Winter host exploitation influences fitness traits in a parasitoid

Organisms can either evade winter's unfavourable conditions by migrating or diapausing, or endure them and maintain their activities. When it comes to foraging during winter, a period of scarce resources, there is strong selective pressure on resource exploitation strategy. Generalist parasitoids are particularly affected by this environmental constraint, as their fitness is deeply linked to the profitability of the available hosts. In this study, we considered a cereal aphid–parasitoid system and investigated (1) the host–parasitoid community structure, host availability, and parasitism rate in winter, (2) the influence of host quality in terms of species and instars on the fitness of the aphid parasitoid Aphidius rhopalosiphi De Stefani‐Perez (Hymenoptera: Braconidae: Aphidiinae), and (3) whether there is a detectable impact of host fidelity on parasitism success of this parasitoid species. Host density was low during winter and the aphid community consisted of the species Rhopalosiphum padi L. and Sitobion avenae Fabricius (both Hemiptera: Aphididae), both parasitized by A. rhopalosiphi at non‐negligible rates. Aphidius rhopalosiphi produced more offspring when parasitizing R. padi compared with S. avenae, whereas bigger offspring were produced when parasitizing S. avenae. Although aphid adults and old larvae were significantly larger hosts than young larvae, the latter resulted in higher emergence rates and larger parasitoids. No impact of host fidelity on emergence rates or offspring size was detected. This study provides some evidence that winter A. rhopalosiphi populations are able to take advantage of an array of host types that vary in profitability, indicating that host selectivity may drop under winter's unfavourable conditions.     

Falling aphids enhance impact of biological control by parasitoids on partially aphid-resistant plant varieties

Cage experiments, in which the population increase of Metopolophium dirhodum was measured either in the absence or presence of the parasitoid Aphidius rhopalosiphi, showed reductions of peak populations in the presence of the parasitoid of 30% on the susceptible wheat cultivar Armada, but of 57% on the partially resistant Rapier. On both cultivars, aphid population curves in the presence and absence of the parasitoid diverged before the first mummies were formed. The number of aphids leaving plants was measured, and was found to increase in the presence of the parasitoid, particularly with Rapier (almost double). Most aphids (about 75%) which left plants fell, and a smaller proportion regained plants when parasitoids were present than when they were absent. A field experiment with Brevicoryne brassicae and natural predation on Brussels sprouts also showed an increase in aphids leaving a less susceptible compared with a more susceptible cultivar.     

Phenological responses in a sycamore–aphid–parasitoid system and consequences for aphid population dynamics: A 20 year case study

Species interactions have a spatiotemporal component driven by environmental cues, which if altered by climate change can drive shifts in community dynamics. There is insufficient understanding of the precise time windows during which inter‐annual variation in weather drives phenological shifts and the consequences for mismatches between interacting species and resultant population dynamics—particularly for insects. We use a 20 year study on a tri‐trophic system: sycamore Acer pseudoplatanus, two associated aphid species Drepanosiphum platanoidis and Periphyllus testudinaceus and their hymenopteran parasitoids. Using a sliding window approach, we assess climatic drivers of phenology in all three trophic levels. We quantify the magnitude of resultant trophic mismatches between aphids and their plant hosts and parasitoids, and then model the impacts of these mismatches, direct weather effects and density dependence on local‐scale aphid population dynamics. Warmer temperatures in mid‐March to late‐April were associated with advanced sycamore budburst, parasitoid attack and (marginally) D. platanoidis emergence. The precise time window during which spring weather advances phenology varies considerably across each species. Crucially, warmer temperatures in late winter delayed the emergence of both aphid species. Seasonal variation in warming rates thus generates marked shifts in the relative timing of spring events across trophic levels and mismatches in the phenology of interacting species. Despite this, we found no evidence that aphid population growth rates were adversely impacted by the magnitude of mismatch with their host plants or parasitoids, or direct impacts of temperature and precipitation. Strong density dependence effects occurred in both aphid species and probably buffered populations, through density‐dependent compensation, from adverse impacts of the marked inter‐annual climatic variation that occurred during the study period. These findings explain the resilience of aphid populations to climate change and uncover a key mechanism, warmer winter temperatures delaying insect phenology, by which climate change drives asynchronous shifts between interacting species.     

Are aphid parasitoids from mild winter climates losing their winter diapause?

Temperature is both a selective pressure and a modulator of the diapause expression in insects from temperate regions. Thus, with climate warming, an alteration of the response to seasonal changes is expected, either through genetic adaptations to novel climatic conditions or phenotypic plasticity. Since the 1980s in western France, the winter guild of aphid parasitoids (Hymenoptera: Braconidae) in cereal fields has been made up of two species: Aphidius rhopalosiphi and Aphidius matricariae. The recent activity of two other species, Aphidius avenae and Aphidius ervi, during the winter months suggests that a modification of aphid parasitoid overwintering strategies has taken place within the guild. In this study, we first performed a field survey in the winter of 2014/15 to assess levels of parasitoid diapause incidence in agrosystems. Then, we compared the capacity of the four parasitoid species to enter winter diapause under nine different photoperiods and temperature conditions in the laboratory. As predicted, historically winter-active species (A. rhopalosiphi and A. matricariae) never entered diapause, whereas the species more recently active during winter (A. avenae and A. ervi) did enter diapause but at a low proportion (maximum of 13.4 and 11.2%, respectively). These results suggest rapid shifts over the last three decades in the overwintering strategies of aphid parasitoids in Western France, probably due to climate warming. This implies that diapause can be replaced by active adult overwintering, with potential consequences for species interactions, insect community composition, ecosystem functioning, and natural pest control.     

Abundance of the rose-grain aphid,Metopolophium dirhodum,on barley in Canterbury,New Zealand, 1984–87

Abstract

Spring populations of Metopolophium dirhodum (Walker) (Hemiptera: Aphididae) on barley, at Lincoln and elsewhere in Canterbury, New Zealand, declined markedly during 1984–87. Spring suction-trap catches of M. dirhodum also declined at the same time. Numbers of immigrant M. dirhodum on young barley, and maximum aphid population density on the crop, were positively correlated with suction-trap catches of M. dirhodum during the preceding week or month, respectively. Egg numbers of the most abundant predator, Micromus tasmaniae Walker (Neuroptera: Hemerobiidae), and mummy numbers of the parasitoid, Aphidius rhopalosiphi De Stefani-Perez (Hymenoptera: Aphidiidae), increased relative to aphid numbers during the study. Entomophagous fungus-disease incidence could not be related to monthly rainfall, and the decline in aphid numbers during the study period was apparently not related to disease incidence. It is suggested that aphid population regulation by predators and parasitoids in the wider habitat of M. dirhodum could reduce the rate of immigration, and hence aphid population growth, in a given crop.     

Effect of wheat resistance, the parasitoid Aphidius rhopalosiphi, and the entomopathogenic fungus Pandora neoaphidis, on population dynamics of the cereal aphid Sitobion avenae

The influence of wheat (Triticum aestivumL.) resistance, the parasitoid Aphidius rhopalosiphiDe Stephani-Perez (Hymenoptera: Braconidae) and the entomopathogenic fungus Pandora neoaphidis(Remaudière et Hennebert) Humber (Zygomycetes: Entomophthorales) on the density and population growth rate of the cereal aphid Sitobion avenae(F.) (Hemiptera: Aphididae) was studied under laboratory conditions. Partial wheat resistance was based on hydroxamic acids, a family of secondary metabolites characteristic of several cultivated cereals. The partial resistance of wheat cultivar Naofén, the action of the parasitoid and the joint action of the parasitoid and fungus, reduced aphid density. The lowest aphid densities were obtained with the combination of the parasitoid and the fungus, but wheat resistance under these circumstances did not improve aphid control. Significant reductions of population growth rate (PGR) of aphids were obtained with the joint action of wheat resistance and natural enemies. In particular, the combined effects of parasitoids and fungi showed significantly lower PGR than the control without natural enemies in both wheat cultivars. Our results support the hypothesis that wheat resistance and the utilization of biological control agents could be complementary strategies in an integrated pest management program against cereal aphids.     

Influence of wheat and oat cultivars on the development of the cereal aphid parasitoid Aphidius rhopalosiphi and the generalist aphid parasitoid Ephedrus plagiator

The effects of three wheat cultivars and two oat cultivars on the development of the cereal aphid parasitoid Aphidius rhopalosiphi De Steph. and the generalist aphid parasitoid Ephedrus plagiator (Nees) (Hymenoptera: Braconidae) were evaluated in the laboratory. The level of hydroxamic acids, a family of secondary metabolites that can affect the mean relative growth rate of cereal aphids in cereals, were measured in the different cultivars. The parasitoids were reared in Sitobion avenae (F.) (Homoptera: Aphididae), using plants grown under greenhouse conditions. A. rhopalosiphi showed a longer developmental time on wheat relative to oat cultivars. This effect was accounted for by a significant increase in the time from oviposition to pupation (mummy formation), while the duration of the pupal stage remained constant between treatments. No further effects were observed in other variables evaluating A. rhopalosiphi performance, such as adult longevity, adult body weight and secondary sex ratio. The generalist E. plagiator did not show significant differences in any of the variables analysed, both between cultivars and cereal species. Hydroxamic acids levels correlated negatively with mean relative growth rates of S. avenae, but positively with the observed developmental time of A. rhopalosiphi. The results are discussed in terms of tritrophic effects and the development of breeding programmes trying to improve plant resistance to aphids.     

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     

When parasitoids deal with the spatial distribution of their hosts: consequences for both partners

Insect parasitoids developing inside hosts face a true challenge: hosts are scattered in the field and their localization and selection require the use of complex and sometime confusing information. It was assumed for a long time that small-brained organisms like parasitoids have evolved simple and efficient behavioral mechanisms, leading them to be adapted to a given ecological situation, for example, the spatial distribution o f hosts in the habitat. However, hosts are not static and their distribution may also vary through generations and within the life of parasitoid individuals. We investigated if and how parasitoids deal with such a spatial com plexity in a m esocosm experiment. We used the Aphidius rhopalosiphi/Sitobion avenae parasitoid/host system to investigate if parasitoid females experiencing different host aggregation levels exhibit different foraging behaviors independently of the number of hosts in the environment. We showed that A. rhopalosiphi females exploited hosts more intensively both within and among patches at higher host aggregation levels. We discussed the adaptiveness of such behaviors in the light of evolution and biological control.     

One step ahead: a parasitoid disperses farther and forms a wider geographic population than its fig wasp host

The structure of populations across landscapes influences the dynamics of their interactions with other species. Understanding the geographic structure of populations can thus shed light on the potential for interacting species to co‐evolve. Host–parasitoid interactions are widespread in nature and also represent a significant force in the evolution of plant–insect interactions. However, there have been few comparisons of population structure between an insect host and its parasitoid. We used microsatellite markers to analyse the population genetic structure of Pleistodontes imperialis sp. 1, a fig‐pollinating wasp of Port Jackson fig (Ficus rubiginosa), and its main parasitoid, Sycoscapter sp. A, in eastern Australia. Besides exploring this host–parasitoid system, our study also constitutes, to our knowledge, the first study of population structure in a nonpollinating fig wasp species. We collected matched samples of pollinators and parasitoids at several sites in two regions separated by up to 2000 km. We found that pollinators occupying the two regions represent distinct populations, but, in contrast, parasitoids formed a single population across the wide geographic range sampled. We observed genetic isolation by distance for each species, but found consistently lower F_ST and R_ST values between sites for parasitoids compared with pollinators. Previous studies have indicated that pollinators of monoecious figs can disperse over very long distances, and we provide the first genetic evidence that their parasitoids may disperse as far, if not farther. The contrasting geographic population structures of host and parasitoid highlight the potential for geographic mosaics in this important symbiotic system.     

The importance of intraguild interactions to the combined effect of a parasitoid and a predator on aphid population suppression

Intraguild predation (IGP) occurs when consumers competing for a resource also engage in predatory interactions. A common type of IGP involves aphid predators and parasitoids: since parasitoid offspring develop within aphid hosts, they are particularly vulnerable to predation by aphid predators such as coccinellid beetles. Other intraguild interactions that include non-lethal behavioral effects, such as interference with foraging and avoidance of IGP, may also hamper parasitoid activity and reduce their effectiveness as biological control agents. In this study, we quantified mortality in and behavioral effects on Aphidius colemani Viereck (Hymenoptera: Aphidiidae) by its IG-predator Coccinella undecimpunctata L. (Coleoptera: Coccinellidae), and compared the impact of two release ratios of these natural enemies on aphid populations. Parasitoids did not leave the plant onto which they were first introduced, regardless of the presence of predators, even when alternative prey was offered on predator-free plants nearby. In 2-hour experiments, predator larvae interfered with wasp activity, and the level of aphid parasitism was lower in the presence of predators than in their absence. In these experiments, the parasitoids contributed more to aphid mortality than the predators and aphid suppression was higher when a parasitoid acted alone than in combination with a predator larva. These results were confirmed in a 5-day experiment, but only at one parasitoid:predator release ratio (4:3) not another (2:3). The over-all impact on aphid population growth was non-the-less stronger when both enemies acted together than when only one of them was present. Results indicate that for given release ratios and time scale, the negative lethal and non-lethal effects of the predator on parasitoid performance did not fully cancelled the direct impact of the predator on the aphid population.     

Effects of wheat foliar fungicides on the aphid endoparasitoid Aphidius rhopalosiphi DeStefani-Perez (Hym., Aphidiidae) on glass plates and on plants

Abstract: The side-effects of several fungicides used in wheat to control disease at heading growth stage were assessed on the aphid parasitoid Aphidius rhopalosiphi by tests conducted in the laboratory on glass plates and in the greenhouse on young wheat plants. Very few formulations containing only one active ingredient (carbendazim, cyproconazole or epoxyconazole) or combinations of two (carbendazim + cyproconazole, carbendazim + hexaconazole) were harmless to A. rhopalosiphi in the glass-plate tests. There was no apparent synergism between fungicides tested in combinations. The parasitoid mortalities in tests carried out on plants were less and chlorothalonil, epoxyconazole, fenpropidin, fenpropimorph, flusilazole, flutriafol, prochloraz, tebuconazole, tridemorph and a number of combinations (carbendazim + flutriafol, chlorothalonil + cyproconazole, epoxyconazole + tridemorph, chlorothalonil + hexaconazole, chlorothalonil + flutriafol, cyproconazole + prochloraz, epoxyconazole + fenpropimorph, fenpropimorph + propiconazole, propiconazole + tridemorph, triadimenol + tridemorph) were harmless or only slightly harmful to the aphid parasitoid. Several combinations (carbendazim + epoxyconazole, carbendazim + fenpropimorph, carbendazim + flusilazole, carbendazim + tebuconazole, chlorothalonil + fenpropimorph, chlorothalonil + flusilazole, fenpropimorph + fenpropidin, fenpropimorph + prochloraz, fenpropidin + propiconazole, fenpropidin + tebuco nazole, tebuconazole + triadimenol) were toxic for wasps on plants. The parasitoid mortalities were less on plants than on glass plates but the wasps spent less time on treated leaves and in some cases parasitism of aphids was reduced to a large extent. These results suggest that in addition to study of the direct effects of pesticides on beneficial insects (mortalities, reduction of fertility) their effects on the behaviour of the insects should also be studied. Products that induced a repellent effect need further testing in field or semi-field conditions. However, many fungicide combinations that have little or no effect on A. rhopalosiphi can protect wheat against a wide range of diseases and the results obtained in this study indicate that an appropriate and effective protection of wheat at earing growth stage can be achieved with products that have no effects on aphid parasitoids.     

Extended larval development time for aphid parasitoids in the presence of plant endosymbionts

Abstract 1. Variation in plant chemistry does not only mediate interactions between plants and herbivores but also those between herbivores and their natural enemies, and plants and natural enemies. 2. Endophytic fungi complete their whole life cycle within the host plant’s tissue and are associated with a large diversity of plant species. Endophytes of the genus Neotyphodium alter the chemistry of the host plant by producing herbivore toxic alkaloids. 3. Here we asked whether the endophyte‐tolerant aphid species Metopolophium festucae could be defended against its parasitoid Aphidius ervi when feeding on endophyte‐infected plants. In a laboratory experiment, we compared life‐history traits of A. ervi when exposed to hosts on endophyte‐infected or endophyte‐free Lolium perenne. 4. The presence of endophytes significantly increased larval and pupal development times, but did not affect the mortality of immature parasitoids or the longevity of the adults. Although the number of parasitoid mummies tended to be reduced on endophyte‐infected plants, the number of emerging parasitoids did not differ significantly between the two treatments. 5. This shows that the metabolism of individual aphids feeding on infected plants may be changed and help in the defence against parasitoids. An increase in parasitoid development time should ultimately reduce the population growth of A. ervi. Therefore, endophyte presence may represent an advantage for endophyte‐tolerant aphid species through extended parasitoid development and its effect on parasitoid population dynamics.     

Interference between parasitoids [Hym.: Aphidiidae] and fungi [Entomophthorales] attacking cereal aphids

In field populations of cereal aphids parasitism levels declined through the season as fungal infection increased. In laboratory trials the fungusErynia neoaphidis Remaudiere & Hennebert took 3 to 4 days to kill the rose-grain aphid,Metopolophium dirhodum (Walker), whereas the parasitoidAphidius rhopalosiphi De Stefani-Perez took 8 to 9 days at 20°C. When aphids were infected by the fungus less than 4 days after being parasitized the parasitoids were prevented from completing their development. Conversely, when infection occurred more than 4 days after parasitization development of the fungus was significantly impaired. There was no histological evidence that the fungus invaded the tissues of the parasitoid when both attacked the same aphid. Interference between parasitoids and fungal pathogens must be taken into account when estimating the impact of these mortality agents on pest populations.     

Introduction and establishment ofTrioxys pallidus [Hym.: Aphidiidae] in Oregon,U.S.A. for control of filbert aphidMyzocallis coryli [Hom.: Aphididae]

Hazelnut orchards in Spain, France, and Italy were searched for parasitoids of the filbert aphid,Myzocallis coryli (Goetze). A biotype ofTrioxys pallidus Haliday was found to parasitize the aphid throughout western Europe. Wasps were imported, quarantined, mass-reared, and released in Oregon orchards. The wasp successfully attacked and completed its development on Oregon populations of the filbert aphid. A greenhouse culture of the parasitoid was maintained continuously for over 50 generations, and approximately 30,000 adult wasps were released in western Oregon. Overwintering survival has been documented in at least 12 different locations. In 3 commercial hazelnut orchards, the parasitoids proved capable of reducing aphid population peaks by 33–48%.      

Aphid parasitoid responses to semiochemicals — Genetic, conditioned or learnt?

Parasitoid foraging behaviour is known to be influenced by interactions of genetic, physiological, environmental and experiential factors. Although the role of genetics, learning and conditioning in determining responses to foraging cues has been studied in lepidopteran parasitoids, aphid parasitoids have been less intensively researched. Using the tritrophic system,Vicia faba — Acyrthosiphon pisum — Aphidius ervi, evidence for the role of genetics and learning in parasitoid foraging is presented, and the difficulty of differentiating between genetic responses and those conditioned during parasitoid development is discussed. Aphidius ervi responds to aphid sex pheromones both in the field and in the laboratory. Since laboratory reared individuals have never experienced sexual aphids, the response must be genetic as it cannot have been conditioned during development. An example of a response conditioned during development is the variable response ofA. rhopalosiphi to different wheat cultivars depending upon host feeding. Aphid parasitoids also are adept at learning as shown by their responses to plant-derived cues which are learnt as Conditioned Stimuli (CS). Host products such as honeydew, as well as the host itself, can act as the Unconditioned Stimulus (US) in the learning process. Aphidius ervi offers a good model for investigating the role of these factors in parasitoid foraging behaviour. Finally, the value of such research for biological control programmes involving aphid parasitoids is discussed.     

Does sex-biased dispersal account for the lack of geographic and host-associated differentiation in introduced populations of an aphid parasitoid?

Host recognition and use in female parasitoids strongly relies on host fidelity, a plastic behavior which can significantly restrict the host preferences of parasitoids, thus reducing the gene flow between parasitoid populations attacking different insect hosts. However, the effect of migrant males on the genetic differentiation of populations has been frequently ignored in parasitoids, despite its known impact on gene flow between populations. Hence, we studied the extent of gene flow mediated by female and male parasitoids by assessing sibship relationships among parasitoids within and between populations, and its impact on geographic and host‐associated differentiation in the aphid parasitoid Aphidius ervi. We report evidences of a high gene flow among parasitoid populations on different aphid hosts and geographic locations. The high gene flow among parasitoid populations was found to be largely male mediated, suggested by significant differences in the distribution of full‐sib and paternal half‐sib dyads of parasitoid populations.     

Rapid evolution of parasitoids when faced with the symbiont-mediated resistance of their hosts

Insects harbour a wild diversity of symbionts that can spread and persist within populations by providing benefits to their host. The pea aphid Acyrthosiphon pisum maintains a facultative symbiosis with the bacterium Hamiltonella defensa, which provides enhanced resistance against the aphid parasitoid Aphidius ervi. Although the mechanisms associated with this symbiotic‐mediated protection have been investigated thoroughly, little is known about its evolutionary effects on parasitoid populations. We used an experimental evolution procedure in which parasitoids were exposed either to highly resistant aphids harbouring the symbiont or to low innate resistant hosts free of H. defensa. Parasitoids exposed to H. defensa gained virulence over time, reaching the same parasitism rate as those exposed to low aphid innate resistance only. A fitness reduction was associated with this adaptation as the size of parasitoids exposed to H. defensa decreased through generations. This study highlighted the considerable role of symbionts in host–parasite co‐evolutionary dynamics.     

Tritrophic interactions between parasitoids and cereal aphids are mediated by nitrogen fertilizer

Host plant nutritional quality can directly and indirectly affect the third trophic levels. The aphid–parasitoid relationship provides an ideal system to investigate tritrophic interactions (as the parasitoids are completely dependent for their development upon their hosts) and assess the bottom up forces operating at different concentrations of nitrogen applications. The effects of varying nitrogen fertilizer on the performance of Aphidius colemani (V.) reared on Sitobion avenae (F.) and Aphidius rhopalosiphi (D.) reared on Rhopalosiphum padi (L.) were measured. Parasitism and percent emergence of parasitoids were positively affected by nitrogen fertilizer treatments while developmental duration (egg, larval, and pupal stages) was not affected by increasing nitrogen inputs. In males and females of both parasitoid species, adult longevity increased with the increasing nitrogen fertilizer. Hind tibia length and mummy weight of both parasitoid species increased with nitrogen fertilizer concentrations, as a result of larger aphids. This study showed that nitrogen application to the soil can have important consequences for aboveground multitrophic interactions.     

Local and spatial dynamics of a host–parasitoid system in a field experiment

Local extinction and colonisation rates are key factors in host–parasitoid metapopulation theory, but experimental evidence from the field is scarce. We studied the host–parasitoid system consisting of the aphid Metopeurum fuscoviride and its specialist parasitoid Lysiphlebus hirticornis. This system is characterised by a patchy distribution of the host plants (Tanacetum vulgare) and by frequent extinctions of local aphid populations. In a first field experiment, we found that the presence of the parasitoid increases the likelihood of extinction of local host populations (=all aphids living on one plant). In a second field experiment, we manipulated the distance between local host populations. Parasitoid colonisation rate strongly decreased with increasing distance between local host populations. Thus, our results show the importance of parasitoids for local host populations extinction and of distance between local host populations for parasitoid colonisation rate, suggesting the importance of spatial processes for host–parasitoid systems in the field.