and their natural enemies on maize and wild host plants in southern Benin

Abstract  The seasonal fluctuation of lepidopteran cereal stemborers on maize and wild host plants (i.e., grasses and a few sedges) was investigated in southern Benin from 1988 to 1998 by time series analysis and repeated-measures analysis of variance (ANOVA). In addition, a walk-in light trap was used to study the flight behavior of adult moths. On both cereals and grasses, the noctuid Sesamia calamistis was the predominant species, followed by the pyralid Eldana saccharina . The noctuid Busseola fusca was rare on both maize and wild host plants. In general, pest populations increased during the course of the year to reach peak densities during the second short rainy season, and then crashed to close to zero during the dry season. On wild host plants, egg masses and other immature stages were collected throughout the year but they were higher on wild grasses than maize during the off-season. Thus wild host plants can be considered as refuge for both borers and natural enemies during the off-season, when maize is not available. However, only four out of the eleven wild host species played a discernable role. S. calamistis egg densities appeared to be influenced by density-dependent factors, suggesting an effect of natural enemies. Temperature and rainfall had a negative effect on egg abundance. Larval parasitism by a Kenyan strain of the braconid Cotesia sesamiae , which was released in southern Benin in the early 1990s, and by the tachinid Sturmiopsis parasitica varied between seasons and years but there were no discernable patterns. For both parasitoids and borer host species, parasitism was positively correlated with trap catches of adult moths. The recovery of C. sesamiae during a 2-year period suggests that the parasitoid has established its population in southern Benin.     

An exotic parasitoid provides an invasional lifeline for native parasitoids

The introduction of an exotic species may alter food webs within the ecosystem and significantly affect the biodiversity of indigenous species at different trophic levels. It has been postulated that recent introduction of the brown marmorated stinkbug (Halyomorpha halys (Stål)) represents an evolutionary trap for native parasitoids, as they accept H. halys egg masses as a host but produce no viable progeny. Interspecific interactions between European egg parasitoid, Trissolcus cultratus (Mayr), and an Asian parasitoid, Trissolcus japonicus (Ashmead), were assessed by providing egg masses to T. cultratus at various time intervals following the initial parasitization by T. japonicus. The suitability of the host for the parasitoid development was re‐assessed by providing T. cultratus with fresh and frozen egg masses of various ages. The likelihood of T. cultratus being able to attack previously parasitized egg masses was determined by assessing the duration of egg mass guarding behavior by T. japonicus following parasitization. The results of experiments examining the interspecific interactions between a native European egg parasitoid, T. cultratus, and an Asian parasitoid, T. japonicus (a candidate for the biological control of H. halys), showed that the native species can act as facultative hyperparasitoid of the exotic one. Although this is only possible during certain stages of T. japonicus development, the presence of the introduced parasitoid may reduce the impact of the evolutionary trap for indigenous parasitoid species. There is a possibility that the occurrence of facultative hyperparasitism between scelionid parasitoids associated with stinkbugs is common. This resulting intraguild predation could promote conservation and stabilization of natural communities by impacting the diversity and population dynamics of native stinkbugs and their parasitoids (e.g., by allowing native parasitoids to avoid wasting reproductive effort on unsuitable hosts), or reduce success of biological control programs (e.g., by reducing the population size of the exotic parasitoids).     

Choice versus no-choice test interpretation and the role of biology and behavior in parasitoid host specificity tests

The need to improve methods and interpretation of host specificity tests for arthropod natural enemies has been clearly identified, yet there remains a paucity of empirical evidence upon which to base recommendations. Factors influencing test outcomes and the mechanisms underlying them must be understood so they can be controlled, and test results can be interpreted correctly. In this study, an established exotic host/parasitoid system was used to assess the outcomes and predictive accuracy of no-choice compared to paired choice tests within small laboratory arenas. Host acceptance by two egg parasitoids, Enoggera nassaui and Neopolycystus insectifurax (Pteromalidae), was interpreted in light of percent parasitism, offspring sex ratios and observed parasitoid behavior. No-choice tests showed that the four host species, Paropsis charybdis, Dicranosterna semipunctata, Trachymela catenata and Trachymela sloanei (Coleoptera: Chrysomelidae) were within the physiological host ranges of both parasitoids. The results of paired choice tests with the first three species supported this interpretation, with two exceptions. Trachymela catenata eggs were not accepted by E. nassaui and were accepted significantly less often by N. insectifurax when compared to no-choice tests. Both test designs predicted that D. semipunctata is within the ecological host range of the two parasitoid species, whereas field evidence suggests this is a false positive result. Percent parasitism of all hosts was higher in no-choice compared to choice tests and was predictive of rank order of host preference in choice tests. Presence of the most preferred host did not increase attack on lower ranked hosts. Offspring sex ratios of E. nassaui were independent of host preference. In contrast, N. insectifurax allocated more females to P. charybdis and mostly males to D. semipunctata and T. catenata. The results support our assertion that both no-choice and choice tests along with detailed behavioral studies should be conducted for correct interpretation of pre-release host specificity tests. This will enable more accurate predictions of parasitoid host ranges and risks parasitoids may pose to non-target organisms in the field.     

Food web structure of three guilds of natural enemies: predators, parasitoids and pathogens of aphids

1. Most communities of insect herbivores are unlikely to be structured by resource competition, but they may be structured by apparent competition mediated by shared natural enemies. 2. The potential of three guilds of natural enemies (parasitoids, fungal entomopathogens and predators) to influence aphid community structure through indirect interactions is assessed. Based on the biology, we predicted that the scope for apparent competition would be greatest for the predator and least for the parasitoid guilds. 3. Separate fully quantitative food webs were constructed for 3 years for the parasitoid guild, 2 years for the pathogen guild and for a single year for the predator guild. The webs were analysed using standard food web statistics designed for binary data, and using information-theory-based metrics that make use of the full quantitative data. 4. A total of 29 aphid, 24 parasitoid, five entomopathogenic fungi and 13 aphid specialist predator species were recorded in the study. Aphid density varied among years, and two species of aphid were particularly common in different years. Omitting these species, aphid diversity was similar among years. 5. The parasitoid web showed the lowest connectance while standard food web statistics suggested the pathogen and predator webs had similar levels of connectance. However, when a measure based on quantitative data was used the pathogen web was intermediate between the other two guilds. 6. There is evidence that a single aphid species had a particularly large effect on the structure of the pathogen food web. 7. The predator and pathogen webs were not compartmentalized, and the vast majority of parasitoids were connected in a single large compartment. 8. It was concluded that indirect effects are most likely to be mediated by predators, a prediction supported by the available experimental evidence.