Drugs and parasites: global experiments in life history evolution?

Recent work has shown that the evolution of Drosophila melanogaster resistance to attack by the parasitoid Asobara tabida is constrained by a trade-off with larval competitive ability. However, there are two very important questions that need to be answered. First, is this a general cost, or is it parasitoid specific? Second, does a selected increase in immune response against one parasitoid species result in a correlated change in resistance to other parasitoid species? The answers to both questions will influence the coevolutionary dynamics of these species, and also may have a previously unconsidered, yet important, influence on community structure.     

Tritrophic Choice Experiments with Bt Plants,the Diamondback Moth (Plutella xylostella) and the parasitoid Cotesia plutellae

Parasitoids are important natural enemies of many pest species and are used extensively in biological and integrated control programmes. Crop plants transformed to express toxin genes derived from Bacillus thuringiensis (Bt) provide high levels of resistance to certain pest species, which is likely to have consequent effects on parasitoids specialising on such pests. A better understanding of the interaction between transgenic plants, pests and parasitoids is important to limit disruption of biological control and to provide background knowledge essential for implementing measures for the conservation of parasitoid populations. It is also essential for investigations into the potential role of parasitoids in delaying the build-up of Bt-resistant pest populations. The diamondback moth (Plutella xylostella), a major pest of brassica crops, is normally highly susceptible to a range of Bt toxins. However, extensive use of microbial Bt sprays has led to the selection of resistance to Bt toxins in P. xylostella. Cotesia plutellae is an important endoparasitoid of P. xylostella larvae. Although unable to survive in Bt-susceptible P. xylostella larvae on highly resistant Bt oilseed rape plants due to premature host mortality, C. plutellae is able to complete its larval development in Bt-resistant P. xylostella larvae. Experiments of parasitoid flight and foraging behaviour presented in this paper showed that adult C. plutellae females do not distinguish between Bt and wildtype oilseed rape plants, and are more attracted to Bt plants damaged by Bt-resistant hosts than by susceptible hosts. This stronger attraction to Bt plants damaged by resistant hosts was due to more extensive feeding damage. Population scale experiments with mixtures of Bt and wildtype plants demonstrated that the parasitoid is as effective in controlling Bt-resistant P. xylostella larvae on Bt plants as on wildtype plants. In these experiments equal or higher numbers of parasitoid adults emerged per transgenic as per wildtype plant. The implications for integrated pest management and the evolution of resistance to Bt in P. xylostella are discussed.     

Volatile cues used by the parasitoid, Aphytis melinus, for host location: California red scale revisited

Aphytis melinus DeBach (Hymenoptera: Aphelinidae) is a biological control agent of diaspidid scale insects. The parasitoid has a narrow host range but its hosts are polyphagous. We determined the source of volatile cues the wasp uses to locate its few host species when those hosts occur on more than one host plant species. We addressed four questions in regard to the use of volatile cues in host location of California red scale, Aonidiella aurantii (Maskell) (Homoptera: Diaspididae): (1) Does A. melinus use volatile cues to assist in host location? (2) Are these cues innately recognized or learned? (3) Are cues produced by female California red scale, or from other sources? (4) Are the cues specific to the host or host plant? These questions were tested through the use of a Y-tube olfactometer. Female A. melinus used volatile cues to orient toward both infested and uninfested host plant material. Wasps learned these cues by associating odors from the host plant with host presence. They had no innate preferences for scale insect or host plant volatile stimuli. Contrary to previous studies, we found no evidence of orientation toward the female-produced sex pheromone of California red scale, nor to volatile cues from the attacked host stage. Wasps given experience with scale insects growing on lemon fruit subsequently oriented toward lemon and orange fruit and leaves. The scale species with which the wasp was given experience did not affect this preference. Wasps given experience with California red scale growing on squash did not orient toward infested lemon fruit. The host ranges of the parasitoid and its hosts are used to explain the adaptive value for the evolution of learned rather than fixed responses to cues used in foraging behavior.     

Effects of selected insecticides on adults of two parasitoid species of Liriomyza trifolii: Ganaspidium nigrimanus (Figitidae) and Neochrysocharis formosa (Eulophidae)

Abstract Liriomyza trifolii is an important pest of vegetables and ornamental crops around the world. This pest is attacked by many parasitoid species. The principal management tactic used against L. trifolii is insecticide application. Insecticides vary in their effects on parasitoid species and insecticides that have less harmful effects should be preferred for the control of this pest. In this study, novaluron, abamectin, λ‐cyhalothrin and spinetoram were investigated for their lethal effects on adults of Neochrysocharis formosa and Ganaspidium nigrimanus, two important parasitoids of L. trifolii. Three different bioassays were used on adult parasitoids: direct insecticide application, insecticide intake and insecticide residue. Adult parasitoid response to novaluron exhibited the least lethal effects among the bioassays and insecticides tested. Abamectin had significant mortality to both parasitoid species in the direct application and insecticide intake bioassays and mortality were high for G. nigrimanus in the residue bioassay. Spinetoram was the most harmful insecticide to the adult parasitoids in all three bioassays. λ‐cyhalothrin effects varied between the two parasitoids. In the direct application, it was harmful to G. nigrimanus and had no effect on N. formosa. In the insecticide intake bioassay λ‐cyhalothrin had no effect in survival of either species, and in the residue bioassay it reduced parasitoid survival of both species. Potential tolerance of N. formosa to λ‐cyhalothrin is discussed.     

Symbiont‐conferred protection against Hymenopteran parasitoids in aphids: how general is it?

1. Hosts are often targeted by multiple species of parasites, leading to a confluence of selective pressures on them. In response, hosts may either evolve defences that act very generally, or specific defences against particular parasites. Aphids are attacked by multiple species of endoparasitoid wasps, and there is clear evidence that heritable endosymbionts can confer resistance against some of these wasps. Less clear is how symbiont‐conferred resistance in a single host acts against multiple parasitoid species. 2. This question was addressed in the black bean aphid, Aphis fabae (Scopoli). Unprotected aphids and aphids protected by three different strains of the defensive endosymbiont Hamiltonella defensa were exposed to four species of parasitic wasps: the parthenogenetic species Lysiphlebus fabarum (Marshall), which was represented by three different asexual lines, and the sexual species Aphidius colemani (Viereck), Binodoxys angelicae (Halliday), and Aphelinus chaonia (Walker). 3. Hamiltonella defensa provided strong protection against L. fabarum and Aphidius colemani, but there was no evidence that H. defensa‐infected aphids were more resistant to the other parasitoid species. While Aphidius colemani was virtually unable to parasitise any aphids harbouring H. defensa, there was variation among the three asexual lines of L. fabarum in how susceptible they were to the defence provided by the different symbiont strains, resulting in a significant genotype‐by‐genotype interaction. 4. The present results suggest that symbiosis with H. defensa does not provide aphids with a general defence against parasitoid wasps, possibly because some species have evolved specific counter adaptations or because biological differences preclude the symbiont's effectiveness against these species.     

Intrinsic and extrinsic competitive interactions between two larval parasitoids of Heliothis virescens

1. Competition between parasitoid species may be a key factor in the community dynamics of plant–herbivore-parasitoid systems and is an important consideration in the selection and management of effective biological control agents. 2. Interspecific competition can occur between adult parasitoids searching for hosts (extrinsic competition) and between multiple parasitoid larvae developing within a single host individual (intrinsic competition). A model system comprising the lepidopteran pest Heliothis virescens and two key hymenopteran endoparasitoids, Microplitis croceipes and Cardiochiles nigriceps, was employed to explore parasitoid host-location strategies and the consequences of intrinsic and extrinsic competitive interactions between parasitoid species. 3. The less specialised of the two parasitoids, M. croceipes, was found to have a shorter hatching time and to dominate intrinsic competition, except when its oviposition followed that of the more specialised parasitoid, C. nigriceps, by 16 h or more. This interval corresponded to the differential in hatching time between the two species. 4. Cardiochiles nigriceps, however, displayed superior host-searching efficiency that may compensate for its disadvantage in intrinsic competition. This parasitoid was more effective at detecting host infestation sites via airborne odours and at locating and attacking early instar host larvae than was M. croceipes.     

The invasive stink bug Halyomorpha halys affects the reproductive success and the experience-mediated behavioural responses of the egg parasitoid Trissolcus basalis

Invasive species, because of their lack of co-evolutionary history with recipient communities, can act as “evolutionary traps” causing disconnects between natural enemy behavioural responses and the suitability of the invasive species as a prey/host resource. Invasion of exotic species in non-native environments may have several ecological effects, including consequences for the experience-mediated behavioural responses of indigenous foragers. Experience is usually thought to help resident species to buffer against negative impacts of new invasive species, including escaping from evolutionary traps. Here we hypothesized that the impact of foraging experience depends on whether an indigenous egg parasitoid can correctly assess the resource suitability of a new invasive species for offspring development. We showed that the invasive stink bug Halyomorpha halys acts as an evolutionary trap for the indigenous egg parasitoid Trissolcus basalis leading to unsuccessful development of?~?95% of the eggs laid in this host species. In a mixed scenario in which the associated resident stink bug Nezara viridula co-occurs with the invasive H. halys, we showed that oviposition experience in the low quality invasive host induces in T. basalis similar responses to those of the associated host. These results suggest that foraging experience does not lead to avoidance of an evolutionary trap. We discuss parasitoid foraging experience and reproductive success in the light of the evolutionary trap framework with implication for biological control.

     

Differential susceptibility and suitability of domestic and wild apple species for a florivorous weevil and its parasitoids

Crop plant domestication can change plant resistance to herbivores leading to differences in pest pressure experienced by crop plants and their wild relatives. To compare resistance to herbivores between domesticated and wild fruit trees, we quantified direct resistance and indirect resistance to a pest insect, the florivorous apple blossom weevil Anthonomus pomorum (Coleoptera: Curculionidae), for the cultivated apple Malus domestica and two wild apple species, the European crab apple M. sylvestris and the exotic M. kirghisorum. We measured weevil infestation and performance (weight, sex ratio), and weevil parasitism by parasitoid wasps for different cultivars of M. domestica and for the two wild apple species. To explain weevil and parasitoid responses to different apple species, we quantified tree characteristics including nitrogen content, size of flower buds, bark roughness, tree size, tree phenology and tree position. We found significant differences in susceptibility to weevil infestation between apple species, with lowest infestation (highest apple resistance) in M. domestica and highest infestation in M. kirghisorum. The suitability of apple species also varied significantly: weevils emerging from M. sylvestris were significantly lighter than those from M. kirghisorum. Parasitism of A. pomorum by different parasitoid species was significantly higher in M. sylvestris than in M. domestica. Infestation, weevil weight and parasitism were positively related to tree characteristics: infestation to bud nitrogen content and bark roughness, weevil size to nitrogen content and bud size, and parasitism to tree height and bud density. Our study revealed marked differences between apple species in susceptibility and suitability for the pest herbivore, but also for antagonistic parasitoids. Whereas direct resistance appeared to be higher in cultivated apple, indirect resistance via parasitoids was apparently higher in wild apple trees. Our findings suggest that wild and cultivated apple trees possess different resistance traits that may be combined to optimize resistance in commercial apple cultivars.     

Friendly food for fitter flies? – Influence of dietary microbial species on food choice and parasitoid resistance in Drosophila

Nutrition fuels any activity performed by an organism and has been shown to affect its ability to withstand pathogens and parasites. Furthermore, animals over a wide range of taxa have been shown to exhibit a choice of foods and nutrients that are beneficial to their fitness. Saprophagous animals most often feed on microorganisms growing on dead organic matter rather than the organic matter itself. Various yeast species play an important role in both larval and adult nutrition of saprophagous Drosophila melanogaster. We hypothesised the dietary microbial species to affect life‐history traits of D. melanogaster, including the ability to fend offparasitoids, and larvae to prefer to devour those yeast species beneficial to their development and immunocompetence. Particular yeast species known to be associated with D. melanogaster could be shown to have a substantial influence on various larval and adult fitness traits including the ability to encapsulate eggs of the parasitoid wasp Asobara tabida. It also turned out that larvae chose to devour those yeast species which supported their ability to encapsulate parasitoid eggs. Which yeast species was preferred and had a beneficial impact on encapsulation ability, was subject to inter‐individual variability within the investigated population, hinting at the existence of an adaptive heritable variability regarding individual choice and salubriousness of food. The results suggest that the dietary microbial species of saprophagous insects may influence the resistance against parasitoid attacks and thus the outcome of the interaction between a saprophagous host and its parasitoids.     

A molecular tool to identify Anastatus parasitoids of the brown marmorated stink bug

Globally, Anastatus species (Hymenoptera: Eupelmidae) are associated with the invasive agricultural pest Halyomorpha halys (Stål) (Hemiptera: Pentatomidae). In Europe, the polyphagous Anastatus bifasciatus (Geoffroy) is the most prevalent native egg parasitoid on H. halys eggs and is currently being tested as a candidate for augmentative biological control. Anastatus bifasciatus frequently displays behavior without oviposition, and induces additional host mortality through oviposition damage and host feeding that is not measured with offspring emergence. This exacerbates accurate assessment of parasitism and host impact, which is crucial for efficacy evaluation as well as for pre‐ and post‐release risk assessment. To address this, a general Anastatus primer set amplifying a 318‐bp fragment within the barcoding region of the cytochrome oxidase I (COI) gene was developed. When challenged with DNA of three Anastatus species —A. bifasciatus, Anastatus japonicus Ashmead, and Anastatus sp.—, five scelionid parasitoid species that might be encountered in the same host environments and 11 pentatomid host species, only Anastatus DNA was successfully amplified. When applied to eggs of the target host, H. halys, and an exemplary non‐target host, Dendrolimus pini L. (Lepidoptera: Lasiocampidae), subjected to host feeding, no Anastatus amplicons were produced. Eggs of the two host species containing A. bifasciatus parasitoid stages, from 1‐h‐old eggs to pupae, and emerged eggs yielded Anastatus fragments. Confirmation of parasitoid presence with dissections and subsequent PCRs with the developed primer pair resulted in 95% success for 1‐h‐old parasitoid eggs. For both host species, field‐exposed sentinel emerged eggs stored dry for 6 months, 100% of the specimens produced Anastatus amplicons. This DNA‐based screening method can be used in combination with conventional methods to better interpret host‐parasitoid and parasitoid‐parasitoid interactions. It will help address ecological questions related to an environmentally friendly approach for the control of H. halys in invaded areas.     

Survey of brown soft scale Coccus hesperidum L. parasitoids in southern California citrus

The parasitoid complex of brown soft scale, Coccus hesperidum L., a multivoltine soft scale, was determined in southern California citrus over the period February 2004–March 2006. The survey was conducted by placing brown soft scale-infested yucca leaves in the canopy of citrus trees and subsequently rearing individually isolated parasitized scales in the laboratory. A total of 14 species parasitized brown soft scale in the field, the most abundant ones belonging to the genus Metaphycus Mercet (75%). The most abundant parasitoid species was Metaphycus angustifrons Compere (38% parasitism), and this is a new record of establishment for this species in California. Coccophagus species accounted for only 11% parasitism. There were important spatio-temporal differences across the parasitoid complex survey locations. We also found that the five most abundant encyrtid parasitoid species showed preferences for scales of different sizes. Our results have implications for biological control of citricola scale, Coccus pseudomagnoliarum (Kuwana), an important pest of citrus in the San Joaquin Valley of central California. Notably, this species is nearly absent in southern California. Brown soft scale is considered to be an alternate host for parasitoids of citricola scale, a univoltine soft scale, at times when the latter species is unavailable for parasitism.     

Patch residence decisions made by Aphidius colemani in the presence of a facultative predator

One of the key questions in ecology is how animals optimally allocate their time in an environment with patchily distributed resources and competing organisms. Here we investigate the effects that an aphid predator, Macrolophus caliginosus (Wagner) (Hemiptera: Miridae), has on the searching behavior and the patch residence decisions of an aphid parasitoid, Aphidius colemani (Viereck) (Hymenoptera: Aphidiidae). A computer programme was designed that allowed the recording and saving of direct observations. The time allocated to different activities by a female parasitoid wasp in the presence or absence of the predator M. caliginosus was investigated. The experiments were conducted under controlled environment conditions using leaves of sweet pepper, Capsicum annuum L. (Solanaceae) and Myzus persicae (Sulzer) (Hemiptera: Aphididae) as the host plant–prey species system. The parasitoid spent significantly less time on ‘secondary’ activities, such as preening and resting, when the predator was present. Survival analysis showed that the parasitoid had a higher patch-leaving tendency when the predator was present.     

ASSOCIATION BETWEEN FEEDING RATE AND PARASITOID RESISTANCE IN DROSOPHILA MELANOGASTER

Replicate lines of Drosophila melanogaster have been selected for increased resistance against one of two species of parasitoid wasp, Asobara tabida and Leptopilina boulardi. In both cases, it has been shown that an improved ability to mount an immunological defense against the parasitoid's egg is associated with reduced survival when the larvae are reared under conditions of low resource availability and thus high competition. We show here that in both sets of selected lines, lower competitive ability is associated with reduced rates of larval feeding, as measured by the frequency of retractions of the cephalopharyngeal skeleton. This suggests that the same or similar physiological processes are involved in the trade-off between competition and resistance against either parasitoid and shows how the interaction between adaptations for competition and natural enemy resistance may be mediated.     

CROSS-RESISTANCE FOLLOWING ARTIFICIAL SELECTION FOR INCREASED DEFENSE AGAINST PARASITOIDS IN DROSOPHILA MELANOGASTER

An increase in resistance to one natural enemy may result in no correlated change, a positive correlated change, or a negative correlated change in the ability of the host or prey to resist other natural enemies. The type of specificity is important in understanding the evolutionary response to natural enemies and was studied here in a Drosophila-paxasitoid system. Drosophila melanogaster lines selected for increased larval resistance to the endoparasitoid wasps Asobara tabida or Leptopilina boulardi were exposed to attack by A. tabida, L. boulardi and Leptopilina heterotoma at 15°C, 20°C, and 25°C. In general, encapsulation ability increased with temperature, with the exception of the lines selected against L. boulardi, which showed the opposite trend. Lines selected against L. boulardi showed large increases in resistance against all three parasitoid species, and showed similar levels of defense against A. tabida to the lines selected against that parasitoid. In contrast, lines selected against A. tabida showed a large increase in resistance to A. tabida and generally to L. heterotoma, but displayed only a small change in their ability to survive attack by L. boulardi. Such asymmetries in correlated responses to selection for increased resistance to natural enemies may influence host-parasitoid community structure.     

Evaluating potential sugar food sources from the olive grove agroecosystems for Prays oleae parasitoid Chelonus elaeaphilus

Chelonus elaeaphilus Silvestri (Hymenoptera: Braconidae) is a host-specific parasitoid of the olive moth, Prays oleae (Bernard), that can cause parasitism rates of up to 80% in Mediterranean olive groves. A laboratory study was carried out to assess the potential of sugars provided by wild plant species in olive grove agroecosystem to enhance the fitness of C. elaeaphilus. Insects were reared in a climate-controlled chamber at 25?±?2°C, 60?±?5% relative humidity (RH) with a photoperiod of 16:8 (L:D) h. Five naturally occurring wild plant nectar sugars (sucrose, fructose, glucose, maltose and mannose) were tested for their effect on insect longevity. The nectar sugar content of sucrose, fructose and glucose in 12 selected olive grove agroecosystem plant species was analysed and categorised on the basis of sugar ratios. Female insect longevity was increased when they were fed on both sucrose and glucose compared to either maltose or fructose, suggesting that sucrose-dominant nectars would bene?t this parasitoid. Sucrose was predominant in the nectar of five of the studied plant species (Silene gallica, Borago officinalis, Echium plantagineum, Lavandula stoechas and Lonicera hispânica). The results are discussed in terms of potential enhancement of the biological control of P. oleae.     

Effects of pea aphid secondary endosymbionts on aphid resistance and development of the aphid parasitoid Aphidius ervi: a correlative study

In order to reduce parasite‐induced mortality, hosts may be involved in mutualistic interactions in which the partner contributes to resistance against the parasite. The pea aphid, Acyrthosiphon pisum Harris (Hemiptera: Aphididae), harbours secondary bacterial endosymbionts, some of which have been reported to confer resistance against aphid parasitoids. Although this resistance often results in death of the developing parasitoid larvae, some parasitoid individuals succeed in developing into adults. Whether these individuals suffer from fitness reduction compared to parasitoids developing in pea aphid clones without symbionts has not been tested so far. Using 30 pea aphid clones that differed in their endosymbiont complement, we studied the effects of these endosymbionts on aphid resistance against the parasitoid Aphidius ervi Haliday (Hymenoptera: Braconidae: Aphidiinae), host–parasitoid physiological interactions, and fitness of emerging adult parasitoids. The number of symbiont species in an aphid clone was positively correlated with a number of resistance measurements but there were also clear symbiont‐specific effects on the host–parasitoid interaction. As in previous studies, pea aphid clones infected with Hamiltonella defensa Moran et al. showed resistance against the parasitoid. In addition, pea aphid clones infected with Regiella insecticola Moran et al. and co‐infections of H. defensa–Spiroplasma, R. insecticola–Spiroplasma, and R. insecticola–H. defensa showed reduced levels of parasitism and mummification. Parasitoids emerging from symbiont‐infected aphid clones often had a longer developmental time and reduced mass. The number of teratocytes was generally lower when parasitoids oviposited in aphid clones with a symbiont complement. Interestingly, unparasitized aphids infected with Serratia symbiotica Moran et al. and R. insecticola had a higher fecundity than unparasitized aphids of uninfected pea aphid clones. We conclude that in addition to conferring resistance, pea aphid symbionts also negatively affect parasitoids that successfully hatch from aphid mummies. Because of the link between aphid resistance and the number of teratocytes, the mechanism underlying resistance by symbiont infection may involve interference with teratocyte development.     

Plant species variation in bottom‐up effects across three trophic levels: a test of traits and mechanisms

1. An increasing number of studies have addressed the mechanisms by which plant inter‐specific variation influence interactions at higher trophic levels, but little is known about the underlying plant traits driving these dynamics. 2. Here we investigated the effects of host plant species on herbivore‐parasitoid interactions and the underlying traits driving such effects. For this, we measured the abundance of seed‐eating bruchids and their parasitoids across seven sympatric populations of the bean species Phaseolus coccineus and Phaseolus vulgaris in Central Mexico. To investigate the mechanisms underlying differences between bean species in bruchid‐parasitoid interactions, we carried out two laboratory experiments to test whether bruchid and parasitoid performance differed between plant species. We also measured seed size and phenolic compounds to investigate if seed traits mediate bruchid‐parasitoid interactions by influencing herbivore susceptibility or resistance to parasitoids. 3. Field surveys revealed that the rate of parasitoid recruitment to bruchids was significantly higher on P. vulgaris than on P. coccineus. Subsequent laboratory bioassays indicated that bruchids developed more slowly and exhibited lower fitness on P. vulgaris seeds than on P. coccineus seeds. Accordingly, we found that bean species differed in seed size, with P. vulgaris having smaller (less nutritious) seeds, which explains why bruchid development was slower on this plant species. 4. These results provide a mechanism for why bruchids exhibited higher parasitism rates on seeds of P. vulgaris in the field which could be due to Slow‐Growth/High‐Mortality effects, a smaller physical refuge provided by the seed, or both factors. The roles of these mechanisms remain inconclusive without further study.     

Host specificity of the egg pupal parasitoid Fopius arisanus (Hymenoptera: Braconidae) in La Reunion

Fopius arisanus is a polyphagous parasitoid of Tephritidae, which has been recently introduced to La Réunion Island as part of a classical biological control programme. We carried out laboratory experiments to assess the host specificity of this parasitoid, initially reared on Bactrocera zonata, and then offered for parasitization the eight local tephritid pest species. Naive or experienced parasitoid females were given tephritid eggs in no choice tests. Fopius arisanus females parasitize all fly species but parasitism varies with host species. No adult wasps emerge from Bactrocera cucurbitae and the survival of this species is only slightly affected by parasitism. Dissections show that the late instars of this fly may eliminate the parasitoid by encapsulation. When developing on Ceratitis capitata, Ceratitis rosa, Dacus ciliatus, Dacus demmerezi, and Neoceratitis cyanescens, parasitoid survival rate ranges from 10 to 25%. Bactrocera zonata and Ceratitis catoirii are the best hosts, yielding parasitoid survival rates of more than 70% with no premature mortality. The egg-larval mortality of C. capitata, C. rosa, D. ciliatus, and N. cyanescens, and the pupal mortality of D. demmerezi, are significantly increased by parasitism. The size of emerging adults is affected by host species and is correlated to pupal weight. Bactrocera zonata would be a favorable host to support routine colonization of F. arisanus for mass production of this parasitoid.     

Presence of an unsuitable host diminishes the competitive superiority of an insect parasitoid: a distraction effect

Competitive interactions between parasitoid species are traditionally evaluated when they compete for a single host species. Yet, the presence of additional host species can alter competitive interactions, even if the host is unsuitable for parasitoid development. In alfalfa of the mid-western USA, a native parasitoid species, Praon pequodorum, was once a dominant natural enemy, but it has become rare since the introduction of another parasitoid, Aphidius ervi. Despite A. ervi’s competitive superiority for their most common host, the pea aphid Acyrthosiphum pisum, P. pequodorum still persists at low densities. We performed a suite of laboratory and field studies to determine if the presence of an alternative host, the spotted alfalfa aphid Therioaphis maculata, may mitigate A. ervi’s competitive superiority and facilitate P. pequodorum’s persistence. We show that spotted alfalfa aphids reduce the foraging efficiency of both parasitoid species for pea aphids, despite spotted alfalfa aphids being an unsuitable host. This decrease in efficiency, however, was not symmetrical; the presence of spotted alfalfa aphids had a greater detrimental effect on A. ervi foraging for pea aphids. This might facilitate the persistence of the competitively inferior P. pequodorum. Our study suggests that indirect effects generated by the presence of alternative hosts are important for understanding parasitoid–host dynamics and overall insect community structure.     

The effect of multi‐species host density on superparasitism and sex ratio in a gregarious parasitoid

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